Skip to main content Accessibility help
×
×
Home

Melatonin enhances the in vitro maturation and developmental potential of bovine oocytes denuded of the cumulus oophorus

  • Xue-Ming Zhao (a1), Jiang-Tao Min (a1) (a2), Wei-Hua Du (a1), Hai-Sheng Hao (a1), Yan Liu (a1), Tong Qin (a1), Dong Wang (a1) and Hua-Bin Zhu (a3)...

Summary

This study was designed to determine the effect of melatonin on the in vitro maturation (IVM) and developmental potential of bovine oocytes denuded of the cumulus oophorus (DOs). DOs were cultured alone (DOs) or with 10−9 M melatonin (DOs + MT), cumulus–oocyte complexes (COCs) were cultured without melatonin as the control. After IVM, meiosis II (MII) rates of DOs, and reactive oxygen species (ROS) levels, apoptotic rates and parthenogenetic blastocyst rates of MII oocytes were determined. The relative expression of ATP synthase F0 Subunit 6 and 8 (ATP6 and ATP8), bone morphogenetic protein 15 (BMP-15) and growth differentiation factor 9 (GDF-9) mRNA in MII oocytes and IFN-tau (IFN-τ), Na+/K+-ATPase, catenin-beta like 1 (CTNNBL1) and AQP3 mRNA in parthenogenetic blastocysts were quantified using real-time polymerase chain reaction (PCR). The results showed that: (1) melatonin significantly increased the MII rate of DOs (65.67 ± 3.59 % vs. 82.29 ± 3.92%; P < 0.05), decreased the ROS level (4.83 ± 0.42 counts per second (c.p.s) vs. 3.78 ± 0.29 c.p.s; P < 0.05) and apoptotic rate (36.99 ± 3.62 % vs. 21.88 ± 2.08 %; P < 0.05) and moderated the reduction of relative mRNA levels of ATP6, ATP8, BMP-15 and GDF-9 caused by oocyte denudation; (2) melatonin significantly increased the developmental rate (24.17 ± 3.54 % vs. 35.26 ± 4.87%; P < 0.05), and expression levels of IFN-τ, Na+/K+-ATPase, CTNNBL1 and AQP3 mRNA of blastocyst. These results indicated that melatonin significantly improved the IVM quality of DOs, leading to an increased parthenogenetic blastocyst formation rate and quality.

Copyright

Corresponding author

All correspondence to: Hua-Bin Zhu. Embryo Biotechnology and Reproduction Laboratory, Institute of Animal Science (IAS), Chinese Academy of Agricultural Sciences (CAAS), no. 2 Yuanmingyuan Western Road, Haidian District, Beijing 100193, P.R. China. Tel: +86 10 62815892. Fax: +86 10 62895971. e-mail address: zhuhuabin@iascaas.net.cn

