Skip to main content
SpringerLink
Log in

Mitochondria of the Oocyte

  • Chapter
  • First Online:
Development of In Vitro Maturation for Human Oocytes

Abstract

Oocyte quality depends on nuclear and cytoplasmic factors. Because structure and subcellular localization of mitochondria significantly change during oocyte maturation, their dynamics might play critical roles in their maturation and fertilization and in embryonal development. Quality of cytoplasm and mitochondria in oocytes could be improved practically by dietary intake of foods and some supplements, such as L-carnitine, that suppress oxidative stress in and around mitochondria. The present work describes ultrastructure, function, and intracellular traffics of mitochondria and the property of their energy transduction in developing mammalian oocytes. The importance of epigenetic control of mitochondria and possible effect of mitochondrial transfer on the development of oocytes and clinical outcomes are also described.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 109.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 139.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 139.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  1. Faddy MJ, Gosden RG, Gougeon A, Richardson SJ, Nelson JF. Accelerated disappearance of ovarian follicles in mid-life: implications for forecasting menopause. Hum Reprod. 1992;7:1342–6.

    Article  CAS  PubMed  Google Scholar 

  2. Tessa L, John R. A. Oxidative stress and ageing of the post-ovulatory oocyte. Reproduction 2013;146:217–27.

    Google Scholar 

  3. Inoue M, Sato E, Nishikawa M, et al. Free radical theory of apoptosis and metamorphosis. Redox Rep. 2004;9(5):237–47. doi:10.1179/135100004225006010.

    Article  CAS  PubMed  Google Scholar 

  4. Miyamoto K, Sato E, Kasahara E, et al. Effect of oxidative stress during repeated ovulation on the structure and functions of the ovary, oocytes, and their mitochondria. Free Radic Biol Med. 2010;49(4):674–81. doi:10.1016/j.freeradbiomed.2010.05.025.

    Article  CAS  PubMed  Google Scholar 

  5. Liu N, Wu YG, Lan GC, Sui HS, Ge L, Wang JZ, Liu Y, Qiao TW, Tan JH. Pyruvate prevents aging of mouse oocytes. Reproduction. 2009;138(2):223–34. doi:10.1530/REP-09-0122 Epub 2009 May 22.

    Article  CAS  PubMed  Google Scholar 

  6. Pincus G, Enzmann EV. The comparative behavior of mammalian eggs in vivo and in vitro: I. The activation of ovarian eggs. J Exp Med. 1935;62:655–75.

    Article  Google Scholar 

  7. Edwards R. Maturation in vitro of mouse, sheep, cow, pig, rhesus monkey and human ovarian oocytes. Nature. 1965;20:349–51.

    Article  Google Scholar 

  8. Edwards R, Bavister B, Steptoe P. Early stages of fertilization in vitro of human oocytes matured in vitro. Nature. 1969;221:632–5.

    Article  CAS  PubMed  Google Scholar 

  9. Veeck LL, Wortham JW Jr, Witmyer J, et al. Maturation and fertilization of morphologically immature human oocytes in a program of in vitro fertilization. Fertil Steril. 1983;39:594–602.

    Article  CAS  PubMed  Google Scholar 

  10. Cha KY, Koo JJ, Ko JJ, et al. Pregnancy after in vitro fertilization of human follicular oocytes collected from nonstimulated cycles, their culture in vitro and their transfer in a donor oocyte program. Fertil Steril. 1991;55:109–13.

    Article  CAS  PubMed  Google Scholar 

  11. Chian RC, Buckett WM, Tulandi T, Tan SL. Prospective randomized study of human chorionic gonadotrophin priming before immature oocyte retrieval from unstimulated women with polycystic ovarian syndrome. Hum Reprod. 2000;15:165–70.

    Article  CAS  PubMed  Google Scholar 

  12. Wang LY, Wang DH, Zou XY, Xu CM. Mitochondrial functions on oocytes and preimplantation embryos. J Zhejiang Univ Sci B. 2009;10:483–92.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Wilding M, Dale B, Marino M, Matteo L, Alviggi C, Pisaturo ML, Lombardi L, de Placido G. Mitochondrial aggregation patterns and activity in human oocytes and preimplantationembryos. Hum Reprod. 2001;16:909–17. doi:10.1093/humrep/16.5.909.

    Article  CAS  PubMed  Google Scholar 

  14. 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;14:431–44. doi:10.1038/ng.95.

    Article  PubMed  CAS  Google Scholar 

  15. Mitchell T, Chacko B, Ballinger SW, Bailey SM, Zhang J, Darley-Usmar V. Convergent mechanisms for dysregulation of mitochondrial quality control in metabolic disease: implications for mitochondrial therapeutics. Biochem Soc Trans. 2013;41(1):127–33. doi:10.1042/BST20120231.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Barritt J, Willadsen S, Brenner C, Cohen J. Cytoplasmic transfer in assisted reproduction. Hum Reprod Update. 2001;7(4):428–35.

    Article  CAS  PubMed  Google Scholar 

  17. Krisher RL, Bavister BD. Responses of oocytes and embryos to the culture environment. Theriogenology. 1998;59:103–14.

    Article  Google Scholar 

  18. Van Blerkom J, Davis P, Lee J. ATP content of human oocytes and developmental potential and outcome after in-vitro fertilization and embryo transfer. Hum Reprod. 1995;10:415–24.

