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Vertebrate reproductive science and technology
RESEARCH ARTICLE

Oocyte glutathione and fertilisation outcome of Macaca nemestrina and Macaca fascicularis in in vivo- and in vitro-matured oocytes

E. C. Curnow A B C D , J. P. Ryan B C , D. M. Saunders B C and E. S. Hayes A
+ Author Affiliations
- Author Affiliations

A Washington National Primate Research Center, University of Washington, Seattle, WA 98121, USA.

B Sydney Medical School, Edward Ford Building, A27, University of Sydney, NSW 2006, Australia.

C IVF Australia, 176 Pacific Highway, Greenwich, NSW 2065, Australia.

D Corresponding author. Email: ecurnow@wanprc.org

Reproduction, Fertility and Development 22(6) 1032-1040 https://doi.org/10.1071/RD09308
Submitted: 18 December 2009  Accepted: 1 February 2010   Published: 1 July 2010

Abstract

Fertilisation and development of IVM non-human primate oocytes is limited compared with that of in vivo-matured (IVO) oocytes. The present study describes the IVM of macaque oocytes with reference to oocyte glutathione (GSH). Timing of maturation, comparison of IVM media and cysteamine (CYS) supplementation as a modulator of GSH were investigated. A significantly greater proportion of oocytes reached MII after 30 h compared with 24 h of IVM. Following insemination, IVM oocytes had a significantly lower incidence of normal fertilisation (i.e. 2PN = two pronuclei and at least one polar body) and a higher rate of abnormal fertilisation (1PN = one pronucleus and at least one polar body) compared with IVO oocytes. Immunofluorescence of 1PN zygotes identified incomplete sperm head decondensation and failure of male pronucleus formation as the principal cause of abnormal fertilisation in IVM oocytes. The IVO oocytes had significantly higher GSH content than IVM oocytes. Cumulus-denuded oocytes had significantly lower GSH following IVM compared with immature oocytes at collection. Cysteamine supplementation of the IVM medium significantly increased the GSH level of cumulus-intact oocytes and reduced the incidence of 1PN formation, but did not improve GSH levels of the denuded oocyte. Suboptimal GSH levels in macaque IVM oocytes may be related to reduced fertilisation outcomes.

Additional keywords: cumulus-denuded oocyte, cysteamine, male pronucleus formation.


Acknowledgements

This work was supported by the National Center for Research Resources (P51 grant RR00166). The authors thank the Washington National Primate Research Center Tissue Distribution Program for their assistance with the collection of reproductive tissues, C. Astley and J. Aherns for surgery support and C. Ferrier for animal care.


References

Bing, Y. Z. , Hirao, Y. , Iga, K. , Che, L. M. , Takenouchi, N. , Kuwayama, M. , Fuchimoto, D. , Rodriguez-Martinez, H. , and Nagai, T. (2002). In vitro maturation and glutathione synthesis of porcine oocytes in the presence or absence of cysteamine under different oxygen tensions: role of cumulus cells. Reprod. Fertil. Dev. 14, 125–131.
Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |

Brad, A. M. , Bormann, C. L. , Swain, J. E. , Durkin, R. E. , Johnson, A. E. , Clifford, A. L. , and Krisher, R. L. (2003). Glutathione and adenosine triphosphate content of in vivo and in vitro matured porcine oocytes. Mol. Reprod. Dev. 64, 492–498.
Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |

Chian, R.-C. , Buckett, W. M. , Jalil, A. K. A. , Son, W.-Y. , Sylvestre, C. , Rao, D. , and Tan, S.-L. (2004). Natural-cycle in vitro fertilization combined with in vitro maturation of immature oocytes is a potential approach in infertility treatment. Fertil. Steril. 82, 1675–1678.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Curnow, E. C. , Ryan, J. P. , Saunders, D. M. , and Hayes, E. S. (2010). Developmental potential of bovine oocytes following in vitro maturation in the presence of glutathione ethyl ester. Reprod. Fertil. Dev. 22, 597–605.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |

de Matos, D. G. , Furnus, C. C. , Moses, D. F. , Martinez, A. G. , and Matkovic, M. (1996). Stimulation of glutathione synthesis of in vitro matured bovine oocytes and its effect on embryo development and freezability. Mol. Reprod. Dev. 45, 451–457.
Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |

de Matos, D. G. , Furnus, C. C. , and Moses, D. F. (1997). Glutathione synthesis during in vitro maturation of bovine oocytes: role of cumulus cells. Biol. Reprod. 57, 1420–1425.
Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |

de Matos, D. G. , Gasparrini, B. , Pasqualini, S. R. , and Thompson, J. G. (2002). Effect of glutathione synthesis stimulation during in vitro maturation of ovine oocytes on embryo development and intracellular peroxide content. Theriogenology 57, 1443–1451.
Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |

de Matos, D. G. , Nogueira, D. , Cortvrindt, R. , Herrera, C. , Adriaenssens, T. , Pasqualini, R. S. , and Smitz, J. (2003). Capacity of adult and prepubertal mouse oocytes to undergo embryo development in the presence of cysteamine. Mol. Reprod. Dev. 64, 214–218.
Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |

Delimitreva, S. , Zhivkova, R. , Isachencko, E. , Umland, N. , and Nayudu, P. U. (2006). Meiotic abnormalities in in vitro-matured marmoset monkey (Callithrix jacchus) oocytes: development of non-human primate model to investigate causal factors. Hum. Reprod. 21, 240–247.
Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |

Deneke, S. M. , and Fanburg, B. L. (1989). Regulation of cellular glutathione. Am. J. Physiol. 257, L163–L173.
PubMed |  CAS |

Downs, S. M. (1995). The influence of glucose, cumulus cells, and metabolic coupling on ATP levels and meiotic control in the isolated mouse oocytes. Dev. Biol. 167, 502–512.
Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |

Eppig, J. J. (1996). Coordination of nuclear and cytoplasmic oocyte maturation in eutherian mammals. Reprod. Fertil. Dev. 8, 485–489.
Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |

Gasparrini, B. , Sayoud, H. , Neglia, G. , de Matos, D. G. , Donnay, I. , and Zicarelli, L. (2003). Glutathione synthesis during in vitro maturation of buffalo (Bubalus bubalis) oocytes: effects of cysteamine on embryos development. Theriogenology 60, 943–952.
Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |

Griffith, O. W. , and Meister, A. (1979). Potent and specific inhibition of glutathione synthesis by buthionine sulfoximine (S-n-butyl homocysteine sulfoximine). J. Biol. Chem. 254, 7558–7560.
PubMed |  CAS |

Grupen, C. G. , Nagashima, H. , and Nottle, M. B. (1995). Cysteamine enhances in vitro development of porcine oocytes matured and fertilized in vitro. Biol. Reprod. 53, 173–178.
Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |

Hewitson, L. C. , Simerly, C. R. , Tengowski, M. W. , Sutovsky, P. , Navara, C. S. , Haavisto, A. J. , and Schatten, G. (1996). Microtubule and chromatin configurations during rhesus intracytoplasmic sperm injection: successes and failures. Biol. Reprod. 55, 271–280.
Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |

Ishii, T. , and Bannai, S. (1985). The synergistic action of the copper chelator bathocuproine sulphonate and cysteine in enhancing growth of L1210 cells in vitro. J. Cell. Physiol. 125, 151–155.
Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |

Issels, R. D. , Nagele, A. , Eckert, K. G. , and Wilmanns, W. (1988). Promotion of cystine uptake and its utilization for glutathione biosynthesis induced by cysteamine and N-acetylcysteine. Biochem. Pharmacol. 37, 881–888.
Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |

Luciano, A. M. , Lodde, V. , Beretta, M. S. , Colleoni, S. , Lauria, A. , and Modina, S. (2005). Developmental capability of denuded bovine oocyte in a co-culture system with intact cumulus–oocyte complexes: role of cumulus cells, cyclic adenosine 3′,5′-monophosphate, and glutathione. Mol. Reprod. Dev. 71, 389–397.
Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |

Luderer, U. , Kavanagh, T. J. , White, C. C. , and Faustman, E. M. (2001). Gonadotrophin regulation of glutathione synthesis in the rat ovary. Reprod. Toxicol. 15, 495–504.
Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |

Maedomari, N. , Kikuchi, K. , Ozawa, M. , Noguchi, M. , Kaneko, H. , Ohnuma, K. , Nakai, M. , Shino, M. , Nagai, T. , and Kashiwazaki, N. (2007). Cytoplasmic glutathione regulated by cumulus cells during porcine oocytes maturation affects fertilization and embryonic development in vitro. Theriogenology 67, 983–993.
Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |

Mattioli, M. , Galeati, G. , Bacci, M. L. , and Seren, E. (1988). Follicular factors influence oocyte fertilizability by modulating the intercellular cooperation between cumulus cells and oocyte. Gamete Res. 21, 223–232.
Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |

Morgan, P. M. , Warikoo, P. K. , and Bavister, B. D. (1991). In vitro maturation of ovarian oocytes from unstimulated rhesus monkeys: assessment of cytoplasmic maturity by embryonic development after in vitro fertilization. Biol. Reprod. 45, 89–93.
Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |

Mori, T. , Amano, T. , and Shimizu, H. (2000). Roles of gap junctional communication of cumulus cells in cytoplasmic maturation of porcine oocytes cultured in vitro. Biol. Reprod. 62, 913–919.
Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |

Pelland, A. M. D. , Corbett, H. E. , and Baltz, J. M. (2009). Amino acid transport mechanisms in mouse oocytes during growth and meiotic maturation. Biol. Reprod. 81, 1041–1054.
Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |

Roberts, R. , Franks, S. , and Hardy, K. (2002). Culture environment modulates maturation and metabolism of human oocytes. Hum. Reprod. 17, 2950–2956.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Rodríguez-González, E. , López-Bejar, M. , Mertens, M.-J. , and Paramio, M.-T. (2003). Effects on in vitro embryo development and intracellular glutathione content of the presence of thiol compounds during maturation of prepubertal goat oocytes. Mol. Reprod. Dev. 65, 446–453.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Salmen, J. J. , Skufca, F. , Matt, A. , Gushansky, G. , Mason, A. , and Gardiner, C. S. (2005). Role of glutathione in reproductive tract secretions on mouse preimplantation embryo development. Biol. Reprod. 73, 308–314.
Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |

Schramm, R. D. , and Bavister, B. D. (1995). Effects of granulosa cells and gonadotrophins on meiotic and developmental competence of oocytes in vitro in non-stimulated rhesus monkeys. Hum. Reprod. 10, 887–895.
PubMed |  CAS |

Schramm, R. D. , and Bavister, B. D. (1999). A macaque model for studying mechanisms controlling oocyte development and maturation in human and non-human primates. Hum. Reprod. 14, 2544–2555.
Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |

Schramm, R. D. , and Paprocki, A. M. (2000). Birth of rhesus monkey infant after transfer of embryos derived from in-vitro matured oocytes. Hum. Reprod. 15, 2411–2414.
Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |

Schramm, R. D. , Tenner, M. T. , Boatman, D. E. , and Bavister, B. D. (1994). Effects of gonadotrophins upon the incidence and kinetics of meiotic maturation of macaque oocytes in vitro. Mol. Reprod. Dev. 37, 467–472.
Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |

Schramm, R. D. , Paprocki, A. M. , and VandeVoort, C. A. (2003). Causes of development failure of in-vitro matured rhesus monkey oocytes: impairments in embryonic genome activation. Hum. Reprod. 18, 826–833.
Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |

Smith, S. D. , Mikkelsen, A. A. , and Lindenberg, S. (2000). Development of human oocytes matured in vitro for 28 or 36 hours. Fertil. Steril. 73, 541–544.
Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |

Söderström-Anttila, V. , Makinen, S. , Tuuri, T. , and Suikkari, A.-M. (2005). Favourable pregnancy results with insemination of in vitro matured oocytes from unstimulated patients. Hum. Reprod. 20, 1534–1540.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Tsai-Turton, M. , and Luderer, U. (2005). Gonadotrophin regulation of glutamate cysteine ligase catalytic and modifier subunit expression in rat ovary is subunit and follicle stage specific. Am. J. Physiol. Endocrinol. Metab. 289, E391–E402.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |

Van Soom, A. , Yuan, Y. Q. , Peelman, L. J. , de Matos, D. G. , Dewulf, J. , Laevens, H. , and de Kruif, A. (2002). Prevalence of apoptosis and inner cell allocation in bovine embryos cultured under different oxygen tensions with or without cysteine addition. Theriogenology 57, 1453–1465.
Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |

VandeVoort, C. A. , Leibo, S. P. , and Tarantal, A. F. (2003). Improved collection and developmental competence of immature macaque oocytes. Theriogenology 59, 699–707.
Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |

Whitaker, B. D. , and Knight, J. W. (2004). Exogenous γ-glutamyl cycle compounds supplemented to in vitro maturation medium influence in vitro fertilization, culture, and viability parameters of porcine oocytes and embryos. Theriogenology 62, 311–322.
Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |

Yamauchi, N. , and Nagai, T. (1999). Male pronuclear formation in denuded porcine oocytes after in vitro maturation in the presence of cysteamine. Biol. Reprod. 61, 828–833.
Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |

Yoshida, M. (1993). Role of glutathione in the maturation and fertilization of pig oocytes in vitro. Mol. Reprod. Dev. 35, 76–81.
Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |

Yoshida, M. , Ishigaki, K. , and Pursel, V. G. (1992). Effect of maturation media on male pronucleus formation in pig oocytes matured in vitro. Mol. Reprod. Dev. 31, 68–71.
Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |

Zheng, P. (2007). Effects of in vitro maturation of monkey oocytes on their developmental capacity. Anim. Reprod. Sci. 98, 56–71.
Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |

Zheng, P. , Bavister, B. D. , and Weizhi, J. (2001). Energy substrate requirement for in vitro maturation of oocytes from unstimulated adult rhesus monkeys. Mol. Reprod. Dev. 58, 348–355.
Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |

Zhou, P. , Wu, Y.-G. , Li, Q. , Lan, G.-C. , Wang, G. , Gao, D. , and Tan, J.-H. (2008). The interactions between cysteamine, cystine and cumulus cells increase the intracellular glutathione level and developmental capacity of goat cumulus-denuded oocytes. Reproduction 135, 605–611.
Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |

Zuelke, K. A. , Jones, D. P. , and Perreault, S. D. (1997). Glutathione oxidation is associated with altered microtubule function and disrupted fertilization in mature hamster oocytes. Biol. Reprod. 57, 1413–1419.
Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |