Advertisement

Asymmetries and Symmetries in the Mouse Oocyte and Zygote

  • Agathe Chaigne
  • Marie-Emilie Terret
  • Marie-Hélène VerlhacEmail author
Chapter
Part of the Results and Problems in Cell Differentiation book series (RESULTS, volume 61)

Abstract

Mammalian oocytes grow periodically after puberty thanks to the dialogue with their niche in the follicle. This communication between somatic and germ cells promotes the accumulation, inside the oocyte, of maternal RNAs, proteins and other molecules that will sustain the two gamete divisions and early embryo development up to its implantation. In order to preserve their stock of maternal products, oocytes from all species divide twice minimizing the volume of their daughter cells to their own benefit. For this, they undergo asymmetric divisions in size where one main objective is to locate the division spindle with its chromosomes off-centred. In this chapter, we will review how this main objective is reached with an emphasis on the role of actin microfilaments in this process in mouse oocytes, the most studied example in mammals. This chapter is subdivided into three parts: I—General features of asymmetric divisions in mouse oocytes, II—Mechanism of chromosome positioning by actin in mouse oocytes and III—Switch from asymmetric to symmetric division at the oocyte-to-embryo transition.

Keywords

Actin Filament Meiotic Division Mouse Oocyte Asymmetric Division Meiotic Spindle 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgements

This work was supported by the Fondation pour la Recherche Médicale (Equipe FRM to MHV), the ANR (ANR-14-CE11-0002 to MHV) and the Fondation ARC (PJA20131200412 to MET). This work has received support from the Fondation Bettencourt Schueller, support under the programme “Investissements d’Avenir” launched by the French Government and implemented by the ANR, with the references: ANR-10-LABX-54 MEMO LIFE, ANR-11-IDEX-0001-02 PSL* Research University.

References

  1. Almonacid M, Terret M-É, Verlhac M-H (2014) Actin-based spindle positioning: new insights from female gametes. J Cell Sci 127:477–483CrossRefPubMedGoogle Scholar
  2. Almonacid M, Ahmed WW, Bussonnier M, Mailly P, Betz T, Voituriez R, Gov NS, Verlhac M-H (2015) Active diffusion positions the nucleus in mouse oocytes. Nat Cell Biol 17:470–479CrossRefPubMedGoogle Scholar
  3. Azoury J, Lee K, Georget V, Rassinier P, Leader B, Verlhac M (2008) Spindle positioning in mouse oocytes relies on a dynamic meshwork of actin filaments. Curr Biol 18:1514–1519CrossRefPubMedGoogle Scholar
  4. Azoury J, Lee KW, Georget V, Hikal P, Verlhac M-H (2011) Symmetry breaking in mouse oocytes requires transient F-actin meshwork destabilization. Development 138:2903–2908CrossRefPubMedGoogle Scholar
  5. Brunet S, Maro B (2007) Germinal vesicle position and meiotic maturation in mouse oocyte. Reproduction 133:1069–1072CrossRefPubMedGoogle Scholar
  6. Brunet S, Verlhac MH (2011) Positioning to get out of meiosis: the asymmetry of division. Hum Reprod Update 17:68–75CrossRefPubMedGoogle Scholar
  7. Cadart C, Zlotek-Zlotkiewicz E, Le Berre M, Piel M, Matthews HK (2014) Exploring the function of cell shape and size during mitosis. Dev Cell 29:159–169CrossRefPubMedGoogle Scholar
  8. Cakmak H, Franciosi F, Zamah AM, Cedars MI, Conti M (2016) Dynamic secretion during meiotic reentry integrates the function of the oocyte and cumulus cells. Proc Natl Acad Sci USA 113:2424–2429CrossRefPubMedPubMedCentralGoogle Scholar
  9. Calarco-Gillam PD, Siebert MC, Hubble R, Mitchison T, Kirschner M (1983) Centrosome development in early mouse embryos as defined by an autoantibody against pericentriolar material. Cell 35:621–629CrossRefPubMedGoogle Scholar
  10. Chaigne A, Campillo C, Gov NS, Voituriez R, Azoury J, Umaña-Diaz C, Almonacid M, Queguiner I, Nassoy P, Sykes C et al (2013) A soft cortex is essential for asymmetric spindle positioning in mouse oocytes. Nat Cell Biol 15:958–966CrossRefPubMedGoogle Scholar
  11. Chaigne A, Campillo C, Gov NS, Voituriez R, Sykes C, Verlhac MH, Terret ME (2015) A narrow window of cortical tension guides asymmetric spindle positioning in the mouse oocyte. Nat Commun 6:6027CrossRefPubMedGoogle Scholar
  12. Chaigne A, Campillo C, Voituriez R, Gov NS, Sykes C, Verlhac M-H, Terret M-E (2016) F-actin mechanics control spindle centring in the mouse zygote. Nat Commun 7:10253CrossRefPubMedPubMedCentralGoogle Scholar
  13. Chen J, Torcia S, Xie F, Lin C-J, Cakmak H, Franciosi F, Horner K, Onodera C, Song JS, Cedars MI et al (2013) Somatic cells regulate maternal mRNA translation and developmental competence of mouse oocytes. Nat Cell Biol 15:1415–1423CrossRefPubMedPubMedCentralGoogle Scholar
  14. Chew TG, Lorthongpanich C, Ang WX, Knowles BB, Solter D (2012) Symmetric cell division of the mouse zygote requires an actin network. Cytoskeleton 69:1040–1046CrossRefPubMedGoogle Scholar
  15. Clift D, Schuh M (2013) Restarting life: fertilization and the transition from meiosis to mitosis. Nat Rev Mol Cell Biol 14:549–562CrossRefPubMedPubMedCentralGoogle Scholar
  16. Courtois A, Schuh M, Ellenberg J, Hiiragi T (2012) The transition from meiotic to mitotic spindle assembly is gradual during early mammalian development. J Cell Biol 198:357–370CrossRefPubMedPubMedCentralGoogle Scholar
  17. Dalton CM, Carroll J (2013) Biased inheritance of mitochondria during asymmetric cell division in the mouse oocyte. J Cell Sci 126:2955–2964CrossRefPubMedPubMedCentralGoogle Scholar
  18. Dehapiot B, Carrière V, Carroll J, Halet G (2013) Polarized Cdc42 activation promotes polar body protrusion and asymmetric division in mouse oocytes. Dev Biol 377:20212CrossRefGoogle Scholar
  19. Dumont J, Million K, Sunderland K, Rassinier P, Lim H, Leader B, Verlhac M-H (2007a) Formin-2 is required for spindle migration and for the late steps of cytokinesis in mouse oocytes. Dev Biol 301:254–265CrossRefPubMedGoogle Scholar
  20. Dumont J, Petri S, Pellegrin F, Terret M-E, Bohnsack MT, Rassinier P, Georget V, Kalab P, Gruss OJ, Verlhac M-H (2007b) A centriole- and RanGTP-independent spindle assembly pathway in meiosis I of vertebrate oocytes. J Cell Biol 176:295–305CrossRefPubMedPubMedCentralGoogle Scholar
  21. Fink J, Carpi N, Betz T, Bétard A, Chebah M, Azioune A, Bornens M, Sykes C, Fetler L, Cuvelier D et al (2011) External forces control mitotic spindle positioning. Nat Cell Biol 13:771–778CrossRefPubMedGoogle Scholar
  22. Fitzharris G (2009) A shift from kinesin 5-dependent metaphase spindle function during preimplantation development in mouse. Development 136:2111–2119CrossRefPubMedPubMedCentralGoogle Scholar
  23. FitzHarris G, Marangos P, Carroll J (2007) Changes in endoplasmic reticulum structure during mouse oocyte maturation are controlled by the cytoskeleton and cytoplasmic dynein. Dev Biol 305:133–144CrossRefPubMedGoogle Scholar
  24. Gilula NB, Epstein ML, Beers WH (1978) Cell-to-cell communication and ovulation. A study of the cumulus-oocyte complex. J Cell Biol 78:58–75CrossRefPubMedGoogle Scholar
  25. Gönczy P (2002) Mechanisms of spindle positioning: focus on flies and worms. Trends Cell Biol 12:332–339CrossRefPubMedGoogle Scholar
  26. Green RA, Paluch E, Oegema K (2012) Cytokinesis in animal cells. Annu Rev Cell Dev Biol 28:29–58CrossRefPubMedGoogle Scholar
  27. Gueth-Hallonet C, Antony C, Aghion J, Santa-Maria A, Lajoie-Mazenc I, Wright M, Maro B (1993) gamma-Tubulin is present in acentriolar MTOCs during early mouse development. J Cell Sci 105:157–166PubMedGoogle Scholar
  28. Halet G, Carroll J (2007) Rac activity is polarized and regulates meiotic spindle stability and anchoring in mammalian oocytes. Dev Cell 12:309–317CrossRefPubMedGoogle Scholar
  29. Hiiragi T, Solter D (2004) First cleavage plane of the mouse egg is not predetermined but defined by the topology of the two apposing pronuclei. Nature 430:360–364CrossRefPubMedGoogle Scholar
  30. Holubcová Z, Howard G, Schuh M (2013) Vesicles modulate an actin network for asymmetric spindle positioning. Nat Cell Biol 15:937–947CrossRefPubMedPubMedCentralGoogle Scholar
  31. Huang X, Ding L, Pan R, Ma P-F, Cheng P-P, Zhang C-H, Shen Y-T, Xu L, Liu Y, He X-Q et al (2013) WHAMM is required for meiotic spindle migration and asymmetric cytokinesis in mouse oocytes. Histochem Cell Biol 139:525–534CrossRefPubMedGoogle Scholar
  32. Kovar DR (2006) Molecular details of formin-mediated actin assembly. Curr Opin Cell Biol 18:11–17CrossRefPubMedGoogle Scholar
  33. Kunda P, Pelling AE, Liu T, Baum B (2008) Moesin controls cortical rigidity, cell rounding, and spindle morphogenesis during mitosis. Curr Biol 18:91–101CrossRefPubMedGoogle Scholar
  34. Kwon M, Bagonis M, Danuser G, Pellman D (2015) Direct microtubule-binding by myosin-10 orients centrosomes toward retraction fibers and subcortical actin clouds. Dev Cell 34:323–337CrossRefPubMedPubMedCentralGoogle Scholar
  35. Lancaster OM, Baum B (2014) Shaping up to divide: coordinating actin and microtubule cytoskeletal remodelling during mitosis. Semin Cell Dev Biol 34:109–115CrossRefPubMedGoogle Scholar
  36. Lancaster OM, Le Berre M, Dimitracopoulos A, Bonazzi D, Zlotek-Zlotkiewicz E, Picone R, Duke T, Piel M, Baum B (2013) Mitotic rounding alters cell geometry to ensure efficient bipolar spindle formation. Dev Cell 25:270–283CrossRefPubMedGoogle Scholar
  37. Larson SM, Lee HJ, Hung P, Matthews LM, Robinson DN, Evans JP (2010) Cortical mechanics and meiosis II completion in mammalian oocytes are mediated by myosin-II and ezrin-radixin-moesin (ERM) proteins. Mol Biol Cell 21:3182–3192CrossRefPubMedPubMedCentralGoogle Scholar
  38. Leader B, Lim H, Carabatsos MJ, Harrington A, Ecsedy J, Pellman D, Maas R, Leder P (2002) Formin-2, polyploidy, hypofertility and positioning of the meiotic spindle in mouse oocytes. Nat Cell Biol 4:921–928CrossRefPubMedGoogle Scholar
  39. Levi M, Ghetler Y, Shulman A, Shalgi R (2013) Morphological and molecular markers are correlated with maturation-competence of human oocytes. Hum Reprod 28:2482–2489CrossRefPubMedGoogle Scholar
  40. Liu J, Wang Q-C, Wang F, Duan X, Dai X-X, Wang T, Liu H-L, Cui X-S, Kim N-H, Sun S-C (2012) Nucleation promoting factors regulate the expression and localization of Arp2/3 complex during meiosis of mouse oocytes. PLoS One 7:e52277CrossRefPubMedPubMedCentralGoogle Scholar
  41. Longo FJ, Chen DY (1985) Development of cortical polarity in mouse eggs: involvement of the meiotic apparatus. Dev Biol 107:382–394CrossRefPubMedGoogle Scholar
  42. Luksza M, Queguigner I, Verlhac M-H, Brunet S (2013) Rebuilding MTOCs upon centriole loss during mouse oogenesis. Dev Biol 382:48–56CrossRefPubMedGoogle Scholar
