Issue

Vol. 64 No. 10: Issue 10

The undersigned hereby assign all rights, included but not limited to copyright, for this manuscript to CMB Association upon its submission for consideration to publication on Cellular and Molecular Biology. The rights assigned include, but are not limited to, the sole and exclusive rights to license, sell, subsequently assign, derive, distribute, display and reproduce this manuscript, in whole or in part, in any format, electronic or otherwise, including those in existence at the time this agreement was signed. The authors hereby warrant that they have not granted or assigned, and shall not grant or assign, the aforementioned rights to any other person, firm, organization, or other entity. All rights are automatically restored to authors if this manuscript is not accepted for publication.

Energy requirements in mammalian oogenesis

https://doi.org/10.14715/cmb/2018.64.10.3
Samuel Kofi Arhin
Department of Obstetrics and Gynecology, the Second Affiliated Hospital and Yuying Children's Hospital of Wenzhou Medical University, Wenzhou, Zhejiang 325027, China
Jieqiang Lu
Department of Obstetrics and Gynecology, the Second Affiliated Hospital and Yuying Children's Hospital of Wenzhou Medical University, Wenzhou, Zhejiang 325027, China
Haitao Xi
Department of Obstetrics and Gynecology, the Second Affiliated Hospital and Yuying Children's Hospital of Wenzhou Medical University, Wenzhou, Zhejiang 325027, China
Xingliang Jin
Department of Obstetrics and Gynecology, the Second Affiliated Hospital and Yuying Children's Hospital of Wenzhou Medical University, Wenzhou, Zhejiang 325027, China

Corresponding Author(s) : Xingliang Jin

jinxingsz4@hotmail.com

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.