References

Hide All
Acuña-Castroviejo, D., Reiter, R.J., Menéndez-Peláez, A., Pablos, M.I. & Burgos, A. (1994). Characterization of high-affinity melatonin binding sites in purified cell nuclei of rat liver. J. Pineal. Res. 16, 100–12.
Acuña-Castroviejo, D., Martín, M., Macías, M., Escames, G., León, J., Khaldy, H. & Reiter, R.J. (2001). Melatonin, mitochondrial, and cellular bioenergetics. J. Pineal. Res. 30, 6574.
Anguita, B., Vandaele, L., Mateusen, B., Maes, D., & Van Soom, A. (2007). Developmental competence of bovine oocytes is not related to apoptosis incidence in oocytes, cumulus cells and blastocysts. Theriogenology 67, 537–49.
Becker-André, M., Wiesenberg, I., Schaeren-Wiemers, N., André, E., Missbach, M., Saurat, J.H. & Carlberg, C. (1994). Pineal gland hormone melatonin binds and activates an orphan of the nuclear receptor superfamily. J. Biol. Chem. 269, 28531–4.
Berlinguer, F., Leoni, GG., Succu, S., Spezzigu, A., Madeddu, M., Satta, V., Bebbere, D., Contreras-Solis, I., Gonzalez-Bulnes, A. & Naitana, S. (2009). Exogenous melatonin positively influences follicular dynamics, oocyte developmental competence and blastocyst output in a goat model. J. Pineal. Res. 46, 383–91.
Brzezinski, A., Seibel, M.M., Lynch, H.J., Deng, M.H. & Wurtman, R.J. (1987). Melatonin in human preovulatory follicular fluid. J. Clin. Endocrinol. Metab. 64, 865–7.
Carlberg, C. & Wiesenberg, I. (1995). The orphan receptor family RZR/ROR, melatonin and 5-lipoxygenase: an unexpected relationship. J. Pineal. Res. 18, 171–8.
Chan, A., Reiter, R., Wiese, S., Fertig, G. & Gold, R. (1998). Plasma membrane phospholipid asymmetry precedes DNA fragmentation in different apoptotic cell models. Histochem. Cell Biol. 110, 553–8.
Chen, H.Y., Chen, T.Y., Lee, M.Y., Chen, S.T., Hsu, Y.S., Kuo, Y.L., Chang, G.L., Wu, T.S. & Lee, E.J. (2006). Melatonin decreases neurovascular oxidative/nitrosative damage and protects against early increases in the blood-brain barrier permeability after transient focal cerebral ischemia in mice. J. Pineal. Res. 41, 175–82.
Cui, MS., Fan, YP., Wu, Y., Hao, ZD., Liu, S., Chen, X.J. & Zeng, S.M. (2009). Porcine cumulus cell influences ooplasmic mitochondria-lipid distributions, GSH-ATP contents and calcium release pattern after electro-activation. Theriogenology 71, 412–21.
de Matos, D.G., Furnus, C.C. & Moses, D.F. (1997). Glutathione synthesis during in vitro maturation of bovine oocytes: role of cumulus cells. Biol. Reprod. 57, 1420–5.
El Mouatassim, S., Guérin, P. & Ménézo, Y. (1999). Expression of genes encoding antioxidant enzymes in human and mouse oocytes during the final stages of maturation. Mol. Hum. Reprod. 5, 720–5.
El-Raey, M., Geshi, M., Somfai, T., Kaneda, M., Hirako, M., Abdel-Ghaffar, A.E., Sosa, G.A., El-Roos, M.E. & Nagai, T. (2011). Evidence of melatonin synthesis in the cumulus oocyte complexes and its role in enhancing oocyte maturation in vitro in cattle. Mol. Reprod. Dev. 78, 250–62.
Gasparrini, B., Boccia, L., Marchandise, J., Di Palo, R., George, F., Donnay, I. & Zicarelli, L. (2006). Enrichment of in vitro maturation medium for buffalo (Bubalus bubalis) oocytes with thiol compounds: effects of cystine on glutathione synthesis and embryo development. Theriogenology 65, 275–87.
Ge, L., Han, D., Lan, G.C., Zhou, P., Liu, Y., Zhang, X., Sui, H.S. & Tan, J.H. (2008a). Factors affecting the in vitro action of cumulus cells on the maturing mouse oocytes. Mol. Reprod. Dev. 75, 136–42.
