ORIGINAL_ARTICLE
Potential angiotensin converting enzyme (ACE) inhibitors from Iranian traditional plants described by Avicenna’s Canon of Medicine
Objective: Hypertension is an important cause of cardiovascular disorders. The angiotensin converting enzyme (ACE) plays an important role in hypertension; therefore, inhibition of ACE in treatment of chronically elevated blood pressure is an important therapeutic approach. In the current review, we have provided information from Persian Traditional Plants described by Avicenna in the Canon of Medicine and a number of more current scientific databases, with a focus on angiotensin converting enzyme inhibitory activity of the following six plants: Allium sativum, Cinnamomum zeylanicum, Jasminum grandiflorum, Tribulus terrestris, Vaccinium myrtillus and Vitis vinifera. Materials and Methods: A literature search was conducted and information on different traditional plants used for hypertension was collected from the Canon of Medicine and several other databases including PubMed, Scopus, Google Scholar and Web of Science. Results: The present article highlights the antihypertensive potential of the above-noted six plants. Administered doses, manner of consumption, types of extracts, preparations and derivatives, personal habits, and other geographic and epidemiologic variables have an important role in the potential efficacy of these plants. Conclusion: Recent studies indicated a significant correlation between the traditional use of Persian plants to reduce blood pressure and angiotensin converting enzyme inhibitory activity.
https://ajp.mums.ac.ir/article_12233_4f24ac85f4f23e842588149d22d320e5.pdf
2019-07-01
291
309
10.22038/ajp.2019.12233
Hypertension
Angiotensin converting enzyme
Avicenna
Canon of medicine
Traditional plants
Zohreh
Kamrani
kamraniz941@mums.ac.ir
1
Department of Pharmacodynamics and Toxicology, School of Pharmacy, Mashhad University of Medical Sciences, Mashhad, Iran.
AUTHOR
Behjat
Javadi
javadib@mums.ac.ir
2
Department of Traditional Pharmacy, School of Pharmacy, Mashhad University of Medical Sciences, Mashhad, Iran.
AUTHOR
Awallace
Hayes
awallacehayes@comcast.net
3
University of South Florida College of Public Health, Tampa, FL USA and Michigan State University Institute for Integrative Toxicology, East Learning; MI USA.
AUTHOR
Gholamreza
Karimi
karimig@mums.ac.ir
4
Department of Pharmacodynamics and Toxicology, School of Pharmacy, Mashhad University of Medical Sciences, Mashhad, Iran.
LEAD_AUTHOR
Abirami P, Rajendran A. 2011. GC-MS analysis of tribulus terrestris. Asian J Plant Sci Res, 1: 13-16.
1
Adisakwattana S, Moonrat J, Srichairat S, Chanasit C, Tirapongporn H, Chanathong B, Ngamukote S, Mauml K, Sapwarobol S. 2010. Lipid-lowering mechanisms of grape seed extract (Vitis vinifera L) and its antihyperlidemic activity. J Med Plant Res, 4: 2113-2120.
2
Afonso J, Passos CP, Coimbra MA, Silva C M, Soares-Da-Silva P. 2013. Inhibitory effect of phenolic compounds from grape seeds (Vitis vinifera L.) on the activity of angiotensin I converting enzyme. LWT-food Sci Technol, 54: 265-270.
3
Agrawal M, Nandini D, Sharma V, Chauhan N. 2010. Herbal remedies for treatment of hypertension. Int J Pharm Sci Res, 1: 1-21.
4
Akilen R, Pimlott Z, Tsiami A, Robinson N. 2013. Effect of short-term administration of cinnamon on blood pressure in patients with prediabetes and type 2 diabetes. Nutrition, 29: 1192-1196.
5
Aldini G, Carini M, Piccoli A, Rossoni G, Facino RM. 2003. Procyanidins from grape seeds protect endothelial cells from peroxynitrite damage and enhance endothelium-dependent relaxation in human artery: new evidences for cardio-protection. Life Sci, 73: 2883-2898.
6
Arun APM, Satish S, Anima P. 2016. Phytopharmacological profile of Jasminum grandiflorum Linn (Oleaceae). Chin J Integr Med, 22: 311-320.
7
Arzanlou M, Bohlooli S. 2010. Introducing of green garlic plant as a new source of allicin. Food chem, 120: 179-183.
8
Asdaq S, Inamdar M. 2010. Potential of garlic and its active constituent, S-allyl cysteine, as antihypertensive and cardioprotective in presence of captopril. Phytomedicine, 17: 1016-1026.
9
Aviello G, Abenavoli L, Borrelli F, Capasso R, Izzo AA, Lembo F, Romano B, Capasso F. 2009. Garlic: empiricism or science? Nat prod commun, 4: 1785-1796.
10
Baharvand-Ahmadi B, Asadi-Samani M. 2016. A mini-review on the most important effective medicinal plants to treat hypertension in ethnobotanical evidence of Iran. J Nephropharmacol, 6: 3.
11
Barbosa-Filho JM, Martins VK, Rabelo LA, Moura MD, Silva MS, Cunha EV, Souza MF, Almeida RN, Medeiros IA. 2006. Natural products inhibitors of the angiotensin converting enzyme (ACE): A review between 1980-2000. Rev Bras Farmacogn, 16: 421-446.
12
Basha SM, Musingo M, Colova VS. 2004. Compositional differences in the phenolics compounds of muscadine and bunch grape wines. Afr J Biotechnol, 3: 523-528.
13
Basheer L, Kerem Z. 2015. Interactions between CYP3A4 and dietary polyphenols. Oxid Med Cell Longev, 2015: 15.
14
Bayan L, Koulivand PH, Gorji A. 2014. Garlic: a review of potential therapeutic effects. Avicenna J Phytomed, 4: 1-14.
15
Biesinger S, Michaels H, Quadros A, Qian Y, Rabovsky A, Badger R, Jalili T. 2016. A combination of isolated phytochemicals and botanical extracts lowers diastolic blood pressure in a randomized controlled trial of hypertensive subjects. Eur J Clin Nutr, 70: 10-16.
16
Bombardelli E, Morazzoni P, Carini M, Aldini G, Maffei Facino R. 1997. Biological activity of procyanidins from Vitis vinifera L. BioFactors, 6: 429-431.
17
Borde P, Mohan M, Kasture S. 2011. Effect of myricetin on deoxycorticosterone acetate (DOCA)-salt-hypertensive rats. Nat Prodt Res, 25: 1549-1559.
18
Capraz M, Dilek M, Akpolat T. 2007. Garlic, hypertension and patient education. Int J Cardiol, 121: 130-131.
19
Chaturvedi AP, Kumar M, Tripathi Y. B. 2013. Efficacy of Jasminum grandiflorum L. leaf extract on dermal wound healing in rats. Int Wound J, 10: 675-682.
20
Chaturvedi AP, Tripathi YB. 2011. Methanolic extract of leaves of Jasminum grandiflorum Linn modulates oxidative stress and inflammatory mediators. Inflammopharmacology, 19: 273-281.
21
Chhatre S, Nesari T, Somani G, Kanchan D, Sathaye S. 2014. Phytopharmacological overview of Tribulus terrestris. Pharmacogn Rev, 8: 45.
22
Chobanian AV, Bakris GL, Black HR, Cushman WC, Green LA, Izzo JL, Jones DW, Materson BJ, Oparil S, Wright JT. 2003. Seventh report of the joint national committee on prevention, detection, evaluation, and treatment of high blood pressure. Hypertension, 42: 1206-1252.
23
Chu WK, Cheung SC, Lau RA, Benzie IF, Wachtel-Galor S. 2011. Herbal medicine: biomolecular and clinical aspects. CRC Press, Boca Raton (FL): 55.
24
Corzo-Martínez M, Corzo N, Villamiel M 2007. Biological properties of onions and garlic. Trends Food Sci Technol, 18: 609-625.
25
Cravotto G, Boffa L, Genzini L, Garella D. 2010. Phytotherapeutics: an evaluation of the potential of 1000 plants. J Clin Pharm Ther, 35: 11-48.
26
Dennison-Himmelfarb C, Handler J, Lackland DT, Lefevre ML, Mackenzie TD, Ogedegbe O, Smith Jr, SC, Svetkey LP, Taler SJ, Townsend RR. 2013. 2014 Evidence-based guideline for the management of high blood pressure in adults report from the panel members appointed to the eighth joint national committee (JNC 8). JAMA. 311:507-520.
27
Dinchev D, Janda B, Evstatieva L, Oleszek W, Aslani MR, Kostova I. 2008. Distribution of steroidal saponins in Tribulus terrestris from different geographical regions. Phytochemistry, 69: 176-186.
28
Duda G, Suliburska J, Pupek-Musialik D. 2007. Effects of short-term garlic supplementation on lipid metabolism and antioxidant status in hypertensive adults. Pharmacol Rep, 60: 163-170.
29
Elkayam A, Mirelman D, Peleg E, Wilchek M, Miron T, Rabinkov A, Sadetzki S, Rosenthal T. 2001. The effects of allicin and enalapril in fructose-induced hyperinsulinemic hyperlipidemic hypertensive rats. Am J Hypertens, 14: 377-381.
30
Emtiazy M, Choopani R, Khodadoost M, Tansaz M, Dehghan S, Ghahremani Z. 2014. Avicenna’s doctrine about arterial hypertension. Acta Med Hist Adriat, 12: 157-162.
31
Evstatieva L, Tchorbanov B. 2011. Complex investigations of Tribulus terrestris L. for sustainable use by pharmaceutical industry. Biotechnol Biotechnol Equip, 25: 2341-2347.
32
Facino RM, Carini M, Aldini G, Berti F, Rossoni G, Bombardelli E, Morazzoni P. 1999. Diet enriched with procyanidins enhances antioxidant activity and reduces myocardial post-ischaemic damage in rats. Life Sci, 64: 627-642.
33
Fan P, Lou H, Yu W, Ren D, Ma B, Ji M. 2004. Novel flavanol derivatives from grape seeds. Tetrahedron Lett, 45: 3163-3166.
34
Faridi P, Moatamedi M, Zarshenas MM, Abolhassanzadeh Z, Mohagheghzadeh A. 2015. Natural remedies in the Canon of Medicine for dentistry and oral biology. Trends Pharm Sci, 1: 4-9.
35
Fauconneau B, Waffo-Teguo P, Huguet F, Barrier L, Decendit A, Merillon JM. 1997. Comparative study of radical scavenger and antioxidant properties of phenolic compounds from Vitis vinifera cell cultures using in vitro tests. Life Sci, 61: 2103-2110.
36
Ferreres F, Grosso C, Gil-Izquierdo A, Valentão P, Andrade PB. 2014. Assessing Jasminum grandiflorum L. authenticity by HPLC-DAD-ESI/MS n and effects on physiological enzymes and oxidative species. J Pharm Biomed anal, 88: 157-161.
37
Fugh-Berman A. 2000. Herb-drug interactions. Lancet, 355: 134-138.
38
Ganzera M, Bedir E, Khan I. 2001. Determination of steroidal saponins in Tribulus terrestris by reversed‐phase high‐performance liquid chromatography and evaporative light scattering detection. J Pharm Sci, 90: 1752-1758.
39
Gharib Naseri MK, Heidari A. 2006. Bronchodilatory activity of Vitis vinifera leaf hydroalcoholic extract in rat. Iran Biomed J, 10: 79-83.
40
Gharib Naseri MK, Navid Hamidi M, Heidari A. 2010. Vasorelaxatory effect of Vitis vinifera extract on rat aorta. Iran J Pharm Res, 4: 93-99.
41
Godse S, Mohan M, Kasture V, Kasture S. 2010. Effect of myricetin on blood pressure and metabolic alterations in fructose hypertensive rats. Pharm biol, 48: 494-498.
42
Hashim S, Bakht T, Khan B, Jan J. 2014. Medicinal properties, phyto-chemistry and pharmacology of Tribulus terrestris L. (Zygophyllaceae). Pak J Bot, 46: 399-404.
43
Hosseini M, Shafiee SM, Baluchnejadmojarad T. 2007. Garlic extract reduces serum angiotensin converting enzyme (ACE) activity in nondiabetic and streptozotocin-diabetic rats. Pathophysiology, 14: 109-112.
44
Hussain AA, Mohammed AA, Ibrahim HH, Abbas AH. 2009. Study the biological activities of tribulus terrestris extracts. World Acad Sci Eng Technol, 57: 433-435.
45
Ichiyanagi T, Hatano Y, Matsugo S, Konishi T. 2004. Structural dependence of HPLC separation pattern of anthocyanins from bilberry (Vaccinium myrtillus L.). Chem Pharm P Bull, 52: 628-630.
46
Inokuchi J, Okabe H, Yamauchi T, Nagamatsu A. 1984. Inhibitors of angiotensin converting enzyme in crude drugs. I. Chem pharm bull, 32: 3615-3619
47
Inoue M, Craker LE. 2014. Medicinal and aromatic plants—uses and functions. Horticulture: Plants for People and Places , 2: 645-669.
48
Ismail EH, Khalil MM, Al Seif FA, El-Magdoub F. 2014. Biosynthesis of gold nanoparticles using extract of grape (vitis vinifera) leaves and seeds. Prog Nanotechnol Nanomater, 3: 1-12.
49
Jain S, Sangma T, Shukla SK, Mediratta PK. 2015. Effect of Cinnamomum zeylanicum extract on scopolamine-induced cognitive impairment and oxidative stress in rats. Nutr Neur, 18: 210-216.
50
Jayaprakasha G, Rao LJM. 2011. Chemistry, biogenesis, and biological activities of Cinnamomum zeylanicum. Crit Rev Food Sci Nutr, 51: 547-562.
51
Jorjani S, Zakhirehkharazmshahi. Treasure of Kharazmshahi), Saeedisirjani AA. 1976. Photo print of the manuscript dated 1206 A.D Tehran. The lranian Culture Foundation, 3.
52
Kardeh S, Choopani R, Mahmoudi NG, Zargaran A. 2014. The urinary catheter and its significant applications described by Avicenna (980-1037 AD) in the canon of medicine. Urology, 84: 993-996.
53
Kavitha A, Jagadeesan G. 2006. Role of Tribulus terrestris (Linn.) (Zygophyllacea) against mercuric chloride induced nephrotoxicity in mice, Mus musculus (Linn.). J Environ Biol, 37: 397-400.
54
Kesari A, Mahto PK, Kishan S, Singh S. 2014. Herbal anti hypertension drugs. Pharma Tutor, 2: 49-61.
55
Khan M, Matsui T, Matsumoto Y, Jabbar S. 2001. In vitro ACE inhibitory effects of some Bangladeshi plant extracts. Die Pharmazie, 56: 902-903.
56
Kiss AK, Mańk M, Melzig M. 2008. Dual inhibition of metallopeptidases ACE and NEP by extracts, and iridoids from Ligustrum vulgare L. J Ethnopharmacol, 120: 220-225.
57
Koo M, Kim S, Lee N, Yoo M, Ryu S, Kwon D, Kim Y. 2008. 3-Hydroxy-3-methylglutaryl-CoA (HMG-CoA) reductase inhibitory effect of Vitis vinifera. Fitoterapia, 79: 204-206.
58
Kostova I, Dinchev D. 2005. Saponins in Tribulus terrestris–chemistry and bioactivity. Phytochem Rev, 4: 111-137.
59
Lee C, Han D, Kim B, Baek N, Baik BK. 2013. Antioxidant and anti‐hypertensive activity of anthocyanin‐rich extracts from hulless pigmented barley cultivars. Int J Food Sci Technol, 48: 984-991.
60
Loizzo MR, Saab AM, Tundis R, Menichini F, Bonesi M, Piccolo V, Statti GA, De Cindio B, Houghton PJ, Menichini F. 2008. In vitro inhibitory activities of plants used in Lebanon traditional medicine against angiotensin converting enzyme (ACE) and digestive enzymes related to diabetes. J Ethnopharmacol, 119: 109-116.
61
Mahdizadeh S, Ghadiri MK, Gorji A. 2015. Avicenna's Canon of Medicine: a review of analgesics and anti-inflammatory substances. Avicenna J phytomed, 5: 182.
62
Malik J, Munjal K, Deshmukh R. 2015. Attenuating effect of standardized lyophilized Cinnamomum zeylanicum bark extract against streptozotocin-induced experimental dementia of Alzheimer’s type. J Basic Clinic Physiol Pharmacol, 26: 275-285.
63
Martino-Andrade AJ, Morais RN, Spercoski KM, Rossi SC, Vechi MF, Golin M, Lombardi NF, Greca CS, Dalsenter PR. 2010. Effects of Tribulus terrestris on endocrine sensitive organs in male and female Wistar rats. J Ethnopharmacol, 127: 165-170.
64
Matsunaga N, Imai S, Inokuchi Y, Shimazawa M, Yokota S, Araki Y, Hara H. 2009. Bilberry and its main constituents have neuroprotective effects against retinal neuronal damage in vitro and in vivo. Mol Nutr Food Res, 53: 869-877.
65
Mcmahon FG, Vargas R. 1993. Can garlic lower blood pressure? A pilot study. Pharmacotherapy: Hum Gene Ther Clin Dev, 13: 406-407.
66
Mcrae MP. 2006. A review of studies of garlic (Allium sativum) on serum lipids and blood pressure before and after 1994: does the amount of allicin released from garlic powder tablets play a role? J Chiropr Med, 4: 182-190.
67
Meunier MT, Villié F, Jonadet M, Bastide J, Bastide P. 1987. Inhibition of angiotensin I converting enzyme by flavanolic compounds: in vitro and in vivo studies. Planta med, 53: 12-15
68
Moosavi J. 2009. The place of avicenna in the history of medicine. Avicenna J Med Biotechnol, 1: 3-8.
