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Reproduction, Fertility and Development Reproduction, Fertility and Development Society
Vertebrate reproductive science and technology
RESEARCH ARTICLE

Effect of hexoses and gonadotrophin supplementation on bovine oocyte nuclear maturation during in vitro maturation in a synthetic follicle fluid medium

Melanie L. Sutton-McDowall A , Robert B. Gilchrist A and Jeremy G. Thompson A B
+ Author Affiliations
- Author Affiliations

A Research Centre for Reproductive Health, Department of Obstetrics and Gynaecology, The University of Adelaide, The Queen Elizabeth Hospital, Woodville Road, Woodville, SA 5011, Australia.

B Corresponding author. Email: jeremy.thompson@adelaide.edu.au

Reproduction, Fertility and Development 17(4) 407-415 https://doi.org/10.1071/RD04135
Submitted: 12 November 2004  Accepted: 25 January 2005   Published: 15 March 2005

Abstract

In vitro oocyte maturation (IVM) culture conditions have been relatively unchanged over the past few decades and remain suboptimal. In contrast, studies of the in vivo environment have led to significant improvements to in vitro embryo culture technologies. The aim of the present study was to determine the effect of maturing bovine cumulus–oocyte complexes (COCs) in medium based on the composition of bovine follicular fluid (Bovine VitroMat; Cook Australia, Eight Mile Plain, Qld, Australia). In particular, the effect of different glucose concentrations and glucosamine supplementation on meiotic maturation was determined. Culturing COCs in the presence of gonadotrophins in Bovine VitroMat, containing either physiological glucose concentrations (2.3 mm) or 5.6 mm (equivalent to levels in Tissue Culture Medium 199 (TCM199)) supplemented with glucosamine resulted in comparable cumulus expansion to COCs cultured in TCM199 plus gonadotrophins. However, nuclear maturation was 1.3-fold lower in Bovine VitroMat cultures containing 2.3 mm glucose compared with 5.6 mm glucose and this effect was independent of glucosamine supplementation. Investigations into the effects of different glucose concentrations and gonadotrophin supplementation during the initial 6 h of maturation demonstrated that COCs cultured in Bovine VitroMat with 5.6 mm glucose without gonadotrophins had a twofold acceleration of the rate of meiotic resumption, yet the rate of polar body formation was decreased by approximately 20% compared with cultures in 2.3 mm glucose and TCM199. However, this effect was not seen when COCs were cultured for the initial 16 h in Bovine VitroMat + 5.6 mm minus gonadotrophins or in Bovine VitroMat + 2.3 mm glucose ± gonadotrophins. These data demonstrate that glucose concentrations and the timing of the introduction of gonadotrophin during IVM have variable effects on nuclear maturation. Manipulation of glucose concentrations may be a mechanism to influence oocyte meiotic progression and may lead to the development of improved IVM systems, allowing for an increased developmental capacity of bovine oocytes.


Acknowledgments

The authors thank Jenny Hayes and Chris Kraft for ovary collections. M. S.-M. is supported by the Australia Research Council (SPIRT, C00107702) and Cook Australia Pty Ltd.


References

Avery, B. , Strobech, L. , Jacobsen, T. , Bogh, I. B. , and Greve, T. (2003). In vitro maturation of bovine cumulus–oocyte complexes in undiluted follicular fluid: effect on nuclear maturation, pronucleus formation and embryo development. Theriogenology 59, 987–999.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Berg, D. K. , Beaumont, S. E. , Berg, M. C. , Hull, C. D. , and Tervit, H. R. (2003). Oxygen and carbon dioxide tension in days 14–15 dominant bovine follicles measured in vivo or 4 hours post-mortem. Theriogenology 59, 406.
Crossref | GoogleScholarGoogle Scholar |

