Abstract

In most animal species female germ cells are the source of mitochondrial genome for the whole body of individuals. As a source of mitochondrial DNA for future generations the mitochondria in the female germ line undergo dynamic quantitative and qualitative changes. In addition to maintaining the intact template of mitochondrial genome from one generation to another, mitochondrial role in oocytes is much more complex and pleiotropic. The quality of mitochondria determines the ability of meiotic divisions, fertilization ability, and activation after fertilization or sustaining development of a new embryo. The presence of normal number of functional mitochondria is also crucial for proper implantation and pregnancy maintaining. This article addresses issues of mitochondrial role and function in mammalian oocyte and presents new approaches in studies of mitochondrial function in female germ cells.

References

• 1. Acton B.M., Jurisicova A., Jurisica I., Casper R.F.: Alterations in mitochondrial membrane potential during preimplantation stages of mouse and human embryo development. Mol. Hum. Reprod., 2004; 10: 23-32
  Google Scholar
• 2. Alexeyev M., Shokolenko I., Wilson G., LeDoux S.: The maintenance of mitochondrial DNA integrity – critical analysis and update. Cold Spring Harb. Perspect. Biol., 2013; 5: a012641
  Google Scholar
• 3. Amaral A., Lourenço B., Marques M., Ramalho-Santos J.: Mitochondria functionality and sperm quality. Reproduction, 2013; 146: R163-R174
  Google Scholar
• 4. Ameur A., Stewart J.B., Freyer C., Hagström E., Ingman M., Larsson N.G., Gyllensten U.: Ultra-deep sequencing of mouse mitochondrial DNA: mutational patterns and their origins. PLoS Genet., 2011; 7: e1002028
  Google Scholar
• 5. Ankel-Simons F., Cummins J.M.: Misconceptions about mitochondria and mammalian fertilization: implications for theories on human evolution. Proc. Natl. Acad. Sci. USA, 1996; 93: 13859-13863
  Google Scholar
• 6. Assou S., Haouzi D., De Vos J., Hamamah S.: Human cumulus cells as biomarkers for embryo and pregnancy outcomes. Mol. Hum. Reprod., 2010; 16: 531-538
  Google Scholar
• 7. Baumann C.G., Morris D.G., Sreenan J.M., Leese H.J.: The quiet embryo hypothesis: molecular characteristics favoring viability. Mol. Reprod. Dev., 2007; 74: 1345-1353
  Google Scholar
• 8. Bavister B.D., Squirrell J.M.: Mitochondrial distribution and function in oocytes and early embryos. Hum. Reprod., 2000; 15: 189-198
  Google Scholar
• 9. Ben-Meir A., Yahalomi S., Moshe B., Shufaro Y., Reubinoff B., Saada A.: Coenzyme Q-dependent mitochondrial respiratory chain activity in granulosa cells is reduced with aging. Fertil. Steril., 2015; 104: 724-727
  Google Scholar
• 10. Bentov Y., Casper R.F.: The aging oocyte – can mitochondrial function be improved? Fertil. Steril, 2013; 99: 18-22
  Google Scholar
• 11. Boucret L., Chao de la Barca J.M., Morinière C., Desquiret V., Ferré-L’Hôtellier V., Descamps P., Marcaillou C., Reynier P., Procaccio V., May-Panloup P.: Relationship between diminished ovarian reserve and mitochondrial biogenesis in cumulus cells. Hum Reprod., 2015; 30: 1653-1664
  Google Scholar
• 12. Bratic I., Hench J., Henriksson J., Antebi A., Bürglin T.R., Trifunovic A.: Mitochondrial DNA level, but not active replicase, is essential for Caenorhabditis elegans development. Nucleic Acids Res., 2009; 37: 1817-1828