69
Nyadjeu P, Dongmo A, Nguelefack TB, Kamanyi A. 2011. Antihypertensive and vasorelaxant effects of Cinnamomum zeylanicum stem bark aqueous extract in rats. J Complement Integr Med, 8: 1553-3840.
70
Nyadjeu P, Nguelefack-Mbuyo EP, Atsamo AD, Nguelefack TB, Dongmo AB, Kamanyi A. 2013. Acute and chronic antihypertensive effects of Cinnamomum zeylanicum stem bark methanol extract in L-NAME-induced hypertensive rats. BMC Complement Alternat Med, 13: 27.
71
Oboh G, Akinyemi AJ, Ademiluyi AO. 2013. Inhibitory effect of phenolic extract from garlic on angiotensin-1 converting enzyme and cisplatin induced lipid peroxidation-in vitro. Int J Biomed Sci, 9: 98-106.
72
Öztürk Y, Aydin S, Koşar M, Başer KHC. 1994. Endothelium-dependent and independent effects of garlic on rat aorta. J Ethnopharmacol, 44: 109-116.
73
Patnaik N. 1993. The garden of life: an introduction to the healing plants of India, New York: Doubleday 195p. ISBN.
74
Patten GS, Abeywardena MY, Bennett LE. 2016. Inhibition of angiotensin converting enzyme, angiotensin II receptor blocking, and blood pressure lowering bioactivity across plant families. Crit Rev Food Sci Nutr, 56: 181-214.
75
Persson IAL, Persson K, Andersson RG. 2009. Effect of Vaccinium myrtillus and its polyphenols on angiotensin-converting enzyme activity in human endothelial cells. J Agric Food Chem, 57: 4626-4629.
76
Phillips OA, Mathew KT, Oriowo MA. 2006. Antihypertensive and vasodilator effects of methanolic and aqueous extracts of Tribulus terrestris in rats. J Ethnopharmacol, 104: 351-355.
77
Pourghassem-Gargari B, Abedini S, Babaei H, Aliasgarzadeh A, Pourabdollahi P. 2011. Effect of supplementation with grape seed (Vitis vinifera) extract on antioxidant status and lipid peroxidation in patient with type diabetes. J Med Plant Res, 5: 2029-2034.
78
Puupponen-Pimiä R, Nohynek L, Ammann S, Oksman-Caldentey KM, Buchert J. 2008. Enzyme-assisted processing increases antimicrobial and antioxidant activity of bilberry. J Agric Food Chem, 56: 681-688.
79
Quiñones M, Guerrero L, Suarez M, Pons Z, Aleixandre A, Arola L, Muguerza B. 2013. Low-molecular procyanidin rich grape seed extract exerts antihypertensive effect in males spontaneously hypertensive rats. Food Res Int, 51: 587-595.
80
Ranasinghe P, Pigera S, Premakumara GS, Galappaththy P, Constantine GR, Katulanda P. 2013. Medicinal properties of ‘true’cinnamon (Cinnamomum zeylanicum): a systematic review. BMC Complement Alternat Med, 13: 275.
81
Ranjini H, Udupa PE, Kamath SU, Setty MM, Hadapad BS, Kamath A. 2016. An in vitro study of cinnamomum zeylanicum as natural inhibitor of angiotensin-converting enzyme (ace) on sheep (ovis aries) tissues. Asian J Pharm Clin Res, 9: 249-252.
82
Rastogi S, Pandey MM, Rawat A. 2016. Traditional herbs: a remedy for cardiovascular disorders. Phytomedicine. 15; 23: 1082-1089
83
Rathi B, Bodhankar S, Mohan V, Thakurdesai P. 2013. Ameliorative effects of a polyphenolic fraction of Cinnamomum zeylanicum L. Bark in animal models of inflammation and arthritis. Sci Pharm, 81: 567-89.
84
Ried K, Fakler P. 2014. Potential of garlic (Allium sativum) in lowering high blood pressure: mechanisms of action and clinical relevance. Integr Blood Press Control, 7: 71-82.
85
Ried K, Frank O, Stocks N. 2013. Aged garlic extract reduces blood pressure in hypertensives: a dose–response trial. Eur J Clin Nutr, 67: 64-70.
86
Ried K, Frank OR, Stocks NP. 2010. Aged garlic extract lowers blood pressure in patients with treated but uncontrolled hypertension: a randomised controlled trial. Maturitas, 67: 144-150.
87
Ried K, Travica N, Sali A. 2016. The effect of aged garlic extract on blood pressure and other cardiovascular risk factors in uncontrolled hypertensives: the age at heart trial. Integr Blood Press Control, 9: 9-21.
88
Rosenkranz B, Fasinu P, Bouic P. 2012. An overview of the evidence and mechanisms of herb–drug interactions. Front Pharmacol, 30: 69.
89
Sadhu SK, Khan MS, Ohtsuki T, Ishibashi M. 2007. Secoiridoid components from Jasminum grandiflorum. Phytochemistry, 68: 1718-1721.
90
Saleem M, Bhatti HN, Jilani MI, Hanif MA. 2015. Bioanalytical evaluation of Cinnamomum zeylanicum essential oil. Nat prodres, 29: 1857-1859.
91
Sandeep PP. 2009. Jasminum grandiflorum Linn (Chameli): ethnobotany, phytochemistry and pharmacology–a review. Pharma-cologyonline, 2: 586-595.
92
Sendl A, Elbl G, Steinke B, Redl K, Breu W, Wagner H. 1992. Comparative pharmacological investigations of Allium ursinum and Allium sativum. Planta med, 58: 1-7.
93
Shakeri A, Sahebkar A, Javadi B. 2016. Melissa officinalis L.–A review of its traditional uses, phytochemistry and pharmacology. J Ethnopharmacol, 188: 204-228.
94
Sharifi AM, Darabi R, Akbarloo N. 2003a. Investigation of antihypertensive mechanism of garlic in 2K1C hypertensive rat. J Ethnopharmacol, 86: 219-224.
95
Sharifi AM, Darabi R, Akbarloo N. 2003b. Study of antihypertensive mechanism of Tribulus terrestris in 2K1C hypertensive rats: role of tissue ACE activity. Life Sci, 73: 2963-2971.
96
Shouk R, Abdou A, Shetty K, Sarkar D, Eid AH. 2014. Mechanisms underlying the antihypertensive effects of garlic bioactives. Nutr Res, 34: 106-115.
97
Sobhani Z, Reza Nami S, Ahmad Emami S, Sahebkar A, Javadi B. 2017. Medicinal plants targeting cardiovascular diseases in view of Avicenna.Curr Pharm Des, 23: 2428-2443.
98
Somanadhan B, Smitt UW, George V, Pushpangadan P, Rajasekharan S, Duus JØ, Nyman U, Olsen CE, Jaroszewski JW. 1998. Angiotensin converting enzyme (ACE) inhibitors from Jasminum azoricum and Jasminum grandiflorum. Planta med, 64: 246-250.
99
Somanadhan B, Varughese G, Palpu P, Sreedharan R, Gudiksen L, Smitt UW, Nyman U. 1999. An ethnopharmacological survey for potential angiotensin converting enzyme inhibitors from Indian medicinal plants. J Ethnopharmacol, 65: 103-112.
100
Song J, Li Y, Ge J, Duan Y, Sze SCW, Tong Y, Shaw PC, Ng TB, Tsui KC, Zhuo Y. 2010. Protective effect of bilberry (Vaccinium myrtillus L.) extracts on cultured human corneal limbal epithelial cells (HCLEC). Phytother Res, 24: 520-524.
101
Sultana S, Khan A, Alhazmi MMSHA. 2016. Cough suppressant herbal drugs: a review. Int J Pharm Sci Invent. 5:15-28.
102
Terral J.-F, Tabard E, Bouby L, Ivorra S, Pastor T, Figueiral I, Picq S, Chevance J.-B, Jung C, Fabre L. 2010. Evolution and history of grapevine (Vitis vinifera) under domestication: new morphometric perspectives to understand seed domestication syndrome and reveal origins of ancient European cultivars. Ann Bot, 105: 443-455.
103
Tuncer MA, Yaymaci B, Sati L, Cayli S, Acar G, Altug T, Demir, R. 2009. Influence of Tribulus terrestris extract on lipid profile and endothelial structure in developing atherosclerotic lesions in the aorta of rabbits on a high-cholesterol diet. Acta histochem, 111: 488-500.
104
Ukani M, Nanavati D, Mehta N. 1997. A review on the ayurvedic herb tribulus terrestris L. Anc Sci Life, 17: 144.
105
Ulbricht C, Basch E, Basch S, Bent S, Boon, Burke D, Costa D, Falkson C, Giese N, Goble M. 2009. An evidence-based systematic review of bilberry (Vaccinium myrtillus) by the natural standard research collaboration. J Diet Suppl, 6: 162-200.
106
Venkataiah G, Kumar CP, Rejeena D. 2013. Effect of methanolic extract of Jasminum grandiflorum linn leaves on gentamicin induced nephrotoxicity in rats. Indo Am J Pharm Res, 3: 7462-7467.
107
Wiseman W, Egan JM, Slemmer JE, Shaughnessy KS, Ballem K, Gottschall-Pass KT, Sweeney MI. 2010. Feeding blueberry diets inhibits angiotensin II-converting enzyme (ACE) activity in spontaneously hypertensive stroke-prone rats. Can J Physiol Pharmacol, 89: 67-71.
108
Xiong X, Wang P, Li S, Li X, Zhang Y, Wang J. 2015. Garlic for hypertension: a systematic review and meta-analysis of randomized controlled trials. Phytomedicine, 22: 352-361.
109
Yilancioglu K, Cetiner S. 2013. Rediscovery of historical Vitis vinifera varieties from the South Anatolia region by using amplified fragment length polymorphism and simple sequence repeat DNA fingerprinting methods. Genome, 56: 295-302.
110
Yüce A, Türk G, Çeribaşı S, Güvenç M, Çiftçi M, Sönmez M, Özer Kaya Ş, Cay M, Aksakal, M. 2014. Effectiveness of cinnamon (Cinnamomum zeylanicum) bark oil in the prevention of carbon tetrachloride‐induced damages on the male reproductive system. Andrologia, 46: 263-272.
111
Zhou T, Zhang T, Liu W, Zhao G. 2011. Physicochemical characteristics and functional properties of grape (Vitis vinifera L.) seeds protein. Int J Food Sci Technol, 46: 635-641.
112
ORIGINAL_ARTICLE
The effect of a natural vaginal product based on honey on the success of intrauterine insemination (IUI) in infertility treatment
Objective: Due to high prevalence of infertility and increasing tendency towards complementary medicine, this study was conducted to investigate the effect of a vaginal natural product based on honey and 1% extract of Myristica fragrans on the extent of success of intrauterine insemination (IUI). Materials and Methods: This non-randomized clinical trial study with a historic control group, was performed on infertile women. In this trial, 159 patients were assigned to the intervention group, and 288 patients were recruited to the control group. All the participants received clomiphene or letrozole from the third up to seventh day of menstruation, and on days 6, 7, and 8, they received human menopausal gonadotrophin (HMG) injections. IUI was performed 36 hours after human chorionic gonadotrophin (HCG) injection. In the intervention group, a natural vaginal product was used besides the above treatments, from menstruation day 7 until the day before performing IUI. Sixteen days after IUI, serum beta HCG was measured to investigate chemical pregnancy, and six weeks following IUI, vaginal sonography was performed to investigate clinical pregnancy. Results: Analysis showed that the pregnancy rate was higher in the group that receiving the natural product compared to the control group. Chemical pregnancy rate was 18.1% vs. 15.4%, and clinical pregnancy rate was 15.2% vs. 13.8% for intervention and control groups, respectively; but, this difference was not significant. Conclusion: It seems that the use of this vaginal product for a longer period of time and across several menses cycles before IUI, may produce more positive results. Further studies, however, are needed to be done.
https://ajp.mums.ac.ir/article_12588_55d34ba01381fa2b57cb6521993571a5.pdf
2019-07-01
310
321
10.22038/ajp.2019.12588
Infertility
Honey
Myristica fragrans
Mace
Intrauterine Insemination (IUI)
Maryam
Kavousi
kavousim921@mums.ac.ir
1
Department of Persian Medicine, School of Persian and Complementary Medicine, Mashhad University of Medical Sciences, Mashhad, Iran
AUTHOR
Nayereh
Khadem
khademn@mums.ac.ir
2
Department of Obstetrics and Gynecology, Faculty of Medicine, Mashhad University of Medical Sciences, Mashhad, Iran
AUTHOR
Mona
Najaf Najafi
najafnm@mums.ac.ir
3
Clinical Research Unit, Mashhad University of Medical Sciences, Mashhad, Iran
AUTHOR
Roshanak
Mokaberinejad
rmokaberi@gmail.com
4
Department of Traditional Medicine, School of Traditional Medicine, Shahid Beheshti University of Medical Sciences, Tehran, Iran.
AUTHOR
Zohre
Feyzabadi
feyzabadi_8823@yahoo.com
5
Department of Persian Medicine, School of Persian and Complementary Medicine, Mashhad University of Medical Sciences, Mashhad, Iran.
LEAD_AUTHOR
Roshanak
Salari
salarir@mums.ac.ir
6
Department of pharmaceutical sciences in Persian Medicine, School of Persian and Complementary Medicine, Mashhad University of Medical Sciences, Mashhad, Iran.
AUTHOR
Abdelhafiz AT, Muhamad JA. 2008. Midcycle pericoital intravaginal bee honey and royal jelly for male factor infertility. Int J Gynaecol Obstet, 101: 146-149.
1
Abdelkader AM, Yeh J. 2009. The potential use of intrauterine insemination as a basic option for infertility: a review for technology-limited medical settings. Obstet Gynecol Int, 2009: 584837.
2
Akhondi MM, Kamali K, Ranjbar F, Shirzad M, Shafeghati S, Behjati Ardakani Z, Goodjani A, Parsaeian M. 2013. Prevalence of Primary Infertility in Iran in 2010. Iran J Public Health, 42: 1398-1404.
3
Allahbadia, GN. 2017. Intrauterine Insemination: Fundamentals Revisited. J Obstet Gynaecol India, 67: 385-392.
4
Azamkhan, M. 2008. Exir Azam. Tehran, Institute of Medical History, pp. 704-753
5
Brudzynski K, Sjaarda C. 2015. Honey glycoproteins containing antimicrobial peptides, Jelleins of the Major Royal Jelly Protein 1, are responsible for the cell wall lytic and bactericidal activities of honey. PLoS One, 10: e0120238.
6
Cabry-Goubet R, Scheffler F, Belhadri-Mansouri N, Belloc S, Lourdel E, Devaux A, Chahine H, De Mouzon J, Copin H. 2017. Effect of gonadotropin types and indications on homologous intrauterine insemination success: A study from 1251 cycles and a review of the literature. Biomed Res Int, 2017: 3512784.
7
Campisciano G, Florian F, D'Eustacchio A, Stankovic D, Ricci G, De Seta F. 2017. Subclinical alteration of the cervical-vaginal microbiome in women with idiopathic infertility. J Cell Physiol, 232: 1681-1688.
8
Checker R, Chatterjee S, Sharma D, Gupta S, Variyar P, Sharma A. 2008. Immunomodulatory and radioprotective effects of lignans derived from fresh nutmeg mace (Myristica fragrans) in mammalian splenocytes. Int Imp, 8: 661-669.
9
Chiu S, Wang T, Belski M, Abourashed EA. 2016. HPLC-guided isolation, purification and characterization of phenylpropanoid and phenolic constituents of nutmeg kernel (Myristica fragrans). Nat Prod Commun, 11: 483-488.
10
El-Sheshtawy RI, El-Badry DA, Gamal A, El-Nattat WS, Almaaty AMA. 2016. Natural honey as a cryoprotectant to improve Arab stallion post-thawing sperm parameters. Asian Pac J Reprod, 5: 331-334.
11
Eskew AM, Bedrick BS, Hardi A, Stoll CRT, Colditz GA, Tuuli MG. 2019. Letrozole compared with clomiphene citrate for unexplained infertility: A systematic review and meta-analysis. Obstet Gynecol, 3: 437-444
12
Fakhrildin MB, Alsaadi RA. 2014. Honey Supplementation to semen-freezing medium improveshuman sperm parameters post-thawing. J Family Reprod Health, 8: 27-31.
13
Ghahiri A, Mogharehabed N, Mamourian M. 2016. Letrozole as the first-line treatment of infertile women with poly cystic ovarian syndrome (PCOS) compared with clomiphene citrate: A clinical trial. Adv Biomed Res, 5: 6.
14
Grembecka M, Szefer P. 2013. Evaluation of honeys and bee products quality based on their mineral composition using multivariate techniques. Environ Monit Assess, 185: 4033-4047.
15
Grossi E, Castiglioni S, Moscheni C, Antonazzo P, Cetin I, Savasi VM. 2017. Serum magnesium and calcium levels in infertile women during a cycle of reproductive assistance. Magnes Res, 30: 35-41.
16
Hosseini A, Mollazadeh H, Amiri MS, Sadeghnia HR, Ghorbani 2017. Effects of a standardized extract of Rheum turkestanicum Janischew root on diabetic changes in the kidney, liver and heart of streptozotocin-induced diabetic rats. Biomed Pharmacother, 86: 605-611.
17
Irani M, Chow S, Keating D, Elder S, Rosenwaks Z, Palermo G. 2018. Optimizing the first-line fertility treatment. Gynecol Endocrinol, 20: 1-5.
18
Kazemijaliseh H, Ramezani Tehrani F, Behboudi-Gandevani S, Hosseinpanah F, Khalili D, Azizi F. 2015. The Prevalence and Causes of Primary Infertility in Iran: A Population-Based Study. Glob J Health Sci, 7: 226-232.