    Article  CAS  PubMed  Google Scholar 

  19. Van Blerkom J. Mitochondria in human oogenesis and preimplantation embryogenesis: engines of metabolism, ionic regulation and developmental competence. Reproduction. 2004;128:269–80.

    Article  PubMed  CAS  Google Scholar 

  20. Takeuchi T, Neri QV, Katagiri Y, Rosenwaks Z, Palermo GD. Effect of treating induced mitochondrial damage on embryonic development and epigenesis. Biol Reprod. 2005;72:584–92.

    Article  CAS  PubMed  Google Scholar 

  21. Schon EA, Kim SH, Ferreira JC, Magalhães P, Grace M, Warburton D, Gross SJ. Chromosomal non-disjunction in human oocytes: Is there a mitochondrial connection? Hum Reprod. 2000;Suppl 2:160–72.

    Article  Google Scholar 

  22. Piko L, Matsumoto L. Number of mitochondria and some properties of mitochondrial DNA in the mouse egg. Dev Biol. 1976;49:1–10.

    Article  CAS  PubMed  Google Scholar 

  23. Ankel-Simons F, Cummins JM. Misconceptions about mitochondria and mammalian fertilization: implications for theories on human evolution. Proc Natl Acad Sci USA. 1996;93:13859–63.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Van Blerkom J. Mitochondrial function in the human oocyte and embryo and their role in developmental competence. Mitochondrion. 2011;11:797–813.

    Article  PubMed  CAS  Google Scholar 

  25. Sathananthan AH, Trounson A. Mitochondrial morphology during preimplantional human embryogenesis. Hum Reprod. 2000;15:148–59.

    Article  PubMed  Google Scholar 

  26. Sathananthan AH, Selvaraj K, Trounson A. Fine structure of human oogoniain the featalovary. Mol Cell Endocrinol. 2000;161:3–8.

    Article  CAS  PubMed  Google Scholar 

  27. Sathananthan AH, Selvaraj K, Girijashankar M, Ganesh V, Selvaraj P, Trounson A. From oogonia to mature oocytes: inactivation of the maternal centrosome in humans. Microsc Res Tech. 2006;69:396–407.

    Article  PubMed  Google Scholar 

  28. Motta PM, Nottola SA, Makabe S, Heyn R. Mitochondrial morphology in human fetal and adult female germ cell. Hum Reprod. 2000;15:129–47.

    Article  PubMed  Google Scholar 

  29. Dvorak M, Tesarik J. Ultrastructure of human ovarian follicles. In: Motta PM, Hafez ESE, editors. Biology of the ovary. Developments in obstetrics and gynecology. The Hague, The Netherlands: Martinus Nijhoff Publishers; 1980. p. 121–37.

    Google Scholar 

  30. Pozo J, Corral E, Pereda J. Subcellular structure of prenatal human ovary: mitochondrial distribution during meiotic prophase. J Submicrosc Cytol Pathol. 1990;22:601–7.

    CAS  PubMed  Google Scholar 

  31. Jansen RPS. Germline passage of mitochondria: quantitative considerations and possible embryological sequelae. Hum Reprod. 2000;15:112–28.

    Article  PubMed  Google Scholar 

  32. Rosália S, Mariana C, Joaquina S, Ana L, Cristiano O, José T, Alberto B, Mário S. Ultrastructure of tubular smooth endoplasmic reticulum aggregates in human metaphase II oocytes and clinical implications. Fertil Steril. 2011;96:143–9.

    Article  Google Scholar 

  33. Hirokawa N, Niwa S, Tanaka Y. Molecular motors in neurons: transport mechanisms and roles in brain function, development, and disease. Neuron. 2010;68(4):610–38. doi:10.1016/j.neuron.2010.09.039.

    Article  CAS  PubMed  Google Scholar 

  34. Morris RL, Hollenbeck PJ. Axonal transport of mitochondria along microtubules and F-actin in living vertebrate neurons. J Cell Biol. 1995;131(5):1315–26.

    Google Scholar 

  35. Waterman-Storer CM, Karki SB, Kuznetsov SA, et al. The interaction between cytoplasmic dynein and dynactin is required for fast axonal transport. Proc Natl Acad Sci U S A. 1997;94(22):12180–5.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Tanaka Y, Kanai Y, Okada Y, et al. Targeted disruption of mouse conventional kinesin heavy chain, kif5B, results in abnormal perinuclear clustering of mitochondria. Cell. 1998;93(7):1147–58.

    Article  CAS  PubMed  Google Scholar 

  37. Martin MA, Iyadurai SJ, Gassman A, et al. Cytoplasmic dynein, the dynactin complex, and kinesin are interdependent and essential for fast axonal transport. Mol Biol Cell. 1999;10(11):3717–28.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Zhao C, Takita J, Tanaka Y, et al. Charcot-marie-tooth disease type 2A caused by mutation in a microtubule motor KIF1B. Cell. 2001;105(5):587–97.

    Article  CAS  PubMed  Google Scholar 

  39. Habermann A, Schroer TA, Griffiths G, et al. Immunolocalization of cytoplasmic dynein and dynactin subunits in cultured macrophages: enrichment on early endocytic organelles. J Cell Sci. 2001;114(Pt 1):229–40.

    CAS  PubMed  Google Scholar 

  40. LaMonte B, Wallace KE, Holloway BA, et al. Disruption of dynein/dynactin inhibits axonal transport in motor neurons causing late-onset progressive degeneration. Neuron. 2002;34(5):715–27.

