Hostname: page-component-78c5997874-dh8gc Total loading time: 0 Render date: 2024-11-16T15:06:23.590Z Has data issue: false hasContentIssue false
  • English
  • Français

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

Published online by Cambridge University Press:  29 May 2014

Xue-Ming Zhao ,
Jiang-Tao Min ,
Wei-Hua Du ,
Hai-Sheng Hao ,
Yan Liu ,
Tong Qin ,
Dong Wang  and
Hua-Bin Zhu
Xue-Ming Zhao
Affiliation:
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.
Jiang-Tao Min
Affiliation:
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. College of Animal Science and Technology, Nanjing Agricultural University, 210095, Nanjing, Jiangsu, PRChina.
Wei-Hua Du
Affiliation:
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.
Hai-Sheng Hao
Affiliation:
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.
Yan Liu
Affiliation:
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.
Tong Qin
Affiliation:
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.
Dong Wang
Affiliation:
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.
Hua-Bin Zhu*
Affiliation:
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.
*
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: [email protected]
Get access Rights & Permissions [Opens in a new window]

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.

Keywords

BovineDenuded oocytesDevelopment potentialIn vitro maturationMelatonin
Type
Research Article
Information
Zygote , Volume 23 , Issue 4 , August 2015 , pp. 525 - 536
Copyright
Copyright © Cambridge University Press 2014 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

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.CrossRefGoogle ScholarPubMed
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, 65–74.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
Carlberg, C. & Wiesenberg, I. (1995). The orphan receptor family RZR/ROR, melatonin and 5-lipoxygenase: an unexpected relationship. J. Pineal. Res. 18, 171–8.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Hussein, T.S., Thompson, J.G. & Gilchrist, R.B. (2006). Oocyte-secreted factors enhance oocyte developmental competence. Dev. Biol. 296, 514–21.CrossRefGoogle ScholarPubMed
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, 48–51.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Kalo, D & Roth, Z. (2011). Involvement of the sphingolipid ceramide in heat-shock-induced apoptosis of bovine oocytes. Reprod. Fertil. Dev. 23, 876–8.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Kidder, G.M. & Watson, A.J. (2005). Roles of Na,K-ATPase in early development and trophectoderm differentiation. Semin. Nephrol. 25, 352–5.CrossRefGoogle ScholarPubMed
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, 887–919.CrossRefGoogle Scholar
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, 1–11.CrossRefGoogle ScholarPubMed
Lin, M.T. & Beal, M.F. (2006). Mitochondrial dysfunction and oxidative stress in neurodegenerative diseases. Nature 443, 787–95.CrossRefGoogle ScholarPubMed
Lincoln, G.A., Clarke, I.J., Hut, R.A. & Hazlerigg, D.G. (2006). Characterizing a mammalian circannual pacemaker. Science 314, 1941–4.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Meister, A. (1983). Selective modification of glutathione metabolism. Science 220, 472–7.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Reiter, R.J., Tan, D.X. & Fuentes-Broto, L. (2010). Melatonin: a multitasking molecule. Prog. Brain. Res. 181, 127–51.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Schmittgen, T.D. & Livak, K.J. (2008). Analyzing real-time PCR data by the comparative CT method. Nat. Protoc. 3, 1101–8.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Simon, H.U., Haj-Yehia, A. & Levi-Schaffer, F. (2000). Role of reactive oxygen species (ROS) in apoptosis induction. Apoptosis 5, 415–8.CrossRefGoogle ScholarPubMed
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, 17–43.CrossRefGoogle ScholarPubMed
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, 64–73.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Tarín, J.J. (1996). Potential effects of age-associated oxidative stress on mammalian oocytes/embryos. Mol. Hum. Reprod. 2, 717–24.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Vanecek, J. (1995) Cellular mechanism of melatonin action in neonatal rat pituitary. Neuroendocrinology 61, 27–30.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
von Gall, C., Stehle, J.H. & Weaver, D.R. (2002). Mammalian melatonin receptors: molecular biology and signal transduction. Cell Tissue Res. 309, 151–62.CrossRefGoogle ScholarPubMed
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.Google Scholar
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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, 67–73.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed