Hostname: page-component-cd9895bd7-gbm5v Total loading time: 0 Render date: 2024-12-24T12:12:16.118Z Has data issue: false hasContentIssue false

Effect of melatonin treatment on the developmental potential of parthenogenetic and somatic cell nuclear-transferred porcine oocytes in vitro

Published online by Cambridge University Press:  01 July 2011

Mayu Nakano
Affiliation:
Laboratory of Animal Reproduction, College of Agriculture, Kinki University, Nara, 631–8505, Japan.
Yoko Kato
Affiliation:
Laboratory of Animal Reproduction, College of Agriculture, Kinki University, Nara, 631–8505, Japan.
Yukio Tsunoda*
Affiliation:
Laboratory of Animal Reproduction, College of Agriculture, Kinki University, Nara, 631–8505, Japan.
*
All correspondence to: Yukio Tsunoda. Laboratory of Animal Reproduction, College of Agriculture, Kinki University, Nara, 631–8505, Japan. Tel: +81 742 43 5143. Fax: +81 742 43 5393. e-mail: [email protected]

Summary

Melatonin secreted from the mammalian pineal gland is a free-radical scavenger that protects tissues from cell damage. The present study examined the effects of addition of melatonin to the culture medium on the developmental potential of parthenogenetic and somatic cell nuclear-transferred (SCNT) porcine oocytes. Supplementation of the maturation medium with melatonin did not increase the maturation rate, the proportion of oocytes that cleaved and developed into blastocysts after parthenogenetic activation, or the blastocyst cell number compared to controls. When 10−7 M melatonin was added to the culture medium, the proportion of parthenogenetic oocytes that developed to the 2-cell and 4-cell stages was significantly higher than that of controls. The potential of melatonin-treated oocytes to develop into blastocysts was high but not significantly different from that of controls. The addition of 10−7 M melatonin to the culture medium did not increase the preimplantation development of SCNT oocytes. Melatonin treatment significantly reduced the levels of reactive oxygen species in 4-cell parthenogenetic and SCNT embryos, but did not reduce the proportion of apoptotic cells in parthenogenetic and SCNT blastocysts. Although the results indicated that parthenogenetic and SCNT melatonin -treated embryos had significantly lower levels of reactive oxygen species than controls, the potential of melatonin-treated embryos to develop into blastocysts was not significantly higher than that of controls, in contrast to previous reports. The beneficial effects of melatonin on the developmental potential of oocytes might depend on the culture conditions.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2011

