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

Glucose can reverse the effects of acute fasting on mouse ovulation and oocyte maturation

Jun Yan A , Bo Zhou A , Jie Yang A , Ping Tai A , Xiufen Chen A , Hua Zhang A , Meijia Zhang A and Guoliang Xia A B
+ Author Affiliations
- Author Affiliations

A State Key Laboratory of Agrobiotechnology, College of Biological Sciences, China Agricultural University, Beijing 100094, People’s Republic of China.

B Corresponding author. Email: glxiachina@sohu.com

Reproduction, Fertility and Development 20(6) 703-712 https://doi.org/10.1071/RD08034
Submitted: 21 February 2008  Accepted: 26 May 2008   Published: 9 July 2008

Abstract

Food deprivation suppresses ovulation. Although nutritional elements are responsible for this suppression, it is not clear whether energy metabolism has any effect on oocyte development under these circumstances. The aim of the present study was to determine which nutritional element is responsible for the effect of acute fasting on mouse ovulation and how oocyte development is affected. The results demonstrate that 64 h food deprivation blocks mouse ovulation. This was reversed by glucose feeding, oil feeding or short-term feeding, all of which elevated serum glucose levels. Furthermore, 48 h food deprivation inhibited follicle-stimulating hormone-induced oocyte maturation in vitro. However, 48 h glucose feeding increased serum glucose levels and restored oocyte maturation. Food deprivation increased serum progesterone levels and decreased serum oestradiol levels. Food deprivation also impaired follicle development, caused the death of oocytes and attenuated glucose consumption by cumulus–oocyte complexes. Taken together, the results indicate that: (1) the suppression of ovulation by acute fasting may be due to the control of oocyte development; and (2) maintaining serum glucose concentrations at a certain level is important for normal ovulation.

Additional keyword: nutrition.


Acknowledgements

This research was supported by the National Basic Research Program of China (Project no. 2007CB947401, 2004CB117502) and the Chinese Natural Science Foundation (No. 30571358).


References

Abecia, J. A. , Rhind, S. M. , Bramley, T. A. , and McMillen, S. M. (1995). Steroid production and LH receptor concentrations of ovarian follicles and corpora lutea and associated rates of ova wastage in ewes given high and low levels of food intake before and after mating. Anim. Sci. 61, 57–62.
Creed J., McEvoy T., Robinson J., Aitken R., Palmer R., and Robertson I. (1994). The effect of preovulatory nutrition on the subsequent development of superovulated sheep ova in an in vitro culture system. Anim. Prod. 58, 82.

Diskin, M. G. , Mackey, D. R. , Roche, J. F. , and Sreenan, J. M. (2003). Effects of nutrition and metabolic status on circulating hormones and ovarian follicle development in cattle. Anim. Reprod. Sci. 78, 345–370.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Downing, J. A. , Joss, J. , and Scaramuzzi, R. J. (1995a). Ovulation rate and the concentrations of gonadotrophins and metabolic hormones in ewes infused with glucose during the late luteal phase of the oestrous cycle. J. Endocrinol. 146, 403–410.
PubMed |

Downing, J. A. , Joss, J. , and Scaramuzzi, R. J. (1995b). A mixture of the branched chain amino acids, leucine, isoleucine and valine, increases ovulation rate in ewes when infused during the late luteal phase of the oestrous cycle: an effect that may be mediated by insulin. J. Endocrinol. 145, 315–323.
PubMed |

Downing, J. A. , Joss, J. , Connell, P. , and Scaramuzzi, R. J. (1995c). Ovulation rate and the concentrations of gonadotrophic and metabolic hormones in ewes fed lupin grain. J. Reprod. Fertil. 103, 137–145.
PubMed |

Downs, S. M. , and Mastropolo, A. M. (1994). The participation of energy substrates in the control of meiotic maturation in murine oocytes. Dev. Biol. 162, 154–168.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Downs, S. M. , and Utecht, A. M. (1999). Metabolism of radiolabeled glucose by mouse oocytes and oocyte–cumulus cell complexes. Biol. Reprod. 60, 1446–1452.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Downs, S. M. , Humpherson, P. G. , Martin, K. L. , and Leese, H. J. (1996). Glucose utilization during gonadotropin-induced meiotic maturation in cumulus cell-enclosed mouse oocytes. Mol. Reprod. Dev. 44, 121–131.
Crossref | GoogleScholarGoogle Scholar | 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.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Drickamer, L. C. , and Meikle, D. B. (1988). Food deprivation affects reproduction in adult female mice (Mus musculus) and the age of puberty for their female progeny. Acta Biol. Hung. 39, 361–375.
PubMed |

Eppig, J. J. , and Koide, S. L. (1978). Effects of progesterone and oestradiol-17beta on the spontaneous meiotic maturation of mouse oocytes. J. Reprod. Fertil. 53, 99–101.
PubMed |

Etienne, M. , Camous, S. , and Cuvillier, A. (1983). [Effects of feed restrictions during the growth of sows on their sexual maturity and subsequent reproduction]. Reprod. Nutr. Dev. 23, 309–319.[In French]
Crossref | GoogleScholarGoogle Scholar | PubMed |

Fagbohun, C. F. , and Downs, S. M. (1992). Requirement for glucose in ligand-stimulated meiotic maturation of cumulus cell-enclosed mouse oocytes. J. Reprod. Fertil. 96, 681–697.
PubMed |

Fu, M. , Chen, X. , Yan, J. , Lei, L. , Jin, S. , Yang, J. , Song, X. , Zhang, M. , and Xia, G. (2007). Luteinizing hormone receptors expression in cumulus cells closely related to mouse oocyte meiotic maturation. Front. Biosci. 12, 1804–1813.
PubMed |

Glick, Z. , Yamini, S. , Lupien, J. , and Sod-Moriah, U. (1990). Estrous cycle irregularities in overfed rats. Physiol. Behav. 47, 307–310.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Goren, S. , Piontkewitz, Y. , and Dekel, N. (1994). Meiotic arrest in incompetent rat oocytes is not regulated by cAMP. Dev. Biol. 166, 11–17.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Griffin, M. L. , South, S. A. , Yankov, V. I. , Booth, R. A. , Asplin, C. M. , Veldhuis, J. D. , and Evans, W. S. (1994). Insulin-dependent diabetes mellitus and menstrual dysfunction. Ann. Med. 26, 331–340.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Herrick, J. R. , Lane, M. , Gardner, D. K. , Behboodi, E. , Memili, E. , Blash, S. , Echelard, Y. , and Krisher, R. L. (2006). Metabolism, protein content, and in vitro embryonic development of goat cumulus–oocyte complexes matured with physiological concentrations of glucose and l-lactate. Mol. Reprod. Dev. 73, 256–266.
Crossref | l
-lactate.&journal=Mol. Reprod. Dev.&volume=73&pages=256-266&publication_year=2006&author=J%2E%20R%2E%20Herrick&hl=en&doi=10.1002/MRD.20407" target="_blank" rel="nofollow noopener noreferrer" class="reftools">GoogleScholarGoogle Scholar | PubMed |

I’Anson, H. , Foster, D. L. , Foxcroft, G. R. , and Booth, P. J. (1991). Nutrition and reproduction. Oxf. Rev. Reprod. Biol. 13, 239–311.
PubMed |

I’Anson, H. , Terry, S. K. , Lehman, M. N. , and Foster, D. L. (1997). Regional differences in the distribution of gonadotropin-releasing hormone cells between rapidly growing and growth-restricted prepubertal female sheep. Endocrinology 138, 230–236.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Krackow, S. (1989). Effect of food restriction on reproduction and lactation in house mice mated post partum. J. Reprod. Fertil. 86, 341–347.
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.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Landau, S. , Bor, A. , Leibovich, H. , Zoref, Z. , Nistan, Z. , and Madar, Z. (1995). The effect of ruminal starch degradability in the diet of Booroola crossbred ewes on induced ovulation rate and prolificacy. Anim. Reprod. Sci. 38, 97–108.
Crossref | GoogleScholarGoogle Scholar |

Li, J. H. , Ling, Y. Q. , Fan, J. J. , Zhang, X. P. , and Cui, S. (2006). Expression of cysteine sulfinate decarboxylase (CSD) in male reproductive organs of mice. Histochem. Cell Biol. 125, 607–613.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Linné, Y. (2004). Effects of obesity on women’s reproduction and complications during pregnancy. Obes. Rev. 5, 137–143.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Lozano, J. M. , Lonergan, P. , Boland, M. P. , and O’Callaghan, D. (2003). Influence of nutrition on the effectiveness of superovulation programmes in ewes: effect on oocyte quality and post-fertilization development. Reproduction 125, 543–553.
Crossref | GoogleScholarGoogle Scholar | PubMed |

McFarland, K. C. , Sprengel, R. , Phillips, H. S. , Kohler, M. , Rosemblit, N. , Nikolics, K. , Segaloff, D. L. , and Seeburg, P. H. (1989). Lutropin–choriogonadotropin receptor: an unusual member of the G protein-coupled receptor family. Science 245, 494–499.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Mishra, A. , and Joy, K. P. (2004). Ovarian monosaccharides (glucose and fructose): hormonal effects and their role in final oocyte maturation and egg quality in catfish Heteropneustes fossilis, Bloch. Indian J. Exp. Biol. 42, 1084–1090.
PubMed |

Munoz-Gutierrez, M. , Blache, D. , Martin, G. B. , and Scaramuzzi, R. J. (2002). Folliculogenesis and ovarian expression of mRNA encoding aromatase in anoestrous sheep after 5 days of glucose or glucosamine infusion or supplementary lupin feeding. Reproduction 124, 721–731.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Parr, R. A. , Davis, I. F. , Airclough, R. J. , and Miles, M. A. (1987). Overfeeding during early pregnancy reduces peripheral progesterone concentration and pregnancy rate in sheep. J. Reprod. Fertil. 80, 317–320.
PubMed |

Prunier, A. , and Quesnel, H. (2000). Influence of the nutritional status on ovarian development in female pigs. Anim. Reprod. Sci. 60–61, 185–197.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Rhind, S. , McKelvey, W. , McMillen, S. , Gunn, R. , and Elston, D. (1989). Effect of restricted food intake, before and/or after mating, on the reproductive performance of Greyface ewes. Anim. Prod. 48, 149–155.


Saiduddin, S. , Bray, G. A. , York, D. A. , and Swerdloff, R. S. (1973). Reproductive function in the genetically obese ‘fatty’ rat. Endocrinology 93, 1251–1256.
PubMed |

Schneider, J. E. (2004). Energy balance and reproduction. Physiol. Behav. 81, 289–317.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Spicer, L. J. , Sejrsen, K. , Tucker, H. A. , and Huber, J. T. (1984). Secretion of luteinizing hormone and follicle-stimulating hormone from overfeeding dairy heifers. J. Dairy Sci. 67, 1993–2000.
PubMed |

Spindler, R. E. , Pukazhenthi, B. S. , and Wildt, D. E. (2000). Oocyte metabolism predicts the development of cat embryos to blastocyst in vitro. Mol. Reprod. Dev. 56, 163–171.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Steger, R. W. , and Rabe, M. B. (1997). The effect of diabetes mellitus on endocrine and reproductive function. Proc. Soc. Exp. Biol. Med. 214, 1–11.
PubMed |

Vinoles, C. , Forsberg, M. , Martin, G. B. , Cajarville, C. , Repetto, J. , and Meikle, A. (2005). Short-term nutritional supplementation of ewes in low body condition affects follicle development due to an increase in glucose and metabolic hormones. Reproduction 129, 299–309.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Wade, G. N. , and Jones, J. E. (2004). Neuroendocrinology of nutritional infertility. Am. J. Physiol. Regul. Integr. Comp. Physiol. 287, R1277–R1296.
PubMed |

Wade, G. N. , and Schneider, J. E. (1992). Metabolic fuels and reproduction in female mammals. Neurosci. Biobehav. Rev. 16, 235–272.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Wallace, J. M. , Aitken, R. P. , and Cheyne, M. A. (1994). Effect of post-ovulation nutritional status in ewes on early conceptus survival and growth in vivo and luteotrophic protein secretion in vitro. Reprod. Fertil. Dev. 6, 253–259.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Williams, S. A. , Blache, D. , Martin, G. B. , Foot, R. , Blackberry, M. A. , and Scaramuzzi, R. J. (2001). Effect of nutritional supplementation on quantities of glucose transporters 1 and 4 in sheep granulosa and theca cells. Reproduction 122, 947–956.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Wongsrikeao, P. , Otoi, T. , Taniguchi, M. , Karja, N. W. , Agung, B. , Nii, M. , and Nagai, T. (2006). Effects of hexoses on in vitro oocyte maturation and embryo development in pigs. Theriogenology 65, 332–343.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Zamiri, M. J. (1978). Effects of reduced food intake on reproduction in mice. Aust. J. Biol. Sci. 31, 629–639.
PubMed |