Ge, L., Sui, H.S., Lan, G.C., Liu, N., Wang, J.Z. & Tan, J.H. (2008b). Coculture with cumulus cells improves maturation of mouse oocytes denuded of the cumulus oophorus: observations of nuclear and cytoplasmic events. Fertil. Steril. 90, 2376–88.
Geshi, M., Takenouchi, N., Yamauchi, N. & Nagai, T. (2000). Effects of sodium pyruvate in nonserum maturation medium on maturation, fertilization, and subsequent development of bovine oocytes with or without cumulus cells. Biol. Reprod. 63, 1730–4.
Gupta, M.K., Uhm, S.J. & Lee, H.T. (2010). Effect of vitrification and beta-mercaptoethanol on reactive oxygen species activity and in vitro development of oocytes vitrified before or after in vitro fertilization. Fertil. Steril. 93, 2602–7.
Hsieh, R.H., Au, H.K., Yeh, T.S., Chang, S.J., Cheng, Y.F. & Tzeng, C.R. (2004). Decreased expression of mitochondrial genes in human unfertilized oocytes and arrested embryos. Fertil. Steril. 81, Suppl1, 912–8.
Hussein, T.S., Thompson, J.G. & Gilchrist, R.B. (2006). Oocyte-secreted factors enhance oocyte developmental competence. Dev. Biol. 296, 514–21.
Ishizuka, B., Kuribayashi, Y., Murai, K., Amemiya, A. & Itoh, M.T. (2000).The effect of melatonin on in vitro fertilization and embryo development in mice. J. Pineal. Res. 28, 4851.
Johnston, J.D., Tournier, B.B., Andersson, H., Masson-Pévet, M., Lincoln, G.A. & Hazlerigg, D.G. (2006). Multiple effects of melatonin on rhythmic clock gene expression in the mammalian pars tuberalis. Endocrinology 147, 959–65.
Kalo, D & Roth, Z. (2011). Involvement of the sphingolipid ceramide in heat-shock-induced apoptosis of bovine oocytes. Reprod. Fertil. Dev. 23, 876–8.
Kang, J.T., Koo, O.J., Kwon, D.K., Park, H.J., Jang, G., Kang, S.K. & Lee, B.C. (2009). Effects of melatonin on in vitro maturation of porcine oocyte and expression of melatonin receptor RNA in cumulus and granulosa cells. J. Pineal. Res. 46, 22–8.
Kidder, G.M. & Watson, A.J. (2005). Roles of Na,K-ATPase in early development and trophectoderm differentiation. Semin. Nephrol. 25, 352–5.
Lahorte, C.M., Vanderheyden, J.L., Steinmetz, N., Van de Wiele, C., Dierckx, R.A. & Slegers, G. (2004). Apoptosis-detecting radio ligands: current state of the art and future perspectives. Eur. J. Nucl. Med. Mol. Imaging 31, 887919.
Lanoix, D., Lacasse, A.A., Reiter, R.J. & Vaillancourt, C. (2012). Melatonin: the smart killer the human trophoblast as a model. Mol. Cell. Endocrinol 348, 111.
Lin, M.T. & Beal, M.F. (2006). Mitochondrial dysfunction and oxidative stress in neurodegenerative diseases. Nature 443, 787–95.
Lincoln, G.A., Clarke, I.J., Hut, R.A. & Hazlerigg, D.G. (2006). Characterizing a mammalian circannual pacemaker. Science 314, 1941–4.
Liu, F. & Ng, T.B. (2000). Effect of pineal indoles on activities of the antioxidant defense enzymes superoxide dismutase, catalase, and glutathione reductase, and levels of reduced and oxidized glutathione in rat tissues. Biochem. Cell Biol. 78, 447–53.
Maedomari, N., Kikuchi, K., Ozawa, M., Noguchi, J., Kaneko, H., Ohnuma, K., Nakai, M., Shino, M., Nagai, T. & Kashiwazaki, N. (2007). Cytoplasmic glutathione regulated by cumulus cells during porcine oocyte maturation affects fertilization and embryonic development in vitro. Theriogenology 67, 983–93.
Mamo, S., Mehta, J.P., McGettigan, P., Fair, T., Spencer, T.E., Bazer, F.W. & Lonergan, P. (2011). RNA sequencing reveals novel gene clusters in bovine conceptuses associated with maternal recognition of pregnancy and implantation. Biol. Reprod. 85, 1143–51.
Manda, K., Ueno, M. & Anzai, K. (2007). AFMK, a melatonin metabolite, attenuates X-ray-induced oxidative damage to DNA, proteins and lipids in mice. J. Pineal. Res. 42, 386–93.
Manjunatha, B.M., Devaraj, M., Gupta, P.S., Ravindra, J.P. & Nandi, S. (2009). Effect of taurine and melatonin in the culture medium on buffalo in vitro embryo development. Reprod. Domest. Anim. 44, 12–6.
Mayo, J.C., Sainz, R.M., Antoli, I., Herrera, F., Martin, V. & Rodriguez, C. (2002). Melatonin regulation of antioxidant enzyme gene expression. Cell Mol. Life. Sci. 59, 1706–13.
Meister, A. (1983). Selective modification of glutathione metabolism. Science 220, 472–7.
Messer, L.A., Wang, L., Tuggle, C.K., Yerle, M., Chardon, P., Pomp, D., Womack, J.E., Barendse, W., Crawford, A.M., Notter, D.R. & Rothschild, M.F. (1997). Mapping of the melatonin receptor 1a (MTNR1A) gene in pigs, sheep, and cattle. Mamm. Genome. 8, 368–70.
Ozturk, G., Coşkun, S., Erbaş, D. & Hasanoglu, E. (2000). The effect of melatonin on liver superoxide dismutase activity, serum nitrate and thyroid hormone levels. Jpn. J. Physiol. 50, 149–53.
Papis, K., Poleszczuk, O., Wenta-Muchalska, E. & Modlinski, J.A. (2007). Melatonin effect on bovine embryo development in vitro in relation to oxygen concentration. J. Pineal. Res. 43, 321–6.
Park, S.W., Choi, S.M. & Lee, S.M. (2007). Effect of melatonin on altered expression of vasoregulatory genes during hepatic ischemia/reperfusion. Arch. Pharm. Res. 30, 1619–24.
Rahimi, G., Isachenko, E., Sauer, H., Isachenko, V., Wartenberg, M., Hescheler, J., Mallmann, P. & Nawroth, F. (2003). Effect of different vitrification protocols for human ovarian tissue on reactive oxygen species and apoptosis. Reprod. Fertil. Dev. 15, 343–9.
Reiter, R.J., Tan, D.X. & Fuentes-Broto, L. (2010). Melatonin: a multitasking molecule. Prog. Brain. Res. 181, 127–51.
Rodriguez-Osorio, N., Kim, I.J., Wang, H., Kaya, A. & Memili, E. (2007). Melatonin increases cleavage rate of porcine preimplantation embryos in vitro. J. Pineal. Res. 43, 283–8.
Rönnberg, L., Kauppila, A., Leppäluoto, J., Martikainen, H. & Vakkuri, O. (1990). Circadian and seasonal variation in human preovulatory follicular fluid melatonin concentration. J. Clin. Endocrinol. Metab. 71, 492–6.
Rosenkrans, C.F. Jr. & First, N.L. (1994). Effect of free amino acids and vitamins on cleavage and developmental rate of bovine zygotes in vitro. J. Anim. Sci. 72, 434–7.
Schmittgen, T.D. & Livak, K.J. (2008). Analyzing real-time PCR data by the comparative CT method. Nat. Protoc. 3, 1101–8.
Shi, J.M., Tian, X.Z., Zhou, G.B., Wang, L., Gao, C., Zhu, S.E., Zeng, S.M., Tian, J.H. & Liu, G.S. (2009). Melatonin exists in porcine follicular fluid and improves in vitro maturation and parthenogenetic development of porcine oocytes. J. Pineal. Res. 47, 318–23.
Shimizu, T., Numata, T. & Okada, Y. (2004). A role of reactive oxygen species in apoptotic activation of volume-sensitive Cl channel. Proc. Natl. Acad. Sci. USA 101, 6770–3.
Simon, H.U., Haj-Yehia, A. & Levi-Schaffer, F. (2000). Role of reactive oxygen species (ROS) in apoptosis induction. Apoptosis 5, 415–8.
Stehle, J.H., Saade, A., Rawashdeh, O., Ackermann, K., Jilg, A., Sebestény, T. & Maronde, E. (2011). A survey of molecular details in the human pineal gland in the light of phylogeny, structure, function and chronobiological diseases. J. Pineal. Res. 51, 1743.
