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Resveratrol has dose-dependent effects on DNA fragmentation and mitochondrial activity of ovine secondary follicles cultured in vitro

Published online by Cambridge University Press:  11 July 2017

T.J.S. Macedo ,
V.R.P. Barros ,
A.P.O. Monte ,
B.B. Gouveia ,
M.É.S. Bezerra ,
A.Y.P. Cavalcante ,
R.S. Barberino ,
V.G. Menezes  and
M.H.T. Matos
T.J.S. Macedo
Affiliation:
Nucleus of Biotechnology Applied to Ovarian Follicle Development, Federal University of São Francisco Valley, Petrolina-PE, Brazil.
V.R.P. Barros
Affiliation:
Nucleus of Biotechnology Applied to Ovarian Follicle Development, Federal University of São Francisco Valley, Petrolina-PE, Brazil.
A.P.O. Monte
Affiliation:
Nucleus of Biotechnology Applied to Ovarian Follicle Development, Federal University of São Francisco Valley, Petrolina-PE, Brazil.
B.B. Gouveia
Affiliation:
Nucleus of Biotechnology Applied to Ovarian Follicle Development, Federal University of São Francisco Valley, Petrolina-PE, Brazil.
M.É.S. Bezerra
Affiliation:
Nucleus of Biotechnology Applied to Ovarian Follicle Development, Federal University of São Francisco Valley, Petrolina-PE, Brazil.
A.Y.P. Cavalcante
Affiliation:
Nucleus of Biotechnology Applied to Ovarian Follicle Development, Federal University of São Francisco Valley, Petrolina-PE, Brazil.
R.S. Barberino
Affiliation:
Nucleus of Biotechnology Applied to Ovarian Follicle Development, Federal University of São Francisco Valley, Petrolina-PE, Brazil.
V.G. Menezes
Affiliation:
Nucleus of Biotechnology Applied to Ovarian Follicle Development, Federal University of São Francisco Valley, Petrolina-PE, Brazil.
M.H.T. Matos*
Affiliation:
Universidade Federal do Vale do São Francisco (UNIVASF), Campus de Ciências Agrárias. Colegiado de Medicina Veterinária – Laboratório de Biologia Celular, Citologia e Histologia, Rodovia BR 407, Km 12, Lote 543 - Projeto de Irrigação Nilo Coelho – S/N, C1.,CEP: 56300–990 – Petrolina – PE – Brasil.
*
All correspondence to: M.H.T. Matos. Universidade Federal do Vale do São Francisco (UNIVASF), Campus de Ciências Agrárias. Colegiado de Medicina Veterinária – Laboratório de Biologia Celular, Citologia e Histologia, Rodovia BR 407, Km 12, Lote 543 - Projeto de Irrigação Nilo Coelho – S/N, C1.,CEP: 56300–990 – Petrolina – PE – Brasil. Tel: +55.87.2101.4839. E-mail: [email protected]
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Summary

The worldwide consumption of red wine, nuts and grapes has resulted in increased human exposure to resveratrol, which could affect reproductive function. However, the effect of resveratrol on in vitro culture of early-stage ovarian follicles has never been investigated. The aims of the present study were to evaluate the effect of resveratrol on sheep secondary follicle morphology, growth, DNA fragmentation, intracellular levels of glutathione (GSH) and active mitochondria. Secondary follicles were isolated from the ovaries and cultured for 18 days in supplemented α-MEM+ (control medium) or in control medium containing resveratrol (2, 10 or 30 µM). The parameters analyzed were morphology, antrum formation, follicle diameter, DNA fragmentation, GSH levels and mitochondrial activity. After 18 days, all resveratrol groups significantly decreased the percentages of morphologically normal follicles compared with the control group (α-MEM+). Antrum formation was higher in both α-MEM+ and 2 µM resveratrol groups than in the 10 µM resveratrol group. In addition, 30 µM resveratrol increased the percentage of oocytes with DNA damage compared with the control. Oocytes from follicles treated with 10 or 30 µM resveratrol significantly decreased intracellular GSH levels compared with the 2 µM resveratrol group. Moreover, follicles in α-MEM+ (control) showed more active mitochondria than those in 10 or 30 µM resveratrol. In conclusion, ovine isolated secondary follicles are able to grow to the antral stage after in vitro culture in medium containing 2 µM resveratrol, maintaining the same rates of DNA damage, GSH levels and mitochondrial function as the control medium. However, the addition of 30 µM resveratrol increased DNA fragmentation and oxidative stress through decreasing mitochondrial activity.

Keywords

ApoptosisGSHOocyteOxidative stressPolyphenol
Type
Research Article
Information
Zygote , Volume 25 , Issue 4 , August 2017 , pp. 434 - 442
Copyright
Copyright © Cambridge University Press 2017 

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References

Baur, J.A. & Sinclair, D.A. (2006). Therapeutic potential of resveratrol: the in vivo evidence. Nat. Rev. Drug. Discov. 5, 493–506.Google Scholar
Chaves, R.N., Martins, F.S., Saraiva, M.V.A., Celestino, J.J.H., Lopes, C. A.P., Correia, J.C., Lima Verde, I.B., Matos, M.H.T., Báo, S.N., Name, K.P.O., Campello, C.C., Silva, J.R.V. & Figueiredo, J.R. (2008). Chilling ovarian fragments during transportation improves viability and growth of goat preantral follicles cultured in vitro. Reprod. Fertil. Dev. 20, 640–47.CrossRefGoogle ScholarPubMed
Delmas, D. Aires, V. Dutartre, P., Mazué, F., Ghiringhelli, F. & Latruffe, N. (2011). Transport, stability, and biological activity of resveratrol. Ann. N Y Acad. Sci. 1215, 48–59.Google Scholar
Demirci, B., Lornage, J., Salle, B., Poirela, M.T., Guerin, J.F. & Franck, M. (2003). The cryopreservation of ovarian tissue: uses and indications in veterinary medicine. Theriogenology 60, 999–1010.Google Scholar
Ducolomb, Y., Casas, E., Valdez, A., González, G., Altamirano-Lozano, M. & Betancourt, M. (2009). In vitro effect of malathion and diazinon on oocytes fertilization and embryo development in porcine. Cell. Biol. Toxicol. 25, 623–33.Google Scholar
Erickson, G.F. & Shimasaki, S., (2001). The physiology of folliculogenesis: the role of novel growth factors. Fertil. Steril. 76, 5.Google Scholar
Fransolet, M., Labied, S., Henry, L., Masereel, M-C., Rozet, E., Kirschvink, N., Nisolle, M. & Munaut, C. (2014). Strategies for using the sheep ovarian cortex as a model in reproductive medicine. PLoS One 9, 1–7.Google Scholar
Giaretta, E., Spinaci, M., Bucci, D., Tamanini, C. & Galeati, G. (2013). Effects of resveratrol on vitrified porcine oocytes. Oxid. Med. Cell Longev. 2013, 1–7.Google Scholar
Goldberg, D.M., Yan, J. & Soleas, G.J. (2003). Absorption of three wine-related polyphenols in three different matrices by healthy subjects. Clin. Biochem. 36, 79–87.Google Scholar
Gosden, R.G., Baird, D.T., Wade, J.C. & Webb, R. (1994). Restoration of fertility to oophorectomized sheep by ovarian autografts stored at −196 °C. Hum. Reprod. 9, 597–603.Google Scholar
Gupta, R.K., Miller, K.P., Babus, J.K. & Flaws, J.A. (2006). Methoxychlor inhibits growth and induces atresia of antral follicles through an oxidative stress pathway. Toxicol. Sci. 93, 382–89.CrossRefGoogle ScholarPubMed
Luberda, Z. (2005). The role of glutathione in mammalian gametes. Biol. Reprod. 5, 1–17.Google ScholarPubMed
Li, H.J., Liu, D.J., Cang, M., Wang, L.M. & Shorgan, B. (2009). Early apoptosis is associated with improved developmental potential in bovine oocytes. Anim. Reprod. Sci. 114, 89–98.CrossRefGoogle ScholarPubMed
Li, Y., Wang, J., Zhang, Z., Yi, J., He, C., Wang, F., Tian, X., Yang, M., Song, Y., He, P. & Liu, G. (2016). Resveratrol compares with melatonin in improving in vitro porcine oocyte maturation under heat stress. J. Anim. Sci. Biotechnol. 7, 1–10.Google Scholar
Kalra, N., Roy, P., Prasad, S., Shukla, Y. (2008). Resveratrol induces apoptosis involving mitochondrial pathways in mouse skin tumorigenesis. Life Sci. 82, 348–358.Google Scholar