19
Lavaf M, Simbar M, Mojab F, Alavi Majd H, Samimi M. 2017. Comparison of honey and phenytoin (PHT) cream effects on intensity of pain and episiotomy wound healing in nulliparous women. J Complement Integr Med, 15: 28981445.
20
Mojahedi M, Naseri M, Majdzadeh R, Keshavarz M, Ebadini M, Nazem E. 2014. Reliability and validity assessment of mizaj questionnaire: A novel self-report scale in iranian traditional medicine. Iran Red Crescent Med J, 16: e15924.
21
Monraisin O, Chansel-Debordeaux L, Chiron A, Floret S, Cens S, Bourrinet S. 2016. Evaluation of intrauterine insemination practices: a 1-year prospective study in seven French assisted reproduction technology centers. Fertil Steril, 105: 1589-1593.
22
Moreno I, Codoner FM, Vilella F, Valbuena D, Martinez-Blanch JF, Jimenez-Almazan J. 2016. Evidence that the endometrial microbiota has an effect on implantation success or failure. Am J Obstet Gynecol, 215: 684-703.
23
Moreno I, Franasiak JM. 2017. Endometrial microbiota-new player in town. Fertil Steril, 108: 32-39.
24
Pharmacopeia U. 2004. Bacterial endotoxin test. USP32/NF27: United States Pharmacopeia and National Formulary, 2004: 93-96.
25
Ranjbar AM, Sadeghpour O, Khanavi M, Shams Ardekani MR, Moloudian H, Hajimahmoodi M. 2015. Effects of the deslagging process on some physicochemical parameters of honey. Iran J Pharm Res, 14: 657-662.
26
Salim R, Ben-Shlomo I, Colodner R, Keness Y, Shalev E. 2002. Bacterial colonization of the uterine cervix and success rate in assisted reproduction: results of a prospective survey. Hum Reprod, 17: 337-340.
27
Seifi Nader Goli Z, Nahidi F, Safaeean AR, Javadzadeh Y, Eteraf Oskouee T. 2016. The effect of honey vaginal gel and clotrimazole vaginal cream on vaginal normal flour in women with vaginitis candidiasis. IJOGI, 19: 32-39.
28
Shahin AY, Ismail AM, Zahran KM, Makhlouf AM. 2008. Adding phytoestrogens to clomiphene induction in unexplained infertility patients--a randomized trial. Reprod Biomed Online 16: 580-588.
29
Shahin AY, Mohammed SA. 2014. Adding the phytoestrogen Cimicifugae Racemosae to clomiphene induction cycles with timed intercourse in polycystic ovary syndrome improves cycle outcomes and pregnancy rates - A randomized trial. Gynecol Endocrinol, 30: 505-510.
30
Sohrabvand F, Nazem E, Tansaz M, Keshavarz M, Hashem Dabaghian F, Nikbakht Nasrabady A, Ghooshehghir A, Bioos S, Mokaberinejad R. 2014. Investigation of the personal and uterine humor in infertile women referred to Vali-E-As hospital of Tehran, Iran in 2012. IJOGI, 17: 10-19.
31
Tajuddin, Ahmad S, Latif A, Qasmi IA. 2003. Aphrodisiac activity of 50% ethanolic extracts of Myristica fragrans Houtt. (nutmeg) and Syzygium aromaticum (L) Merr. & Perry. (clove) in male mice: a comparative study. BMC Complement Altern Med, 3: 6.
32
Tajuddin, Ahmad S, Latif A, Qasmi IA, Amin KM. 2005. An experimental study of sexual function improving effect of Myristica fragrans Houtt. (nutmeg). BMC Complement Altern Med, 5: 16.
33
USDA N. 2007. The PLANTS Database (http://plants. usda. gov, 6 August 2007). National Plant Data Center. Baton Rouge, 2007: 70874-74490.
34
Veltman-Verhulst SM, Hughes E, Ayeleke RO, Cohlen BJ. 2016. Intra-uterine insemination for unexplained subfertility. Cochrane Database Syst Rev, 2: CD001838.
35
Zaid SS, Othman S, Kassim NM. 2014. Potential protective effect of Tualang honey on BPA-induced ovarian toxicity in prepubertal rat. BMC Complement Altern Med, 14: 509.
36
Zaid SS, Sulaiman SA, Sirajudeen KN, Othman NH. 2010. The effects of Tualang honey on female reproductive organs, tibia bone and hormonal profile in ovariectomised rats--animal model for menopause. BMC Complement Altern Med, 10: 82.
37
Zhang C, Qi X, Shi Y, Sun Y, Li S, Gao X. 2012. Estimation of trace elements in mace (Myristica fragrans Houtt) and their effect on uterine cervix cancer induced by methylcholanthrene. Biol Trace Elem Res, 149: 431-434.
38
ORIGINAL_ARTICLE
The effect of saffron (Crocus sativus L.) supplementation on blood pressure, and renal and liver function in patients with type 2 diabetes mellitus: A double-blinded, randomized clinical trial
Objective: Microalbuminuria and hypertension are the risk factors for diabetic nephropathy, and increased levels of liver enzymes are prevalent among diabetic patients. The aim of this research was to examine the effects of Crocus sativus supplementation on nephropathy indices, liver enzymes, and blood pressure in patients with type 2 diabetes (T2D). Materials and Methods: This placebo-controlled, randomized clinical trial was performed among 80 T2D patients. Subjects were randomly assigned to either Crocus sativus (n = 40) or placebo (n = 40) groups and treated with C. sativus and or placebo for 12 weeks, respectively. Alkaline phosphatase (ALP), aspartate aminotransferase (AST), alanine aminotransferase (ALT), serum urea, creatinine, 24-hr urine albumin, systolic blood pressure (SBP), diastolic blood pressure (DBP), physical activity, and dietary intakes were measured and blood samples were taken at baseline and after the 12‑week intervention to assess the differences between the two groups. Results: C. sativus supplementation compared with the placebo resulted in a significant reduction of SBP (P<0.005). However, changes in other indices including liver enzymes, serum creatinine, serum urea, and 24-hr urine albumin, and DBP were not significantly different between the two groups (p>0.05). Also, no significant changes in dietary intakes and physical activity were seen between the two groups. Conclusion: This report shows that daily supplementation with 100 mg C. sativus powder improved SBP. However, it did not considerably improve DBP, nephropathy indices and liver functions in T2D patients after 12 weeks of administration.
https://ajp.mums.ac.ir/article_12785_ee1c5af664edd1fe718cfbe88f40e5f1.pdf
2019-07-01
322
333
10.22038/ajp.2019.12785
Crocus sativus
Diabetes mellitus type 2
Herbal Medicine
blood pressure
Nephropathy
Fatemeh
Ebrahimi
febrahimi4jan@gmail.com
1
Skull Base Research Center, Loghman Hakim Hospital, Shahid Beheshti University of Medical Sciences, Tehran, Iran
AUTHOR
Naheed
Aryaeian
aryaeian.n@iums.ac.ir
2
Department of Nutrition, School of Public Health, Iran University of Medical Sciences, Tehran, Iran
LEAD_AUTHOR
Naseh
Pahlavani
pahlavanin951@mums.ac.ir
3
Department of Nutrition, Faculty of Medicine, Mashhad University of Medical Sciences, Mashhad, Iran
AUTHOR
Davood
Abbasi
abbasid@yahoo.com
4
Faculty of Medicine, Iran University of Medical Sciences, Tehran, Iran
AUTHOR
Agha Fatemeh
Hosseini
hossenif@iums.ac.ir
5
Department of Biostatistics, School of Public Health, Iran University of Medical Sciences, Tehran, Iran
AUTHOR
Soudabeh
Fallah
fallah@iums.ac.ir
6
Department of Clinical Biochemistry, Faculty of Medicine, Iran University of Medical Sciences, Tehran, Iran
AUTHOR
Nariman
Moradi
moradinariman@yahoo.com
7
Department of Clinical Biochemistry, Faculty of Medicine, Kurdistan University of Medical Sciences, Sanandaj, Iran
AUTHOR
Iraj
Heydari
heydari.i@iums.ac.ir
8
Department of Endocrinology, School of Medicine, Iran University of Medical Sciences, Tehran, Iran
AUTHOR
Ayatollahi H, Javan AO, Khajedaluee M, Shahroodian M, Hosseinzadeh H. 2014. Effect of Crocus sativus L. (saffron) on coagulation and anticoagulation systems in healthy volunteers. Phytother Res, 28: 539-543.
1
Azadmehr A, Ziaee A, Ghanei L, Huseini HF, Hajiaghaee R, Tavakoli-far B, Kordafshari G. 2014. A randomized clinical trial study: anti-oxidant, anti-hyperglycemic and anti-hyperlipidemic effects of olibanum gum in type 2 diabetic patients. Iran J Pharm Res, 13: 1003-1009.
2
Beckman JA, Creager MA, Libby P. 2002. Diabetes and atherosclerosis: epidemiology, pathophysiology, and management. Jama, 287:2570-2581.
3
Broadhead GK, Grigg JR, McCluskey P, Hong T, Schlub TE, Chang AA. 2019. Saffron therapy for the treatment of mild/moderate age-related macular degeneration: a randomised clinical trial. Graefes Arch Clin Exp Ophthalmol, 257: 31-40.
4
Caramori ML, Kim YH, Chunmei F, Alfred J, Rich SS, Miller ME, Mauer M. 2002. Cellular basis of diabetic nephropathy: 1. Study design and renal structural-functional relationships in patients with long-standing type 1 diabetes. Diabetes, 51: 506-513.
5
Darko D, Dornhorst A, Kelly FJ, Ritter JM, Chowienczyk PJ. 2002. Lack of effect of oral vitamin C on blood pressure, oxidative stress and endothelial function in Type II diabetes. Clin Sci, 103: 339-344.
6
De Vriese AS, Verbeuren TJ, Van de V, Johan L, Norbert H, Vanhoutte PM. 2000. Endothelial dysfunction in diabetes. Br J Pharmacol, 130: 963-974.
7
Elshater AE, Salman Muhammad MA, Moussa Mahrous MA. 2009. Effect of ginger extract consumption on levels of blood glucose, lipid profile and kidney functions in alloxan induced-diabetic rats. Egypt Acad J Biosci, 2: 153-162.
8
Esteghamati A, Gouya MM, Abbasi M, Delavari A, Alikhani S, Alaedini F, Gregg EW. 2008. Prevalence of diabetes and impaired fasting glucose in the adult population of Iran. Diabetes care, 31: 96-98.
9
Fatehi M, Rashidabady T, Fatehi-Hassanabad Z. 2003. Effects of Crocus sativus petals’ extract on rat blood pressure and on responses induced by electrical field stimulation in the rat isolated vas deferens and guinea-pig ileum. J Ethnopharmacol, 84: 199-203.
10
Ghaffarpour M, Houshiar-Rad A, Kianfar H. 1999. The manual for household measures, cooking yields factors and edible portion of foods. Tehran: Nashre Olume Keshavarzy, 7: 213.
11
Hanley AJG, Wagenknecht LE, Festa A, D'agostino RB, Haffner SM. 2007. Alanine aminotransferase and directly measured insulin sensitivity in a multiethnic cohort. Diabetes care, 30: 1819-1827.
12
Hofman DL, Van Buul VJ, Brouns Fred JPH. 2016. Nutrition, health, and regulatory aspects of digestible maltodextrins. Crit Rev Food Sci Nutr, 56: 2091-2100.
13
Huang HY, Chen YC, Wang PC, Tsai MA, Yeh SC, Liang HJ, Chen SC. 2014. Efficacy of a formalin-inactivated vaccine against Streptococcus iniae infection in the farmed grouper Epinephelus coioides by intraperitoneal immunization. Vaccine, 32, 7014-7020.
14
Imenshahidi M, Hosseinzadeh H, Javadpour Y. 2010. Hypotensive effect of aqueous saffron extract (Crocus sativus L.) and its constituents, safranal and crocin, in normotensive and hypertensive rats. Phytother Res, 24: 990-994.
15
Imenshahidi M, Razavi BM, Faal A, Gholampoor A, Mousavi SM, Hosseinzadeh H. 2014. Effects of chronic crocin treatment on desoxycorticosterone acetate (doca)-salt hypertensive rats. Iran J Basic Med Sci, 17: 9-13.
16
Jelodar G, Javid Z, Sahraian A, Jelodar S. 2018. Saffron improved depression and reduced homocysteine level in patients with major depression: A Randomized, double-blind study. Avicenna J Phytomed, 8: 43-50.
17
Jyothirmayi B, Kumar JS. 2011. Insulin resistance and alanine amino transaminase (ALT) levels in first degree relatives of type 2 diabetes mellitus. Diabetes & Metab-Res, 5: 143-147.
18
Kaur R, Khanna N. 2012. Pathophysiology and risk factors related to hypertension and its cure using herbal drugs. Spatula DD, 2: 245-256.
19
Larejani B, Zahedi F. 2001. Epidemiology of diabetes mellitus in Iran. IJDLD, 1: 1-8.
20
Lavie CJ, Osman AF, Milani RV, Mehra MR. 2003. Body composition and prognosis in chronic systolic heart failure: the obesity paradox. Am J Cardiol, 91: 891-894.
21
Li Y, Tran VH, Duke CC, Roufogalis BD. 2012. Gingerols of Zingiber officinale enhance glucose uptake by increasing cell surface GLUT4 in cultured L6 myotubes. Planta medica, 78: 1549-1555.
22
Mashmoul M, Azlan A, Mohtarrudin N, Yusof BNM, Khaza’ai H, Khoo HE, Boroushaki MT. 2016. Protective effects of saffron extract and crocin supplementation on fatty liver tissue of high-fat diet-induced obese rats. BMC Complement Altern Med, 16: 401-407.
23
Milajerdi A, Jazayeri S, Bitarafan V, Hashemzadeh N, Shirzadi E, Derakhshan Z, Akhondzadeh S. 2017. The effect of saffron (Crocus sativus L.) hydro-alcoholic extract on liver and renal functions in type 2 diabetic patients: A double-blinded randomized and placebo control trial. J Nutr Intermed Metab, 9: 6-11.
24
Mirfeizi M, Mehdizadeh TZ, Mirfeizi SZ, Asghari Jafarabadi M, Rezvani HR, Afzali M. 2016. Controlling type 2 diabetes mellitus with herbal medicines: A triple‐blind randomized clinical trial of efficacy and safety. J Diabetes, 8: 647-656.
25
Moazen-Zadeh E, Abbasi SH, Safi-Aghdam H, Shahmansouri N, Arjmandi-Beglar A, Hajhosseinn Talasaz A, Akhondzadeh S. 2018. Effects of saffron on cognition, anxiety, and depression in patients undergoing coronary artery bypass grafting: a randomized double-blind placebo-controlled trial. J Altern Complement Med, 24: 361-368.
26
Modaghegh MH, Shahabian M, Esmaeili HA, Rajbai O, Hosseinzadeh H. 2008. Safety evaluation of saffron (Crocus sativus) tablets in healthy volunteers. J Phymed, 15: 1032-1037.
27
Mohammadifard N, Sajjadi F, Maghroun M, Alikhasi H, Nilforoushzadeh F, Sarrafzadegan N. 2015. Validation of a simplified food frequency questionnaire for the assessment of dietary habits in Iranian adults: Isfahan Healthy Heart Program, Iran. ARYA atheroscler, 11: 139.
28
Moradabadi L, Kouhsari SM, Sani MF. 2013. Hypoglycemic effects of three medicinal plants in experimental diabetes: inhibition of rat intestinal α-glucosidase and enhanced pancreatic insulin and cardiac glut-4 mrnas expression. Iran J Pharm Res, 12: 387-397.
29
Naghizadeh B, Mansouri SM, Mashhadian NV. 2010. Crocin attenuates cisplatin-induced renal oxidative stress in rats. Food Chem Toxicol, 48: 2650-2655.
30
Omidi A, Riahinia N, Montazer Torbati MB. Behdani MA. 2014. Hepatoprotective effect of Crocus sativus (saffron) petals extract against acetaminophen toxicity in male Wistar rats. Avicenna J Phytomed, 4, 330-336.
31
Parving HH, Lehnert H, Bröchner-Mortensen J, Gomis R, Andersen S, Arner P. 2001. The effect of irbesartan on the development of diabetic nephropathy in patients with type 2 diabetes. N Engl J Med, 345: 870-878.
32
Pitsikas N, Boultadakis A, Georgiadou G, Tarantilis PA, Sakellaridis N. 2008. Effects of the active constituents of Crocus sativus L., crocins, in an animal model of anxiety. J Phymed, 15: 1135-1139.
33
Schulz KF, Altman DG, Moher D. 2010. CONSORT 2010 statement: updated guidelines for reporting parallel group randomised trials. BMC Med, 8: 18.
34
Shanmugam KR, Ramakrishana Ch, Mallikarjuna K, Reddy KS. 2009. The impact of ginger on kidney carbohydrate metabolic profiles in STZ induced diabetic rats. Asian J Exp Sci, 23: 127-134.
35
Shemshian M, Mousavi SH, Norouzy A, Kermani T, Moghiman T, Sadeghi A, Ferns GA. 2014. Saffron in metabolic syndrome: its effects on antibody titers to heat-shock proteins 27, 60, 65 and 70. J Complement Integr Med, 11: 43-49.
36
Tajadadi-Ebrahimi M, Bahmani F, Shakeri H, Hadaegh H, Hijijafari M, Abedi F, Asemi Z. 2014. Effects of daily consumption of synbiotic bread on insulin metabolism and serum high-sensitivity C-reactive protein among diabetic patients: a double-blind, randomized, controlled clinical trial. Ann Nutr Metab, 65, 34-41.