  Google Scholar
• 13. Brown D.T., Herbert M., Lamb V.K., Chinnery P.F., Taylor R.W., Lightowlers R.N., Craven L., Cree L., Gardner J.L., Turnbull D.M.: Transmission of mitochondrial DNA disorders: possibilities for the future. Lancet, 2006; 368: 87-89
  Google Scholar
• 14. Cam H., Balciunaite E., Blais A., Spektor A., Scarpulla R.C., Young R., Kluger Y., Dynlacht B.D.: A common set of gene regulatory networks links metabolism and growth inhibition. Mol. Cell., 2004; 16: 399-411
  Google Scholar
• 15. Carroll J., Marangos P.: The DNA damage response in mammalian oocytes. Front. Genet., 2013; 4: 117
  Google Scholar
• 16. Cetica P.D., Pintos L.N., Dalvit G.C., Beconi M.T.: Antioxidant enzyme activity and oxidative stress in bovine oocyte in vitro maturation. IUBMB Life, 2001; 51: 57-64
  Google Scholar
• 17. Chen X., Prosser R., Simonetti S., Sadlock J., Jagiello G., Schon E.A.: Rearranged mitochondrial genomes are present in human oocytes. Am. J. Hum. Genet., 1995; 57: 239-247
  Google Scholar
• 18. Cheng Y., Yata A., Klein C., Cho J.H., Deguchi M., Hsueh A.J.: Oocyte-expressed interleukin 7 suppresses granulosa cell apoptosis and promotes oocyte maturation in rats. Biol. Reprod., 2011; 84: 707-714
  Google Scholar
• 19. Chinnery P.F., Hudson G.: Mitochondrial genetics. Br. Med. Bull., 2013; 106: 135-159
  Google Scholar
• 20. Cotterill M., Harris S.E., Collado Fernandez E., Lu J., Huntriss J.D., Campbell B.K., Picton H.M.: The activity and copy number of mitochondrial DNA in ovine oocytes throughout oogenesis in vivo and during oocyte maturation in vitro. Mol. Hum. Reprod., 2013; 19: 444-450
  Google Scholar
• 21. Cree L.M., Hammond E.R., Shelling A.N., Berg M.C., Peek J.C., Green M.P.: Maternal age and ovarian stimulation independently affect oocyte mtDNA copy number and cumulus cell gene expression in bovine clones. Hum. Reprod., 2015; 30: 1410-1420
  Google Scholar
• 22. Cree L.M., Samuels D.C., Chinnery P.F.: The inheritance of pathogenic mitochondrial DNA mutations. Biochim. Biophys. Acta, 2009; 1792: 1097-1102
  Google Scholar
• 23. Cummins J.M.: Mitochondria: potential roles in embryogenesis and nucleocytoplasmic transfer. Hum. Reprod. Update, 2001; 7: 217-228
  Google Scholar
• 24. Dal-Cim T., Molz S., Egea J., Parada E., Romero A., Budni J., Martín de Saavedra M.D., del Barrio L., Tasca C.I., López M.G.: Guanosine protects human neuroblastoma SH-SY5Y cells against mitochondrial oxidative stress by inducing heme oxigenase-1 via PI3K/Akt/GSK-3β pathway. Neurochem. Int., 2012; 61: 397-404
  Google Scholar
• 25. Dalton C.M., Carroll J.: Biased inheritance of mitochondria during asymmetric cell division in the mouse oocyte. J. Cell Sci., 2013; 126: 2955–2964
  Google Scholar
• 26. Dalton C.M., Szabadkai G., Carroll J.: Measurement of ATP in single oocytes: impact of maturation and cumulus cells on levels and consumption. J. Cell. Physiol., 2014; 229: 353–361
  Google Scholar
• 27. de Paula W.B., Agip A.N., Missirlis F., Ashworth R., Vizcay-Barrena G., Lucas C.H., Allen J.F.: Female and male gamete mitochondria are distinct and complementary in transcription, structure, and genome function. Genome Biol. Evol., 2013; 5: 1969-1977