Kwak, S.S., Cheong, S.A., Jeon, Y., Lee, E., Choi, K-C., Jeung, E-B. & Hyun, S-H. (2012). The effects of resveratrol on porcine oocyte in vitro maturation and subsequent embryonic development after parthenogenetic activation and in vitro fertilization. Theriogenology 78, 86–101.Google Scholar
Ku, C.R., Cho, Y.H., Hong, Z-Y., Lee, H., Lee, S.J., Hong, S-S. & Lee, E.J. (2016). The effects of high fat diet and resveratrol on mitochondrial activity of brown adipocytes. Endocrinol. Metab. 31, 328–35.Google Scholar
Madreiter-Sokolowski, C.T., Gottschalk, B., Parichatikanonda, W., Eroglu, E., Klec, C., Waldeck-Weiermair, M., Malli, R. & Graier, W.F. (2016). Resveratrol specifically kills cancer cells by a devastating increase in the Ca2+ coupling between the greatly tethered endoplasmic reticulum and mitochondria. Cell. Physiol. Biochem. 39, 1404–20.Google Scholar
Mukherjee, S., Dubley, J.I. & Das, D.K. (2010). Dose-dependency of resveratrol in providing health benefits. Dose-Response 8, 478–500.Google Scholar
Mukherjee, A., Malik, H., Saha, A.P., Dubey, A., Singhal, D.K., Boateng, S., Saugandhika, S., Kumar, S., De, S., Guha, S.K. & Malakar, D. (2014). Resveratrol treatment during goat oocytes maturation enhances developmental competence of parthenogenetic and hand-made cloned blastocysts by modulating intracellular glutathione level and embryonic gene expression. J. Assist. Reprod. Genet. 31, 229–39.Google Scholar
Ortega, I., Wong, D.H., Villanueva, J.A., Cress, A.B., Sokalska, A., Stanley, S.D. & Duleba, A.J. (2012). Effects of resveratrol on growth and function of rat ovarian granulosa cells. Fertil. Steril. 98, 1563–73.Google Scholar
Pangeni, R., Sahni, J.K., Ali, J., Sharma, S. & Baboota, S. (2014). Resveratrol: review on therapeutic potential and recent advances in drug delivery. Expert Opin. Drug Deliv. 11, 1–13.CrossRefGoogle ScholarPubMed
Simsek, Y., Gurocak, S., Turkoz, Y., Akpolat, N., Celik, O., Ozer, A., Yilmaz, E., Turhan, U. & Ozyalin, F. (2012). Ameliorative effects of resveratrol on acute ovarian toxicity induced by total body irradiation in young adult rats. J. Ped. Adol. Gynecol. 25, 262–66.Google Scholar
Stefansdottir, A., Fowler, P.A., Powles-Glover, N., Anderson, R.A., Spears, N. (2014). Use of ovary culture techniques in reproductive toxicology. Reprod. Toxicol. 49, 117–35.Google Scholar
Tanabe, M., Tamura, H., Taketani, T., Okada, M., Lee, L., Tamura, I., Maekawa, R., Asada, H., Yamagata, Y. & Sugino, N. (2015). Melatonin protects the integrity of granulosa cells by reducing oxidative stress in nuclei, mitochondria, and plasm membranes in mice. J. Reprod. Dev. 61,35–41.Google Scholar
Ünal, S.G., Take, G., Erdogan, D., Göktas, G. & Sahin, E. (2013). The effect of di-n-butyl phthalate on testis and the potential protective effects of resveratrol. Toxicol. Ind. Health 32, 1–14.Google Scholar
Valentovic, M., Ball, J.G., Brown, J.M., Terneus, M.V., McQuade, E., Van Meter, S., Hedrick, H.M., Roy, A.A. & Williams, T. (2014). Resveratrol attenuates cisplatin renal cortical cytotoxicity by modifying oxidative stress. Toxicol. In Vitro 28, 248–57.Google Scholar
Wang, F., Tian, X., Zhang, L., He, C., Ji, P., Li, Y., Tan, D. & Liu, G. (2014). Beneficial effect of resveratrol on bovine oocyte maturation and subsequent embryonic development after in vitro fertilization. Fertil. Steril. 101, 577–86.Google Scholar
Wong, D.H., Villanueva, J.A., Cress, A.B. & Duleba, A. (2010). Effects of resveratrol on proliferation and apoptosis in rat ovarian theca-interstitial cells. Mol. Hum. Reprod. 16, 251–9.Google Scholar