37
Tavafi M, Ahmadvand H, Khalatbari A, Tamjidipoor A. 2011. Rosmarinic acid ameliorates diabetic nephropathy in uninephrectomized diabetic rats. IJBMS, 14: 275-283.
38
Vasheghani-Farahani A, Tahmasbi M, Asheri, Hossein A, Haleh Nedjat S, Kordi R. 2011. The Persian, last 7-day, long form of the International Physical Activity Questionnaire: translation and validation study. Asian J Sports Med, 2: 106-116.
39
Whiting DR, Guariguata L, Weil C, Shaw J. 2011. IDF diabetes atlas: global estimates of the prevalence of diabetes for 2011 and 2030. Diabetes Res Clin Pract, 94: 311-321.
40
Xi L, Qian Z, Xu G, Zheng S, Sun S, Wen N, Zhang Y 2007. Beneficial impact of crocetin, a carotenoid from saffron, on insulin sensitivity in fructose-fed rats. J Nutr Biochem, 18: 64-72.
41
Xiang M, Qian ZY, Zhou CH, Liu J, Li WN. 2006. Crocetin inhibits leukocyte adherence to vascular endothelial cells induced by AGEs. J Ethnopharmacol, 107: 25-31.
42
Zheng S, Qian Z, Tang F, Sheng L. 2005. Suppression of vascular cell adhesion molecule-1 expression by crocetin contributes to attenuation of atherosclerosis in hypercholesterolemic rabbits. Biochem Pharmacol, 70: 1192-1199.
43
ORIGINAL_ARTICLE
Cytotoxic effects of auraptene against a human malignant glioblastoma cell line
Objective: Glioblastoma multiforme (GBM) is the deadliest type of primary brain tumors, and the survival of patients is estimated to be only about one year. This study, for the first time, investigated the cytotoxic effects of auraptene on U87 GBM cell line. Materials and Methods: The cellular toxicity was measured by the MTT assay following 24 and 48-hr treatment with different concentrations of auraptene (0-400μg/ml). Apoptosis was evaluated by sub-G1 peak in cell cycle analysis of propidium-iodide- stained nuclei. Moreover, to determine the Bax, Bcl-2, MCP-1, NF-κB, IL-1β, and p53 genes expression, we used real-time polymerase chain reaction (RT-PCR). Results: The results revealed that auraptene reduced the viability of U87 cells concentration- and time-dependently with IC50 values of 108.9 and 79.17μg/ml obtained for 24 and 48-hr treatments, respectively. Also, sub-G1 population was significantly increased following 24 (p real-time RT-PCR showed an up-regulation in Bax, NF-κB, IL-1β, and p53 but a down-regulation in MCP-1 and Bcl-2 genes expression. Conclusion: This study showed that auraptene triggered apoptosis probably through Bax/Bcl-2 regulation, blocked cell cycle progression and inhibited proliferation in U87 GBM cells. Taken together, auraptene can be utilized as an effective natural medicine against GBM, after complementary studies.
https://ajp.mums.ac.ir/article_12384_d147a2d0ad870da6d0d193b6a5b199e4.pdf
2019-07-01
334
346
10.22038/ajp.2019.12384
Brain tumors
Glioblastoma multiforme
Auraptene
Cytotoxicity
Apoptosis
Amir R.
Afshari
afshariar921@mums.ac.ir
1
Department of Pharmacology, Faculty of Medicine, Mashhad University of Medical Sciences, Mashhad, Iran
AUTHOR
Mostafa
Karimi Roshan
karimirm941@mums.ac.ir
2
Department of Clinical Biochemistry, Faculty of Medicine, Mashhad University of Medical Sciences, Mashhad, Iran
AUTHOR
Mohammad
Soukhtanloo
soukhtanloom@mums.ac.ir
3
Department of Clinical Biochemistry, Faculty of Medicine, Mashhad University of Medical Sciences, Mashhad, Iran
AUTHOR
Ahmad
Ghorbani
ghorbania@mums.ac.ir
4
Pharmacological Research Center of Medicinal Plants, Mashhad University of Medical Sciences, Mashhad, Iran
AUTHOR
Farzad
Rahmani
rahmanif@mums.ac.ir
5
Department of Clinical Biochemistry, Faculty of Medicine, Mashhad University of Medical Sciences, Mashhad, Iran
AUTHOR
Mohammad
Jalili-nik
jalilinm951@mums.ac.ir
6
Department of Clinical Biochemistry, Faculty of Medicine, Mashhad University of Medical Sciences, Mashhad, Iran
AUTHOR
Mohammad Mahdi
Vahedi
vahedimm901@mums.ac.ir
7
Health Promotion Research Center, Zahedan University of Medical Sciences, Zahedan, Iran
AUTHOR
Azar
Hoseini
8
Pharmacological Research Center of Medicinal Plants, Mashhad University of Medical Sciences, Mashhad, Iran
AUTHOR
Hamid R.
Sadeghnia
9
Department of Pharmacology, Faculty of Medicine, Mashhad University of Medical Sciences, Mashhad, Iran
AUTHOR
Hamid
Mollazadeh
mollazadeh.h@nkums.ac.ir
10
Department of Physiology and Pharmacology, Faculty of Medicine, North Khorasan University of Medical Sciences, Bojnurd, Iran
AUTHOR
Seyed Hadi
Mousavi
mousavih@mums.ac.ir
11
Medical Toxicology Research Center, Mashhad University of Medical Sciences, Mashhad, Iran
LEAD_AUTHOR
Afshari AR, Roshan MK, Soukhtanloo M, Askari VR, Mollazadeh H, Nik MJ, Yazdi AAJ, Kia FA,Mousavi SH. 2018. Investigation of cytotoxic and apoptogenic effects of terminalia chebula hydro-alcoholic extract on glioblastoma cell line. Shefaye Khatam, 5:14-23.
1
Afshari AR, Sadeghnia HR, Mollazadeh H. 2016. A review on potential mechanisms of terminalia chebula in alzheimer's disease. Adv Pharmacol Sci, 2016:8964849.
2
Asadbeigi M, Mohammadi T, Rafieian-Kopaei M, Saki K, Bahmani M, Delfan M. 2014. Traditional effects of medicinal plants in the treatment of respiratory diseases and disorders: An ethnobotanical study in the urmia. Asian Pac J Trop Med, 7S1:S364-368.
3
Awad A, Karsy M, Sanai N, Spetzler R, Zhang Y, Xu YZ, Mahan MA. 2017. Impact of removed tumor volume and location on patient outcome in glioblastoma. J Neurooncol, 135:161-171.
4
Aylon Y, Oren M. 2017. Tumor suppression by p53: Bring in the hippo! Cancer Cell, 32:397-399.
5
Boroushaki MT, Mollazadeh H, Afshari AR. 2016. Pomegranate seed oil: A comprehensive review on its therapeutic effects. Int J Pharm Sci Res, 7:430-442.
6
Bukhari SI, Manzoor M, Dhar MK. 2018. A comprehensive review of the pharmacological potential of crocus sativus and its bioactive apocarotenoids. Biomed Pharmacother, 98:733-745.
7
Cerrato JA, Khan T, Koul D, Lang FF, Conrad CA, Yung WK, Liu TJ. 2004. Differential activation of the fas/cd95 pathway by ad-p53 in human gliomas. Int J Oncol, 24:409-417.
8
Desbaillets I, Tada M, Detribolet N, Diserens AC, Hamou MF,Van Meir EG. 1994. Human astrocytomas and glioblastomas express monocyte chemoattractant protein-1 (mcp-1) in-vivo and in-vitro. Int J Cancer, 58:240-247.
9
Dolcet X, Llobet D, Pallares J,Matias-Guiu X. 2005. Nf-kb in development and progression of human cancer. Virchows Arch, 446:475-482.
10
erraz da Costa DC, Fialho E,Silva JL. 2017. Cancer chemoprevention by resveratrol: The p53 tumor suppressor protein as a promising molecular target. Molecules, 22:1014.
11
Furnari FB, Fenton T, Bachoo RM, Mukasa A, Stommel JM, Stegh A, Hahn WC, Ligon KL, Louis DN, Brennan C, Chin L, DePinho RA,Cavenee WK. 2007. Malignant astrocytic glioma: Genetics, biology, and paths to treatment. Genes Dev, 21:2683-2710.
12
Gamet-Payrastre L, Li P, Lumeau S, Cassar G, Dupont MA, Chevolleau S, Gasc N, Tulliez J,Terce F. 2000. Sulforaphane, a naturally occurring isothiocyanate, induces cell cycle arrest and apoptosis in ht29 human colon cancer cells. Cancer Res, 60:1426-1433.
13
Gholami O,Shamsara J. 2016. Comparison of the cytotoxic effects of umbelliprenin and auraptene. Int J Pharm Pharm Sci, 8:1-4.
14
Graña X,Reddy EP. 1995. Cell cycle control in mammalian cells: Role of cyclins, cyclin dependent kinases (cdks), growth suppressor genes and cyclin-dependent kinase inhibitors (ckis). Oncogene, 11:211-220.
15
Ha ET, Antonios JP, Soto H, Prins RM, Yang I, Kasahara N, Liau LM,Kruse CA. 2014. Chronic inflammation drives glioma growth: Cellular and molecular factors responsible for an immunosuppressive microenvironment. Neuroimmunol Neuroinflammation, 1:66-76.
16
Hadjzadeh M, Tavakol Afshari J, Ghorbani A,Shakeri M. 2006. The effects of aqueous extract of garlic (allium sativum l.) on laryngeal cancer cells (hep-2) and l929 cells in vitro. J Med Plants, 2:41-48.
17
Hambardzumyan D, Gutmann DH,Kettenmann H. 2016. The role of microglia and macrophages in glioma maintenance and progression. Nat Neurosci, 19:20-27.
18
Hao C, Beguinot F, Condorelli G, Trencia A, Van Meir EG, Yong VW, Parney IF, Roa WH, Petruk KC. 2001. Induction and intracellular regulation of tumor necrosis factor-related apoptosis-inducing ligand (trail) mediated apotosis in human malignant glioma cells. Cancer Res, 61:1162-1170.
19
Harris BRE, Wang DF, Zhang Y, Ferrari M, Okon A, Cleary MP, Wagner CR,Yang DQ. 2018. Induction of the p53 tumor suppressor in cancer cells through inhibition of cap-dependent translation. Mol Cell Biol, 38:e00367-00317.
20
Hilliard T, Miklossy G, Chock C, Yue P, Williams P, Turkson J. 2017. 15∝-methoxypuupehenol induces antitumor effects in vitro and in vivo against human glioblastoma and breast cancer models. Mol Cancer Ther, 4:601-613.
21
Hou LC, Veeravagu A, Hsu AR, Tse VC. 2006. Recurrent glioblastoma multiforme: A review of natural history and management options. Neurosurg. Focus, 20:E5.
22
Huang J, Samson P, Perkins SM, Ansstas G, Chheda MG, DeWees TA, Tsien CI, Robinson CG, Campian JL. 2017. Impact of concurrent chemotherapy with radiation therapy for elderly patients with newly diagnosed glioblastoma: A review of the national cancer data base. J Neurooncol, 131:593-601.
23
Jalili-Nik M, Soltani A, Moussavi S, Ghayour-Mobarhan M, Ferns GA, Hassanian SM, Avan A. 2018. Current status and future prospective of curcumin as a potential therapeutic agent in the treatment of colorectal cancer. J Cell Physiol, 233:6337-6345.
24
Jun DY, Kim JS, Park HS, Han CR, Fang Z, Woo MH, Rhee IK, Kim YH. 2007. Apoptogenic activity of auraptene of zanthoxylum schinifolium toward human acute leukemia jurkat t cells is associated with er stress-mediated caspase-8 activation that stimulates mitochondria-dependent or -independent caspase cascade. Carcinogenesis, 28:1303-1313.
25
Kastan MB, Canman CE,Leonard CJ. 1995. P53, cell cycle control and apoptosis: Implications for cancer. Cancer Metastasis Rev, 14:3-15.
26
Kaufmann SH,Earnshaw WC. 2000. Induction of apoptosis by cancer chemotherapy. Exp Cell Res, 256:42-49.
27
Kaur V, Kumar M, Kumar A, Kaur K, Dhillon VS, Kaur S. 2018. Pharmacotherapeutic potential of phytochemicals: Implications in cancer chemoprevention and future perspectives. Biomed Pharmacother, 97:564-586.
28
Kawabata K, Tanaka T, Yamamoto T, Hara A, Murakami A, Koshimizu K, Ohigashi H, Stoner GD, Mori H. 2000. Suppression of n-nitrosomethylbenzylamine-induced rat esophageal tumorigenesis by dietary feeding of auraptene. J Exp Clin Cancer Res, 19:45-52.
29
Kohno H, Suzuki R, Curini M, Epifano F, Maltese F, Gonzales SP,Tanaka T. 2006. Dietary administration with prenyloxycoumarins, auraptene and collinin, inhibits colitis-related colon carcinogenesis in mice. Int J Cancer, 118:2936-2942.
30
Krakstad C,Chekenya M. 2010. Survival signalling and apoptosis resistance in glioblastomas: Opportunities for targeted therapeutics. Mol Cancer, 9:135.
31
Lee BL, Lee HS, Jung J, Cho SJ, Chung H-Y, Kim WH, Jin Y-W, Kim CS, Nam SY. 2005. Nuclear factor-κb activation correlates with better prognosis and akt activation in human gastric cancer. Clin. Cancer Res, 11:2518-2525.
32
Lee DH, Lee TH, Jung CH, Kim YH. 2012. Wogonin induces apoptosis by activating the ampk and p53 signaling pathways in human glioblastoma cells. Cell Signal, 24:2216-2225.
33
Lefranc F, Sauvage S, Van Goietsenoven G, Megalizzi V, Lamoral-Theys D, Debeir O, Spiegl-Kreinecker S, Berger W, Mathieu V, Decaestecker C,Kiss R. 2009. Narciclasine, a plant growth modulator, activates rho and stress fibers in glioblastoma cells. Mol Cancer Ther, 8:1739-1750.
34
Leonard EJ, Yoshimura T. 1990.Human monocyte chemoattractant protein-1 (mcp-1). Elsevier, 3:97-101
35
Li YL, Gan GP, Zhang HZ, Wu HZ, Li CL, Huang YP, Liu YW, Liu JW. 2007. A flavonoid glycoside isolated from smilax china l. Rhizome in vitro anticancer effects on human cancer cell lines. J Ethnopharmacol, 113:115-124.
36
Liu AJ, Wang SH, Chen KC, Kuei HP, Shih YL, Hou SY, Chiu WT, Hsiao SH,Shih CM. 2013. Evodiamine, a plant alkaloid, induces calcium/jnk-mediated autophagy and calcium/mitochondria-mediated apoptosis in human glioblastoma cells. Chem Biol Interact, 205:20-28.
37
Liu YY, Fan CH, Pu L, Wei C, Jin HQ, Teng YM, Zhao MM, Yu ACH, Jiang F, Shu JL, Li F, Peng Q, Kong J, Pan B, Zheng LM,Huang YN. 2016. Phloretin induces cell cycle arrest and apoptosis of human glioblastoma cells through the generation of reactive oxygen species. J Neurooncol, 128:217-223.
38
Lowe SW, Lin AW. 2000. Apoptosis in cancer. Carcinogenesis, 21:485-495.
39
Massagué J. 2004. G1 cell-cycle control and cancer. Nature, 432:298-306.
40
Mollazadeh H, Afshari AR,Hosseinzadeh H. 2017. Review on the potential therapeutic roles of nigella sativa in the treatment of patients with cancer: Involvement of apoptosis: - black cumin and cancer. J Pharmacopuncture, 20:158-172.
41
Moradzadeh M, Sadeghnia HR, Mousavi SH, Mahmoodi M, Hosseini A. 2017. Ferula gummosa gum induces apoptosis via ros mechanism in human leukemic cells. Cell Mol Biol (Noisy-le-grand), 63:17-22.
42
Mosmann T. 1983. Rapid colorimetric assay for cellular growth and survival: Application to proliferation and cytotoxicity assays. J Immunol Methods, 65:55-63.
43
Mousavi SH, Tavakkol-Afshari J, Brook A,Jafari-Anarkooli I. 2009. Role of caspases and bax protein in saffron-induced apoptosis in mcf-7 cells. Food Chem Toxicol, 47:1909-1913.
44
Murakami A, Kuki W, Takahashi Y, Yonei H, Nakamura Y, Ohto Y, Ohigashi H,Koshimizu K. 1997. Auraptene, a citrus coumarin, inhibits 12‐0‐tetradecanoylphorbol‐13‐acetate‐induced tumor promotion in icr mouse skin, possibly through suppression of superoxide generation in leukocytes. Cancer Sci, 88:443-452.
45
Naumann U, Kugler S, Wolburg H, Wick W, Rascher G, Schulz JB, Conseiller E, Bahr M,Weller M. 2001. Chimeric tumor suppressor 1, a p53-derived chimeric tumor suppressor gene, kills p53 mutant and p53 wild-type glioma cells in synergy with irradiation and cd95 ligand. Cancer Res, 61:5833-5842.
46
Omuro A, DeAngelis LM. 2013. Glioblastoma and other malignant gliomas: A clinical review. JAMA, 310:1842-1850.
47
Park JY, Kim H, Lim DW, Kim JE, Park WH,Park SD. 2018. Ethanol extract of lycopodium serratum thunb. Attenuates lipopolysaccharide-induced c6 glioma cells migration via matrix metalloproteinase-9 expression. Chin J Integr Med, 24:860-866.