Keywords

Oogenesis Oocyte metabolism Energy requirements Glucose transporters.
Arhin, S. K., Lu, J., Xi, H., & Jin, X. (2018). Energy requirements in mammalian oogenesis. Cellular and Molecular Biology, 64(10), 12–19. https://doi.org/10.14715/cmb/2018.64.10.3
Download Citation
Endnote/Zotero/Mendeley (RIS)
BibTeX
References
  1. References
  2. R. G. Edwards, A. H. Gates, Timing of the stages of the maturation divisions, ovulation, fertilization and the first cleavage of eggs of adult mice treated with gonadotrophins. J Endocrinol 18, 292-304 (1959).
  3. K. Theiler, The house mouse: atlas of embryonic development. (Springer Science & Business Media, 2013).
  4. K. Reynaud et al., In vivo meiotic resumption, fertilization and early embryonic development in the bitch. Reproduction 130, 193-201 (2005).
  5. 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).
  6. K. Jewgenow, N. Songsasen, in Reproductive sciences in animal conservation. (Springer, 2014), pp. 205-239.
  7. M. Pepling, Oocyte Development before and during folliculogenesis. Oocyte Physiology and Development in Domestic Animals, 1-19 (2013).
  8. D. F. Albertini, S. D. Limback, The natural life cycle of the mammalian oocyte. In Borini, A. and Coticchio, G. (eds), Preservation of Human Oocytes. Informa Healthcare, London. pp. 83-94, (2009).
  9. A. J. Watson, Oocyte cytoplasmic maturation: a key mediator of oocyte and embryo developmental competence. J Anim Sci 85, E1-3 (2007).
  10. 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).
  11. L. Gu et al., Metabolic control of oocyte development: linking maternal nutrition and reproductive outcomes. Cellular and molecular life sciences 72, 251-271 (2015).
  12. M. A. Edson, A. K. Nagaraja, M. M. Matzuk, The mammalian ovary from genesis to revelation. Endocr Rev 30, 624-712 (2009).
  13. H. M. Wear, M. J. McPike, K. H. Watanabe, From primordial germ cells to primordial follicles: a review and visual representation of early ovarian development in mice. Journal of ovarian research 9, 36 (2016).
  14. C. Tingen, A. Kim, T. K. Woodruff, The primordial pool of follicles and nest breakdown in mammalian ovaries. Mol Hum Reprod 15, 795-803 (2009).
  15. H. Peter, K. P. McNatty, The Ovary University of California Press, Berkley and Los Angeles. 175 pp., (1980).
  16. J. Xu, T. Gridley, Notch2 is required in somatic cells for breakdown of ovarian germ-cell nests and formation of primordial follicles. BMC biology 11, 13 (2013).
  17. A. Gougeon, Human ovarian follicular development: from activation of resting follicles to preovulatory maturation. Ann Endocrinol (Paris) 71, 132-143 (2010).
  18. H. M. Picton, Activation of follicle development: the primordial follicle. Theriogenology 55, 1193-1210 (2001).
  19. I. Kawashima, K. Kawamura, Disorganization of the germ cell pool leads to primary ovarian insufficiency. Reproduction 153, R205-R213 (2017).
  20. A. J. Hsueh, K. Kawamura, Y. Cheng, B. C. Fauser, Intraovarian control of early folliculogenesis. Endocrine reviews 36, 1-24 (2015).
  21. J. Griffin, B. R. Emery, I. Huang, C. M. Peterson, D. T. Carrell, Comparative analysis of follicle morphology and oocyte diameter in four mammalian species (mouse, hamster, pig, and human). J Exp Clin Assist Reprod 3, 2 (2006).
  22. K. Reynaud et al., Folliculogenesis and morphometry of oocyte and follicle growth in the feline ovary. Reprod Domest Anim 44, 174-179 (2009).
  23. N. Songsasen, A. Fickes, B. S. Pukazhenthi, D. E. Wildt, Follicular morphology, oocyte diameter and localisation of fibroblast growth factors in the domestic dog ovary. Reprod Domest Anim 44 Suppl 2, 65-70 (2009).
  24. N. Songsasen, D. E. Wildt, Oocyte biology and challenges in developing in vitro maturation systems in the domestic dog. Anim Reprod Sci 98, 2-22 (2007).
  25. J. J. Eppig, M. O'Brien, K. Wigglesworth, Mammalian oocyte growth and development in vitro. Mol Reprod Dev 44, 260-273 (1996).
  26. J. Van Blerkom, Mitochondria in human oogenesis and preimplantation embryogenesis: engines of metabolism, ionic regulation and developmental competence. Reproduction 128, 269-280 (2004).
  27. J. Ramalho-Santos et al., Mitochondrial functionality in reproduction: from gonads and gametes to embryos and embryonic stem cells. Hum Reprod Update 15, 553-572 (2009).
  28. K. Facecchia, L. A. Fochesato, S. D. Ray, S. J. Stohs, S. Pandey, Oxidative toxicity in neurodegenerative diseases: role of mitochondrial dysfunction and therapeutic strategies. J Toxicol 2011, 683728 (2011).
  29. M. G. Perrelli, P. Pagliaro, C. Penna, Ischemia/reperfusion injury and cardioprotective mechanisms: Role of mitochondria and reactive oxygen species. World J Cardiol 3, 186-200 (2011).
  30. D. Voet, J. G. Voet, Biochemistry. 3 edn, John, Wiley & Sons, Inc., Hoboken, NJ. 1591 pp, (2004).
  31. M. Ott, V. Gogvadze, S. Orrenius, B. Zhivotovsky, Mitochondria, oxidative stress and cell death. Apoptosis 12, 913-922 (2007).
  32. 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).
  33. 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).
  34. 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).
  35. 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).
  36. 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).
  37. 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).
  38. J. Van Blerkom, P. Davis, Mitochondrial signaling and fertilization. Mol Hum Reprod 13, 759-770 (2007).
  39. 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).
