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Supply and Demand of Energy in the Oocyte and the Role of Mitochondria

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Oocytes

Part of the book series: Results and Problems in Cell Differentiation ((RESULTS,volume 63))

Abstract

The sole purpose of any mammalian oocyte is to combine with a spermatozoon and form a viable embryo that implants into the uterus and forms a viable foetus. Most of the structures and mechanisms for this reside within the oocyte itself. The sperm limits itself to fertilisation of the oocyte; apart from this, its only contribution is the male genome and the centrosome, required for cell division. Both intrinsic and extrinsic factors determine the formation of a viable embryo. However, the fundamental necessity for successful reproduction resides within the capacity for the developing embryo to generate sufficient levels of energy for optimal development to occur. Energy is generated principally within mitochondria. In this chapter, we discuss some of the fundamental processes of preimplantation embryo development and the role of mitochondria in providing sufficient energy for the successful completion of these processes. We discuss mitochondrial genetics, replication and energy production. Ageing appears to affect the capacity of the mitochondrion to produce sufficient energy to balance the requirements of the embryo. We discuss some of the theories of the effect of maternal age on mitochondrial physiology and the role this plays in reproduction. We propose that maternal age has longer-term effects on individuals than simply on the efficiency of reproduction. We also discuss some of the procedures assisted reproduction has proposed to alleviate the effect of maternal age on reproduction.

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References

  • Adiele RC, Adiele CA (2016) Mitochondrial regulatory pathways in the pathogenesis of alzheimer’s disease. J Alzheimers Dis 53(4):1257–1270

    Article  CAS  PubMed  Google Scholar 

  • Almeida-Santos T, El Shourbagy S, St. John JC (2006) Mitochondrial content reflects oocyte variability and fertilization outcome. Fertil Steril 85:584–591

    Article  Google Scholar 

  • Ancora M, Orsini M, Colosimo A, Marcacci M, Russo V, De Santo M, De Aurora M, Stuppia L, Barboni B, Camma C, Gstta V (2016) Complete sequence of human mitochondrial DNA obtained by combining multiple displacement amplification and next-generation sequencing on a single oocyte. Mitochondrial DNA A DNA Mapp. Seq Anal 24:1–2

    Google Scholar 

  • Anderson S, Bankier AT, Barrell BG, de Bruijn MH, Coulson AR, Drouin J, Eperon IC, Nierlich DP, Roe BA, Sanger F et al (1981) Sequence and organization of the human mitochondrial genome. Nature 290:457–465

    Article  CAS  PubMed  Google Scholar 

  • Babayev E, Wang T, Szigeti-Buck K, Lowther K, Taylor H, Horvath T, Seli E (2016) Reproductive ageing is associated with changes in oocyte mitochondrial dynamics, function and mtDNA quality. Maturitas 16:30145–30141

    Google Scholar 

  • Barritt JA, Brenner CA, Cohen J, Matt DW (1999) Mitochondrial DNA rearrangements in human oocytes and embryos. Mol Hum Reprod 5(10):927–933

    Article  CAS  PubMed  Google Scholar 

  • Barritt JA, Brenner CA, Malter HE, Cohen J (2001a) Mitochondria in human offspring derived from ooplasmic transplantation. Hum Reprod 16(3):513–516

    Article  CAS  PubMed  Google Scholar 

  • Barritt J, Willadsen S, Brenner C, Cohen J (2001b) Cytoplasmic transfer in assisted reproduction. Hum Reprod Update 7(4):428–435

    Article  CAS  PubMed  Google Scholar 

  • Barritt JA, Kokot M, Cohen J, Steuerwald N, Brenner CA (2002) Quantification of human ooplasmic mitochondria. Reprod Biomed Online 4(3):243–247

    Article  CAS  PubMed  Google Scholar 

  • Bavister BD, Squirrell JM (2000) Mitochondrial distribution and function in oocytes and early embryos. Hum Reprod 15(Suppl 2):189–198

    Article  PubMed  Google Scholar 

  • Björkholm P, Harish A, Hagström E, Ernst AM, Andersson SGE (2015) Mitochondrial genomes are retained by selective constraints on protein targeting. Proc Natl Acad Sci 112(33):10154–10161

    Article  PubMed  PubMed Central  Google Scholar 

  • Braude P, Bolton V, Moore S (1988) Human gene expression first occurs between the four and eight-cell stages of preimplantation development. Nature 332:459–461

    Article  CAS  PubMed  Google Scholar 

  • Butcher L, Coates A, Martin KL, Rutherford AJ, Leese HJ (1998) Metabolism of pyruvate by the early human embryo. Biol Reprod 58(4):1054–1056

    Article  CAS  PubMed  Google Scholar 

  • Cohen J, Scott R, Schimmel T, Levron J, Willadsen S (1997) Birth of infant after transfer of anucleate donor oocyte cytoplasm into recipient eggs. Lancet 350(9072):186–187

    Article  CAS  PubMed  Google Scholar 

  • Craven L, Tuppen HA, Greggains GD, Harbottle SJ, Murphy JL, Cree LM, Murdoch AP, Chinnery PF, Taylor RW, Lightowlers RN, Herbert M, Turnbull DM (2010) Pronuclear transfer in human embryos to prevent transmission of mitochondrial DNA disease. Nature 465(7294):82–85

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cummins J (2002) The role of maternal mitochondria during oogenesis, fertilisation and embryogenesis. Reprod Biomed Online 4:176–182

    Article  CAS  PubMed  Google Scholar 

  • Dailey T, Dale B, Cohen J, Munné S (1996) Association between nondisjunction and maternal age in meiosis-II human oocytes. Am J Hum Genet 59(1):176–184

    CAS  PubMed  PubMed Central  Google Scholar 

  • Dale B, Defelice L, Ehrenstein G (1985) Injection of a soluble sperm extract into sea urchin eggs triggers the cortical reaction. Experentia 41:1068–1070

    Article  CAS  Google Scholar 

  • Dale B, Gualtieri R, Talevi R, Tosti E, Santella L, Elder K (1991) Intercellular communication in the early human embryo. Mol Reprod Dev 29:22–28

    Article  CAS  PubMed  Google Scholar 

  • Diot A, Morten K, Poulton J (2016) Mitophagy plays a central role in mitochondrial ageing. Mamm Genome 27:381–395

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Eichenlaub-Ritter U, Wieczorek M, Lüke S, Seidel T (2011) Age related changes in mitochondrial function and new approaches to study redox regulation in mammalian oocytes in response to age or maturation conditions. Mitochondrion 11:783–796

    Article  CAS  PubMed  Google Scholar 

  • Findlay JK, Hutt KJ, Hickey M, Anderson RA (2015) How is the number of primordial follicles in the ovarian reserve established? Biol Reprod 93(5):111

    Article  PubMed  Google Scholar 

  • Fragouli E, Spath K, Alfarawati S, Kaper F, Craig A, Michel CE, Kokocinski F, Cohen J, Munne S, Wells D (2015) Altered levels of mitochondrial DNA are associated with female age, aneuploidy, and provide an independent measure of embryonic implantation potential. PLoS Genet 11(6):e1005241

    Article  PubMed  PubMed Central  Google Scholar 

  • García-Palomares S, Pertusa JF, Miñarro J, García-Pérez MA, Hermenegildo C, Rausell F, Cano A, Tarín JJ (2009) Long-term effects of delayed fatherhood in mice on postnatal development and behavioral traits of offspring. Biol Reprod 80:337–342

    Article  PubMed  Google Scholar 

  • Guantes R, Rastrojo A, Neves R, Lima A, Aguado B, Iborra FJ (2015) Global variability in gene expression and alternative splicing is modulated by mitochondrial content. Genome Res 25(5):633–644

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guo Y, Cai Q, Samuels DC, Ye F, Long J, Li C, Winther J, Tawn E, Stovall M, Lahteenmaki P, Malila N, Levy S, Shaffer C, Shyr Y, Shu X, Boice J (2012) The use of next generation sequencing to study the effect of radiation therapy on mitochondrial DNA mutations. Mutat Res 744:154–160