  Google Scholar
• 28. de Paula W.B., Lucas C.H., Agip A.N., Vizcay-Barrena G., Allen J.F.: Energy, ageing, fidelity and sex: oocyte mitochondrial DNA as a protected genetic template. Philos. Trans. R. Soc. Lond. B. Biol. Sci., 2013; 368: 20120263
  Google Scholar
• 29. Eiachenlaub-Ritter U.: Oocyte ageing and its cellular basis. Int. J. Dev. Biol., 2012; 56: 841-852
  Google Scholar
• 30. Eichenlaub-Ritter U., Wieczorek M., Lüke S., Seidel T.: Age related changes in mitochondrial function and new approaches to study redox regulation in mammalian oocytes in response to age or maturation conditions. Mitochondrion, 2011; 11: 783-796
  Google Scholar
• 31. El Shourbagy S.H., Spikings E.C., Freitas M., St John J.C.: Mitochondria directly influence fertilisation outcome in the pig. Reproduction, 2006; 131: 233-245
  Google Scholar
• 32. Elson J.L., Samuels D.C., Turnbull D.M., Chinnery P.F.: Random intracellular drift explains the clonal expansion of mitochondrial DNA mutations with age. Am. J. Hum. Genet., 2001; 68: 802-806
  Google Scholar
• 33. Faddy M.J., Gosden R.G., Gougeon A., Richardson S.J., Nelson J.F.: Accelerated disappearance of ovarian follicles in mid-life: implications for forecasting menopause. Hum. Reprod., 1992; 7: 1342-1346
  Google Scholar
• 34. Fischer B., Bavister B.D.: Oxygen tension in the oviduct and uterus of rhesus monkeys, hamsters and rabbits. J. Reprod. Fertil., 1993; 99: 673-679
  Google Scholar
• 35. Ge H.S., Zhang F., Li X.H., Chen H., Xi H.T., Huang J.Y., Zhu C.F., Lü J.Q.: Effects of controlled ovarian hyperstimulation on mitochondria copy number and functions in murine oocytes. Zhonghua Fu Chan Ke Za Zhi, 2013; 48: 858-861
  Google Scholar
• 36. Ghaffari Novin M., Noruzinia M., Allahveisi A., Saremi A., Fadaei Fathabadi F., Mastery Farahani R., Dehghani Fard A., Pooladi A., Mazaherinezhad Fard R., Yousefian E.: Comparison of mitochondrial- -related transcriptional levels of TFAM, NRF1 and MT-CO1 genes in single human oocytes at various stages of the oocyte maturation. Iran. Biomed. J., 2015; 19: 23-28
  Google Scholar
• 37. Ghiselli F., Milani L., Guerra D., Chang P.L., Breton S., Nuzhdin S.V., Passamonti M.: Structure, transcription, and variability of metazoan mitochondrial genome: perspectives from an unusual mitochondrial inheritance system. Genome Biol. Evol., 2013; 5: 1535-1554
  Google Scholar
• 38. Gibson T.C., Kubisch H.M., Brenner C.A.: Mitochondrial DNA deletions in rhesus macaque oocytes and embryos. Mol. Hum. Reprod., 2005; 11: 785-789
  Google Scholar
• 39. Goo C.K., Lim H.Y., Ho Q.S., Too H.P., Clement M.V., Wong K.P.: PTEN/Akt signaling controls mitochondrial respiratory capacity through 4E-BP1. PLoS One, 2012; 7: e45806
  Google Scholar
• 40. Grindler N.M., Moley K.H.: Maternal obesity, infertility and mitochondrial dysfunction: potential mechanisms emerging from mouse model systems. Mol. Hum. Reprod., 2013; 19: 486-494
  Google Scholar
• 41. Grupen C.G., Armstrong D.T.: Relationship between cumulus cell apoptosis, progesterone production and porcine oocyte developmental competence: temporal effects of follicular fluid during IVM. Reprod. Fertil. Dev., 2010; 22: 1100-1109
  Google Scholar