48
Platten M, Kretz A, Naumann U, Aulwurm S, Egashira K, Isenmann S,Weller M. 2003. Monocyte chemoattractant protein-1 increases microglial infiltration and aggressiveness of gliomas. Ann Neurol, 54:388-392.
49
Ryan KM, Ernst MK, Rice NR,Vousden KH. 2000. Role of nf-κb in p53-mediated programmed cell death. Nature, 404:892-897.
50
Sadeghnia HR, Jamshidi R, Afshari AR, Mollazadeh H, Forouzanfar F,Rakhshandeh H. 2017. Terminalia chebula attenuates quinolinate-induced oxidative pc12 and oln-93 cell death. Mult Scler Relat Disord, 14:60-67.
51
Salcedo R, Ponce ML, Young HA, Wasserman K, Ward JM, Kleinman HK, Oppenheim JJ, Murphy WJ. 2000. Human endothelial cells express ccr2 and respond to mcp-1: Direct role of mcp-1 in angiogenesis and tumor progression. Blood, 96:34-40.
52
Shafiee-Nick R, Afshari AR, Mousavi SH, Rafighdoust A, Askari VR, Mollazadeh H, Fanoudi S, Mohtashami E, Rahimi VB, Mohebbi M,Vahedi MM. 2017. A comprehensive review on the potential therapeutic benefits of phosphodiesterase inhibitors on cardiovascular diseases. Biomed Pharmacother, 94:541-556.
53
Solowey E, Lichtenstein M, Sallon S, Paavilainen H, Solowey E,Lorberboum-Galski H. 2014. Evaluating medicinal plants for anticancer activity. Sci World J, 2014:721402.
54
Soltani F, Mosaffa F, Iranshahi M, Karimi G, Malekaneh M, Haghighi F, Behravan J. 2010. Auraptene from ferula szowitsiana protects human peripheral lymphocytes against oxidative stress. Phytother Res, 24:85-89.
55
Song CJ, Fan B, Xiao ZZ. 2018. Overexpression of alk4 inhibits cell proliferation and migration through the inactivation of jak/stat3 signaling pathway in glioma. Biomed Pharmacother, 98:440-445.
56
Takeda K, Utsunomiya H, Kakiuchi S, Okuno Y, Oda K, Inada K, Tsutsumi Y, Tanaka T, Kakudo K. 2007. Citrus auraptene reduces helicobacter pylori colonization of glandular stomach lesions in mongolian gerbils. J Oleo Sci, 56:253-260.
57
Tanaka T, de Azevedo M, Durán N, Alderete JB, Epifano F, Genovese S, Tanaka M, Tanaka T, Curini M. 2010. Colorectal cancer chemoprevention by 2 β‐cyclodextrin inclusion compounds of auraptene and 4′‐geranyloxyferulic acid. Int J Cancer, 126:830-840.
58
Tanaka T, Kawabata K, Kakumoto M, Hara A, Murakami A, Kuki W, Takahashi Y, Yonei H, Maeda M, Ota T, Odashima S, Yamane T, Koshimizu K,Ohigashi H. 1998. Citrus auraptene exerts dose-dependent chemopreventive activity in rat large bowel tumorigenesis: The inhibition correlates with suppression of cell proliferation and lipid peroxidation and with induction of phase ii drug-metabolizing enzymes. Cancer Res, 58:2550-2556.
59
Tanaka T, Kawabata K, Kakumoto M, Makita H, Hara A, Mori H, Satoh K, Hara A, Murakami A, Kuki W, Takahashi Y, Yonei H, Koshimizu K,Ohigashi H. 1997. Citrus auraptene inhibits chemically induced colonic aberrant crypt foci in male f344 rats. Carcinogenesis, 18:2155-2161.
60
Tanaka T, Kawabata K, Kakumoto M, Matsunaga K, Mori H, Murakami A, Kuki W, Takahashi Y, Yonei H, Satoh K, Hara A, Maeda M, Ota T, Odashima S, Koshimizu K, Ohigashi H. 1998. Chemoprevention of 4-nitroquinoline 1-oxide-induced oral carcinogenesis by citrus auraptene in rats. Carcinogenesis, 19:425-431.
61
Tanaka T, Kohno H, Murakami M, Kagami S, El-Bayoumy K. 2000. Suppressing effects of dietary supplementation of the organoselenium 1,4phenylenebis(methylene)selenocyanate and the citrus antioxidant auraptene on lung metastasis of melanoma cells in mice. Cancer Res, 60:3713-3716.
62
Tang SL, Gao YL, Hu WZ. 2017. Paqr3 inhibits the proliferation, migration and invasion in human glioma cells. Biomed. Pharmacother, 92:24-32.
63
Tavakkol-Afshari J, Brook A,Mousavi SH. 2008. Study of cytotoxic and apoptogenic properties of saffron extract in human cancer cell lines. Food Chem Toxicol, 46:3443-3447.
64
van Hogerlinden M, Rozell BL, Ährlund-Richter L, ToftgÅrd R. 1999. Squamous cell carcinomas and increased apoptosis in skin with inhibited rel/nuclear factor-κb signaling. Cancer Res, 59:3299-3303.
65
Vazifedan V, Mousavi SH, Sargolzaei J, Soleymanifard S,Fani Pakdel A. 2017. Study of crocin & radiotherapy-induced cytotoxicity and apoptosis in the head and neck cancer (hn-5) cell line. Iran J Pharm Res, 16:230-237.
66
Wang ZS, Luo P, Dai SH, Liu ZB, Zheng XR,Chen T. 2013. Salvianolic acid b induces apoptosis in human glioma u87 cells through p38-mediated ros generation. Cell Mol Neurobiol, 33:921-928.
67
Yang BY, Song JW, Sun HZ, Xing JC, Yang ZH, Wei CY, Xu TY, Yu ZN, Zhang YN, Wang YF, Chang H, Xu ZP, Hou M, Ji MJ, Zhang YS. 2018. Psmb8 regulates glioma cell migration, proliferation, and apoptosis through modulating erk1/2 and pi3k/akt signaling pathways. Biomed Pharmacother, 100:205-212.
68
ORIGINAL_ARTICLE
Effect of crocin on biochemical parameters, oxidative/antioxidative profiles, sperm characteristics and testicular histopathology in streptozotocin-induced diabetic rats
Objective: Chronic hyperglycemia and overproduction of reactive oxygen species (ROS) are strong predictors of the development of reproductive complications of diabetes. The present study was conducted to determine the effects of crocin on biochemical parameters, oxidative stress, and sperm characteristics as well as testes histopathology in diabetic rats. Materials and Methods: Twenty-four rats were divided into the four groups as follows: control, untreated diabetic and two crocin (40 and 60 mg/kg/day)-treated diabetic groups. Diabetes was induced by injection of a single dose of streptozotocin (STZ, 60 mg/kg). Administration of crocin (intraperitoneally) was started three days after STZ injection and was continued until the 28th day. At the end of the experiment, rats were anesthetized after weighing. Blood samples and epididymal sperm were subsequently collected to measure biochemical parameters (glucose and lipid profile), total oxidant and antioxidant status (TOS and TAS, respectively), oxidative stress index (OSI), and sperm characteristics (count, motility, and viability); also, testes were dissected out for histopathology examination. Results: Our result indicated that blood glucose, cholesterol, triglyceride, LDL cholesterol levels, as well as TOS, and OSI decreased, but body weight, sperm counts, motility and viability, as well as TAS and HDL levels increased significantly in the crocin-treated diabetic rats (P˂0.05). In testis sections from diabetic rats treated with crocin (40 and 60 mg/kg), seminiferous tubules exhibited normal shape and restoration of testis architecture was observed. Conclusion: Administration of crocin in the present study, ameliorated blood glucose, lipid abnormalities, oxidative stress, sperm characteristics and testis damage in STZ-diabetic rats.
https://ajp.mums.ac.ir/article_12596_086278940b5ebba0abfd8c427936dc5b.pdf
2019-07-01
347
361
10.22038/ajp.2019.12596
Biochemical Parameters
Crocin
Oxidative stress index
Sperm characteristics
Streptozotocin
Testicular histopathology
Seyed Mersad
Sefidgar
mersad.orbit@yahoo.com
1
Student Research Committee, Faculty of Veterinary Medicine, Semnan University, Semnan, Iran
AUTHOR
Mahmood
Ahmadi-hamedani
ahmadi.hamedani@semnan.ac.ir
2
Department of Clinical Sciences, Faculty of Veterinary Medicine, Semnan University, Semnan, Iran
LEAD_AUTHOR
Ashkan
Jebelli Javan
jebellija@semnan.ac.ir
3
Department of Food Hygiene, Faculty of Veterinary Medicine, Semnan University, Semnan, Iran
AUTHOR
Reza
Narenji Sani
rezasani_vet@semnan.ac.ir
4
Department of Clinical Sciences, Faculty of Veterinary Medicine, Semnan University, Semnan, Iran
AUTHOR
Abbas
Javaheri vayghan
ajavaheri@semnan.ac.ir
5
Department of Pathobiology, Faculty of Veterinary Medicine, Semnan University, Semnan, Iran
AUTHOR
Adedara IA, Awogbindin IO, Anamelechi JP, Farombi EO. 2015. Garcinia kola seed ameliorates renal, hepatic, and testicular oxidative damage in streptozotocin-induced diabetic rats. Pharm Biol, 53:695-704.
1
Afifi M, Almaghrabi OA, Kadasa NM. 2015. Ameliorative effect of zinc oxide nanoparticles on antioxidants and sperm characteristics in streptozotocin-induced diabetic rat testes. BioMed Res Int, 2015: 153573.
2
Agbaje I, Rogers DA, McVicar CM, McClure N, Atkinson AB, Mallidis C, Lewis SE. 2007. Insulin dependant diabetes mellitus: implications for male reproductive function. Hum Reprod, 22:1871-1877.
3
Ahmadi M, Rajaei Z, Hadjzadeh MA, Nemati H, Hosseini M. 2017. Crocin improves spatial learning and memory deficits in the Morris water maze via attenuating cortical oxidative damage in diabetic rats. Neurosci Lett, 642:1-6.
4
Asadi MH, Zafari F, Sarveazad A, Abbasi M, Safa M, Koruji M, Yari A, Miran RA. 2014. Saffron improves epididymal sperm parameters in rats exposed to cadmium. Nephro-urology monthly, 6: e12125.
5
Asri-Rezaei S, Tamaddonfard E, Ghasemsoltani-Momtaz B, Erfanparast A, Gholamalipour S. 2015. Effects of crocin and zinc chloride on blood levels of zinc and metabolic and oxidative parameters in streptozotocin-induced diabetic rats. Avicenna J phytomed, 5:403-412.
6
Baccetti B, La Marca A, Piomboni P, Capitani S, Bruni E, Petraglia F, De Leo V. 2002. Insulin-dependent diabetes in men is associated with hypothalamo-pituitary derangement and with impairment in semen quality. Hum Reprod, 17:2673-2677.
7
Bahojb Soldozi H, Jalili F, Sohrabi M, Keshtmand Z, Jalili C. 2018. The effects of crocin on the serum levels of sex hormone and NO in streptozotocin–induced diabetic rats. J Kurd Univers Med Sci, 23:103-113. (In Persian).
8
Bakhtiary Z, Shahrooz R, Ahmadi A, Soltanalinejad F. 2014. Protective effect of Crocin on DNA damage of sperm and in vitro fertilization (IVF) in adult male mice treated with cyclophosphamide. J Mazandaran Univ Med Sci, 24:49-59. (In Persian)
9
Bakhtiary Z, Shahrooz R, Ahmadi A, Zarei L. 2014. Evaluation of antioxidant effects of crocin on sperm quality in cyclophosphamide treated adult mice. Vet Res Forum, 5:213-218.
10
Bathaie SZ, Shams A, Kermani FM. 2011. Crocin bleaching assay using purified di-gentiobiosyl crocin (-crocin) from Iranian saffron. Iran J Basic Med Sci, 14:399-406.
11
Bayatpoor ME, Mirzaee S, Mohammadi MT. (2018). Effect of crocin on spermatogenesis in streptozotocin-induced diabetic rats. J Mazandaran Univ Med Sci, 28: 24-35. (In Persian)
12
Bolhassani A, Khavari A, Bathaie SZ. 2014. Saffron and natural carotenoids: Biochemical activities and anti-tumor effects. Biochim Biophys Acta Rev Cancer, 1845:20-30.
13
Bors W, Michel C, Saran M. 1984. Inhibition of the bleaching of the carotenoid crocin a rapid test for quantifying antioxidant activity. Biochim Biophys Acta Lipids Lipid Metab, 796:312-319.
14
Bountagkidou O, van der Klift EJ, Tsimidou MZ, Ordoudi SA, van Beek TA. 2012. An on-line high performance liquid chromatography-crocin bleaching assay for detection of antioxidants. J Chromatogr A, 1237:80-85.
15
Brüning JC, Gautam D, Burks DJ, Gillette J, Schubert M, Orban PC, Klein R, Krone W, Müller-Wieland D, Kahn CR. 2000. Role of brain insulin receptor in control of body weight and reproduction. Science, 289:2122-2125.
16
Cavallini G. 2006. Male idiopathic oligoasthenoteratozoospermia. Asian J Androl, 8:143-157.
17
Ding C, Wang Q, Hao Y, Ma X, Wu L, Li W, Wu Y, Guo F, Ma S, Huang F, Qin G. 2016. Vitamin D supplement improved testicular function in diabetic rats. Biochem Biophys Res Commun, 473:161-167.
18
Dokuyucu R, Karateke A, Gokce H, Kurt RK, Ozcan O, Ozturk S, Tas ZA, Karateke F, Duru M. 2014. Antioxidant effect of erdosteine and lipoic acid in ovarian ischemia–reperfusion injury. Eur J Obstet Gynecol Reprod Biol, 183:23-27.
19
Erel O. 2004. A novel automated direct measurement method for total antioxidant capacity using a new generation, more stable ABTS radical cation. Clin Biochem, 37:277-285.
20
Erel O. 2005. A new automated colorimetric method for measuring total oxidant status. Clin Biochem, 38:1103-1111.
21
Evans JL, Goldfine ID, Maddux BA, Grodsky GM. 2002. Oxidative stress and stress-activated signaling pathways: a unifying hypothesis of type 2 diabetes. Endocr Rev, 23:599-622.
22
Farahmand SK, Samini F, Samini M, Samarghandian S. 2013. Safranal ameliorates antioxidant enzymes and suppresses lipid peroxidation and nitric oxide formation in aged male rat liver. Biogerontol, 14:63-71.
23
Ghanbari E, Nejati V, Najafi G, Khazaei M, Babaei M. 2015. Study on the effect of royal jelly on reproductive parameters in streptozotocin-induced diabetic rats. Int J fertil Steril. 9:113-120.
24
Gómez O, Ballester B, Romero A, Arnal E, Almansa I, Miranda M, Mesonero JE, Terrado J. 2009. Expression and regulation of insulin and the glucose transporter GLUT8 in the testes of diabetic rats. Horm Metab Res, 41:343-349.
25
Guneli E, Tugyan K, Ozturk H, Gumustekin M, Cilaker S, Uysal N. 2008. Effect of melatonin on testicular damage in streptozotocin-induced diabetes rats. Eur Surg Res, 40:354-360.
26
Heidari S, Mehri S, Hosseinzadeh H. 2017. Memory enhancement and protective effects of crocin against D-galactose aging model in the hippocampus of Wistar rats. Iran J Basic Med Sci, 20:1250-1259.
27
Hosseinzadeh H, Sadeghnia HR. 2005. Safranal, a constituent of Crocus sativus (saffron), attenuated cerebral ischemia induced oxidative damage in rat hippocampus. J Pharm Pharm Sci, 8:394-399.
28
Hosseinzadeh H, Shamsaie F, Mehri S. 2009. Antioxidant activity of aqueous and ethanolic extracts of Crocus sativus L. stigma and its bioactive constituents, crocin and safranal. Pharmacogn Mag, 5:419-424.
29
Hosseinzadeh H, Younesi HM. 2002. Antinociceptive and anti-inflammatory effects of Crocus sativus L. stigma and petal extracts in mice. BMC Pharmacol, 2:7.
30
Jain GC, Jangir RN. 2014. Modulation of diabetes-mellitusinduced male reproductive dysfunctions in experimental animal models with medicinal plants. Pharmacogn Rev, 8:13-21.
31
Kalantari Hesari A, Shahrooz R, Ahmadi A, Malekinejad H, Saboory E. 2015. Crocin prevention of anemia-induced changes in structural and functional parameters of mice testes. J Appl Biomed, 13:213-223.
32
Kampa M, Nistikaki A, Tsaousis V, Maliaraki N, Notas G, Castanas E. 2002. A new automated method for the determination of the Total Antioxidant Capacity (TAC) of human plasma, based on the crocin bleaching assay. BMC Clin Pathol, 2:3.
33
Kang C, Lee H, Jung ES, Seyedian R, Jo M, Kim J, Kim JS, Kim E. 2012. Saffron (Crocus sativus L.) increases glucose uptake and insulin sensitivity in muscle cells via multipathway mechanisms. Food Chem, 135:2350-2358.
34
Kanter M, Aktas C, Erboga M. 2012. Protective effects of quercetin against apoptosis and oxidative stress in streptozotocin-induced diabetic rat testis. Food Chem Toxicol, 50:719-725.
35
Khazdair MR, Boskabady MH, Hosseini M, Rezaee R, Tsatsakis AM. 2015. The effects of Crocus sativus (saffron) and its constituents on nervous system: A review. Avicenna J phytomed, 5:376-391.
36
Kilarkaje N, Al-Bader MM. 2015. Diabetes-induced oxidative DNA damage alters p53-p21CIP1/Waf1 signaling in the rat testis. Reprod Sci, 22:102-112.