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hammond ER, Green MP, Shelling AN, Berg MC, Peek JC, Cree LM (2016) Oocyte mitochondrial deletions and heteroplsmy in a bovine model of ageing and ovarian stimulation. Mol Hum Reprod 22:261–271

    Article  PubMed  Google Scholar 

  • Harman D (1956) Aging: a theory based on free radical and radiation chemistry. J Gerontol 11(3):298–300

    Article  CAS  PubMed  Google Scholar 

  • Harman D (2009) Origin and evolution of the free radical theory of aging: a brief personal history, 1954–2009. Biogerontology 10(6):773–781

    Article  CAS  PubMed  Google Scholar 

  • Hassold T, Chiu D (1985) Maternal age-specific rates of numerical chromosome abnormalities with special reference to trisomy. Hum Genet 70:11–17

    Article  CAS  PubMed  Google Scholar 

  • Hellebrekers DM, Wolfe R, Hendrickx AT, de Coo IF, de Die CE, Geraedts JP, Chinnery PF, Smeets HJ (2012) PGD and heteroplasmic mitochondrial DNA point mutations: a systematic review estimating the chance of healthy offspring. Hum Reprod Update 18:341–349

    Article  CAS  PubMed  Google Scholar 

  • Hyslop LA, Blakeley P, Craven L, Richardson J, Fogarty NM, Fragouli E, Lamb M, Wamaitha SE, Prathalingam N, Zhang Q, O’Keefe H, Takeda Y, Arizzi L, Alfarawati S, Tuppen HA, Irving L, Kalleas D, Choudhary M, Wells D, Murdoch AP, Turnbull DM, Niakan KK, Herbert M (2016) Towards clinical application of pronuclear transfer to prevent mitochondrial DNA disease. Nature 534(7607):383–386

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kloc M, Kubiak JZ (2017) Exogenous molecules and organelles delivery in oogenesis. In: Kloc M (ed) Oocytes: maternal information and functions. Springer, Cham

    Chapter  Google Scholar 

  • Krebs HA (1965) Gluconeogenesis. Expos Annu Biochim Med 26:13–30

    CAS  PubMed  Google Scholar 

  • Lansing AI (1947) A transmissible, cumulative and reversible factor in aging. J Gerontol 2:228–239

    Article  CAS  PubMed  Google Scholar 

  • Lansing AI (1948) Evidence for aging as a consequence of growth cessation. Proc Natl Acad Sci 34:304–310

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Leese HJ (2012) Metabolism of the preimplantation embryo: 40 years on. Reproduction 143(4):417–427

    Article  CAS  PubMed  Google Scholar 

  • Leese HJ, Conaghan J, Martin KL, Hardy K (1993) Early human embryo metabolism. Bioessays 15(4):259–264

    Article  CAS  PubMed  Google Scholar 

  • Linnane AW, Marzuki S, Ozawa T et al (1989) Mitochondrial mutations as an important contributor to ageing and degenerative diseases. Lancet 1:642–645

    Article  CAS  PubMed  Google Scholar 

  • Linnane AW, Zhang C, Baumer A, Nagley P (1992) Mitochondrial DNA mutations and the ageing process: bioenergy and pharmacological intervention. Mutat Res 275:195–208

    Article  CAS  PubMed  Google Scholar 

  • López-Otín C, Blasco MA, Partridge L, Serrano M, Kroemer G (2013) The hallmarks of aging. Cell 153(6):1194–1217

    Article  PubMed  PubMed Central  Google Scholar 

  • Martin KH, Winston RML, Leese HJ (1993) Activity of enzymes of energy metabolism in single human preimplantation embryos. J Reprod Fertil 99:259–266