  40. 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).
  41. 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).
  42. 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).
  43. 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).
  44. 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).
  45. 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).
  46. 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).
  47. Q. Wang et al., Mitochondrial dysfunction and apoptosis in cumulus cells of type I diabetic mice. PLoS One 5, e15901 (2010).
  48. S. A. Colton, G. M. Pieper, S. M. Downs, Altered meiotic regulation in oocytes from diabetic mice. Biol Reprod 67, 220-231 (2002).
  49. S. H. Purcell, K. H. Moley, Glucose transporters in gametes and preimplantation embryos. Trends Endocrinol Metab 20, 483-489 (2009).
  50. R. Augustin et al., Glucose transporter expression is developmentally regulated in in vitro derived bovine preimplantation embryos. Mol Reprod Dev 60, 370-376 (2001).
  51. 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).
  52. 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).
  53. 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).
  54. R. L. Brinster, Oxidation of pyruvate and glucose by oocytes of the mouse and rhesus monkey. J Reprod Fertil 24, 187-191 (1971).
  55. 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).
  56. 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).
  57. N. Songsasen, S. Wesselowski, J. W. Carpenter, D. E. Wildt, The ability to achieve meiotic maturation in the dog oocyte is linked to glycolysis and glutamine oxidation. Mol Reprod Dev 79, 186-196 (2012).
  58. S. M. Downs, The influence of glucose, cumulus cells, and metabolic coupling on ATP levels and meiotic control in the isolated mouse oocyte. Dev Biol 167, 502-512 (1995).
  59. D. Rieger, N. M. Loskutoff, Changes in the metabolism of glucose, pyruvate, glutamine and glycine during maturation of cattle oocytes in vitro. J Reprod Fertil 100, 257-262 (1994).
  60. R. E. Spindler, B. S. Pukazhenthi, D. E. Wildt, Oocyte metabolism predicts the development of cat embryos to blastocyst in vitro. Mol Reprod Dev 56, 163-171 (2000).
  61. J. Garcia et al., Regulation of mitochondrial glutathione redox status and protein glutathionylation by respiratory substrates. J Biol Chem 285, 39646-39654 (2010).
  62. P. Newsholme et al., Glutamine and glutamate as vital metabolites. Braz J Med Biol Res 36, 153-163 (2003).
  63. S. M. Downs, P. G. Humpherson, H. J. Leese, Meiotic induction in cumulus cell-enclosed mouse oocytes: involvement of the pentose phosphate pathway. Biol Reprod 58, 1084-1094 (1998).
  64. F. Urner, D. Sakkas, Involvement of the pentose phosphate pathway and redox regulation in fertilization in the mouse. Mol Reprod Dev 70, 494-503 (2005).
  65. H. Funahashi, T. Koike, R. Sakai, Effect of glucose and pyruvate on nuclear and cytoplasmic maturation of porcine oocytes in a chemically defined medium. Theriogenology 70, 1041-1047 (2008).
  66. R. Roberts et al., Energy substrate metabolism of mouse cumulus-oocyte complexes: response to follicle-stimulating hormone is mediated by the phosphatidylinositol 3-kinase pathway and is associated with oocyte maturation. Biol Reprod 71, 199-209 (2004).
  67. S. M. Downs, A. M. Utecht, Metabolism of radiolabeled glucose by mouse oocytes and oocyte-cumulus cell complexes. Biol Reprod 60, 1446-1452 (1999).
  68. K. A. Zuelke, B. G. Brackett, Effects of luteinizing hormone on glucose metabolism in cumulus-enclosed bovine oocytes matured in vitro. Endocrinology 131, 2690-2696 (1992).
  69. W. Y. Son, M. Das, E. Shalom-Paz, H. Holzer, Mechanisms of follicle selection and development. Minerva Ginecol 63, 89-102 (2011).
  70. M. Hsieh, K. Thao, M. Conti, Genetic dissection of epidermal growth factor receptor signaling during luteinizing hormone-induced oocyte maturation. PLoS One 6, e21574 (2011).
  71. Q. Y. Sun, Y. L. Miao, H. Schatten, Towards a new understanding on the regulation of mammalian oocyte meiosis resumption. Cell Cycle 8, 2741-2747 (2009).
  72. D. Gardner, H. Leese, The role of glucose and pyruvate transport in regulating nutrient utilization by preimplantation mouse embryos. Development 104, 423-429 (1988).
  73. I. S. Wood, P. Trayhurn, Glucose transporters (GLUT and SGLT): expanded families of sugar transport proteins. British Journal of Nutrition 89, 3-9 (2003).
  74. 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. Molecular human reproduction 13, 361-371 (2007).
  75. 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).
  76. M. Dan-Goor, S. Sasson, A. Davarashvili, M. Almagor, Expression of glucose transporter and glucose uptake in human oocytes and preimplantation embryos. Human reproduction 12, 2508-2510 (1997).
  77. R. Augustin et al., Glucose transporter expression is developmentally regulated in in vitro derived bovine preimplantation embryos. Molecular reproduction and development 60, 370-376 (2001).
  78. H. Nishimoto et al., Gene expression of glucose transporter (GLUT) 1, 3 and 4 in bovine follicle and corpus luteum. Journal of Endocrinology 188, 111-119 (2006).
  79. S. Williams et al., Effect of nutritional supplementation on quantities of glucose transporters 1 and 4 in sheep granulosa and theca cells. Reproduction 122, 947-956 (2001).