37
Kwak JM, Mori IC, Pei ZM, Leonhardt N, Torres MA, Dangl JL, Bloom RE, Bodde S, Jones JD, Schroeder JI. 2003. NADPH oxidase AtrbohD and AtrbohF genes function in ROS-dependent ABA signaling in Arabidopsis. EMBO J, 22:2623-2633.
38
Mohammadi E, Mehri S, Bostan HB, Hosseinzadeh H. 2018. Protective effect of crocin against d-galactose-induced aging in mice. Avicenna J Phytomed, 8:14-23.
39
Mokhber Maleki E, Eimani H, Bigdeli MR, Golkar Narenji A, Abedi R. 2016. Effects of crocin supplementation during in vitro maturation of mouse oocytes on glutathione synthesis and cytoplasmic maturation. Int J Fertil Steril, 10:53-61.
40
Niedowicz DM, Daleke DL. 2005. The role of oxidative stress in diabetic complications. Cell Biochem Biophys, 43:289-330.
41
Ordoudi SA, Befani CD, Nenadis N, Koliakos GG, Tsimidou MZ. 2009. Further examination of antiradical properties of Crocus sativus stigmas extract rich in crocins. J Agric Food Chem, 57:3080-3086.
42
Potnuri AG, Allakonda L, Lahkar M. 2018. Crocin attenuates cyclophosphamide induced testicular toxicity by preserving glutathione redox system. Biomed Pharmacother, 101:174-180.
43
Rajasekaran S, Sivagnanam K, Subramanian S. 2005. Antioxidant effect of Aloe vera gel extract in streptozotocin-induced diabetes in rats. Pharmacol Rep, 57:90-96.
44
Rajender S, Rahul P, Mahdi AA. 2010. Mitochondria, spermatogenesis and male infertility. Mitochondrion. 10:419-428.
45
Rashid K, Sil PC. 2015. Curcumin ameliorates testicular damage in diabetic rats by suppressing cellular stress-mediated mitochondria and endoplasmic reticulum-dependent apoptotic death. Biochim Biophys Acta Mol Basis Dis, 1852:70-82.
46
Rios JL, Recio MC, Giner RM, Manez S. 1996. An update review of saffron and its active constituents. Phyto Res, 10:189-193.
47
Saber TM, Abd El-Aziz RM, Ali HA. 2016. Quercetin mitigates fenitrothion‐induced testicular toxicity in rats. Androl, 48:491-500.
48
Sakhaee E, Emadi L, Azari O, Kheirandish R, Esmaili Nejad MR, Shafiei Bafti H. 2016. Effects of Cuminum cyminum L. essential oil on some epididymal sperm parameters and histopathology of testes following experimentally induced copper poisoning in mice. Androl, 48:542-547.
49
Salahshoor MR, Khazaei M, Jalili C, Keivan M. 2016. Crocin improves damage induced by nicotine on a number of reproductive parameters in male mice. Int J Fertil Steril, 10:71-78.
50
Samarghandian S, Azimi-Nezhad M, Borji A, Farkhondeh T. 2016. Effect of crocin on aged rat kidney through inhibition of oxidative stress and proinflammatory state. Phyto Res, 30:1345-1353.
51
Samarghandian S, Azimi-Nezhad M, Farkhondeh T. 2016. Crocin attenuate Tumor Necrosis Factor-alpha (TNF-α) and interleukin-6 (IL-6) in streptozotocin-induced diabetic rat aorta. Cytokine, 88:20-28.
52
Samarghandian S, Borji A, Delkhosh MB, Samini F. 2013. Safranal treatment improves hyperglycemia, hyperlipidemia and oxidative stress in streptozotocin-induced diabetic rats. J Pharm Pharm Sci, 16:352-362.
53
Samarghandian S, Borji A. 2014. Anticarcinogenic effect of saffron (Crocus sativus L.) and its ingredients. Phcog Res, 6:99-107.
54
Sapanidou V, Taitzoglou I, Tsakmakidis I, Kourtzelis I, Fletouris D, Theodoridis A, Zervos I, Tsantarliotou M. 2015. Antioxidant effect of crocin on bovine sperm quality and in vitro fertilization. Theriogenology, 84:1273-1282.
55
Saumya SM, Basha PM. 2017. Fluoride exposure aggravates the testicular damage and sperm quality in diabetic mice: protective role of ginseng and banaba. Biol Trace Elem Res, 177:331-344.
56
Schoeller EL, Schon S, Moley KH. 2012. The effects of type 1 diabetes on the hypothalamic, pituitary and testes axis. Cell Tissue Res, 349:839-847.
57
Sheng L, Qian Z, Zheng S, Xi L. 2006. Mechanism of hypolipidemic effect of crocin in rats: crocin inhibits pancreatic lipase. Eur J pharmacol, 543:116-122.
58
Shi GJ, Li ZM, Zheng J, Chen J, Han XX, Wu J, Li GY, Chang Q, Li YX, Yu JQ. 2017. Diabetes associated with male reproductive system damages: Onset of presentation, pathophysiological mechanisms and drug intervention. Biomed Pharmaco, 90:562-574.
59
Shi GJ, Li ZM, Zheng J, Chen J, Han XX, Wu J, Li GY, Chang Q, Li YX, Yu JQ. 2017. Diabetes associated with male reproductive system damages: Onset of presentation, pathophysiological mechanisms and drug intervention. Biomed Pharm, 90:562-574.
60
Shirali S, Zahra Bathaie S, Nakhjavani M. 2013. Effect of crocin on the insulin resistance and lipid profile of streptozotocin-induced diabetic rats. Phyto Res, 27:1042-1047.
61
Sifuentes-Franco S, Pacheco-Moisés FP, Rodríguez-Carrizalez AD, Miranda-Díaz AG. 2017. The role of oxidative stress, mitochondrial function, and autophagy in diabetic polyneuropathy. J Diabetes Res, 2017: 1673081.
62
Tubaro F, Micossi E, Ursini F. 1996. The antioxidant capacity of complex mixtures by kinetic analysis of crocin bleaching inhibition. J Am Oil Chem' Soc, 73:173-179.
63
Xu Y, Lei H, Guan R, Gao Z, Li H, Wang L, Song W, Gao B, Xin Z. 2014. Studies on the mechanism of testicular dysfunction in the early stage of a streptozotocin induced diabetic rat model. Biochem biophys Res commun, 450:87-92.
64
Yazdanparast R, Ardestani A, Jamshidi S. 2007. Experimental diabetes treated with Achillea santolina: effect on pancreatic oxidative parameters. J Ethnopharmacol, 112:13-18.
65
ORIGINAL_ARTICLE
The effect of hydroalcoholic extract of Ziziphora clinopodioides L. on spatial memory and neuronal density of hippocampal CA1 region in rats with sporadic Alzheimer's disease
Objective: Alzheimer's disease is a neurodegenerative disorder associated with gradual loss of cognitive and memory abilities. It was shown that the hippocampus is one of the first structures in the brain that is affected by the disease. Ziziphora clinopodioides (Z. clinopodioides) is a member of Lamiaceae family and contains various substances. Materials and Methods: In this experimental study, 72 adult male Wistar rats were used for behavioral and histopathologic studies. They were divided into nine groups included: control, negative control (Alzheimer), positive control (Alzheimer's treated with rivastigmine), aCSF (artificial cerebrospinal fluid) + ziziphora extract with doses of 200,400, and 600 mg/kg, and STZ (stereptozotocine)+ziziphoraextract in 200,400,600 mg/kg doses. The injury was created with bilaterally intraventricular injection. The spatial memory was studied by passive avoidance test and neuronal density was evaluated by dissector method. To examine the histopathological lesions, Congo red and toluidine blue staining were done. Data were analyzed by ANOVA Minitab software. Results: The memory index (neuronal density and passive avoidance test results) showed a significant decrease in negative control group compared to control (p≤0.001). Treatment with the hydroalcoholic extract at the doses of 400 and 600 mg/kg showed a significant increase in memory index in rats with Alzheimer's disease (p≤0.001). The effect of 200 mg/kg extract was not significantly different from that of the negative control group. The results of histological analysis indicated beta-amyloid plaques formation in the control group as compared to the negative control group while treatment with the extract at the doses of 400 and 600 mg/kg, significantly reduced beta-amyloid plaques formation. Conclusion: These findings suggest that the extract of Z. clinopodioides can improve Alzheimer's condition and alleviate memory and histopathologic damages; also, it decreases beta-amyloid plaques and apoptosis in CA1 region of the hippocampus.
https://ajp.mums.ac.ir/article_12700_b2a28aee7e10fee579f50061e95ea68d.pdf
2019-07-01
362
373
10.22038/ajp.2019.12700
Alzheimer
Ziziphora clinopodioides
Hippocampus
Spatial Memory
Samaneh
Sedighi
smn_sedighy@yahoo.com
1
Department of Biology, Damghan Branch, Islamic Azad University, Damghan, Iran
AUTHOR
Maryam
Tehranipour
maryam_tehranipour@mshdiau.ac.ir
2
Department of Biology, Mashhad Branch, Islamic Azad University, Mashhad, Iran.
LEAD_AUTHOR
Gholamhassan
Vaezi
gh.vaezi@yahoo.com
3
Department of Biology, Damghan Branch, Islamic Azad University, Damghan, Iran.
AUTHOR
Vida
Hojati
vida.hojati@gmail.com
4
Department of Biology, Damghan Branch, Islamic Azad University, Damghan, Iran.
AUTHOR
Hamid
Hashemi-Moghaddam
h.hashemimoghadam@damghaniau.ac.ir
5
Department of chemistry, Damghan Branch, Islamic Azad University, Damghan, Iran.
AUTHOR
Agrawal R, Tyagi E, Shukla R, Nath C. 2009. A study of brain insulin receptors, AChE activity and oxidative stress in rat model of ICV STZ induced dementia. Neuropharmacology, 56:779-787.
1
Aliev G, Obrenovich ME, Reddy VP. 2008. Antioxidant therapy in Alzheimer’s disease: theory and practice. Med Chem, 8:1395-1399
2
Babri S, Amani M, Mohaddes G, Alihemmati A, Ebrahimi H. 2012. Effect of aggregated β-amyloid (1-42) on synaptic plasticity of hippocampal dentate gyrus granule cells in vivo. Bio Impacts, BI 2:189-195.
3
Biasibetti R, dos Santos JPA, Rodrigues L. 2017 Hippocampal changes in STZ-model of Alzheimer’s disease are dependent on sex. Behav Brain Res, 316:205-214.
4
Butterfield DA, Drake J, Pocernich C, Castegna A. 2001. Evidence of oxidative damage in Alzheimer's disease brain: central role for amyloid β-peptide. Trends Mol Med, 7:548-554.
5
Carreiras M, Marco J.2004. Recent approaches to novel anti-Alzheimer therapy. Curr Pharm Des, 10:3167-3175.
6
Chen Y, Liang Z, Blanchard J. 2013. A non-transgenic mouse model (icv-STZ mouse) of Alzheimer’s disease: similarities to and differences from the transgenic model (3xTg-AD mouse). Mol Neurobiol, 47:711-725.
7
Cummings J, Winblad B. 2007. A rivastigmine patch for the treatment of Alzheimer’s disease and Parkinson’s disease dementia. Expert Rev Neurother, 7:1457-1463.
8
Dehghan Z, Sefidkon F, Khaniki G, Kalvandi R. 2010. Effects of some ecological factors on essential oil content and composition of Ziziphora clinopodioides Lam. subsp. rigida (Boiss.). Med Aromat Plants, 26:49-63.
9
Gill G, Woodward A, Casson I, Weston P.2009. Cardiac arrhythmia and nocturnal hypoglycaemia in type 1 diabetes—the ‘dead in bed’syndrome revisited. Diabetologia, 52:42-49.
10
Grünblatt E, Salkovic‐Petrisic M, Osmanovic J, Riederer P, Hoyer S. 2007. Brain insulin system dysfunction in streptozotocin intracerebroventricularly treated rats generates hyperphosphorylated tau protein. Neurochemistry, 101:757-770.
11
Hajiaghaee R, Akhondzadeh S. 2012. Herbal medicine in the treatment of Alzheimer’s disease. Med Plants, 1:1-7.
12
Hamann S. 2001. Cognitive and neural mechanisms of emotional memory. Trends Cognit Sci, 5:394-400.
13
Herring A, Ambrée O, Tomm M. 2009. Environmental enrichment enhances cellular plasticity in transgenic mice with Alzheimer-like pathology. Exp Neurol, 216:184-192.
14
Hoyer S, Lee SK, Löffler T, Schliebs R. 2000. Inhibition of the neuronal insulin receptor an in vivo model for sporadic Alzheimer disease? Ann N Y Acad Sci, 920:256-258.
15
Jain S, Shukla SD, Sharma K, Bhatnagar M. 2001. Neuroprotective effects of withania somnifera dunn in hippocampal sub‐regions of female albino rat. Phytother Res, 15:544-548.
16
Janson J, Laedtke T, Parisi JE, O’Brien P, Petersen RC, Butler PC. 2004. Increased risk of type 2 diabetes in Alzheimer disease. Diabetes, 53:474-481.
17
Kazmierski J, Messini-Zachou C, Gkioka M, Tsolaki M. 2018. The impact of a long-term rivastigmine and donepezil treatment on all-cause mortality in patients with Alzheimer’s disease. Alzheimer's Dis. Other Dementias ®:1533317518775044.
18
Kennedy DO, Little W, Scholey A. B 2004. Attenuation of laboratory-induced stress in humans after acute administration of Melissa officinalis (Lemon Balm). Psychosom Med, 66:607-613.
19
Kim J, Huh J, Song S. 1996. The antioxidative mechanism of ursolic acid. Korean J Gerontol, 6:52-56.
20
Klyubin I, Walsh DM, Lemere CA.2005. Amyloid β protein immunotherapy neutralizes Aβ oligomers that disrupt synaptic plasticity in vivo. Nat Med, 11:556-560.
21
Kroner Z.2009.The relationship between Alzheimer's disease and diabetes: Type 3 diabetes? Altern Med, 14:373-378.
22
Kulišić T, Kriško A, Dragović-Uzelac V, Miloš M, Pifat G. 2007. The effects of essential oils and aqueous tea infusions of oregano (Origanum vulgare L. spp. hirtum), thyme (Thymus vulgaris L.) and wild thyme (Thymus serpyllum L.) on the copper-induced oxidation of human low-density lipoproteins. Food Sci Nutr, 58:87-93.
23
Kyari M.2008. Extraction and characterization of seed oils. Int Agrophys, 22:139-143.
24
Lane RM, Kivipelto M, Greig NH.2004. Acetylcholinesterase and its inhibition in Alzheimer disease. Clin Neuropharmacol, 27:141-149.
25
Lannert H, Hoyer S. 1998. Intracerebroventricular administration of streptozotocin causes long-term diminutions in learning and memory abilities and in cerebral energy metabolism in adult rats. Behav Neurosci, 112:1199-1204.
26
Li G, Ma R, Huang C. 2008. Protective effect of erythropoietin on β-amyloid-induced PC12 cell death through antioxidant mechanisms. Neurosci Lett, 442:143-147.
27
Mahdy K, Shaker O, Wafay H, Nassar Y, Hassan H, Hussein A. 2012. Effect of some medicinal plant extracts on the oxidative stress status in Alzheimer’s disease induced in rats. Eur Rev Med Pharmacol Sci, 16:31-42.
28
Mehla J, Pahuja M, Gupta YK. 2013. Streptozotocin-induced sporadic Alzheimer's disease: selection of appropriate dose. Alzheimer's Dis, 33:17-21.
29
Miu AC, Andreescu CE, Vasiu R, Olteanu AI. 2003. A behavioral and histological study of the effects of long-term exposure of adult rats to aluminum. Neuroscience, 113:1197-1211.
30
Moazedi A, Ghotbedin Z, Parham G. 2015. The effect of Zncl2 on passive avoidance and motor activity learing due to administration of Alcl3 in male rats. Physiol Pharmacol, 1386:146-152.
31
Naghizadeh B, Mansouri M, Ghorbanzadeh B, Farbood Y, Sarkaki A. 2013. Protective effects of oral crocin against intracerebroventricular streptozotocin-induced spatial memory deficit and oxidative stress in rats. Phytomedicine, 20:537-542.
32
Nezhadali A, Shirvan BZ. 2010. Separation, Identification and Determination ofVolatile Compounds of Ziziphora persica BungeUsing HS-SPME/GC-MS. Int J Environ Sci Dev, 1:115-119.
33
Nilsson MR. 2004. Techniques to study amyloid fibril formation in vitro. Methods, 34:151-160.
34
Paxinos G, Watson C. 1986. The rat in stereotaxic coordinates. J Anat, 191:315-317.
35
Palazzi X, Bordier N. 2008. The marmoset brain in stereotaxic coordinates. In:Palazzi, X, The Marmoset Brain in Stereotaxic Coordinates, pp. 51-59, New York,Springer.
36
Perry EK, Pickering AT, Wang WW, Houghton P, Perry NS.1998. Medicinal plants and Alzheimer's disease: Integrating ethnobotanical and contemporary scientific evidence. Complementary Altern Med, 4:419-428.
37
Perry N, Menzies R, Hodgson F. 2018. A randomised double-blind placebo-controlled pilot trial of a combined extract of sage, rosemary and melissa, traditional herbal medicines, on the enhancement of memory in normal healthy subjects, including influence of age. Phytomedicine, 39:42-48.
38
Perry NS, Houghton PJ, Theobald A, Jenner P, Perry EK.2000. In‐vitro inhibition of human erythrocyte acetylcholinesterase by Salvia lavandulaefolia essential oil and constituent terpenes. Am J Pharm Pharmacol, 52:895-902.
