Volume 18, Issue 9 (September 2020)                   IJRM 2020, 18(9): 733-746 | Back to browse issues page

XML Persian Abstract Print

Download citation:
BibTeX | RIS | EndNote | Medlars | ProCite | Reference Manager | RefWorks
Send citation to:
Eini F, Joharchi K, Azizi Kutenaei M, Mousavi P. Improvement in the epigenetic modification and development competence in PCOS mice oocytes by hydro-alcoholic extract of Nigella sativa during in-vitro maturation: An experimental study. IJRM 2020; 18 (9) :733-746
URL: http://ijrm.ir/article-1-1430-en.html
Improvement in the epigenetic modification and development competence in PCOS mice oocytes by hydro-alcoholic extract of Nigella sativa during in-vitro maturation: An experimental study
Fatemeh Eini * 1, Khojasteh Joharchi2 , Maryam Azizi Kutenaei3 , Pegah Mousavi4
1- Fertility and Infertility Research Center, Hormozgan University of Medical Sciences, Bandar Abbas, Iran. , feini13@gmail.com
2- Department of Pharmacology, School of Medicine, Shahid Beheshti University of Medical Sciences, Tehran, Iran.
3- Fertility and Infertility Research Center, Hormozgan University of Medical Sciences, Bandar Abbas, Iran.
4- Fertility and Infertility Research Center, Hormozgan University of Medical Sciences, Bandar Abbas, Iran. Department of Medical Genetics, Faculty of Medicine, Hormozgan University of Medical Sciences, Bandar Abbas, Iran.
Abstract:   (1866 Views)
Background: Nigella Sativa (NS) and its active component, thymoquinone, have beneficial protective effects on experimental animal models of polycystic ovary syndrome (PCOS) and different human diseases.
Objective: The present study aimed to investigate the effects of NS hydro-alcoholic extract (NSE) on the oocyte quality of PCOS mice during in vitro maturation.
Materials and Methods: For induction of PCOS, 40 prepubertal 21-days old female B6D2F1 mice (18-22 g body weight) received subcutaneous dehydroepiandrosterone daily. After validation of the model, germinal vesicle-stage oocytes of superovulated mice were collected and placed in the culture medium containing different concentrations (0, 1, 50, and 100 μg/ml) of NSE. For the measurement of developmental competency, some mature oocytes were fertilized with epididymal spermatozoa. Other mature oocytes were assessed for oxidative stress. Also, some mRNA expression levels involved in oocyte maturation and epigenetic modification were evaluated.
Results: The 50 μg/ml NSE treated group showed significantly higher r ates o f maturation, f ertilization, and blastocyst formation in comparison with both control and PCOS groups. A high level of glutathione concentration and glutathione peroxidase mRNA expression, besides a low level of reactive oxygen species content all, were observed in oocytes treated with 50 μg/ml NSE, indicating the modification of oxidative statue. Furthermore, the oocytes in the 50 μg/ml-treated group showed an upregulation of mRNA expression in epigenetic-related genes (Dnmt1 and Hdac1) and maternally derived genes (Mapk and Cdk1), correspondingly downregulation of cyclooxygenase2 mRNA expression, in comparison to other groups.
Conclusion: The results of this study indicated that 50 μg/ml NSE improves oocyte maturation, oxidative statues and epigenetic modifications. These may be the all reasons for the developmental competency in the control and PCOS mice oocytes.
Keywords: Epigenetic modification, In-vitro maturation, Nigella sativa, Oxidative stress, Polycystic ovary syndrome.
Full-Text [PDF 1000 kb]   (755 Downloads) |   |   Full-Text (HTML)  (374 Views)  
Type of Study: Original Article | Subject: Reproductive Biology
References
1. Zhao JZ, Zhou W, Zhang W, Ge HS, Huang XF, Lin JJ. In vitro maturation and fertilization of oocytes from unstimulated ovaries in infertile women with polycystic ovary syndrome. Fertil Steril 2009; 91: 2568-2571. [DOI:10.1016/j.fertnstert.2008.03.059] [PMID]
2. Agarwal A, Durairajanayagam D, Du Plessis SS. Utility of antioxidants during assisted reproductive techniques: an evidence based review. Reprod Biol Endocrinol 2014; 12: 112-130. [DOI:10.1186/1477-7827-12-112] [PMID] [PMCID]
3. Choe C, Shin YW, Kim EJ, Cho SR, Kim HJ, Choi SH, et al. Synergistic effects of glutathione and β-mercaptoethanol treatment during in vitro maturation of porcine oocytes on early embryonic development in a culture system supplemented with L-cysteine. J Reprod Dev 2010; 56: 575-582. [DOI:10.1262/jrd.09-214H] [PMID]
4. Wang X, Falcone T, Attaran M, Goldberg JM, Agarwal A, Sharma RK. Vitamin C and vitamin E supplementation reduce oxidative stress-induced embryo toxicity and improve the blastocyst development rate. Fertil Steril 2002; 78: 1272-1277. [DOI:10.1016/S0015-0282(02)04236-X]
5. Nikmard F, Hosseini E, Bakhtiyari M, Ashrafi M, Amidi F, Aflatoonian R. Effects of melatonin on oocyte maturation in PCOS mouse model. Anim Sci J 2017; 88: 586-592. [DOI:10.1111/asj.12675] [PMID]
6. Goyal SN, Prajapati CP, Gore PR, Patil CR, Mahajan UB, Sharma C, et al. Therapeutic potential and pharmaceutical development of thymoquinone: A multitargeted molecule of natural origin. Front Pharmacol 2017; 8: 656-674. [DOI:10.3389/fphar.2017.00656] [PMID] [PMCID]
7. Chehl N, Chipitsyna G, Gong Q, Yeo CJ, Arafat HA. Anti-inflammatory effects of the Nigella sativa seed extract, thymoquinone, in pancreatic cancer cells. HPB 2009; 11: 373-381. [DOI:10.1111/j.1477-2574.2009.00059.x] [PMID] [PMCID]
8. Ismail M, Al-Naqeep G, Chan KW. Nigella sativa thymoquinone-rich fraction greatly improves plasma antioxidant capacity and expression of antioxidant genes in hypercholesterolemic rats. Free Radic Biol Med 2010; 48: 664-672. [DOI:10.1016/j.freeradbiomed.2009.12.002] [PMID]
9. Sharma NK, Ahirwar D, Jhade D, Gupta S. Medicinal and phamacological potential of nigella sativa: a review. Ethnobotanical Review 2009; 13: 946-955.
10. Barrera AD, García EV, Hamdi M, Sanchez-Calabuig MJ, Lopez-Cardona AP, Balvís NF, et al. Embryo culture in presence of oviductal fluid induces DNA methylation changes in bovine blastocysts. Reproduction 2017; 154: 1-12. [DOI:10.1530/REP-16-0651] [PMID]
11. Uysal F, Akkoyunlu G, Ozturk S. Dynamic expression of DNA methyltransferases (DNMTs) in oocytes and early embryos. Biochimie 2015; 116: 103-113. [DOI:10.1016/j.biochi.2015.06.019] [PMID]
12. Ma P, Pan H, Montgomery RL, Olson EN, Schultz RM. Compensatory functions of histone deacetylase 1 (HDAC1) and HDAC2 regulate transcription and apoptosis during mouse oocyte development. Proc Nati Acad Sci USA 2012; 109: E481-E489. [DOI:10.1073/pnas.1118403109] [PMID] [PMCID]
13. Racedo SE, Wrenzycki C, Lepikhov K, Salamone D, Walter J, Niemann H. Epigenetic modifications and related mRNA expression during bovine oocyte in vitro maturation. Reprod Fertil Dev 2009; 21: 738-748. [DOI:10.1071/RD09039] [PMID]
14. Salhab M, Dhorne‐Pollet S, Auclair S, Guyader‐Joly C, Brisard D, Dalbies‐Tran R, et al. In vitro maturation of oocytes alters gene expression and signaling pathways in bovine cumulus cells. Mol Reprod Dev 2013; 80: 166-182. [DOI:10.1002/mrd.22148] [PMID]
15. Eini F, Ghaffari Novin M, Joharchi K, Hosseini A, Nazarian H, Piryaei A, et al. Intracytoplasmic oxidative stress reverses epigenetic modifications in polycystic ovary syndrome. Reprod Fertil Dev 2017; 29: 2313-2323. [DOI:10.1071/RD16428] [PMID]
16. Parandin R, Yousofvand N, Ghorbani R. The enhancing effects of alcoholic extract of Nigella sativa seed on fertility potential, plasma gonadotropins and testosterone in male rats. Iran J Reprod Med 2012; 10: 355-362.