  80. M. J. Charron, F. C. Brosius, S. L. Alper, H. F. Lodish, A glucose transport protein expressed predominately in insulin-responsive tissues. Proceedings of the National Academy of Sciences 86, 2535-2539 (1989).
  81. M. Aghayan et al., Developmental expression and cellular localization of glucose transporter molecules during mouse preimplantation development. Development 115, 305-312 (1992).
  82. Y. Morita et al., Expression and possible function of glucose transporter protein GLUT1 during preimplantation mouse development from oocytes to blastocysts. Biochemical and biophysical research communications 188, 8-15 (1992).
  83. S. H. Purcell, K. H. Moley, Glucose transporters in gametes and preimplantation embryos. Trends in Endocrinology & Metabolism 20, 483-489 (2009).
  84. K. Moley, M.-Y. Chi, C. Knudson, S. Korsmeyer, M. Mueckler, Hyperglycemia induces apoptosis in pre-implantation embryos through cell death effector pathways. Nature medicine 4, (1998).
  85. S. E. Harris, H. J. Leese, R. G. Gosden, H. M. Picton, Pyruvate and oxygen consumption throughout the growth and development of murine oocytes. Molecular reproduction and development 76, 231-238 (2009).
  86. H. J. Leese, A. M. Barton, Production of pyruvate by isolated mouse cumulus cells. Journal of Experimental Zoology Part A: Ecological Genetics and Physiology 234, 231-236 (1985).
  87. K. Hardy et al., Non-invasive measurement of glucose and pyruvate uptake by individual human oocytes and preimplantation embryos. Human reproduction 4, 188-191 (1989).
  88. A. P. Halestrap, N. T. PRICE, The proton-linked monocarboxylate transporter (MCT) family: structure, function and regulation. Biochemical Journal 343, 281-299 (1999).
  89. K. Pierre, L. Pellerin, Monocarboxylate transporters in the central nervous system: distribution, regulation and function. Journal of neurochemistry 94, 1-14 (2005).
  90. S. Jansen, M. Pantaleon, P. L. Kaye, Characterization and regulation of monocarboxylate cotransporters Slc16a7 and Slc16a3 in preimplantation mouse embryos. Biology of reproduction 79, 84-92 (2008).
  91. E. Harding, M. Day, C. Gibb, M. Johnson, D. Cook, The activity of the H+-monocarboxylate cotransporter during pre-implantation development in the mouse. Pflügers Archiv European Journal of Physiology 438, 397-404 (1999).
  92. F. Hérubel, S. El Mouatassim, P. Guérin, R. Frydman, Y. Ménézo, Genetic expression of monocarboxylate transporters during human and murine oocyte maturation and early embryonic development. Zygote 10, 175-181 (2002).
  93. S. A. Colton, G. M. Pieper, S. M. Downs, Altered meiotic regulation in oocytes from diabetic mice. Biology of reproduction 67, 220-231 (2002).
  94. A. Wyman, A. B. Pinto, R. Sheridan, K. H. Moley, One-cell zygote transfer from diabetic to nondiabetic mouse results in congenital malformations and growth retardation in offspring. Endocrinology 149, 466-469 (2008).
  95. J. Zhou, M. Bievre, C. Bondy, Reduced GLUT1 expression in Igf1–/–null oocytes and follicles. Growth Hormone & IGF Research 10, 111-117 (2000).
  96. A. Frolova et al., Facilitative glucose transporter type 1 is differentially regulated by progesterone and estrogen in murine and human endometrial stromal cells. Endocrinology 150, 1512-1520 (2009).
  97. S. M. Downs, E. D. Hudson, Energy substrates and the completion of spontaneous meiotic maturation. Zygote 8, 339-351 (2000).
  98. J. E. Loewenstein, A. I. Cohen, Dry Mass, Lipid Content and Protein Content of the Intact and Zona-Free Mouse Ovum. J Embryol Exp Morphol 12, 113-121 (1964).
  99. R. G. Sturmey, A. Reis, H. J. Leese, T. G. McEvoy, Role of fatty acids in energy provision during oocyte maturation and early embryo development. Reprod Domest Anim 44 Suppl 3, 50-58 (2009).
  100. E. M. Ferguson, H. J. Leese, A potential role for triglyceride as an energy source during bovine oocyte maturation and early embryo development. Mol Reprod Dev 73, 1195-1201 (2006).
  101. S. M. Downs, P. G. Humpherson, H. J. Leese, Pyruvate utilization by mouse oocytes is influenced by meiotic status and the cumulus oophorus. Mol Reprod Dev 62, 113-123 (2002).
  102. S. M. Downs, A. M. Mastropolo, The participation of energy substrates in the control of meiotic maturation in murine oocytes. Dev Biol 162, 154-168 (1994).
  103. R. G. Sturmey, H. J. Leese, Energy metabolism in pig oocytes and early embryos. Reproduction 126, 197-204 (2003).
  104. K. R. Dunning et al., Beta-oxidation is essential for mouse oocyte developmental competence and early embryo development. Biol Reprod 83, 909-918 (2010).
  105. K. R. Dunning, L. K. Akison, D. L. Russell, R. J. Norman, R. L. Robker, Increased beta-oxidation and improved oocyte developmental competence in response to l-carnitine during ovarian in vitro follicle development in mice. Biol Reprod 85, 548-555 (2011).
Read More

Author Biographies

Jieqiang Lu, Department of Obstetrics and Gynecology, the Second Affiliated Hospital and Yuying Children's Hospital of Wenzhou Medical University, Wenzhou, Zhejiang 325027, China
Medical University, Wenzhou, Zhejiang 325027, China
Xingliang Jin, Department of Obstetrics and Gynecology, the Second Affiliated Hospital and Yuying Children's Hospital of Wenzhou Medical University, Wenzhou, Zhejiang 325027, China

Professor MD, PhD

Department of Obstetrics and Gynecology, the Second Affiliated Hospital and Yuying Children's Hospital of Wenzhou Medical University, Wenzhou, Zhejiang 325027, China

Crossref
Scopus
Google Scholar
Europe PMC
Download this PDF file
PDF
Statistic
Read Counter : 1241 Download : 614