Su, Y.Q., Wu, X., O’Brien, M.J., Pendola, F.L., Denegre, J.N., Matzuk, M.M. & Eppig, J.J. (2004). Synergistic roles of BMP15 and GDF9 in the development and function of the oocyte–cumulus cell complex in mice: genetic evidence for an oocyte–granulosa cell regulatory loop. Dev. Biol. 276, 6473.
Tamura, H., Takasaki, A., Miwa, I., Taniguchi, K., Maekawa, R., Asada, H., Taketani, T., Matsuoka, A., Yamagata, Y., Shimamura, K., Morioka, H., Ishikawa, H., Reiter, R.J. & Sugino, N. (2008). Oxidative stress impairs oocyte quality and melatonin protects oocytes from free radical damage and improves fertilization rate. J. Pineal. Res. 44, 280–7.
Tarín, J.J. (1996). Potential effects of age-associated oxidative stress on mammalian oocytes/embryos. Mol. Hum. Reprod. 2, 717–24.
Ubuka, T., Bentley, G.E., Ukena, K., Wingfield, J.C. & Tsutsui, K. (2005). Melatonin induces the expression of gonadotropin-inhibitory hormone in the avian brain. Proc. Natl. Acad. Sci. USA 102, 3052–7.
Vanecek, J. (1995) Cellular mechanism of melatonin action in neonatal rat pituitary. Neuroendocrinology 61, 2730.
Vázquez, M.I., Abecia, J.A., Forcada, F. & Casao, A. (2010). Effects of exogenous melatonin on in vivo embryo viability and oocyte competence of undernourished ewes after weaning during the seasonal anestrus. Theriogenology 74, 618–26.
von Gall, C., Stehle, J.H. & Weaver, D.R. (2002). Mammalian melatonin receptors: molecular biology and signal transduction. Cell Tissue Res. 309, 151–62.
Weaver, D.R., Liu, C. & Reppert, S.M. (1996). Nature's knockout: the Me11b receptor is not necessary for reproductive and circadian responses to melatonin in Siberian hamsters. Mol. Endocrin01. 10, 1478–87.
Wei, L.N., Liang, X.Y., Fang, C. & Zhang, M.F. (2011). Abnormal expression of growth differentiation factor 9 and bone morphogenetic protein 15 in stimulated oocytes during maturation from women with polycystic ovary syndrome. Fertil. Steril. 96, 464–8.
Yao, N., Wan, P.C., Hao, Z.D., Gao, F.F., Yang, L., Cui, M.S., Wu, Y., Liu, J.H., Liu, S., Chen, H. & Zeng, S.M. (2009). Expression of interferon-tau mRNA in bovine embryos derived from different procedures. Reprod. Domest. Anim. 44, 132–9.
Yeo, C.X., Gilchrist, R.B., Thompson, J.G. & Lane, M. (2008). Exogenous growth differentiation factor 9 in oocyte maturation media enhances subsequent embryo development and fetal viability in mice. Hum. Reprod. 23, 6773.
Zhang, L., Jiang, S., Wozniak, P.J., Yang, X. & Godke, R.A. (1995). Cumulus cell function during bovine oocyte maturation, fertilization, and embryo development in vitro. Mol. Reprod. Dev. 40, 338–44.
Zhao, X.M., Du, W.H., Wang, D., Hao, H.S., Liu, Y., Qin, T. & Zhu, H.B. (2011a). Effect of cyclosporine pretreatment on mitochondrial function in vitrified bovine mature oocytes. Fertil. Steril. 95, 2786–8.
Zhao, X.M., Du, W.H., Wang, D., Hao, H.S., Liu, Y., Qin, T. & Zhu, H.B. (2011b). Recovery of mitochondrial function and endogenous antioxidant systems in vitrified bovine oocytes during extended in vitro culture. Mol. Reprod. Dev. 78, 942–50.
Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

Zygote
  • ISSN: 0967-1994
  • EISSN: 1469-8730
  • URL: /core/journals/zygote
Please enter your name
Please enter a valid email address
Who would you like to send this to? *
×

Keywords

Metrics

Altmetric attention score

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed