Issue
Energy requirements in mammalian oogenesis
Corresponding Author(s) : Xingliang Jin
Cellular and Molecular Biology,
Vol. 64 No. 10: Issue 10
Abstract
Oogenesis is a lengthy, multi-step process occurring in mammals yielding single or multiple oocytes capable of being fertilized upon interaction with male gametes. The overall process is highly complex in nature, starting in the primordial follicles, and its ultimate completion is preceded by the meiotic cycle. There are two major phases in oogenesis: the growth phase, followed by a maturation phase that requires relatively less time. Both phases require energy for the various metabolic processes of the oocytes. The energy requirements and the timing of maturation vary significantly among mammalian species. This review describes the variations in the mammalian oocytes development and their energy requirements. It covers the types of mitochondria, the distribution of their changes, and the metabolic processes occurring during the oogenesis in different mammalian species. Oocyte abnormalities associated with glucose deficiency in mammals are discussed, along with the role of fat and protein as alternative energy substrates. The review concludes with recommendations for future studies on oogenesis in mammalian species in the context of energy requirements.
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- References
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References
References
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K. Theiler, The house mouse: atlas of embryonic development. (Springer Science & Business Media, 2013).
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N. Songsasen, R. E. Spindler, D. E. Wildt, Requirement for, and patterns of, pyruvate and glutamine metabolism in the domestic dog oocyte in vitro. Mol Reprod Dev 74, 870-877 (2007).
K. Jewgenow, N. Songsasen, in Reproductive sciences in animal conservation. (Springer, 2014), pp. 205-239.
M. Pepling, Oocyte Development before and during folliculogenesis. Oocyte Physiology and Development in Domestic Animals, 1-19 (2013).
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A. J. Watson, Oocyte cytoplasmic maturation: a key mediator of oocyte and embryo developmental competence. J Anim Sci 85, E1-3 (2007).
S. Assou et al., Dynamic changes in gene expression during human early embryo development: from fundamental aspects to clinical applications. Human reproduction update 17, 272-290 (2010).
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A. Gougeon, Human ovarian follicular development: from activation of resting follicles to preovulatory maturation. Ann Endocrinol (Paris) 71, 132-143 (2010).
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K. Reynaud et al., Folliculogenesis and morphometry of oocyte and follicle growth in the feline ovary. Reprod Domest Anim 44, 174-179 (2009).
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J. J. Eppig, M. O'Brien, K. Wigglesworth, Mammalian oocyte growth and development in vitro. Mol Reprod Dev 44, 260-273 (1996).
J. Van Blerkom, Mitochondria in human oogenesis and preimplantation embryogenesis: engines of metabolism, ionic regulation and developmental competence. Reproduction 128, 269-280 (2004).
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D. Voet, J. G. Voet, Biochemistry. 3 edn, John, Wiley & Sons, Inc., Hoboken, NJ. 1591 pp, (2004).
M. Ott, V. Gogvadze, S. Orrenius, B. Zhivotovsky, Mitochondria, oxidative stress and cell death. Apoptosis 12, 913-922 (2007).
Q. Y. Sun et al., Translocation of active mitochondria during pig oocyte maturation, fertilization and early embryo development in vitro. Reproduction 122, 155-163 (2001).
Y. Yu, R. Dumollard, A. Rossbach, F. A. Lai, K. Swann, Redistribution of mitochondria leads to bursts of ATP production during spontaneous mouse oocyte maturation. J Cell Physiol 224, 672-680 (2010).
J. Van Blerkom, P. Davis, V. Mathwig, S. Alexander, Domains of high-polarized and low-polarized mitochondria may occur in mouse and human oocytes and early embryos. Hum Reprod 17, 393-406 (2002).
R. G. Sturmey, P. J. O'Toole, H. J. Leese, Fluorescence resonance energy transfer analysis of mitochondrial:lipid association in the porcine oocyte. Reproduction 132, 829-837 (2006).
B. M. Acton, A. Jurisicova, I. Jurisica, R. F. Casper, Alterations in mitochondrial membrane potential during preimplantation stages of mouse and human embryo development. Mol Hum Reprod 10, 23-32 (2004).