    Article  CAS  PubMed  Google Scholar 

  • May-panloup P, Boucref L, Chao de la Barca J, Desquiret-Dumas V, Ferre-L’Hotelier V, Moriniere C, Descamps P, Procaccio V, Reynier P (2016) Ovarian ageing: the role of mitochondria in oocytes and follicles. Hum Reprod Update 22(6):725–743

    Article  PubMed  Google Scholar 

  • Muir R, Diot A, Poulton J (2016) Mitochondrial content is central to nuclear gene expression: Profound implications for human health. BioEssays 38(2):150–156

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Navot D, Bergh PA, Williams MA, Garrisi GJ, Guzman I, Sandler B, Grunfeld L (1991) Poor oocyte quality rather than implantation failure as a cause of age-related decline in female fertility. Lancet 337:1375–1377

    Article  CAS  PubMed  Google Scholar 

  • New Scientist (2016) Exclusive: World’s first baby born with new “3 parent” technique. https://www.newscientist.com/article/2107219-exclusive-worlds-first-baby-born-with-new-3-parent-technique/

  • Ogino M, Tsubamo H, Sakata K, Oohama N, Hyakawa H, Kojima T, Shigeta M, Shibahara H (2016) Mitochondrial DNA copy number in cumulus cells is a strong predictor of obtaining good quality embryos after IVF. J Assist Reprod Genet 33:367–371

    Article  PubMed  PubMed Central  Google Scholar 

  • Pawlak P, Chabowska A, Malyszka N, Lechniak D (2016) Mitochondria and mitochondrial DNA in porcine oocytes and cumulus cells—a search for developmental competence marker. Mitochondrion 27:48–55

    Article  CAS  PubMed  Google Scholar 

  • Piko L, Chase DH (1973) Role of the mitochondrial genome during early development in mice. Effects of ethidium bromide and chloramphenicol. J Cell Biol 58:357–378

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Priest NK, Mackowiak B, Promislow DEL (2002) The role of parental age effects on the evolution of aging. Evolution 56:927–935

    Article  PubMed  Google Scholar 

  • Rambags BP, van Boxtel DC, Tharasanit Y, Lenstra JA, Colenbrander B, Stout TA (2014) Advancing maternal age predisposes to mitochondrial damage and loss during maturation of equine oocytes in vitro. Theriogenology 81:959–965

    Article  CAS  PubMed  Google Scholar 

  • Reynier P, May-Panloup P, Chrétien MF, Morgan CJ, Jean M, Savagner F, Barrière P, Malthièry Y (2001) Mitochondrial DNA content affects the fertilizability of human oocytes. Mol Hum Reprod 7(5):425–429

    Article  CAS  PubMed  Google Scholar 

  • Rich PR (2003) The molecular machinery of Keilin’s respiratory chain. Biochem Soc Trans 31(Pt 6):1095–1105

    Article  CAS  PubMed  Google Scholar 

  • Shahbazi MN, Jedrusik A, Vuoristo S, Recher G, Hupalowska A, Bolton V, Fogarty NM, Campbell A, Devito LG, Ilic D, Khalaf Y, Niakan KK, Fishel S, Zernicka-Goetz M (2016) Self-organization of the human embryo in the absence of maternal tissues. Nat Cell Biol 18(6):700–708

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • St John JC, Facucho-Oliveira J, Jiang Y, Kelly R, Salah R (2010) Mitochondrial DNA transmission, replication and inheritance: a journey from the gamete through the embryo and into offspring and embryonic stem cells. Hum Reprod Update 16:488–509

    Article  CAS  PubMed  Google Scholar 

  • Sturmey RG, Leese HJ (2003) Energy metabolism in pig oocytes and early embryos. Reproduction 126(2):197–204

    Article  CAS  PubMed  Google Scholar 

  • Sutovsky P, Schatten G (2000) Paternal contributions to the mammalian zygote: fertilization after sperm-egg fusion. Int Rev Cytol 195:1–65

    CAS  PubMed  Google Scholar 

  • Tachibana M, Sparman M, Sritanaudomchai H, Ma H, Clepper L, Woodward J, Li Y, Ramsey C, Kolotushkina O, Mitalipov S (2009) Mitochondrial gene replacement in primate offspring and embryonic stem cells. Nature 461(7262):367–372

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tarín JJ, Brines J, Cano A (1998) Long-term effects of delayed parenthood. Hum Reprod 13:2371–2376

    Article  PubMed  Google Scholar 

  • Tarín JJ, Gómez-Piquer V, Manzanedo C, Miñarro J, Hermenegildo C, Cano A (2003) Long-term effects of delayed motherhood in mice on postnatal development and behavioural traits of offspring. Hum Reprod 18:1580–1587

    Article  PubMed  Google Scholar 

  • Tarín JJ, Gómez-Piquer V, Rausell F, Navarro S, Hermenegildo C, Cano A (2005) Delayed motherhood decreases life expectancy of mouse offspring. Biol Reprod 72:1336–1343

    Article  PubMed  Google Scholar 

  • Valero T (2014) Mitochondrial biogenesis: pharmacological approaches. Curr Pharm Des 20(35):5507–5509

    Article  CAS  PubMed  Google Scholar 

  • Van Blerkom J, Davis PW, Lee J (1995) ATP content of human oocytes and developmental potential and outcome after in-vitro fertilization and embryo transfer. Hum Reprod 10(2):415–424

    Article  CAS  PubMed  Google Scholar 

  • Wei YH, CY L, Lee HC, Pang CY, Ma YS (1998) Oxidative damage and mutation to mitochondrial DNA and age-dependent decline of mitochondrial respiratory function. Ann N Y Acad Sci 854:155–170

    Article  CAS  PubMed  Google Scholar 

  • Wilding M (2014) Can we define maternal age as a genetic disease? Facts Views Vis Obgyn 6(2):105–108

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wilding M (2015) Potential long-term risks associated with maternal aging (the role of the mitochondria). Fertil Steril 103(6):1397–1401

    Article  PubMed  Google Scholar 

  • Wilding M, Dale B, Marino M, di Matteo L, Alviggi C, Pisaturo ML, Lombardi L, De Placido G (2001) Mitochondrial aggregation patterns and activity in human oocytes and preimplantation embryos. Hum Reprod 16(5):909–917

    Article  CAS  PubMed  Google Scholar 

  • Wilding M, De Placido G, De Matteo L, Marino M, Alviggi C, Dale B (2003) Chaotic mosaicism in human preimplantation embryos is correlated with a low mitochondrial membrane potential. Fertil Steril 79(2):340–346

    Article  PubMed  Google Scholar 

  • Wilding M, Di Matteo L, Dale B (2005) The maternal age effect: a hypothesis based on oxidative phosphorylation. Zygote 13(4):317–323

    Article  CAS  PubMed  Google Scholar 

  • Wilding M, Coppola G, Dale B, Di Matteo L (2009) Mitochondria and human preimplantation embryo development. Reproduction 137(4):619–624

    Article  CAS  PubMed  Google Scholar 

  • Wilding M, Coppola G, De Icco F, Arenare L, Di Matteo L, Dale B (2014) Maternal non-Mendelian inheritance of a reduced lifespan? A hypothesis. J Assist Reprod Genet 31(6):637–643

    PubMed  PubMed Central  Google Scholar 

  • Yonemura I, Motoyama T, Hasekura H, Boettcher B (1991) Cytoplasmic influence on the expression of nuclear genes affecting life span in Drosophila melanogaster. Heredity (Edinb) 66:259–264

    Article  Google Scholar 

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  1. Centre for Reproduction and Advanced Technology (CREATE), 150 Cheapside, London, EC2V 6ET, UK

    Wilding Martin

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  1. Department of Surgery, The Houston Methodist Hospital, Houston, Texas, USA

    Malgorzata Kloc

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Martin, W. (2017). Supply and Demand of Energy in the Oocyte and the Role of Mitochondria. In: Kloc, M. (eds) Oocytes. Results and Problems in Cell Differentiation, vol 63. Springer, Cham. https://doi.org/10.1007/978-3-319-60855-6_16

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