17. Eini F, Bidadkosh A, Nazarian H, Piryaei A, Ghaffari Novin M, Joharchi K. Thymoquinone reduces intracytoplasmic oxidative stress and improves epigenetic modification in polycystic ovary syndrome mice oocytes, during in-vitro maturation. Mol Reprod Dev 2019; 86: 1053-1066. [DOI:10.1002/mrd.23222] [PMID]
18. Ubaldi F, Rienzi L. Morphological selection of gametes. Placenta 2008; 29 (Suppl.): 115-120. [DOI:10.1016/j.placenta.2008.08.009] [PMID]
19. Wang F, Tian X, Zhang L, He C, Ji P, Li Y, et al. Beneficial effect of resveratrol on bovine oocyte maturation and subsequent embryonic development after in vitro fertilization. Fertil Steril 2014; 101: 577-586. [DOI:10.1016/j.fertnstert.2013.10.041] [PMID]
20. Diaz FJ, O'brien MJ, Wigglesworth K, Eppig JJ. The preantral granulosa cell to cumulus cell transition in the mouse ovary: development of competence to undergo expansion. Dev Biol 2006; 299: 91-104. [DOI:10.1016/j.ydbio.2006.07.012] [PMID]
21. Zimmermann M. Ethical guidelines for investigations of experimental pain in conscious animals. Pain 1983; 16: 109-110. [DOI:10.1016/0304-3959(83)90201-4]
22. Hara M, Abe Y, Tanaka T, Yamamoto T, Okumura E, Kishimoto T. Greatwall kinase and cyclin B-Cdk1 are both critical constituents of M-phase-promoting factor. Nat Commun 2012; 3: 1059-1067. [DOI:10.1038/ncomms2062] [PMID] [PMCID]
23. Salarinia R, Rakhshandeh H, Oliaee D, Ghasemi SG, Ghorbani A. Safety evaluation of Phytovagex, a pessary formulation of Nigella sativa, on pregnant rats. Avicenna J Phytomed 2016; 6: 117-123.
24. Al-Seeni MN, El Rabey HA, Al-Hamed AM, Zamazami MA. Nigella sativa oil protects against tartrazine toxicity in male rats. Toxicol Rep 2017; 5: 146-155. [DOI:10.1016/j.toxrep.2017.12.022] [PMID] [PMCID]
25. Elshama SS, Shehab GM, El-Kenawy AE, Osman H-EH, Farag MM. Role of Nigella Sativa Seeds on modulation testicular toxicity of colchicine repeated use in adult albino rats. Life Sci J 2013; 10: 1629-1639.
26. Rahman SA, Shaik Dawood NF, Basha SS, Kamarzaman S. Protective effect of black seed Nigella sativa (L.) against cyclophosphamide-induced toxicity on reproductive and acrosomal function in mice. Middle East J Sci Res 2013; 17: 955-964.
27. Kamarzaman S, Shaban M, Abdul Rahman S. The prophylactic effect of Nigella sativa against cyclophosphamide in the ovarian follicles of matured adult mice: a preliminary study. J Anim Plant Sci 2014; 24: 81-88.
28. Zhang DX, Park WJ, Sun SC, Xu YN, Li YH, Cui XS, et al. Regulation of maternal gene expression by MEK/MAPK and MPF signaling in porcine oocytes during in vitro meiotic maturation. J Reprod Dev 2011; 57: 49-56. [DOI:10.1262/jrd.10-087H] [PMID]
29. Zare Z, Masteri Farahani R, Salehi M, Piryaei A, Ghaffari Novin M, Fadaei Fathabadi F, et al. Effect of L-carnitine supplementation on maturation and early embryo development of immature mouse oocytes selected by brilliant cresyle blue staining. J Assist Reprod Genet 2015; 32: 635-643. [DOI:10.1007/s10815-015-0430-5] [PMID] [PMCID]
30. Abdelrazek HMA, Kilany OE, Muhammad MAA, Tag HM, Abdelazim AM. Black Seed thymoquinone improved insulin secretion, hepatic glycogen storage, and oxidative stress in streptozotocin-induced diabetic male wistar rats. Oxid Med Cell Longev 2018; 2018: 8104165. [DOI:10.1155/2018/8104165] [PMID] [PMCID]
31. Busari AA, Adejare AA, Shodipe AF, Oduniyi OA, Ismail-Badmus KB, Oreagba IA. Protective but non-synergistic effects of nigella sativa and vitamin E against cisplatin-induced renal toxicity and oxidative stress in wistar rats. Drug Res 2018; 68: 696-703. [DOI:10.1055/a-0626-7003] [PMID]
32. Lian HY, Gao Y, Jiao GZ, Sun MJ, Wu XF, Wang TY, et al. Antioxidant supplementation overcomes the deleterious effects of maternal restraint stress-induced oxidative stress on mouse oocytes. Reproduction 2013; 146: 559-568. [DOI:10.1530/REP-13-0268] [PMID]
33. Alenzi FQ, El-Bolkiny YE, Salem ML. Protective effects of Nigella sativa oil and thymoquinone against toxicity induced by the anticancer drug cyclophosphamide. Br J Biomed Sci 2010; 67: 20-28. [DOI:10.1080/09674845.2010.11730285] [PMID]
34. Arif M, Thakur SC, Datta K. Implication of thymoquinone as a remedy for polycystic ovary in rat. Pharm Biol 2016; 54: 674-685. [DOI:10.3109/13880209.2015.1072565] [PMID]
35. Luchetti CG, Mikó E, Szekeres-Bartho J, Paz DA, Motta AB. Dehydroepiandrosterone and metformin modulate progesterone-induced blocking factor (PIBF), cyclooxygenase 2 (COX2) and cytokines in early pregnant mice. J Steroid Biochem Mol Biol 2008; 111: 200-207. [DOI:10.1016/j.jsbmb.2008.06.007] [PMID]
36. Sancho P, Martín-Sanz P, Fabregat I. Reciprocal regulation of NADPH oxidases and the cyclooxygenase-2 pathway. Free Radic Biol Med 2011; 51: 1789-1798. [DOI:10.1016/j.freeradbiomed.2011.08.011] [PMID]
37. Van den Berg IM, Eleveld C, van der Hoeven M, Birnie E, Steegers EAP, Galjaard RJ, et al. Defective deacetylation of histone 4 K12 in human oocytes is associated with advanced maternal age and chromosome misalignment. Hum Reprod 2011; 26: 1181-1190. [DOI:10.1093/humrep/der030] [PMID]
38. Wang N, Le F, Zhan QT, Li L, Dong MY, Ding GL, et al. Effects of in vitro maturation on histone acetylation in metaphase II oocytes and early cleavage embryos. Obstet Gynecol Int 2010; 2010: 989278: 1-9. [DOI:10.1155/2010/989278] [PMID] [PMCID]
Send email to the article author

Rights and permissions
Creative Commons License This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.

Designed & Developed by : Yektaweb