39
Rabiei Z, Mokhtari S, Asgharzade S, Gholami M, Rahnama S, Rafieian-kopaei M. 2015. Inhibitory effect of Thymus vulgaris extract on memory impairment induced by scopolamine in rat. Asian Pac J Trop Biomed, 5:845-851.
40
Reisi P, Alaei H, Babri S, Sharifi MR, Mohaddes G. 2009. Effects of treadmill running on spatial learning and memory in streptozotocin-induced diabetic rats. Neurosci Lett, 455:79-83.
41
Rice-Evans CA, Miller NJ, Paganga G. 1996. Structure-antioxidant activity relationships of flavonoids and phenolic acids. Adv. Free Radical Biol. Med, 20:933-956.
42
Roig y Mesa JT. 1974. Plantas medicinales, aromáticas o venenosas de Cuba. In:Roig y,Plantas medicinales, pp. 120-122, Cuba, informed.
43
Rowan M, Klyubin I, Wang Q, Hu N, Anwyl R. 2007. Synaptic memory mechanisms: Alzheimer's disease amyloid β-peptide-induced dysfunction. Portland Press Limited, 4:1219-1223.
44
Salkovic‐Petrisic M, Tribl F, Schmidt M, Hoyer S, Riederer P. 2006. Alzheimer‐like changes in protein kinase B and glycogen synthase kinase‐3 in rat frontal cortex and hippocampus after damage to the insulin signalling pathway. J Neurochem, 96:1005-1015.
45
Singh B, Sharma B, Jaggi AS, Singh N. 2013. Attenuating effect of lisinopril and telmisartan in intracerebroventricular streptozotocin induced experimental dementia of Alzheimer’s disease type: possible involvement of PPAR-γ agonistic property. J Renin Angiotensin Aldosterone Syst, 14:124-136.
46
Squire LR, Zola SM. 1996. Structure and function of declarative and nondeclarative memory systems. Proc. Natl Acad Sci, 93:13515-13522.
47
Sul D, Kim H-S, Lee D, Joo SS, Hwang KW, Park S-Y. 2009. Protective effect of caffeic acid against beta-amyloid-induced neurotoxicity by the inhibition of calcium influx and tau phosphorylation. Life Sci, 84:257-262.
48
Tota S, Kamat PK, Shukla R, Nath C. 2011. Improvement of brain energy metabolism and cholinergic functions contributes to the beneficial effects of silibinin against streptozotocin induced memory impairment. Beha. Brain Res, 221:207-215.
49
Williams RJ, Spencer JP.2012. Flavonoids, cognition, and dementia: actions, mechanisms, and potential therapeutic utility for Alzheimer disease. Adv Free Radical Biol Med, 52:35-45.
50
Xiao J, Tundis R.2013. Natural products for Alzheimer's disease therapy: basic and application. J Pharm Pharmacol, 65:1679-1680.
51
Xing S, Zhang P, Ji Q, Jia H, Wang X.2010. Essential oil compositions and antioxidant activities of two Ziziphora species in Xinjiang. Food Sci, 31:154-159.
52
Yang LP, Keating GM.2007. Rivastigmine Transdermal Patch. CNS drugs, 21:957-965.
53
Zhou L, Tan S, Shan Y-l.2016. Baicalein improves behavioral dysfunction induced by Alzheimer’s disease in rats. Neuropsychiatr Dis Treat, 12:3145-3149
54
ORIGINAL_ARTICLE
Administration of troxerutin improves testicular function and structure in type-1 diabetic adult rats by reduction of apoptosis
Objective: The glucose-reducing effects of troxerutin was previously proven. This study was conducted to evaluate troxerutin effect on testicular structure and spermatozoid parameters in type-1 diabetic adult male rats. Materials and Methods: Fifty male Wistar rats were randomly classified into 5 groups as follows: control (C), troxerutin (T), diabetic (DM), troxerutin-treated DM (DT) and insulin-treated DM (DI). Testicular structure, apoptosis, lipid peroxidation and antioxidant activity, and spermatozoid parameters were assessed 4 weeks after initiation of the interventions. Results: The results revealed that diabetes caused testicular stereological changes and significantly increased blood glucose level, testicular MDA content and apoptosis but decreased insulin level, testicular GPX activity, and sperm parameters compared to controls (p Conclusion: Taken together, troxerutin, comparable to insulin, effectively improved DM-induced testicular dysfunction and sperm parameters in diabetic rats and these effects might be mediated through troxerutin’s anti-apoptotic effects.
https://ajp.mums.ac.ir/article_12741_42f5452102d9eef12a47ec3e38cece8a.pdf
2019-07-01
374
385
10.22038/ajp.2019.12741
Diabetes
Troxerutin
Testis
Apoposis
Stress oxidative
Rat
Afsaneh
Qadiri
ghadiri.afsane@gmail.com
1
Department of physiology, Faculty of medicine, Tabriz University of Medical Sciences, Tabriz, Iran.
AUTHOR
Fariba
Mirzaei Bavil
bavil2000@yahoo.com
2
Drug Applied Research Center, Tabriz University of Medical Sciences, Tabriz, Iran.
AUTHOR
Gholamreza
Hamidian
ghamidian@yahoo.com
3
Department of Basic Sciences, Faculty of Veterinary Medicine, University of Tabriz, Tabriz, Iran.
AUTHOR
Zohreh
Zavvari Oskuye
zohre.zavari@gmail.com
4
Department of physiology, Faculty of medicine, Tabriz University of Medical Sciences, Tabriz, Iran
AUTHOR
Mahdi
Ahmadi
mahdi59866@gmail.com
5
Tuberculosis and Lung Diseases Research Center, Tabriz University of Medical Sciences, Tabriz, Iran
AUTHOR
Hajar
Oghbaei
hoghbaei1988@gmail.com
6
Department of physiology, Faculty of medicine, Tabriz University of Medical Sciences, Tabriz, Iran
AUTHOR
Keivan
Mehri
keivanm20@gmail.com
7
Department of physiology, Faculty of medicine, Tabriz University of Medical Sciences, Tabriz, Iran
AUTHOR
Amir Mansour
Vatankhah
amvatankhah1972@gmail.com
8
Drug applied Research Center, Tabriz University of Medical Sciences, Tabriz, Iran.
AUTHOR
Rana
Keyhanmanesh
rkeyhanmanesh@gmail.com
9
Drug Applied Research Center, Tabriz University of Medical Sciences, Tabriz, Iran.
LEAD_AUTHOR
Adaramoye O, Akanni O, Adesanoye O, Labo-Popoola O, Olaremi O. 2012. Evaluation of toxic effects of metformin hydrochloride and glibenclamide on some organs of male rats. Niger J Physiol Sci, 27: 137-44.
1
Alipour MR, Khamaneh AM, Yousefzadeh N, Mohammad-nejad D, Soufi FG. 2013. Upregulation of microRNA-146a was not accompanied bydownregulation of pro-inflammatory markers in diabetic kidney. Mol Biol Rep,40:6477-6483.
2
Amaral S, Moreno AJ, Santos MS, Seiça R, Ramalho-Santos J. 2006. Effects of hyperglycemia on sperm and testicular cells of Goto-Kakizaki and streptozotocin-treated rat models for diabetes. Theriogenology, 66:2056-2067.
3
Aybek H, Aybek Z, Rota S, Şen N, Akbulut M. 2008. The effects of diabetes mellitus, age, and vitamin E on testicular oxidative stress. Fertil Steril, 90:755-760.
4
Badalzadeh R, Layeghzadeh N, Alihemmati A, Mohammadi M. 2015. Beneficial effect of troxerutin on diabetes-induced vascular damages in rat aorta: histopathological alterations and antioxidation mechanism. Int J Endocrinol Metab,13: e25969.
5
Ballester J, Muñoz MC, Domínguez J, Rigau T, Guinovart JJ, Rodríguez‐Gil JE. 2004. Insulin‐dependent diabetes affects testicular function by FSH‐and LH‐linked mechanisms. J Androl, 25:706-719.
6
Choi WS, Kwon OS, Cho SY, Paick JS, Kim SW. 2015. Effect of chronic administration of PDE5 combined with glycemic control on erectile function instreptozotocin‐induced diabetic Rats. J Sex Med,12:600-610.
7
ElangovanP, Jalaludeen A, Ramakrishnan R, Pari L. 2016. Protective Effect of Troxerutin on Nickel-Induced Testicular Toxicity in Wistar Rats. J Environ Patholtoxicol Oncol, 35:133-146.
8
FanS-h, Zhang Z-f, Zheng Y-l, Lu J, Wu D-m, Shan Q, Hu B, Wang YY. 2009. Troxerutin protects the mouse kidney from d-galactose-caused injury through anti-inflammation and anti-oxidation. Int Immunopharmacol,9:91-96.
9
Farajdokht F, Amani M, Bavil FM, Alihemmati A, Mohaddes G, Babri S. 2017. Troxerutin protects hippocampal neurons against amyloid beta-induced oxidative stress and apoptosis. EXCLI, 16:1081–1089.
10
Geetha R, Priya CS, Anuradha CV. 2017. Troxerutin abrogates mitochondrial oxidative stress and myocardial apoptosis in mice fed calorie-rich diet. Chembiol Interac, 278:74-83.
11
Geetha R, Yogalakshmi B, Sreeja S, Bhavani K, Anuradha CV. 2014. Troxerutin suppresses lipid abnormalities in the heart of high-fat–high-fructose diet-fed mice. Mol cellBiochem,387:123-134.
12
Jangir RN, Jain GC. 2014. Diabetes mellitus induced impairment of male reproductive functions: a review.Curr Diabetes Rev, 10:147-157.
13
Kanter M, Aktas C, Erboga M. 2012. Protective effects of quercetin against apoptosis and oxidative stress in streptozotocin-induced diabetic rat testis. Foodchem Toxicol, 50:719-725.
14
Karimi J, Goodarzi M, Tavilani H, Khodadadi I, Amiri I. 2011. Relationship between advanced glycation end products and increased lipid peroxidation in semen of diabetic men. Diabetes ResClin Pract,91:61-66.
15
Kianifard D, Sadrkhanlou RA, Hasanzadeh S. 2012. The ultrastructural changes of the sertoli and leydig cells following streptozotocin induced diabetes. Iran JBasic Med Sci, 15:623-635.
16
Keyhanmanesh R, Hamidian GR, Alipour MR, Ranjbar M,Oghbaei H. 2018. Protective effects of sodium nitrate against testicular apoptosis andspermatogenesis impairments in streptozotocin-induced diabetic male rats.Life Sciences, 211: 63–73.
17
Liu C-M, Ma J-Q, Lou Y. 2010. Chronic administration of troxerutin protects mouse kidney against D-galactose-induced oxidative DNA damage. Food Chem Toxicol, 48:2809-2817.
18
Lu J, Wu D-m, Zheng Z-h, Zheng Y-l, HuB, Zhang Z-f. 2011. Troxerutin protects against high cholesterol-induced cognitive deficits in mice. Brain,134:783-797.
19
Mokhtari B, Badalzadeh R, Alihemmati A, Mohammadi M. 2015. Phosphorylation of GSK-3β and reduction of apoptosis as targets of troxerutin effect on reperfusion injury of diabetic myocardium. Eur JPharmacol, 765:316-321.
20
Naderi R, Mohaddes G, Mohammadi M, Ghaznavi R, Ghyasi R, Vatankhah AM. 2015. Voluntary Exercise Protects Heart from Oxidative Stress in Diabetic Rats. Adv Pharm Bull, 5: 231-236.
21
Nakayama Y, Yamamoto T, Abe S-I. 2004. IGF-I, IGF-II and insulin promote differentiation of spermatogonia to primary spermatocytes in organ culture of newt testes. Int J Develop Biol,43:343-347.
22
Oghbaei H, Alipour MR, Hamidian GR, Ahmadi M, Ghorbanzadeh V, Keyhanmanesh R. 2018. Two months sodium nitrate supplementation alleviates testicular injury in streptozotocin-induced diabetic male rats. Exp Physiol, 103: 1603-1617.
23
Olfati A, Moghadam GH, Baradaran B, Hamidian GH. 2018. The effect of estradiol benzoate and FSH on hormonal levels and stereology structure of testis in Ghezel lambs treated with Tamoxifen citrate. Revue Med Vet, 169: 58-64.
24
Oliveira P, Alves M, Rato L, Laurentino S, Silva J, Sa R, Barros A, Sousa M, Carvalho RA, Cavaco JE, Socorro S. 2012. Effect of insulin deprivation on metabolism and metabolism-associated gene transcript levels of in vitro cultured human Sertoli cells. Biochim Biophys Acta,1820:84-89.
25
Perumal E, Jalaludeen AM, Ramakrishnan R, Amutha K, Pari L. 2017. In vivo andIn vitro antioxidant activity of troxerutin on Nickel induced toxicity in experimental Rats.Iran J Pharm Res, in press.
26
Pourmemar E, Majdi A, Haramshahi M, Talebi M, Karimi P, Sadigh-Eteghad S. 2017. Intranasal cerebrolysin attenuates learning and memory impairments in D-galactose-induced senescence in mice. Exp Gerontol, 87:16-22.
27
Sampath S, Karundevi B. 2014. Effect of troxerutin on insulin signaling molecules in the gastrocnemius muscle of high fat and sucrose-induced type-2 diabetic adult male rat. Mol Cell Biochem,395:11-27.
28
Shokri S, Aitken RJ, Abdolvahhabi M, Abolhasani F, Ghasemi FM, Kashani I, Ejtemaeimehr S, Ahmadian S, Minaei B, Naraghi MA, BarbarestaniM. 2010. Exercise and supraphysiological dose of nandrolone deconoate increase apoptosis in spermatogenic cells. Basic Clin Pharmacol Toxicol, 106: 324-330.
29
Vinothkumar R, Kumar RV, Sudha M, Viswanathan P, Balasubramanian T, Nalini N. 2014. Modulatory effect of troxerutin on biotransformingenzymes and preneoplasic lesions induced by 1, 2-dimethylhydrazine in rat colon carcinogenesis. Expmol Pathol, 96:15-26.
30
Wang H, Yang L-L, Ji Y-L, Chen Y-H, Hu J, Zhang C, Zhang J, Xu DX . 2016. Different fixative methods influence histological morphology and TUNEL staining in mouse testes. Reprod Toxicol, 60:53-61.
31
Yu Y, ZhengG. 2017. Troxerutin protects against diabetic cardiomyopathy through NF‑κB/AKT/IRS1 in a rat model of type 2 diabetes. Mol Med Rep,15:3473-3478.
32
Zavvari Oskuye Z, Mirzaei Bavil F, Hamidian GR, Mehri K, Qadiri A, Ahmadi M, Ogbaei H, Vatankhah AM, Keyhanmanesh R. 2019. The effect of troxerutin on male fertility in prepubertal type 1 diabetic male rats. Iran J Basic Med Sci, 22:197-205.
33
Zhang Z, Wang X, Zheng G, Shan Q, Lu J, Fan S, Sun C, Wu D, Zhang C, Su W, Sui J, Zheng Y. 2017. Troxerutin attenuates enhancement of hepatic gluconeogenesis by inhibiting NOD activation-mediated inflammation in high-fat diet-treated mice. Int JMol Sci,18:31-46.
34
Zhao Y, Tan Y, Dai J, Li B, Guo L, Cui J, Wang G, Shi X, Zhang X, Mellen N, Li W, Cai L.2011. Exacerbation of diabetes-induced testicular apoptosis by zinc deficiency is most likely associated with oxidative stress, p38 MAPK activation, and p53 activation in mice. Toxicol Lett, 200:100-106.
35
ORIGINAL_ARTICLE
Cytotoxic and anti-proliferative effects of Rosa beggeriana Schrenk extracts on human liver and breast cancer cells
Objective: Rosa beggeriana Schrenk has been consumed in Iranian traditional medicine. In contrary to its close species (e.g. R. canina), there is no data on its medicinal properties. Therefore, we explored possible cytotoxic effects of R. beggeriana against two cancer cell lines. Materials and Methods: The cytotoxic and anti-proliferative effects of R. beggeriana ethanolic and aqueous extracts on human liver cancer cells (LCLPI 11), breast cancer cells (MCF-7) and fibroblast-like cells (HSkMC) were evaluated by MTT, BrdU and TUNEL assays. Results: Following 48 h, IC50 values for LCL-PI11 and MCF-7 cells were found to be 3.9 and 4.2 μg/mL for aqueous extract, and 2.3 and 2.7 μg/mL for ethanolic extract, respectively. BrdU assay data verified the MTT results and showed that both extracts inhibit cell proliferation as much as 5-fluorouracil does (p<0.05). The ethanolic extract had a more marked inhibitory effect compared to the aqueous extract (p<0.05). Besides both extracts were less effective against HSKMC cells compared to other cells lines. TUNEL assay results demonstrated that following 48 h, the aqueous extract induced about 19 and 24% apoptotic death in the LCL-PI 11 and MCF-7 cells, respectively (p<0.05). While at the same time, the ethanolic extract was more potent and caused about 83 and 91% death in the LCL-PI 11 and MCF-7 cells, respectively (p<0.05). Conclusion: These data indicate that both extracts have anti-proliferative and pro-apoptotic activities on these two cancer cell lines and these effects were more pronounced then their activities against normal cells. Also, the ethanolic extract was more potent than the aqueous extract. Further researches are necessary for finding and isolating effective anticancer ingredient of R. beggeriana.
https://ajp.mums.ac.ir/article_12780_8e4c2d55093c718d97d46211abc7985e.pdf
2019-07-01
386
395
10.22038/ajp.2019.12780
Rosa beggeriana Schrenk
liver cancer cell
Breast Cancer Cell
Cytotoxicity
Apoptosis
Ozra
Zarei
azrazareilar@gmail.com
1
Department of Biotechnology, Graduate University of Advanced Technology, Kerman, Iran.