    Article  CAS  PubMed  Google Scholar 

  41. Niwa S, Tanaka Y, Hirokawa N. KIF1Bβ-and KIF1A-mediated axonal transport of presynaptic regulator Rab3 occurs in a GTP-dependent manner through DENN/MADD. Nat Cell Biol. 2008;10(11):1269–79. doi:10.1038/ncb1785.

    Article  CAS  PubMed  Google Scholar 

  42. Lee S, Kim S, Sun X, et al. Cell cycle-dependent mitochondrial biogenesis and dynamics in mammalian cells. Biochem Biophys Res Commun. 2007;357(1):111–7.

    Article  PubMed  CAS  Google Scholar 

  43. Sun Qu, Schatten H. Regulation of dynamic events by microfilaments during oocyte maturation and fertilization. Reproduction 2006; 131:193–205. DOI:10.1530/rep.1.00847.

  44. Van Blerkom J. Microtubule mediation of cytoplasmic and nuclear maturation during the early stages of resumed meiosis in cultured mouse oocytes. Proc Natl Acad Sci U S A. 1991;88(11):5031–5.

    Article  PubMed  PubMed Central  Google Scholar 

  45. Calarco PG. The role of microfilaments in early meiotic maturation of mouse oocytes. Microsc Microanal. 2005;11(2):146–53.

    Article  CAS  PubMed  Google Scholar 

  46. Sun QY, Wu GM, Lai L, et al. Translocation of active mitochondria during pig oocyte maturation, fertilization and early embryo development in vitro. Reproduction. 2001;122(1):155–63.

    Article  CAS  PubMed  Google Scholar 

  47. Liu S, LI Y, Feng HL et al. Dynamic modulation of cytoskeleton during in vitro maturation in human oocytes. Am J Obstet Gynecol. 2010; 203(2):151.e1–7. doi:10.1016/j.ajog.2010.05.011.

  48. Yu Y, Dumollard R, Rossback A, et al. Redistribution of mitochondria leads to bursts of ATP production during spontaneous mouse oocyte maturation. J Cell Physiol. 2010;224(3):672–80. doi:10.1002/jcp.22171.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Duan X, Liu J, Dai XX, et al. Rho-GTPase effector ROCK phosphorylates cofilin in actin-meditated cytokinesis during mouse oocyte meiosis. Biol Reprod. 2014;90(2):1–9. doi:10.1095/biolreprod.113.113522.

    Article  CAS  Google Scholar 

  50. Yamoch T, Hashimoto S, Amo A et al. Analysis of mitochondrial dynamics in porcine oocytes during meiotic maturation. International symposium on mitochondria 2013. P-2–18.

    Google Scholar 

  51. Quintero OA, DiVito MM, Adikes RC, et al. Human Myo19 is a novel myosin that associates with mitochondria. Curr Biol. 2009;19(23):2008–13. doi:10.1016/j.cub.2009.10.026.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Förtsch J, Hummel E, Krist M, et al. The myosin-related motor protein Myo2 is an essential mediator of bud-directed mitochondrial movement in yeast. J Cell Biol. 2011;194(3):473–88.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  53. Hollenbeck PJ. The pattern and mechanism of mitochondrial transport in axons. Front. Biosci. 1996;1:91–102.

    Article  Google Scholar 

  54. Hollenbeck PJ, Saxton WM. The axonal transport of mitochondria. J Cell Sci. 2005;125(Pt 9):2095–104. doi:10.1242/jcs.053850.

    Google Scholar 

  55. Dalton CM, John Carroll. Biased inheritance of mitochondria during asymmetric cell division in the mouse oocyte. J Cell Sci. 2013;126(Pt 13):2955–64. doi:10.1242/jcs.128744 10.1083/jcb.201012088.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Leese HJ, Biggers JD, Mroz FA, Lechene C. Nucleotides in a single mammalian ovum or preimplantation embryo. Anal Biochem. 1984;140:443–8.

    Article  CAS  PubMed  Google Scholar 

  57. Hashimoto S, Minami N, Takakura R, Yamada M, Imai H, Kashima N. Low oxygen tension during in vitro maturation is beneficial for supporting the subsequent development of bovine cumulus-oocyte complexes. Mol Reprod Dev. 2000;57:353–60.

    Article  CAS  PubMed  Google Scholar 

  58. Stojkovic M, Machado SA, Stojkovic P, Zakhartchenko V, Hutzler P, Goncalves PB, 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;64:904–9.

    Article  CAS  PubMed  Google Scholar 

  59. Crocco M, Alberio RH, Lauria L, Mariano MI. Effect of serum on the mitochondrial active area on developmental days 1 to 4 in in vitro-produced bovine embryos. Zygote. 2011;19:297–306.

    Article  CAS  PubMed  Google Scholar 

  60. 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;23:424–32.

    Article  CAS  PubMed  Google Scholar 

  61. Dan-Goor M, Sasson S, Davarashvili A, Almagor M. Expression of glucose transporter and glucose uptake in human oocytes and preimplantation embryos. Hum Reprod. 1997;12:2508–10.

    Article  CAS  PubMed  Google Scholar 

  62. Augustin R, Pocar P, Navarrete-Santos A, Wrenzycki C, Gandolfi F, Niemann H, Fischer B. Glucose transporter expression is developmentally regulated in in vitro derived bovine preimplantation embryos. Mol Reprod Dev. 2001;60:370–6.

    Article  CAS  PubMed  Google Scholar 

  63. Zheng P, Vassena R, Latham KE. 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. 2007;13:361–71.

    Article  CAS  PubMed  Google Scholar 

  64. Pisani LF, Antonini S, Pocar P, Ferrari S, Brevini TA, Rhind SM, Gandolfi F. Effects of pre-mating nutrition on mRNA levels of developmentally relevant genes in sheep oocytes and granulosa cells. Reproduction. 2008;136:303–12.

    Article  CAS  PubMed  Google Scholar 

  65. Cetica P, Pintos L, Dalvit G, Beconi M. Activity of key enzymes involved in glucose and triglyceride catabolism during bovine oocyte maturation in vitro. Reproduction. 2002;124:675–81.

    Article  CAS  PubMed  Google Scholar 

  66. Saito T, Hiroi M, Kato T. Development of glucose utilization studied in single oocytes and preimplantation embryos from mice. Biol Reprod. 1994;50:266–70.

    Article  CAS  PubMed  Google Scholar 

  67. Harris SE, Gopichandran N, Picton HM, Leese HJ, Orsi NM. Nutrient concentrations in murine follicular fluid and the female reproductive tract. Theriogenology. 2005;64:992–1006.

    Article  CAS  PubMed  Google Scholar 

  68. Williams SA, Blache D, Martin GB, Foot R, Blackberry MA, Scaramuzzi RJ. Effect of nutritional supplementation on quantities of glucose transporters 1 and 4 in sheep granulosa and theca cells. Reproduction. 2001;122:947–56.

    Article  CAS  PubMed  Google Scholar 

  69. Roberts R, Stark J, Iatropoulou A, Becker DL, Franks S, Hardy K. 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. 2004;71:199–209.

    Article  CAS  PubMed  Google Scholar 

  70. Nishimoto H, Matsutani R, Yamamoto S, Takahashi T, Hayashi KG, Miyamoto A, Hamano S, Tetsuka M. Gene expression of glucose transporter (GLUT) 1, 3 and 4 in bovine follicle and corpus luteum. J Endocrin. 2006;188:111–9.

    Article  CAS  Google Scholar 

  71. Charron MJ, Brosius FC III, Alper SL, Lodish HF. A glucose transport protein expressed predominately in insulin-responsive tissues. Proc Natl Acad Sci 1989; 86:2535–9.

    Google Scholar 

  72. Thompson JG, Lane M, Gilchrist RB. Metabolism of the bovine cumulus–oocyte complex and influence on subsequent developmental competence. Soc Reprod Fertil Suppl. 2007;64:179–90.

    CAS  PubMed  Google Scholar 

  73. Biggers JD, Whittingham DG, Donahue RP. The pattern of energy metabolism in the mouse oöcyte and zygote. Proc Natl Acad Sci U S A. 1967;58(2):560–7.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Baca M, Zamboni L. The fine structure of human follicular oocytes. J Ultrastruct Res. 1967;19:354–81.

    Article  CAS  PubMed  Google Scholar 

  75. Lodde V, Modina S, Maddox-Hyttel P, Franciosi F, Lauria A, Luciano AM. Oocyte morphology and transcriptional silencing in relation to chromatin remodeling during the final phases of bovine oocyte growth. Mol Reprod Dev. 2008;75:915–24.

    Article  CAS  PubMed  Google Scholar 

  76. Fair T, Hulshof SC, Hyttel P, Greve T, Boland M. Oocyte ultrastructure in bovine primordial to early tertiary follicles. Anat Embryol (Berl); 1997;195:327–36.

    Google Scholar 

  77. Thompson JG, Partridge RJ, Houghton FD, Cox CI, Leese HJ. Oxygen uptake and carbohydrate metabolism by in vitro derived bovine embryos. J Reprod Fertil. 1996;106:299–306.

    Article  CAS  PubMed  Google Scholar 

  78. Sugimura S, Matoba S, Hashiyada Y, Aikawa Y, Ohtake M, Matsuda H, Kobayashi S, Konishi K, Imai K. Oxidative phosphorylation-linked respiration in individual bovine oocytes. J Reprod Dev. 2012;58:636–41.

    Article  CAS  PubMed  Google Scholar 

  79. Trimarchi JR, Liu L, Porterfield DM, Smith PJ, Keefe DL. Oxidative phosphorylation-dependent and -independent oxygen consumption by individual preimplantation mouse embryos. Biol Reprod. 2000;62:1866–74.

    Article  CAS  PubMed  Google Scholar 

  80. Brevini TA, Vassena R, Francisci C, Gandolfi F. Role of adenosine triphosphate, active mitochondria, and microtubules in the acquisition of developmental competence of parthenogenetically activated pig oocytes. Biol Reprod. 2005;72(5):1218–23.

    Article  CAS  PubMed  Google Scholar 

  81. Alberts B, Johnson A, Lewis J, Raff M, Roberts K, Walter P. Molecular Biology of the Cell fifth edition Garland Science (2008) .

    Google Scholar 

  82. Smiraglia DJ, Kulawiec M, Bistulfi GL, Gupta SG, Singh KK. A novel role for mitochondria in regulating epigenetic modification in the nucleus. Cancer Biol Ther. 2008;7:1182–90.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Shock LS, Thakkar PV, Peterson EJ, Moran RG, Taylor SM. DNA methyltransferase 1, cytosine methylation, and cytosine hydroxymethylation in mammalian mitochondria. Proc Natl Acad Sci. 2011;108:3630–5.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Barrès R, Osler ME, Yan J, Rune A, Fritz T, Caidahl K, et al. Non-CpG methylation of the PGC-1alpha promoter through DNMT3B controls mitochondrial density. Cell Metab. 2009;10:189–98.

    Article  PubMed  CAS  Google Scholar 

  85. Razin A. CpG methylation, chromatin structure and gene silencing-a three-way connection. EMBO J. 1998;17:4905–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Kriaucionis S, Heintz N. The nuclear DNA base 5-hydroxymethylcytosine is present in Purkinje neurons and the brain. Science. 2009;324:929–30.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Tahiliani M, Koh KP, Shen Y, Pastor WA, Bandukwala H, Brudno Y, et al. Conversion of 5-methylcytosine to 5-hydroxymethylcytosine in mammalian DNA by MLL partner TET1. Science. 2009;324:930–5.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Li E. Chromatin modification and epigenetic reprogramming in mammalian development. Nat Rev Genet. 2002;3:662–73.

    Article  CAS  PubMed  Google Scholar 

  89. Jones PA, Takai D. The role of DNA methylation in mammalian epigenetics. Science. 2001;293:1068–70.

    Article  CAS  PubMed  Google Scholar 

  90. Li X, Wang X, He K, Ma Y, Su N, He H, et al. High-resolution mapping of epigenetic modifications of the rice genome uncovers interplay between DNA methylation, histone methylation, and gene expression. Plant Cell. 2008;20:259–76.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. Lin JC, Jeong S, Liang G, Takai D, Fatemi M, Tsai YC, et al. Role of nucleosomal occupancy in the epigenetic silencing of the MLH1 CpG island. Cancer Cell. 2007;12:432–44. doi:10.1016/j.ccr.2007.10.014.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Lee JT. Lessons from X-chromosome inactivation: long ncRNA as guides and tethers to the epigenome. Genes Dev. 2009;23:1831–42.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Nagano T, Mitchell JA, Sanz LA, Pauler FM, Ferguson-Smith AC, Feil R, et al. The Air noncoding RNA epigenetically silences transcription by targeting G9a to chromatin. Science. 2008;322:1717–20.

    Article  CAS  PubMed  Google Scholar 

  94. Egger G, et al. Epigenetics in human disease and prospects for epigenetic therapy. Nature. 2004;429:457–63.

    Article  CAS  PubMed  Google Scholar 

  95. Dawid IB. 5-Methylcytidylic acid: Absence from mitochondrial DNA of frogs and HeLa cells. Science. 1974;184:80–1.

    Article  CAS  PubMed  Google Scholar 

  96. Nass MM. Differential methylation of mitochondrial and nuclear DNA in cultured mouse, hamster and virus-transformed hamster cells. In vivo and in vitro methylation. J Mol Biol. 1973;80:155–75.

    Article  CAS  PubMed  Google Scholar 

  97. Shmookler Reis RJ, Goldstein S. Mitochondrial DNA in mortal and immortal human cells. Genome number, integrity, and methylation. J Biol Chem 1983;258:9078–85.

    Google Scholar 

  98. Pollack Y, Kasir J, Shemer R, Metzger S, Szyf M. Methylation pattern of mouse mitochondrial DNA. Nucleic Acids Res. 1984;12:4811–24.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  99. Cardon LR, Burge C, Clayton DA, Karlin S. Pervasive CpG suppression in animal mitochondrial genomes. Proc Natl Acad Sci USA. 1994;91:3799–803.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  100. Mokranjac D, Neupert W. Protein import into mitochondria. Biochem Soc Trans. 2005;33:1019–23.

    Article  CAS  PubMed  Google Scholar 

  101. Garrido N, et al. Composition and dynamics of human mitochondrial nucleoids. Mol Biol Cell. 2003;14:1583–96.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  102. Scarpulla RC. Transcriptional paradigms in mammalian mitochondrial biogenesis and function. Physiol Rev. 2008;88:611–38.

    Article  CAS  PubMed  Google Scholar 

  103. Chiang PK, Gordon RK, Tal J, Zeng GC, Doctor BP, Pardhasaradhi K, et al. S-Adenosylmethionine and methylation. FASEB J. 1996;10:471–80.

    CAS  PubMed  Google Scholar 

  104. Wallace DC, Fan W. Energetics, epigenetics, mitochondrial genetics. Mitochondrion. 2010;10:12–31. doi:10.1016/j.mito.2009.09.006.

    Article  CAS  PubMed  Google Scholar 

  105. Ulrey CL, Liu L, Andrews LG, Tollefsbol TO. The impact of metabolism on DNA methylation. Hum Mol Genet. 2005;14:139–47.

    Article  CAS  Google Scholar 

  106. Minocherhomji S, Tollefsbol TO, Singh KK. Mitochondrial regulation of epigenetics and its role in human diseases. Epigenetics. 2012;7:326–34.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  107. Singh KK. Mitochondria damage checkpoint in apoptosis and genome stability. FEMS Yeast Res. 2004;5:127–32.

    Article  CAS  PubMed  Google Scholar 

  108. Liu L, van Groen T, Kadish I, Li Y, Wang D, James S, et al. Insufficient DNA methylation affects healthy aging and promotes age-related health problems. Clinical Epigenetics. 2011;2:1–12.

    Article  CAS  Google Scholar 

  109. Rhee I, Bachman KE, Park BH, Jair K-W, Yen R-WC, Schuebel KE, et al. DNMT1 and DNMT3b cooperate to silence genes in human cancer cells. Nature. 2002;416:552–6.

    Article  CAS  PubMed  Google Scholar 

  110. Dakubo G. Functional importance of mitochondrial genetic alterations in cancer. Mitochondrial Genet Cancer 2010;213–36.

    Google Scholar 

  111. Xie CH, Naito A, Mizumachi T, Evans TT, Douglas MG, Cooney CA, et al. Mitochondrial regulation of cancer associated nuclear DNA methylation. Biochem Biophys Res Commun. 2007;364:656–61.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  112. Gibson GE, Starkov A, Blass JP, Ratan RR, Beal MF. Cause and consequence: mitochondrial dysfunction initiates and propagates neuronal dysfunction, neuronal death and behavioral abnormalities in age-associated neurodegenerative diseases. Biochim Biophys Acta. 2010;1802:122–34.

    Article  CAS  PubMed  Google Scholar 

  113. Sato E, Kobuchi H, Edashige K, et al. Dynamic aspects of ovarian superoxide dismutase isozymes during the ovulatory process in the rat. FEBS Lett. 1992;303(2–3):121–5.

    CAS  PubMed  Google Scholar 

  114. Inoue M, Sato E, Park AM, et al. Cross-talk between NO and oxyradicals, a supersystem that regulates energy metabolism and survival of animals. Free Radic Res. 2000;33(6):757–70. doi:10.1080/10715760000301281.

    Article  CAS  PubMed  Google Scholar 

  115. Corral-Debrinski M, Horton T, Lott MT, et al. Mitochondrial DNA deletions in human brain: regional variability and increase with advanced age. Nat Genet. 1992;2(4):324–9.

    Article  CAS  PubMed  Google Scholar 

  116. Corral-Debrinski M, Shoffner JM, Lott MT, et al. Association of mitochondrial DNA damage with aging and coronary atherosclerotic heart disease. Mutat Res. 1992;275(3–6):169–80.

    Article  CAS  PubMed  Google Scholar 

  117. Shigenaga MK, Hangen TM, Ames BN. Oxidative damage and mitochondrial decay in aging. Proc Natl Acad Sci USA. 1994;91:10771–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  118. Michikawa Y, Mazzucchelli F, Bresolin N, et al. Aging-dependent large accumulation of point mutations in the human mtDNA control region for replication. Science. 1999;286:774.

    Article  CAS  PubMed  Google Scholar 

  119. Wallace DC, Murdock DG. Mitochondria and dystonia: The movement disorder connection? Proc Natl Acad Sci USA. 1999;96:1817–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  120. Wang Q, Ratchford AM, Chi MM, et al. Maternal diabetes causes mitochondrial dysfunction and meiotic defects in murine oocytes. Mol Endocrinol. 2009;23(10):1603–12. doi:10.1210/me.2009-0033.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  121. Igosheva N, Abramov AY, Poston L, et al. Maternal diet-induced obesity alters mitochondrial activity and redox status in mouse oocytes and zygotes. PLoS ONE. 2010;5(4):e10074. doi:10.1371/journal.pone.0010074.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  122. Kushnir VA, Ludaway T, Russ RB, et al. Reproductive aging is associated with decreased mitochondrial abundance and altered structure in murine oocytes. J Assist Reprod Genet. 2012;29(7):637–42. doi:10.1007/s10815-012-9771-5.

    Article  PubMed  PubMed Central  Google Scholar 

  123. Ou XH, Li S, Wang ZB, et al. Maternal insulin resistance causes oxidative stress and mitochondrial dysfunction in mouse oocytes. Hum Reprod. 2012;27(7):2130–45. doi:10.1093/humrep/des137.

    Article  CAS  PubMed  Google Scholar 

  124. Fissore RA, Kurikawa M, Knott J, et al. Mechanisms underlying oocyte activation and postovulatory ageing. Reproduction. 2002;124:745–54.

    Article  CAS  PubMed  Google Scholar 

  125. Ramalho-Santos J, Amaral A, Brito R, et al. Simultaneous analysis of cytoskeleton patterns and chromosome positioning in human fertilization failures. Fertil Steril. 2004;82(6):1654–9. doi:10.1016/j.fertnstert.2004.05.086.

    Article  PubMed  Google Scholar 

  126. Thouas GA, Trounson AO, Wolvetang EJ, et al. Mitochondrial dysfunction in mouse oocytes results in preimplantation embryo arrest in vitro. Biol Reprod. 2004;71(6):1936–42. doi:10.1095/biolreprod.104.033589.

    Article  CAS  PubMed  Google Scholar 

  127. Cummins JM. Fertilization and elimination of the paternal mitochondrial genome. Hum Reprod. 2000;15(Suppl 2):92–101.

    Article  PubMed  Google Scholar 

  128. Inoue K, Nakada K, Ogura A, et al. Generation of mice with mitochondrial dysfunction by introducing mouse mtDNA carrying a deletion into zygotes. Nat Genet. 2000;26(2):176–81.

    Article  CAS  PubMed  Google Scholar 

  129. Kasahara A, Ishikawa K, Yamaoka M, et al. Generation of trans-mitochondrial mice carrying homoplasmic mtDNAs with a missense mutation in a structural gene using ES cells. Hum Mol Genet. 2006;15(6):871–81. doi:10.1093/hmg/ddl005.

    Article  CAS  PubMed  Google Scholar 

  130. Nakada K, Sato A, Yoshida K, et al. Mitochondria-related male infertility. Proc Natl Acad Sci U S A. 2006;103(41):15148–53.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  131. Inoue S, Yokota M, Nakada K, et al. Pathogenic mitochondrial DNA-induced respiration defects in hematopoietic cells result in anemia by suppressing erythroid differentiation. FEBS Lett. 2007;581(9):1910–6. doi:10.1016/j.febslet.2007.03.092.

    Article  CAS  PubMed  Google Scholar 

  132. Tanaka D, Nakada K, Takao K, et al. Normal mitochondrial respiratory function is essential for spatial remote memory in mice. Mol Brain. 2008;1:21. doi:10.1186/1756-6606-1-21.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  133. Inoue M, Nishikawa M, Sato E, et al. Cross-talk of NO, superoxide and molecular oxygen, majesty of aerobic life. Free Radic Res. 1999;31(4):251–60.

    Article  CAS  PubMed  Google Scholar 

  134. Chang B, Nishikawa M, Sato E, et al. L-Carnitine inhibits cisplatin-induced injury of the kidney and small intestine. Arch Biochem Biophys. 2002;405(1):55–64. doi:10.1016/S0003-9861(02)00342-9.

    Article  CAS  PubMed  Google Scholar 

  135. Kira Y, Nishikawa M, Ochi A, et al. L-carnitine suppresses the onset of neuromuscular degeneration and increases the life span of mice with familial amyotrophic lateral sclerosis. Brain Res. 2006;1070(1):206–14.

    Article  CAS  PubMed  Google Scholar 

  136. Hino K, Nishikawa M, Sato E, et al. L-carnitine inhibits hypoglycemia-induced brain damage in the rat. Brain Res. 2005;1053(1–2):77–87.

    Article  CAS  PubMed  Google Scholar 

  137. Moawad AR, Xu B, Tan SL, et al. L-carnitine supplementation during vitrification of mouse germinal vesicle stage–oocytes and their subsequent in vitro maturation improves meiotic spindle configuration and mitochondrial distribution in metaphase II oocytes. Hum Reprod. 2014;29(10):2256–68. doi:10.1093/humrep/deu201.

    Article  PubMed  Google Scholar 

  138. McPherson NO, Zander-Fox D, Lane M. Stimulation of mitochondrial embryo metabolism by dichloroacetic acid in an aged mouse model improves embryo development and viability. Fertil Steril. 2014;101(5):1458–66. doi:10.1016/j.fertnstert.2013.12.057.

    Article  CAS  PubMed  Google Scholar 

  139. Gendelman M, Roth Z. Incorporation of coenzyme Q10 into bovine oocytes improves mitochondrial features and alleviates the effects of summer thermal stress on developmental competence. Biol Reprod. 2012;87(5):118. doi:10.1095/biolreprod.112.101881.

    Article  PubMed  CAS  Google Scholar 

  140. Cohen J, Scott R, Schimmel T et al. Birth of infant after transfer of anucleate donor oocyte cytoplasm into recipient eggs. Lancet. 1997;19;350(9072):186–7.

    Google Scholar 

  141. Cohen J, Scott R, Alikani M, et al. Ooplasmic transfer in mature human oocytes. Mol Hum Reprod. 1998;4(3):269–80.

    Article  CAS  PubMed  Google Scholar 

  142. Huang CC, Cheng TC, Chang HH, et al. Birth after the injection of sperm and the cytoplasm of tripronucleate zygotes into metaphase II oocytes in patients with repeated implantation failure after assisted fertilization procedures. Fertil Steril. 1999;72(4):702–6.

    Article  CAS  PubMed  Google Scholar 

  143. Lanzendorf SE, Mayer JF, Toner J, et al. Pregnancy following transfer of ooplasm from cryopreserved-thawed donor oocytes into recipient oocytes. Fertil Steril. 1999;71(3):575–7.

    Article  CAS  PubMed  Google Scholar 

  144. Brenner CA, Barritt JA, Willadsen S, et al. Mitochondrial DNA heteroplasmy after human ooplasmic transplantation. Fertil Steril. 2000;74(3):573–8.

    Article  CAS  PubMed  Google Scholar 

  145. Barritt JA, Brenner CA, Willadsen S, et al. Spontaneous and artificial changes in human ooplasmic mitochondria. Hum Reprod. 2000;15(Suppl 2):207–17.

    Article  PubMed  Google Scholar 

  146. Barritt JA, Brenner CA, Malter HE, et al. Mitochondria in human offspring derived from ooplasmic transplantation. Hum Reprod. 2001;16(3):513–6.

    Article  CAS  PubMed  Google Scholar 

  147. Barritt JA, Willadsen S, Brenner CA, et al. Epigenetic and experimental modification in early mammalian development: Part II. Cytoplasmic transfer in assisted reproduction. Hum Reprod Update. 2001;7(4):428–35.

    Article  CAS  PubMed  Google Scholar 

  148. Viet Linh N, Kikuchi K, Nakai M et al. Improvement of porcine oocytes with low developmental ability after fusion of cytoplasmic fragments prepared by serial centrifugation. J Reprod Dev. 2011;57(5):620–6.

    Google Scholar 

  149. Chiaratti MB, Ferreira CR, Perecin F, et al. Ooplast-mediated developmental rescue of bovine oocytes exposed to ethidium bromide. Reprod Biomed Online. 2011;22(2):172–83. doi:10.1016/j.rbmo.2010.10.011.

    Article  CAS  PubMed  Google Scholar 

  150. Tachibana M, Sparman M, Sritanaudomchai H, et al. Mitochondrial gene replacement in primate offspring and embryonic stem cells. Nature. 2009;461(7262):367–72. doi:10.1038/nature08368.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  151. Craven L, Tuppen HA, Greggains GD, et al. Pronuclear transfer in human embryos to prevent transmission of mitochondrial DNA disease. Nature. 2010;465(7294):82–5. doi:10.1038/nature08958.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  152. Paull D, Emmanuele V, Weiss KA, et al. Nuclear genome transfer in human oocytes eliminates mitochondrial DNA variants. Nature. 2013;493(7434):632–7. doi:10.1038/nature11800.

    Article  CAS  PubMed  Google Scholar 

  153. Neupane J, Vandewoestyne M, Ghimire S, et al. Assessment of nuclear transfer techniques to prevent the transmission of heritable mitochondrial disorders without compromising embryonic development competence in mice. Mitochondrion. 2014;18C:27–33. doi:10.1016/j.mito.2014.09.003.

    Article  CAS  Google Scholar 

  154. Bai ZD, Liu K, Wang XY. Developmental potential of aged oocyte rescued by nuclear transfer following parthenogenetic activation and in vitro fertilization. Mol Reprod Dev. 2006;73(11):1448–53. doi:10.1002/mrd.20538.

    Article  CAS  PubMed  Google Scholar 

  155. Cui LB, Huang XY, Sun FZ. Transfer of germinal vesicle to ooplasm of young mice could not rescue ageing-associated chromosome misalignment in meiosis of oocytes from aged mice. Hum Reprod. 2005;20(6):1624–31.

    Article  PubMed  Google Scholar 

  156. El Shourbagy SH, Spikings EC, Freitas M, et al. Mitochondria directly influence fertilisation outcome in the pig. Reproduction. 2006;131(2):233–45.

    Article  PubMed  CAS  Google Scholar 

  157. Perez GI, Trbovich AM, Gosden RG, et al. Mitochondria and the death of oocytes. Nature. 2000;403(6769):500–1.

    Article  CAS  PubMed  Google Scholar 

  158. Hua S, Zhang Y, Li XC, et al. Effects of granulosa cell mitochondria transfer on the early development of bovine embryos in vitro. Cloning Stem Cells. 2007;9(2):237–46.

    Article  CAS  PubMed  Google Scholar 

  159. Yi YC, Chen MJ, Ho JY, et al. Mitochondria transfer can enhance the murine embryo development. J Assist Reprod Genet. 2007;24(10):445–9.

    Article  PubMed  PubMed Central  Google Scholar 

  160. Tzeng C, Hsieh R, Chang S et al. Pregnancy derived from mitochondria transfer (MIT) into oocyte from patient’s own cumulus granulosa cells (cGCs). Fertil Seril. 76, S67–8.

    Google Scholar 

  161. Takeda K, Tasai M, Iwamoto M, et al. Microinjection of cytoplasm or mitochondria derived from somatic cells affects parthenogenetic development of murine oocytes. Biol Reprod. 2005;72(6):1397–404. doi:10.1095/biolreprod.104.036129.

    Article  CAS  PubMed  Google Scholar 

  162. Sathananthan H, Pera M, Trounson A. The fine structure of human embryonic stem cells. Reprod Biomed Online. 2002;4(1):56–61.

    Article  PubMed  Google Scholar 

  163. Baharvand H, Matthaei KI. The ultrastructure of mouse embryonic stem cells. Reprod Biomed Online. 2003;7(3):330–5.

    Article  PubMed  Google Scholar 

  164. Ohmine S, Squillace KA, Hartjes KA, et al. Reprogrammed keratinocytes from elderly type 2 diabetes patients suppress senescence genes to acquire induced pluripotency. Aging. 2012;4(1):60–73.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. HORAC Grand Front Osaka Clinic, Osaka, Japan

    Yoshiharu Morimoto MD, PhD

  2. Division of Research, IVF Namba Clinic, Osaka, Japan

    Shu Hashimoto PhD, Takayuki Yamochi, Hiroya Goto, Ami Amo BS, Masaya Yamanaka & Masayasu Inoue

Authors
  1. Yoshiharu Morimoto MD, PhD
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Shu Hashimoto PhD
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Takayuki Yamochi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Hiroya Goto
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Ami Amo BS
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Masaya Yamanaka
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Masayasu Inoue
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Yoshiharu Morimoto MD, PhD .

Editor information

Editors and Affiliations

  1. McGill University, Longueuil, Québec, Canada

    Ri-Cheng Chian

  2. St. George's Hospital, London, United Kingdom

    Geeta Nargund

  3. Stanford University, Palo Alto, California, USA

    Jack Y. J. Huang

Rights and permissions

Reprints and permissions

Copyright information

© 2017 Springer International Publishing AG

About this chapter

Cite this chapter

Morimoto, Y. et al. (2017). Mitochondria of the Oocyte. In: Chian, RC., Nargund, G., Huang, J. (eds) Development of In Vitro Maturation for Human Oocytes. Springer, Cham. https://doi.org/10.1007/978-3-319-53454-1_4

Download citation

  • DOI: https://doi.org/10.1007/978-3-319-53454-1_4

  • Published:

  • Publisher Name: Springer, Cham

  • Print ISBN: 978-3-319-53452-7

  • Online ISBN: 978-3-319-53454-1

  • eBook Packages: MedicineMedicine (R0)

Publish with us

Policies and ethics

Search

Navigation