Bousquet, D. , Twagiramungu, H. , Morin, N. , Brisson, C. , Carboneau, G. , and Durocher, J. (1999). In vitro embryo production in the cow: an effective alternative to the conventional embryo production approach. Theriogenology 51, 59–70.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Byskov, A. G. , Andersen, C. Y. , and Leonardsen, L. (2002). Role of meiosis activating sterols, MAS, in induced oocyte maturation. Mol. Cell. Endocrinol. 187, 189–196.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Combelles, C. M. , Cekleniak, N. A. , Racowsky, C. , and Albertini, D. F. (2002). Assessment of nuclear and cytoplasmic maturation in in-vitro matured human oocytes. Hum. Reprod. 17, 1006–1016.
Crossref | GoogleScholarGoogle Scholar | PubMed |

de Loos, F. , van Maurik, P. , van Beneden, T. , and Kruip, T. A. (1992). Structural aspects of bovine oocyte maturation in vitro. Mol. Reprod. Dev. 31, 208–214.
PubMed |

Dieleman, S. J. , Hendriksen, P. J. , Viuff, D. , Thomsen, P. D. , and Hyttel, P. , et al. (2002). Effects of in vivo prematuration and in vivo final maturation on developmental capacity and quality of pre-implantation embryos. Theriogenology 57, 5–20.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Downs, S. M. (1997). Involvement of purine nucleotide synthetic pathways in gonadotropin-induced meiotic maturation in mouse cumulus cell-enclosed oocytes. Mol. Reprod. Dev. 46, 155–167.
PubMed |

Downs, S. M. , and Eppig, J. J. (1987). Induction of mouse oocyte maturation in vivo by perturbants of purine metabolism. Biol. Reprod. 36, 431–437.
PubMed |

Downs, S. M. , Humpherson, P. G. , and Leese, H. J. (1998). Meiotic induction in cumulus cell-enclosed mouse oocytes: involvement of the pentose phosphate pathway. Biol. Reprod. 58, 1084–1094.
PubMed |

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

Eppig, J. J. , and Downs, S. M. (1984). Chemical signals that regulate mammalian oocyte maturation. Biol. Reprod. 30, 1–11.
PubMed |

Eppig, J. J. , Ward-Bailey, P. F. , and Coleman, D. L. (1985). Hypoxanthine and adenosine in murine ovarian follicular fluid: concentrations and activity in maintaining oocyte meiotic arrest. Biol. Reprod. 33, 1041–1049.
PubMed |

Fortune, J. E. (1994). Ovarian follicular growth and development in mammals. Biol. Reprod. 50, 225–232.
PubMed |

Gardner, D. K. , and Leese, H. J. (1986). Non-invasive measurement of nutrient uptake by single cultured pre-implantation mouse embryos. Hum. Reprod. 1, 25–27.
PubMed |

Gardner, D. K. , and Leese, H. J. (1990). Concentrations of nutrients in mouse oviduct fluid and their effects on embryo development and metabolism in vitro. J. Reprod. Fertil. 88, 361–368.
PubMed |

Gardner, D. K. , Lane, M. , Calderon, I. , and Leeton, J. (1996). Environment of the preimplantation human embryo in vivo: metabolite analysis of oviduct and uterine fluids and metabolism of cumulus cells. Fertil. Steril. 65, 349–353.
PubMed |

Hagemann, L. J. , Beaumont, S. E. , Berg, M. , Donnison, M. J. , Ledgard, A. , Peterson, A. J. , Schurmann, A. , and Tervit, H. R. (1999). Development during single IVP of bovine oocytes from dissected follicles: interactive effects of estrous cycle stage, follicle size and atresia. Mol. Reprod. Dev. 53, 451–458.
PubMed |

Hashimoto, S. , Minami, N. , Takakura, R. , and Imai, H. (2002). Bovine immature oocytes acquire developmental competence during meiotic arrest in vitro. Biol. Reprod. 66, 1696–1701.
PubMed |

Ireland, J. J. , Murphee, R. L. , and Coulson, P. B. (1980). Accuracy of predicting stages of bovine estrous cycle by gross appearance of the corpus luteum. J. Dairy Sci. 63, 155–160.
PubMed |

Johnson, A. E. , Lane, M. , Gardner, D. K. , Diekman, M. A. , and Krisher, R. L. (2001). Changes in follicular fluid environment between 5 mm and 10 mm follicles. Biol. Reprod. 64(Suppl. 1), A128.[Abstract]


Jones, K. T. (2004). Turning it on and off: M-phase promoting factor during meiotic maturation and fertilization. Mol. Hum. Reprod. 10, 1–5.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Khurana, N. K. , and Niemann, H. (2000). Energy metabolism in preimplantation bovine embryos derived in vitro or in vivo. Biol. Reprod. 62, 847–856.
PubMed |

Krisher, R. L. , and Bavister, B. D. (1998). Responses of oocytes and embryos to the culture environment. Theriogenology 49, 103–114.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Krisher, R. L. , and Bavister, B. D. (1999). Enhanced glycolysis after maturation of bovine oocytes in vitro is associated with increased developmental competence. Mol. Reprod. Dev. 53, 19–26.
PubMed |

Leese, H. J. , and Barton, A. M. (1984). Pyruvate and glucose uptake by mouse ova and preimplantation embryos. J. Reprod. Fertil. 72, 9–13.
PubMed |

Leibfried-Rutledge, M. L. , Critser, E. S. , Eyestone, W. H. , Northey, D. L. , and First, N. L. (1987). Development potential of bovine oocytes matured in vitro or in vivo. Biol. Reprod. 36, 376–383.
PubMed |

Lim, J. M. , Lee, B. C. , Lee, E. S. , Chung, H. M. , Ko, J. J. , Park, S. E. , Cha, K. Y. , and Hwang, W. S. (1999). In vitro maturation and in vitro fertilization of bovine oocytes cultured in a chemically defined, protein-free medium: effects of carbohydrates and amino acids. Reprod. Fertil. Dev. 11, 127–132.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Luciano, A. M. , Pocar, P. , Milanesi, E. , Modina, S. , Rieger, D. , Lauria, A. , and Gandolfi, F. (1999). Effect of different levels of intracellular cAMP on the in vitro maturation of cattle oocytes and their subsequent development following in vitro fertilization. Mol. Reprod. Dev. 54, 86–91.
PubMed |

Miyano, T. , Ebihara, M. , Goto, Y. , Hirao, Y. , Nagai, T. , and Kato, S. (1995). Inhibitory action of hypoxanthine on meiotic resumption of denuded pig follicular oocytes in vitro. J. Exp. Zool. 273, 70–75.
PubMed |

Park, J. Y. , Su, Y. Q. , Ariga, M. , Law, E. , Jin, S. L. , and Conti, M. (2004). EGF-like growth factors as mediators of LH action in the ovulatory follicle. Science 303, 682–684.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Park, Y. S. , and Lin, Y. C. (1993). Effect of epidermal growth factor (EGF) and defined simple media on in vitro bovine oocyte maturation and early embryonic development. Theriogenology 39, 475–484.
Crossref | GoogleScholarGoogle Scholar |

Pincus, G. , and Enzmann, E. V. (1935). The comparative behaviour of mammalian eggs in-vivo and in-vitro in the activation of ovarian eggs. J. Exp. Med. 62, 665–675.
Crossref | GoogleScholarGoogle Scholar |

Quinn, P. , Kerin, J. F. , and Warnes, G. M. (1985). Improved pregnancy rate in human in vitro fertilization with the use of a medium based on the composition of human tubal fluid. Fertil. Steril. 44, 493–498.
PubMed |

Rieger, D. , and Loskutoff, N. M. (1994). Changes in the metabolism of glucose, pyruvate, glutamine and glycine during maturation of cattle oocytes in vitro. J. Reprod. Fertil. 100, 257–262.
PubMed |

Rose-Hellekant, T. A. , Libersky-Williamson, E. A. , and Bavister, B. D. (1998). Energy substrates and amino acids provided during in vitro maturation of bovine oocytes alter acquisition of developmental competence. Zygote 6, 285–294.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Sirard, M. A. (2001). Resumption of meiosis: mechanism involved in meiotic progression and its relation with developmental competence. Theriogenology 55, 1241–1254.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Sirard, M. A. , and First, N. L. (1988). In vitro inhibition of oocyte nuclear maturation in the bovine. Biol. Reprod. 39, 229–234.
PubMed |

Sirard, M. A. , Richard, F. , and Mayes, M. (1998). Controlling meiotic resumption in bovine oocytes: a review. Theriogenology 49, 483–497.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Sutton, M. L. , Cetica, P. D. , Beconi, M. T. , Kind, K. L. , Gilchrist, R. B. , and Thompson, J. G. (2003a). Influence of oocyte-secreted factors and culture duration on the metabolic activity of bovine cumulus cell complexes. Reproduction 126, 27–34.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Sutton, M. L. , Gilchrist, R. B. , and Thompson, J. G. (2003b). Effects of in-vivo and in-vitro environments on the metabolism of the cumulus–oocyte complex and its influence on oocyte developmental capacity. Hum. Reprod. Update 9, 35–48.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Sutton-McDowall, M. L. , Gilchrist, R. B. , and Thompson, J. G. (2004). Cumulus expansion and glucose utilisation by bovine cumulus–oocyte complexes during in vitro maturation: the influence of glucosamine and follicle-stimulating hormone. Reproduction 128, 313–319.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Tervit, H. R. , Whittingham, D. G. , and Rowson, L. E. (1972). Successful culture in vitro of sheep and cattle ova. J. Reprod. Fertil. 30, 493–497.
PubMed |

Thibault, C. , Szollosi, D. , and Gerard, M. (1987). Mammalian oocyte maturation. Reprod. Nutr. Dev. 27, 865–896.
PubMed |

Thomas, R. E. , Armstrong, D. T. , and Gilchrist, R. B. (2002). Differential effects of specific phosphodiesterase isoenzyme inhibitors on bovine oocyte meiotic maturation. Dev. Biol. 244, 215–225.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Thomas, R. E. , Armstrong, D. T. , and Gilchrist, R. B. (2003). Bovine cumulus cell–oocyte gap junctional communication during in vitro maturation in response to manipulation of cell-specific cyclic adenosine 3′,5′-monophosophate levels. Biol. Reprod. 70, 548–556.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Thomas, R. E. , Thompson, J. G. , Armstrong, D. T. , and Gilchrist, R. B. (2004). Effect of specific phosphodiesterase isoenzyme inhibitors during in vitro maturation of bovine oocytes on meiotic and developmental capacity. Biol. Reprod. 71, 1142–1149.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Tornell, J. , Brannstrom, M. , Magnusson, C. , and Billig, H. (1990). Effects of follicle stimulating hormone and purines on rat oocyte maturation. Mol. Reprod. Dev. 27, 254–260.
PubMed |

Trounson, A. , Anderiesz, C. , and Jones, G. (2001). Maturation of human oocytes in vitro and their developmental competence. Reproduction 121, 51–75.
Crossref | GoogleScholarGoogle Scholar | PubMed |

van de Leemput, E. E. , Vos, P. L. A. M. , Zeinstra, E. C. , Bevers, M. M. , and Dieleman, S. J. (1996). Comparison of the developmental potential of in vivo and in vitro maturated bovine oocytes in an in vitro test system. Theriogenology 45, 273.
Crossref | GoogleScholarGoogle Scholar |

Wehrend, A. , and Meinecke, B. (2001). Kinetics of meiotic progression, M-phase promoting factor (MPF) and mitogen-activated protein kinase (MAP kinase) activities during in vitro maturation of porcine and bovine oocytes: species specific differences in the length of the meiotic stages. Anim. Reprod. Sci. 66, 175–184.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Yang, M. Y. , and Rajamahendran, R. (2000). Morphological and biochemical identification of apoptosis in small, medium, and large bovine follicles and the effects of follicle-stimulating hormone and insulin-like growth factor-I on spontaneous apoptosis in cultured bovine granulosa cells. Biol. Reprod. 62, 1209–1217.
PubMed |

Zheng, P. , Bavister, B. D. , and Ji, W. (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 |