J. Van Blerkom, P. Davis, S. Alexander, Inner mitochondrial membrane potential (DeltaPsim), cytoplasmic ATP content and free Ca2+ levels in metaphase II mouse oocytes. Hum Reprod 18, 2429-2440 (2003).
J. Van Blerkom, P. Davis, Mitochondrial signaling and fertilization. Mol Hum Reprod 13, 759-770 (2007).
W. Fujii, H. Funahashi, Exogenous adenosine reduces the mitochondrial membrane potential of murine oocytes during the latter half of in vitro maturation and pronuclear formation following chemical activation. J Reprod Dev 55, 187-193 (2009).
M. L. Sutton-McDowall, R. B. Gilchrist, J. G. Thompson, The pivotal role of glucose metabolism in determining oocyte developmental competence. Reproduction 139, 685-695 (2010).
R. L. Krisher, A. M. Brad, J. R. Herrick, M. L. Sparman, J. E. Swain, A comparative analysis of metabolism and viability in porcine oocytes during in vitro maturation. Anim Reprod Sci 98, 72-96 (2007).
H. Sato et al., The effect of glucose on the progression of the nuclear maturation of pig oocytes. Anim Reprod Sci 99, 299-305 (2007).
P. Zheng, B. D. Bavister, W. Ji, Energy substrate requirement for in vitro maturation of oocytes from unstimulated adult rhesus monkeys. Mol Reprod Dev 58, 348-355 (2001).
R. L. Krisher, B. D. Bavister, Enhanced glycolysis after maturation of bovine oocytes in vitro is associated with increased developmental competence. Mol Reprod Dev 53, 19-26 (1999).
J. R. Herrick, A. M. Brad, R. L. Krisher, Chemical manipulation of glucose metabolism in porcine oocytes: effects on nuclear and cytoplasmic maturation in vitro. Reproduction 131, 289-298 (2006).
T. E. Steeves, D. K. Gardner, Metabolism of glucose, pyruvate, and glutamine during the maturation of oocytes derived from pre-pubertal and adult cows. Mol Reprod Dev 54, 92-101 (1999).
Q. Wang et al., Mitochondrial dysfunction and apoptosis in cumulus cells of type I diabetic mice. PLoS One 5, e15901 (2010).
S. A. Colton, G. M. Pieper, S. M. Downs, Altered meiotic regulation in oocytes from diabetic mice. Biol Reprod 67, 220-231 (2002).
S. H. Purcell, K. H. Moley, Glucose transporters in gametes and preimplantation embryos. Trends Endocrinol Metab 20, 483-489 (2009).
R. Augustin et al., Glucose transporter expression is developmentally regulated in in vitro derived bovine preimplantation embryos. Mol Reprod Dev 60, 370-376 (2001).
L. F. Pisani et al., Effects of pre-mating nutrition on mRNA levels of developmentally relevant genes in sheep oocytes and granulosa cells. Reproduction 136, 303-312 (2008).
M. Dan-Goor, S. Sasson, A. Davarashvili, M. Almagor, Expression of glucose transporter and glucose uptake in human oocytes and preimplantation embryos. Hum Reprod 12, 2508-2510 (1997).
P. Zheng, R. Vassena, K. E. Latham, Effects of in vitro oocyte maturation and embryo culture on the expression of glucose transporters, glucose metabolism and insulin signaling genes in rhesus monkey oocytes and preimplantation embryos. Mol Hum Reprod 13, 361-371 (2007).
R. L. Brinster, Oxidation of pyruvate and glucose by oocytes of the mouse and rhesus monkey. J Reprod Fertil 24, 187-191 (1971).
P. Cetica, L. Pintos, G. Dalvit, M. Beconi, Activity of key enzymes involved in glucose and triglyceride catabolism during bovine oocyte maturation in vitro. Reproduction 124, 675-681 (2002).
J. D. Biggers, D. G. Whittingham, R. P. Donahue, The pattern of energy metabolism in the mouse oocyte and zygote. Proc Natl Acad Sci U S A 58, 560-567 (1967).
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