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

Abecia, J.A., Forcada, F. & Zuniga, O. (2002). The effect of melatonin on the secretion of progesterone in sheep and on the development of ovine embryos in vitro. Vet. Res. Commun. 26, 151–8.CrossRefGoogle ScholarPubMed
Ali, A.A., Bilodeau, J.F. & Sirard, M.A. (2003). An antioxidant requirement for bovine oocytes varies during in vitro maturation, fertilization and development. Theriogenology 59, 939–49.Google Scholar
Avery, B. & Greve, T. (2000). Effect of ethanol and dimethylsulphoxide on nuclear and cytoplasmic maturation of bovine cumulus–oocyte complexes. Mol. Reprod. Dev. 55, 438–45.Google Scholar
Berlinguer, F., Leoni, G.C., 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
Betthauser, J., Forsberg, E., Augenstein, M., Childs, L., Eilertsen, K., Enos, J., Forsythe, T., Golueke, P., Jurgella, G., Koppang, R., Lesmeister, T., Mallon, K., Mell, G., Misica, P., Pace, M., Pfister-Genskow, M., Strelchenko, N., Voelker, G., Watt, S., Thompson, S. & Bishop, M. (2000). Production of cloned pigs from in vitro systems. Nat. Biotechnol. 18, 1055–9.CrossRefGoogle ScholarPubMed
Bing, Y.Z., Hirao, Y., Takenouchi, N., Che, L.M., Nakamura, H., Yodoi, J. & Nagai, T. (2003). Effects of thioredoxin on the preimplantation development of bovine embryos. Theriogenology 59, 863–73.Google Scholar
Campbell, K.H., Fisher, P., Chen, W.C., Choi, I., Kelly, R.D., Lee, J.H. & Xhu, J. (2007). Somatic cell nuclear transfer: past, present and future perspectives. Theriogenology 681, S21431.Google Scholar
Carambula, S.F., Oliveira, L.J. & Hansen, P.J. (2009). Repression of induced apoptosis in the 2-cell bovine embryo involves DNA methylation and histone acetylation. Biochem. Biophys. Res. Commun. 388, 418–21.CrossRefGoogle Scholar
Choi, J., Park, S.M., Lee, E., Kim, J.H., Jeong, Y.I., Lee, J.Y., Park, S.W., Kim, H.S., Hossein, M.S., Jeong, Y.W., Kim, S., Hyun, S.H. & Hwang, W.S. (2008). Anti-apoptotic effect of melatonin on preimplantation development of porcine parthenogenetic embryos. Mol. Reprod. Dev. 75, 1127–35.Google Scholar
Fujimura, T., Takahagi, Y., Shigehisa, T., Nagashima, H., Miyagawa, S., Shirakura, R. & Murakami, H. (2008). Production of alpha1,3-galactosyltransferase gene-deficient pigs by somatic cell nuclear transfer: a novel selection method for gal alpha 1,3-Gal antigen-deficient cells. Reprod. Dev. 75, 1372–8.Google Scholar
Fujitani, Y., Kasai, K., Ohtani, S., Nishimura, K., Yamada, M. & Utsumi, K. (1997). Effect of oxygen concentration and free radicals on in vitro development of in vitro-produced bovine embryos. J. Anim. Sci. 75, 483–9.Google Scholar
Funahashi, H., Cantley, T.C. & Day, B.N. (1997). Synchronization of meiosis in porcine oocytes by exposure to dibutyryl cyclic adenosine monophosphate improves development competence following in vitro fertilization. Biol. Reprod. 57, 4953.Google Scholar
Goto, Y., Noda, Y., Mori, T. & Nakano, M. (1993). Increased generation of reactive oxygen species in embryos cultured in vitro. Free. Radic. Biol. Med. 15, 6975.Google Scholar
Guerin, P., Mouatassim, S. & Menezo, Y. (2001). Oxidative stress and protection against reactive oxygen species in the pre-implantation embryo and its surroundings. Hum. Reprod. Update 7, 175–89.CrossRefGoogle ScholarPubMed
Hashimoto, S., Minami, N., Takakura, R., Yamada, M., Imai, H. & Kashima, N. (2000). Low oxygen tension during in vitro maturation is beneficial for supporting the subsequent development of bovine cumulus–oocyte complexes. Mol. Reprod. Dev. 57, 353–60.Google Scholar
Hata, M., Ohkoshi, K., Kato, Y. & Tsunoda, Y. (1996). Parthenogenetic activation of pig oocytes matured in vitro following electrical stimulation. Jpn. J. Fertil. Steril. 41, 305–10.Google Scholar
Ishizuka, B., Kuribayashi, Y., Murai, K., Amemiya, A. & Ito, M.T. (2000). The effect of melatonin on in vitro fertilization and embryo development in mice. J. Pineal. Res. 28, 4851.Google Scholar
Kamjoo, M., Brison, D.R. & Kimber, S.J. (2002). Apoptosis in the preimplantation mouse embryo: effect of strain difference and in vitro culture. Mol. Reprod. Dev. 61, 6777.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
Karbownik, M. & Lewinski, A. (2003). Melatonin reduces Fenton reaction-induced lipid peroxidation in porcine thyroid tissue. J. Cell. Biochem. 90, 806–11.CrossRefGoogle ScholarPubMed