AUTHOR
Mohammad Mehdi
Yaghoobi
m.yaghoobi@kgut.ac.ir
2
Department of Biotechnology, Institute of Science and High Technology and Environmental Sciences, Graduate University of Advanced Technology Kerman, Iran.
LEAD_AUTHOR
Amiri MS, Joharchi MR. 2013. Ethnobotanical investigation of traditional medicinal plants commercialized in the markets of Mashhad, Iran. Avicenna J Phytomed, 3: 254-271.
1
Atanasov AG, Waltenberger B, Pferschy-Wenzig EM, Linder T, Wawrosch C, Uhrin P, Temml V, Wang L, Schwaiger S, Heiss EH, Rollinger JM, Schuster D, Breuss JM, Bochkov V, Mihovilovic MD, Kopp B, Bauer R, Dirsch VM, Stuppner H. 2015. Discovery and resupply of pharmacologically active plant-derived natural products: A review. Biotechnol Adv, 33: 1582-1614.
2
Chrubasik C, Roufogalis BD, Muller-Ladner U, Chrubasik S. 2008. A systematic review on the Rosa canina effect and efficacy profiles. Phytother Res, 22: 725-733.
3
Dai W, Gao Q, Qiu J, Yuan J, Wu G, Shen G. 2015. Quercetin induces apoptosis and enhances 5-FU therapeutic efficacy in hepatocellular carcinoma. Tumor Biol, 5: 6307–6313.
4
Deliorman Orhan D, Hartevioglu A, Kupeli E, Yesilada E. 2007. In vivo anti-inflammatory and antinociceptive activity of the crude extract and fractions from Rosa canina L. fruits. J Ethnopharmacol, 112: 394-400.
5
Duo J, Ying GG, Wang GW, Zhang L. 2012. Quercetin inhibits human breast cancer cell proliferation and induces apoptosis via Bcl-2 and Bax regulation. Mol Med Rep, 5: 1453–1456.
6
Falahi E, Farhadi J, Abdollahpoor F, Ghasemi M, Kakai Z, Karimi Z. 2014. Antioxidant and cytotoxic effects of aqueous and ethanolic extracts of R.canina against U937 cell line. Yafteh, 17: 15-24.
7
Fujii T, Saito M, 2009. Inhibitory effect of quercetin isolated from rose hip (Rosa canina L.) against melanogenesis by mouse melanoma cells. Biosci Biotechnol Biochem, 73: 1989-1993.
8
GLOBOCAN 2018 at: https://gco.iarc.fr/today/data/factsheets/cancers/39-All-cancers-fact-sheet.pdf
9
Jimenez S, Gascon S, Luquin A, Laguna M, Ancin-Azpilicueta C, Rodriguez-Yoldi MJ. 2016. Rosa canina extracts have antiproliferative and antioxidant effects on caco-2 human colon cancer. PLoS One, 11: e0159136.
10
Jimenez S, Jimenez-Moreno N, Luquin A, Laguna M, Rodriguez-Yoldi MJ, Ancin-Azpilicueta C. 2017. Chemical composition of rosehips from different Rosa species: an alternative source of antioxidants for the food industry. Food Addit Contam Part A Chem Anal Control Expo Risk Assess, 34:1121-1130.
11
Lattanzio F, Greco E, Carretta D, Cervellati R, Govoni P, Speroni E. 2011. In vivo anti-inflammatory effect of Rosa canina L. extract. J Ethnopharmacol, 137: 880-885.
12
McCloud TG, 2010. High throughput extraction of plant, marine and fungal specimens for preservation of biologically active molecules. Molecules, 15: 4526-4563.
13
Nadpal JD, Lesjak MM, Sibul FS, Anackov GT, Cetojevic-Simin DD, Mimica-Dukic NM, Beara IN. 2016. Comparative study of biological activities and phytochemical composition of two rose hips and their preserves: Rosa canina L. and Rosa arvensis Huds. Food Chem, 192: 907-914.
14
Newman DJ, Cragg GM. 2016. Natural Products as Sources of New Drugs from 1981 to 2014. J Nat Prod, 79: 629-661.
15
Rajkapoor B, Sankari M, Sumithra M, Anbu J, Harikrishnan N, Gobinath M, Suba V, Balaji R. 2007. Antitumor and cytotoxic effects of Phyllanthus polyphyllus on Ehrlich ascites carcinoma and human cancer cell lines. Biosci Biotechnol Biochem, 71: 2177-2183.
16
Roman I, Stanila A, Stanila S. 2013. Bioactive compounds and antioxidant activity of Rosa canina L. biotypes from spontaneous flora of Transylvania. Chem Cent J, 7:73
17
Tariq A, Sadia S, Pan K, Ullah I, Mussarat S, Sun F, Abiodun OO, Batbaatar A, Li Z, Song D, Xiong Q, Ullah R, Khan S, Basnet BB, Kumar B, Islam R, Adnan M. 2017. A systematic review on ethnomedicines of anti-cancer plants. Phytotherapy Research, 31: 202-264.
18
Tumbas, V. T., J. M. Canadanovic-Brunet, D. D. Cetojevic-Simin, G. S. Cetkovic, S. M. Ethilas, Gille L. 2012. Effect of rosehip (Rosa canina L.) phytochemicals on stable free radicals and human cancer cells. J Sci Food Agric, 92: 1273-1281.
19
WHO (https://www.who.int/news-room/fact sheets/detail/the-top-10-causes-of-death).
20
Zhou Y, Zheng J, Li Y, Xu DP, Li S, Chen YM, Li HB. 2016. Natural Polyphenols for Prevention and Treatment of Cancer. Nutrients, 8: 515.
21
ORIGINAL_ARTICLE
Dryopteris filix-mas (L.) Schott ethanolic leaf extract and fractions exhibited profound anti-inflammatory activity
Objective: Dryopteris filix-mas (D. filix-mas) (L.) Schott, (Dryopteridaceae) is used in traditional medicine, particularly in the Southern parts of Nigeria for the treatment of inflammation, rheumatoid arthritis, wounds and ulcers. In this study, we evaluated the anti-inflammatory activity of its ethanolic leaf extract and fractions. Materials and Methods: The ethanolic leaf extract and fractions were screened for anti-inflammatory properties using egg-albumin-induced paw edema, xylene-induced topical ear edema, formaldehyde-induced arthritis and ulcerogenic models. The ethyl acetate most promising vacuum liquid chromatography fraction (VLC-E7) was purified using size exclusion chromatography technique (Sephadex LH-20) and its structure was elucidated using nuclear magnetic resonance (NMR) and mass spectrometry. Total phenolic and flavonoid contents were also determined. Results: From the study, ethyl acetate and butanol fractions elicited better anti-inflammatory activities in egg-albumin-induced paw edema, formaldehyde-induced arthritis and xylene-induced topical ear edema. The ethanol extract, ethyl acetate and butanol fractions were non-ulcerogenic at 200 and 400 mg/kg. The compound isolated from Sephadex fraction (SPH-E6) was quercetin-3-O-α-L-rhamnopyranoside. Conclusion: Results of this study justify the ethnomedicinal use of D. filix-mas leaf for treatment of inflammation and rheumatoid arthritis. We suggest that D. filix-mas could be a prospective anti-inflammatory agent with no gastric irritation side effect, due to its bioactive component, quercetin-3-O-α-L-rhamnopyranoside.
https://ajp.mums.ac.ir/article_12784_de95ebdc899610d475d7fc3fe04b8c8f.pdf
2019-07-01
396
409
10.22038/ajp.2019.12784
Dryopteris filix-mas
Anti-inflammatory
Rheumatoid arthritis
Quercetin-3O-αL-rhamnopyranoside
Non-ulcerogenic
Earnest
Erhirhie
erhirhieochuko@yahoo.com
1
Department of Pharmacology and Toxicology, Faculty of Pharmaceutical Sciences, Nnamdi Azikiwe University, Awka, Nigeria.
LEAD_AUTHOR
Chika
Emeghebo
emecncos2sin4@yahoo.com
2
Department of Pharmacology and Toxicology, Faculty of Pharmaceutical Sciences, Nnamdi Azikiwe University, Awka, Nigeria
AUTHOR
Emmanuel
Ilodigwe
eilodigwe7@gmail.com
3
Department of Pharmacology and Toxicology, Faculty of pharmaceutical sciences, Nnamdi Azikiwe University, Awka
AUTHOR
Daniel
Ajaghaku
danlotaaja@yahoo.com
4
Department of Pharmacology, Faculty of Pharmaceutical Sciences, Enugu State University of Science and Technology, Enugu State, Nigeria.
AUTHOR
Blessing
Umeokoli
blessingumeokoli@gmail.com
5
Department of Pharmaceutical and Medicinal Chemistry, Faculty of Pharmaceutical Sciences, Nnamdi Azikiwe University, Awka
AUTHOR
Peter
Eze
ezep2004@hotmail.com
6
Department of Pharmaceutical Biology and Biotechnology, Faculty of Pharmaceutical Sciences, Nnamdi Azikiwe University, Awka, Nigeria.
AUTHOR
Kenneth
Ngwoke
kg.ngwoke@unizik.edu.ng
7
Department of Pharmaceutical and Medicinal Chemistry Faculty of Pharmaceutical Sciences, Nnamdi Azikiwe University, Awka, Nigeria.
AUTHOR
Festus
Okoye
fb.okoye@unizik.edu.ng
8
Department of Pharmaceutical and Medicinal Chemistry Faculty of Pharmaceutical Sciences, Nnamdi Azikiwe University, Awka, Nigeria.
AUTHOR
Alam B, Akter A, Parvin N, Pia RS, Akter S, Chowdhury J, Sifath-E-Jahan K, Haque E. 2013. Antioxidant, analgesic and anti-inflammatory activities of the methanolic extract of Piper betle leaves. Avicenna J Phytomed, 3: 112-125.
1
Ajaghaku DL, Ilodigwe EE, Okonta MJ, Ogue CO, Okafor MA, Igboeme SO. 2013. Mechanism of anti-inflammatory activity of the leaf extract and fractions of Millettia aboensis. IRJP, 4:54-59.
2
Ajaghaku DL, Obasi O, Umeokoli BO, Ogbuatu P, Nworu CS, Ilodigwe EE, Okoye FBC. 2017. In vitro and in vivo antioxidant potentials of Alchornea floribunda leaf extract, fractions and isolated bioactive compounds. Avicenna J Phytomed, 7: 80-92.
3
Azubike NC, Okwuosa CN, Achukwu PU, Maduka TC, Chike O. 2015. Acute toxicity and histopathological effects of crude aqueous extract of Jatropha curcas leaves in mice. Res J Med Plant, 9: 340-346.
4
Bafor EE, Omokaro WO, Uwumarongie OH, Elvis-Offiah UB, Omoruyi O, Viegelmann CV, Edrada-Ebel R. 2017. Dryopteris filix-mas (Dryopteridaceae) leaves inhibit mouse uterine activity. JOMPED, 1: 1 -12.
5
Beber AP, de Souza P, Boeing T, Somensi LB, Mariano LN, Cury BJ, Burci LM, de Silva CB, Simionatto E, De Andrade SF, da Silva LM. 2018. Constituents of leaves from Bauhinia curvula Benth. exert gastroprotective activity in rodents: role of quercitrin and kaempferol. Inflammopharmacology, 26: 539-550.
6
Chatterjee A, Bandyopadhyay SK. 2014. Herbal remedy: An alternate therapy of nonsteroidal anti-Inflammatory drug induced gastric ulcer healing. Ulcer, 2014:13.
7
Díaz RJO, Rocha GNE, Gallegos IJA, Moreno JMR, González LRF. 2016. Gastroprotective Activities of Buddleja scordioides-Role of Polyphenols against Inflammation. J Chem Biol Ther, 2: 1-8.
8
Erhirhie EO, Ilodigwe EE, Ihekwereme CP. 2018. Ficus Sycomorus L (Moraceae): A review on its Phytopharmacology and toxicity profile. Discovery Phytomedicine, 5: 64-71.
9
Ezeja MI, Yusuf N, Omeh SO, Ijeoma HU. 2015. Antiinflammatory and antioxidant activities of the methanolic leaf extract of Cissus aralioides. Am J Pharmacol Sci, 3: 1 - 6.
10
Ghaly NS, Melek FR, Abdelwahed NAM. 2010. Flavonoids from Albizia chinensis of Egypt. Rev. Latinoamer Quím, 38: 153-158.
11
Gretzer B, Maricic N, Respondek M, Schuligoli R, Peskar BM. 2001. Effects of specific inhibition of cyclooxygenase-2 in the rat stomach with normal mucosa and after acid challenge. Br J Pharamacol, 132: 1565-1573.
12
Hajhashemi V, Klooshani V. 2013. Antinociceptive and anti-inflammatory effects of Urtica dioica leaf extract in animal models. Avicenna J Phytomed, 3:193-200.
13
Ilavarasana R, Mallikab M, Venkataramanc S. 2005. Anti-inflammatory and antioxidant activities of Cassia fistula linn bark extract. Afr J Tradit Complement Altern Med,2: 70 – 85.
14
Jin JH, Kim JS, Kang SS, Son KH, Chang HW, Kim HP. 2010. Anti-inflammatory and anti-arthritic activity of total flavonoids of the roots of Sophora flavescens. J Ethnopharmacol, 127: 589–595.
15
José M.B, Márcia R.P, Marcelo D.M, Marcelo S.S, Karla VBL, Emídio VL, Ivana MF, Orlando ST. 2006. Anti-inflammatory activity of alkaloids: A twenty-century review. Rev Bras Farmacogn, 16: 109-139.
16
Mei FS, Jong YC. 2012. Potential applications of euphorbia hirta in pharmacology. drug discovery research in pharmacognosy. www.intechopen.com. 165-180. Accessed October 22nd, 2018.
17
Minaiyan M, Sajjadi SE, Amini K. 2018. Antiulcer effects of Zataria multifloraBoiss. on indomethacin-induced gastric ulcer in rats. Avicenna J Phytomed, 8: 408-415.
18
Moke EG, Ilodigwe EE, Erhirhie OE. 2015. Evaluation of the ulcerogenic potential of the aqueous extract of Spondias mombinand Custus afer. IJAPBC, 4: 282-286.
19
Murugesan D, Deviponnuswamy R. 2014. Potent anti-inflammatory medical plant-a review. Int J Pharm Pharm Sci, 6: 43-49.
20
Nworu CS, Nwuke HC, Akah PA, Okoye FBC, Esimone CO. 2012. Extracts of Ficus exasperate leaf inhibit topical and systemic inflammation in rodents and suppress LPS-induced expression of mediators of inflammation in macrophages. J Immunotoxicol, 10: 302-310.
21
Okigbo, RN, Anuagasi CL, Amadi JE. 2009. Advances in selected medicinal and aromatic plants indigenous to Africa. J Med Plants Res, 3: 86-95.
22
Okoye NN, Ajaghaku DL, Okeke HN, Ilodigwe EE, Nworu CS, Okoye FBC. 2014. Beta-amyrin and alpha-amyrin acetate isolated from the stem bark of Alstonia booneidisplayed profound anti-inflammatory activity. Pharm Biol, 52: 1478 – 1486.
23
Qnais, E, Raad D, Bseiso Y. 2014. Analgesic and anti-Inflammatory effects of an extract and flavonoids from Artemisia Herba-Albaand their mechanisms of action. Neurophysiol, 46: 238-246.
24
Randhawa MA. 2009. Calculation of LD50 value from the method of Miller and Tainter, 1944. J Ayub Med CollAbbottabad, 21: 1-3.
25
Ruckmani A, Vinayak M, Vijayashree R, Arunkumar R, Konda VR, Prabhu R, Madhavi E, Devi S. 2018. Anti-rheumatoid activity of ethanolic extract of Sesamum indicum seed extract in Freund's complete adjuvant induced arthritis in Wistar albino rats. JTCM, 8: 377-386.
26
Sekendar AM, Mostafa K, Raihan MO, Rahman MK, Hossain MA, Alam MS. 2012. Antioxidant and cytotoxic activities of methanolic extract of Dryopteris filix-mas (L.) Schott Leaves”. Int J Drug Dev Res, 4: 223-229.
27
Shrestha B, Ravi P, Talib H. 2014. Anti-inflammatory activity of ethnobotanical plants used as traditional medicine: A review. Res Rev J Bot Sci, 3: 8-18.
28
Soare LC, Ferdes M, Stefanov S, Denkova Z, Nicolova R, Denev P, Bejan C, Paunescu A. 2012. Antioxidant activity, polyphenols content and antimicrobial activity of several native Pteridophytes of Romania. Notulae Botanicae. Horti Agrobotanici Cluj-Napoca, 40: 53-57.
29
Tae-Seong L, Hee-Jeong M, Young-Soo B. 2015. Phenolic Glycosides from Cercidiphyllum japonicum leaves. J Korean Wood Sci Technol, 43: 591-599.
30
Urban J, Tauchen J, Langrova I, Kokoska L. 2014. In vitro motility inhibition effect of Czech medicinal plant extracts on Chabertia ovina adults. J Anim Plant Sci, 21: 3293-3302.
31
Uwumarongie HO, Enike MA, Bafor EE. 2016. Pharmacognostic evaluation and gastrointestinal activity of Dryopteris filix-mas(L.) schott (Dryopteridaceae). Ew J Herbal Chem Pharmacol Res, 2: 19 – 25.
32
Yadav RNS, Agarwala M. 2011. Phytochemical analysis of some medicinal plants. J phytol, 3: 10-14.
33