• 42. Haas R.H., Parikh S., Falk M.J., Saneto R.P., Wolf N.I., Darin N., Cohen B.H.: Mitochondrial disease: a practical approach for primary care physicians. Pediatrics, 2007; 120: 1326-1333
  Google Scholar
• 43. Hagström E., Freyer C., Battersby B.J., Stewart J.B., Larsson N.G.: No recombination of mtDNA after heteroplasmy for 50 generations in the mouse maternal germline. Nucleic Acids Res., 2014; 42: 1111- 1116
  Google Scholar
• 44. Harris S.E., Leese H.J., Gosden R.G., Picton H.M.: Pyruvate and oxygen consumption throughout the growth and development of murine oocytes. Mol. Reprod. Dev., 2009; 76: 231-238
  Google Scholar
• 45. Holt I.J., Harding A.E., Morgan-Hughes J.A.: Deletions of muscle mitochondrial DNA in patients with mitochondrial myopathies. Nature, 1988; 331: 717-719
  Google Scholar
• 46. Holt J.E., Jones K.T.: Control of homologous chromosome division in the mammalian oocyte. Mol. Hum. Reprod., 2009; 15: 139-147
  Google Scholar
• 47. Hussein T.S., Froiland D.A., Amato F., Thompson J.G., Gilchrist R.B.: Oocytes prevent cumulus cell apoptosis by maintaining a morphogenic paracrine gradient of bone morphogenetic proteins. J. Cell Sci., 2005; 118: 5257-5268
  Google Scholar
• 48. Igosheva N., Abramov A.Y., Poston L., Eckert J.J., Fleming T.P., Duchen M.R., McConnell J.: Maternal diet-induced obesity alters mitochondrial activity and redox status in mouse oocytes and zygotes. PLoS One, 2010; 5: e10074
  Google Scholar
• 49. Inoue K., Nakada K., Ogura A., Isobe K., Goto Y., Nonaka I., Hayashi J.I.: Generation of mice with mitochondrial dysfunction by introducing mouse mtDNA carrying a deletion into zygotes. Nat. Genet., 2000; 26: 176-181
  Google Scholar
• 50. Iwata H., Goto H., Tanaka H., Sakaguchi Y., Kimura K., Kuwayama T., Monji Y.: Effect of maternal age on mitochondrial DNA copy number, ATP content and IVF outcome of bovine oocytes. Reprod. Fertil. Dev., 2011; 23: 424-432
  Google Scholar
• 51. Kaneko T., Saito H., Takahashi T., Ohta N., Saito T., Hiroi M.: Effects of controlled ovarian hyperstimulation on oocyte quality in terms of the incidence of apoptotic granulosa cells. J. Assist. Reprod. Genet., 2000; 17: 580-585
  Google Scholar
• 52. Kimura N., Tsunoda S., Iuchi Y., Abe H., Totsukawa K., Fujii J.: Intrinsic oxidative stress causes either 2-cell arrest or cell death depending on developmental stage of the embryos from SOD1-deficient mice. Mol. Hum. Reprod., 2010; 16: 441-451
  Google Scholar
• 53. Kitagawa T., Suganuma N., Nawa A., Kikkawa F., Tanaka M., Ozawa T., Tomoda Y.: Rapid accumulation of deleted mitochondrial deoxyribonucleic acid in postmenopausal ovaries. Biol. Reprod., 1993; 49: 730-736
  Google Scholar
• 54. Kogo N., Tazaki A., Kashino Y., Morichika K., Orii H., Mochii M., Watanabe K.: Germ-line mitochondria exhibit suppressed respiratory activity to support their accurate transmission to the next generation. Dev. Biol., 2011; 349: 462-469
  Google Scholar
• 55. Kujjo L.L., Perez G.I.: Ceramide and mitochondrial function in aging oocytes: joggling a new hypothesis and old players. Reproduction, 2012; 143: 1-10
  Google Scholar
• 56. Kushnir V.A., Ludaway T., Russ R.B., Fields E.J., Koczor C., Lewis W.: Reproductive aging is associated with decreased mitochondrial abundance and altered structure in murine oocytes. J. Assist. Reprod. Genet., 2012; 29: 637-642
  Google Scholar
• 57. Larsson N.G.: Somatic mitochondrial DNA mutations in mammalian aging. Annu. Rev. Biochem., 2010; 79: 683-706
  Google Scholar
• 58. Leese H.J., Baumann C.G., Brison D.R., McEvoy T.G., Sturmey R.G.: Metabolism of the viable mammalian embryo: quietness revisited. Mol. Hum. Reprod., 2008; 14: 667-672
  Google Scholar
• 59. Li R., Albertini D.F.: The road to maturation: somatic cell interaction and self-organization of the mammalian oocyte. Nat. Rev. Mol. Cell Biol., 2013; 14: 141-152
  Google Scholar
• 60. Lim J., Luderer U.: Oxidative damage increases and antioxidant gene expression decreases with aging in the mouse ovary. Biol. Reprod., 2011; 84: 775-782
  Google Scholar
• 61. Lin F., Ma X.S., Wang Z.B., Wang Z.W., Luo Y.B., Huang L., Jiang Z.Z., Hu M.W., Schatten H., Sun Q.Y.: Different fates of oocytes with DNA double-strand breaks in vitro and in vivo. Cell Cycle, 2014; 13: 2674-2680
  Google Scholar
• 62. Liu P., Demple B.: DNA repair in mammalian mitochondria: much more than we thought? Environ. Mol. Mutagen., 2010; 51: 417-426
  Google Scholar
• 63. Lord T., Aitken R.J.: Oxidative stress and ageing of the post-ovulatory oocyte. Reproduction, 2013; 146: R217-R227
  Google Scholar
• 64. Luo S.M., Ge Z.J., Wang Z.W., Jiang Z.Z., Wang Z.B., Ouyang Y.C., Hou Y., Schatten H., Sun Q.Y.: Unique insights into maternal mitochondrial inheritance in mice. Proc. Natl. Acad. Sci. USA, 2013; 110: 13038-13043
  Google Scholar
• 65. Luzzo K.M., Wang Q., Purcell S.H., Chi M., Jimenez P.T., Grindler N., Schedl T., Moley K.H.: High fat diet induced developmental defects in the mouse: oocyte meiotic aneuploidy and fetal growth retardation/brain defects. PLoS One, 2012; 7: e49217
  Google Scholar
• 66. Mahrous E., Yang Q., Clarke H.J.: Regulation of mitochondrial DNA accumulation during oocyte growth and meiotic maturation in the mouse. Reproduction, 2012; 144: 177-185
  Google Scholar
• 67. Mao J., Whitworth K.M., Spate L.D., Walters E.M., Zhao J., Prather R.S.: Regulation of oocyte mitochondrial DNA copy number by follicular fluid, EGF, and neuregulin 1 during in vitro maturation affects embryo development in pigs. Theriogenology, 2012; 78: 887-897
  Google Scholar
• 68. Matsuda F., Inoue N., Manabe N., Ohkura S.: Follicular growth and atresia in mammalian ovaries: regulation by survival and death of granulosa cells. J. Reprod. Dev., 2012; 58: 44-50
  Google Scholar
• 69. McGinnis L.K., Limback S.D., Albertini D.F.: Signaling modalities during oogenesis in mammals. Curr. Top. Dev. Biol., 2013; 102: 227-242
  Google Scholar
• 70. McInnes J.: Mitochondrial-associated metabolic disorders: foundations, pathologies and recent progress. Nutr. Metab., 2013; 10: 63
  Google Scholar
• 71. Ménézo Y., Dale B., Cohen M.: DNA damage and repair in human oocytes and embryos: a review. Zygote, 2010; 18: 357-365
  Google Scholar
• 72. Miao Y., Liu X., Qiao T.W., Miao D.Q., Luo M.J., Tan J.H.: Cumulus cells accelerate aging of mouse oocytes. Biol. Reprod., 2005; 73: 1025-1031
  Google Scholar
• 73. Motta P.M., Nottola S.A., Makabe S., Heyn R.: Mitochondrial morphology in human fetal and adult female germ cells. Hum. Reprod., 2000; 15: 129-147
  Google Scholar
• 74. Muftuoglu M., Mori M.P., de Souza-Pinto N.C.: Formation and repair of oxidative damage in the mitochondrial DNA. Mitochondrion, 2014; 17: 164-181
  Google Scholar
• 75. Nagano M., Katagiri S., Takahashi Y.: Relationship between bovine oocyte morphology and in vitro developmental potential. Zygote, 2006; 14: 53-61
  Google Scholar
• 76. Nakada K., Hayashi J.I.: Transmitochondrial mice as models for mitochondrial DNA-based diseases. Exp. Anim., 2011; 60: 421-431
  Google Scholar
• 77. Niu X., Trifunovic A., Larsson N.G., Canlon B.: Somatic mtDNA mutations cause progressive hearing loss in the mouse. Exp. Cell Res., 2007; 313:3924-3934
  Google Scholar
• 78. Opiela J., Lipiński D., Słomski R., Katska-Ksiazkiewicz L.: Transcript expression of mitochondria related genes is correlated with bovine oocyte selection by BCB test. Anim. Reprod. Sci., 2010; 118: 188-193
  Google Scholar
• 79. Palmer C.S., Osellame L.D., Stojanovski D., Ryan M.T.: The regulation of mitochondrial morphology: intricate mechanisms and dynamic machinery. Cell. Signal., 2011; 23: 1534-1545
  Google Scholar
• 80. Perez G.I., Jurisicova A., Wise L., Lipina T., Kanisek M., Bechard A., Takai Y., Hunt P., Roder J., Grynpas M., Tilly J.L.: Absence of the proapoptotic Bax protein extends fertility and alleviates age-related health complications in female mice. Proc. Natl. Acad. Sci. USA, 2007; 104: 5229-5234
  Google Scholar
• 81. Piganeau G., Gardner M., Eyre-Walker A.: A broad survey of recombination in animal mitochondria. Mol. Biol. Evol., 2004; 21: 2319-2325
  Google Scholar
• 82. Prasad S., Tiwari M., Koch B., Chaube S.K.: Morphological, cellular and molecular changes during postovulatory egg aging in mammals. J. Biomed. Sci., 2015; 22: 36
  Google Scholar
• 83. Qiao T.W., Liu N., Miao D.Q., Zhang X., Han D., Ge L., Tan J.H.: Cumulus cells accelerate aging of mouse oocytes by secreting a soluble factor (s). Mol. Reprod. Dev., 2007; 75: 521-528
  Google Scholar
• 84. Ramalho-Santos J.: A sperm’s tail: the importance of getting it right. Hum. Reprod., 2011; 26: 2590-2591
  Google Scholar
• 85. Reynier P., May-Panloup P., Chrétien M.F., Morgan C.J., Jean M., Savagner F., Barrière P., Malthièry Y.: Mitochondrial DNA content affects the fertilizability of human oocytes. Mol. Hum. Reprod., 2001; 7: 425-429
  Google Scholar
• 86. Rieger D., Luciano A.M., Modina S., Pocar P., Lauria A., Gandolfi F.: The effects of epidermal growth factor and insulin-like growth factor I on the metabolic activity, nuclear maturation and subsequent development of cattle oocytes in vitro. J. Reprod. Fertil, 1998; 112: 123-130
  Google Scholar
• 87. Ross J.M., Coppotelli G., Hoffer B.J., Olson L.: Maternally transmitted mitochondrial DNA mutations can reduce lifespan. Sci. Rep., 2014; 4: 6569
  Google Scholar
• 88. Ruder E.H., Hartman T.J., Goldman M.B.: The role of mitochondria from mature oocyte to viable blastocyst. Curr. Opin. Obstet. Gynecol., 2009; 21: 219-222
  Google Scholar
• 89. Ruder E.H., Hartman T.J., Goldman M.B.: Impact of oxidative stress on female fertility. Curr. Opin. Obstet. Gynecol., 2009; 21: 219- 222
  Google Scholar
• 90. Russell O., Turnbull D.: Mitochondrial DNA disease-molecular insights and potential routes to a cure. Exp. Cell Res., 2014; 325: 38-43
  Google Scholar
• 91. Santos T.A., El Shourbagy S., St John J.C.: Mitochondrial content reflects oocyte variability and fertilization outcome. Fertil. Steril., 2006; 85: 584-591
  Google Scholar
• 92. Sathananthan A.H., Trounson A.O.: Mitochondrial morphology during preimplantational human embryogenesis. Hum. Reprod., 2000; 15: 148-159
  Google Scholar
• 93. Shkolnik K., Tadmor A., Ben-Dor S., Nevo N., Galiani D., Dekel N.: Reactive oxygen species are indispensable in ovulation. Proc. Natl. Acad. Sci. USA, 2011; 108: 1462-1467
  Google Scholar
• 94. Soleimani R., Heytens E., Darzynkiewicz Z., Oktay K.: Mechanisms of chemotherapy-induced human ovarian aging: double strand DNA breaks and microvascular compromise. Aging, 2011; 3: 782-793
  Google Scholar
• 95. St. John J.C., Facucho-Oliveira J., Jiang Y., Kelly R., Salah R.: Mitochondrial DNA transmission, replication and inheritance: a journey from the gamete through the embryo and into offspring and embryonic stem cells. Hum. Reprod. Update, 2010; 16: 488-509
  Google Scholar
• 96. Stojkovic M., Machado S.A., Stojkovic P., Zakhartchenko V., Hutzler P., Gonçalves P.B., Wolf E.: Mitochondrial distribution and adenosine triphosphate content of bovine oocytes before and after in vitro maturation: correlation with morphological criteria and developmental capacity after in vitro fertilization and culture. Biol. Reprod., 2001; 64: 904-909
  Google Scholar
• 97. Sutton-McDowall M.L., Gilchrist R.B., Thompson J.G.: The pivotal role of glucose metabolism in determining oocyte developmental competence. Reproduction, 2010; 139: 685-695
  Google Scholar
• 98. Tatemoto H., Sakurai N., Muto N.: Protection of porcine oocytes against apoptotic cell death caused by oxidative stress during in vitro maturation: role of cumulus cells. Biol. Reprod., 2000; 63: 805-810
  Google Scholar
• 99. Tatone C., Eichenlaub-Ritter U., Amicarelli F.: Dicarbonyl stress and glyoxalases in ovarian function. Biochem. Soc. Trans., 2014; 42: 433-438
  Google Scholar
• 100. Tiwari M., Chaube S.K.: Moderate increase of reactive oxygen species triggers meiotic resumption in rat follicular oocytes. J. Obstet. Gynaecol. Res., 2016; 42: 536-546
  Google Scholar
• 101. Tiwari M., Prasad S., Tripathi A., Pandey A.N., Ali I., Singh A.K., Shrivastav T.G., Chaube S.K.: Apoptosis in mammalian oocytes: a review. Apoptosis, 2015; 20: 1019-1025
  Google Scholar
• 102. Trifunovic A., Wredenberg A., Falkenberg M., Spelbrink J.N., Rovio A.T., Bruder C.E., Bohlooly-Y. M., Gidlöf S., Oldfors A., Wibom R., Törnell J., Jacobs H.T., Larsson N.G.: Premature ageing in mice expressing defective mitochondrial DNA polymerase. Nature, 2004; 429: 417-423
  Google Scholar
• 103. Tsai H.D., Hsieh Y.Y., Hsieh J.N., Chang C.C., Yang C.Y., Yang J.G., Cheng W.L., Tsai F.J., Liu C.S.: Mitochondria DNA deletion and copy numbers of cumulus cells associated with in vitro fertilization outcomes. J. Reprod. Med., 2010; 55: 491-497
  Google Scholar
• 104. Van Blerkom J.: Mitochondria as regulatory forces in oocytes, preimplantation embryos and stem cells. Reprod. Biomed. Online, 2008; 16: 553-569
  Google Scholar
• 105. Van Blerkom J.: Mitochondria in human oogenesis and preimplantation embryogenesis: engines of metabolism, ionic regulation and developmental competence. Reproduction, 2004; 128: 269-280
  Google Scholar
• 106. Van Blerkom J., Davis P.: Mitochondrial signaling and fertilization. Mol. Hum. Reprod., 2007; 13: 759-770
  Google Scholar
• 107. Van Blerkom J., Davis P., Alexander S.: Inner mitochondrial membrane potential (∆Ψm), cytoplasmic ATP content and free Ca2+ levels in metaphase II mouse oocytes. Hum. Reprod., 2003; 18: 2429- 2440
  Google Scholar
• 108. Van Blerkom J., Davis P.W., Lee J.: ATP content of human oocytes and developmental potential and outcome after in-vitro fertilization and embryo transfer. Hum. Reprod., 1995; 10: 415-424
  Google Scholar
• 109. Van Blerkom J., Davis P., Thalhammer V.: Regulation of mitochondrial polarity in mouse and human oocytes: the influence of cumulus derived nitric oxide. Mol. Hum. Reprod., 2008; 14: 431-444
  Google Scholar
• 110. Venkatesh S., Kumar M., Sharma A., Kriplani A., Ammini A.C., Talwar P., Agarwal A., Dada R.: Oxidative stress and ATPase6 mutation is associated with primary ovarian insufficiency. Arch. Gynecol. Obstet, 2010; 282: 313-318
  Google Scholar
• 111. Wai T., Ao A., Zhang X., Cyr D., Dufort D., Shoubridge E.A.: The role of mitochondrial DNA copy number in mammalian fertility. Biol. Reprod., 2010; 83: 52-62
  Google Scholar
• 112. Wakefield S.L., Lane M., Mitchell M.: Impaired mitochondrial function in the preimplantation embryo perturbs fetal and placental development in the mouse. Biol. Reprod., 2011; 84: 572-580
  Google Scholar
• 113. Wang L.Y., Wang D.H., Zou X.Y., Xu C.M.: Mitochondrial functions on oocytes and preimplantation embryos. J. Zhejiang Univ. Sci. B, 2009; 10: 483-492
  Google Scholar
• 114. Wang R.S., Chang H.Y., Kao S.H., Kao C.H., Wu Y.C., Yeh S., Tzeng C.R., Chang C.: Abnormal mitochondrial function and impaired granulosa cell differentiation in androgen receptor knockout mice. Int. J. Mol. Sci., 2015; 16: 9831-9849
  Google Scholar
• 115. Wu Y., Wang X., Liu J., Bao Z., Tang D., Wu Y., Zeng S.: BIMEL- -mediated apoptosis in cumulus cells contributes to degenerative changes in aged porcine oocytes via a paracrine action. Theriogenology, 2011; 76: 1487-1495
  Google Scholar
• 116. Yeon Lee J., Baw C.K., Gupta S., Aziz N., Agarwal A.: Role of oxidative stress in polycystic ovary syndrome. Curr. Womens. Health Rev., 2010; 6: 96-107
  Google Scholar
• 117. Yesodi V., Yaron Y., Lessing J.B., Amit A., Ben-Yosef D.: The mitochondrial DNA mutation (ΔmtDNA 5286) in human oocytes : correlation with age and IVF outcome. J. Assist. Reprod. Genet., 2002; 19: 60-66
  Google Scholar
• 118. Yu Y., Dumollard R., Rossbach A., Lai F.A., Swann K.: Redistribution of mitochondria leads to bursts of ATP production during spontaneous mouse oocyte maturation. J. Cell. Physiol., 2010; 224: 672-680
  Google Scholar
• 119. Zeng H.T., Richani D., Sutton-McDowall M.L., Ren Z., Smitz J.E., Stokes Y., Gilchrist R.B., Thompson J.G.: Prematuration with cyclic adenosine monophosphate modulators alters cumulus cell and oocyte metabolism and enhances developmental competence of in vitro-matured mouse oocytes. Biol. Reprod., 2014; 91: 47
  Google Scholar
• 120. Zheng W., Khrapko K., Coller H.A., Thilly W.G., Copeland W.C.: Origins of human mitochondrial point mutations as DNA polymerase g-mediated errors. Mutat. Res., 2006; 599: 11-20
  Google Scholar

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