Kawakami, M., Kato, Y. & Tsunoda, Y. (2005). Maintenance of meiotic arrest and developmental potential of porcine oocytes after parthenogenetic activation and somatic cell nuclear transfer. Cloning Stem Cells 7, 167–77.Google Scholar
Kishigami, S., Wakayama, S., Thuan, N.V., Ohta, H., Mizutani, E., Hikichi, T., Bui, H.T., Balbach, S., Ogura, A., Boiani, M. & Wakayama, T. (2006). Production of cloned mice by somatic cell nuclear transfer. Nat. Protoc. 1, 125–38.Google Scholar
Klymiuk, N., Aigner, B., Brem, G. & Wolf, E. (2010). Genetic modification of pigs as organ donors for xenotransplantation. Mol. Reprod. Dev. 77, 209–21.CrossRefGoogle ScholarPubMed
Luvoni, G.C., Keskintepe, L. & Brackett, B.G. (1996). Improvement of bovine embryo production in vitro by glutathione-containing media. Mol. Reprod. Dev. 43, 437–43.3.0.CO;2-Q>CrossRefGoogle ScholarPubMed
Naito, K., Fukuda, Y. & Toyoda, Y. (1988). Effects of porcine follicular fluid on male pronucleus formation in porcine oocytes matured in vitro. Gamete Res. 21, 289–95.Google Scholar
Noda, Y., Mori, A., Liburdy, R. & Packer, L. (1999). Melatonin and its precursors scavenge nitric oxide. J. Pineal. Res. 27, 159–63.CrossRefGoogle ScholarPubMed
Neuber, E., Luetjens, C.M., Chan, A.W. & Schatten, G.P. (2002). Analysis of DNA fragmentation of in vitro cultured bovine blastocysts using TUNEL. Theriogenology 57, 2193–202.Google Scholar
Okada, K., Krylov, V., Kren, R. & Fulka, J. Jr. (2006). Development of pig embryos after electro-activation and in vitro fertilization in PZM-3 or PZM supplemented with fetal bovine serum. J. Reprod. Dev. 52, 91–8.Google Scholar
Onishi, A., Iwamoto, M., Akita, T., Mikawa, S., Takeda, K., Awata, T., Hanada, H., & Perry, A.C. (2000). Pig cloning by microinjection of fetal fibroblast nuclei. Science 289, 11881190.Google Scholar
Papaioannou, V.E. & Ebert, K.M. (1988). The preimplantation pig embryo: cell number and allocation to trophectoderm and inner cell mass of the blastocyst in vivo and in vitro. Development 102, 793803.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.Google Scholar
Petters, R.M. & Wells, K.D. (1993). Culture of pig embryos. J. Reprod. Fertil. Suppl. 48, 6173.Google Scholar
Polejaeva, I.A., Chen, S.H., Vaught, T.D., Page, R.L., Mullins, J., Ball, S., Dai, Y., Boonem, J., Walkerm, S., Ayares, D.L., Colman, A. & Campbell, K.H. (2000). Cloned pigs produced by nuclear transfer from adult somatic cells. Nature 407, 8690.Google Scholar
Reiter, R.J., Tan, D.X., Manchester, L.C., Paredes, S.D., Mayo, J.C. & Sainz, R.M. (2009). Melatonin and reproduction revisited. Biol. Reprod. 81, 445–56.Google Scholar
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.Google Scholar
Rybouchkin, A., Kato, Y. & Tsunoda, Y. (2006). Role of histone acetylation in reprogramming of somatic nuclei following nuclear transfer. Biol. Reprod. 74, 1083–9.Google 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
Takahashi, M., Nagai, T., Okamura, N., Takahashi, H. & Okano, A. (2002). Promoting effect of beta-mercaptoethanol on in vitro development under oxidative stress and cystine uptake of bovine embryos. Biol. Reprod. 66, 562–7.Google Scholar
Wakayama, T., Perry, A.C., Zuccotti, M., Johnson, K.R. & Yanagimachi, R. (1998). Full-term development of mice from enucleated oocytes injected with cumulus cell nuclei. Nature 394, 369–74.Google Scholar
Yang, H.W., Hwang, K.J., Kwon, H.C., Kim, H.S., Choi, K.W. & Oh, K.S. (1998). Detection of reactive oxygen species (ROS) and apoptosis in human fragmented embryos. Hum. Reprod. 13, 9981002.CrossRefGoogle ScholarPubMed
Yin, X.J., Tani, T., Yonemura, I., Kawakami, M., Miyamoto, K., Hasegawa, R., Kato, Y. & Tsunoda, Y. (2002). Production of cloned pigs from adult somatic cells by chemically assisted removal of maternal chromosomes. Biol. Reprod. 67, 442–6.Google Scholar
Yoshioka, K., Suzuki, C., Tanaka, A., Anas, I.M. & Iwamura, S. (2002). Birth of piglets derived from porcine zygotes cultured in a chemically defined medium. Biol. Reprod. 66, 112–9.Google Scholar
Zhang, Y., Li, J., Villemoes, K., Pedersen, A.M., Purup, S. & Vajta, G. (2007). An epigenetic modifier results in improved in vitro blastocyst production after somatic cell nuclear transfer. Cloning Stem Cells 9, 357–63.CrossRefGoogle ScholarPubMed
Zhao, J., Hao, Y., Ross, J.W., Spate, L.D., Walters, E.M., Samuel, M.S., Rieke, A., Murphy, C.N. & Prather, R.S. (2010). Histone deacetylase inhibitors improve in vitro and in vivo developmental competence of somatic cell nuclear transfer porcine embryos. Cell. Reprogram. 12, 7583.Google Scholar