  43. Manandhar G, Feng D, Yi Y-J, Lai L, Letko J, Laurincik J, Sutovsky M, Salisbury JL, Prather RS, Schatten H et al (2006) Centrosomal protein centrin is not detectable during early pre-implantation development but reappears during late blastocyst stage in porcine embryos. Reproduction 132:423–434CrossRefPubMedGoogle Scholar
  44. Maro B, Verlhac M-H (2002) Polar body formation: new rules for asymmetric divisions. Nat Cell Biol 4:E281–E283CrossRefPubMedGoogle Scholar
  45. Maro B, Johnson MH, Pickering SJ, Flach G (1984) Changes in actin distribution during fertilization of the mouse egg. J Embryol Exp Morphol 81:211–237PubMedGoogle Scholar
  46. Mori M, Monnier N, Daigle N, Bathe M, Ellenberg J, Lénárt P (2011) Intracellular transport by an anchored homogeneously contracting F-actin meshwork. Curr Biol 21:606–611CrossRefPubMedGoogle Scholar
  47. Motosugi N, Bauer T, Polanski Z, Solter D, Hiiragi T (2005) Polarity of the mouse embryo is established at blastocyst and is not prepatterned. Genes Dev 19:1081–1092CrossRefPubMedPubMedCentralGoogle Scholar
  48. Norris RP, Freudzon M, Mehlmann LM, Cowan AE, Simon AM, Paul DL, Lampe PD, Jaffe LA (2008) Luteinizing hormone causes MAP kinase-dependent phosphorylation and closure of connexin 43 gap junctions in mouse ovarian follicles: one of two paths to meiotic resumption. Development 135:3229–3238CrossRefPubMedPubMedCentralGoogle Scholar
  49. Otsuki J, Nagai Y, Lopata A, Chiba K, Yasmin L, Sankai T (2012) Symmetrical division of mouse oocytes during meiotic maturation can lead to the development of twin embryos that amalgamate to form a chimeric hermaphrodite. Hum Reprod 27:380–387CrossRefPubMedGoogle Scholar
  50. Pfender S, Kuznetsov V, Pleiser S, Kerkhoff E, Schuh M (2011) Spire-type actin nucleators cooperate with Formin-2 to drive asymmetric oocyte division. Curr Biol 21:955–960CrossRefPubMedPubMedCentralGoogle Scholar
  51. Propst F, Rosenberg MP, Iyer A, Kaul K, Vande Woude GF (1987) c-mos proto-oncogene RNA transcripts in mouse tissues: structural features, developmental regulation, and localization in specific cell types. Mol Cell Biol 7:1629–1637CrossRefPubMedPubMedCentralGoogle Scholar
  52. Quinlan ME (2013) Direct interaction between two actin nucleators is required in Drosophila oogenesis. Development 140:4417–4425CrossRefPubMedPubMedCentralGoogle Scholar
  53. Quinlan ME, Heuser JE, Kerkhoff E, Mullins RD (2005) Drosophila spire is an actin nucleation factor. Nature 433:382–388CrossRefPubMedGoogle Scholar
  54. Quinlan ME, Hilgert S, Bedrossian A, Mullins RD, Kerkhoff E (2007) Regulatory interactions between two actin nucleators, Spire and Cappuccino. J Cell Biol 179:117–128CrossRefPubMedPubMedCentralGoogle Scholar
  55. Rappaport R, Rappaport BN (1974) Establishment of cleavage furrows by the mitotic spindle. J Exp Zool 189:189–196CrossRefPubMedGoogle Scholar
  56. Renault L, Bugyi B, Carlier M-F (2008) Spire and cordon-bleu: multifunctional regulators of actin dynamics. Trends Cell Biol 18:494–504CrossRefPubMedGoogle Scholar
  57. Romero S, Le Clainche C, Didry D, Egile C, Pantaloni D, Carlier M-F (2004) Formin is a processive motor that requires profilin to accelerate actin assembly and associated ATP hydrolysis. Cell 119:419–429CrossRefPubMedGoogle Scholar
  58. Romero S, Didry D, Larquet E, Boisset N, Pantaloni D, Carlier M-F (2007) How ATP hydrolysis controls filament assembly from profilin-actin: implication for formin processivity. J Biol Chem 282:8435–8445CrossRefPubMedGoogle Scholar
  59. Roth S, Lynch JA (2009) Symmetry breaking during drosophila oogenesis. Cold Spring Harb Perspect Biol 1:a001891CrossRefPubMedPubMedCentralGoogle Scholar
  60. Roubinet C, Cabernard C (2014) Control of asymmetric cell division. Curr Opin Cell Biol 31:84–91CrossRefPubMedGoogle Scholar
  61. Schatten G, Simerly C, Schatten H (1985) Microtubule configurations during fertilization, mitosis, and early development in the mouse and the requirement for egg microtubule-mediated motility during mammalian fertilization. Proc Natl Acad Sci U S A 82:4152–4156CrossRefPubMedPubMedCentralGoogle Scholar
  62. Schmerler S, Wessel G (2011) Polar Bodies—more a lack of understanding than a lack of respect. Mol Reprod Dev 78:3–8CrossRefPubMedGoogle Scholar
  63. Schuh M (2011) An actin-dependent mechanism for long-range vesicle transport. Nat Cell Biol 13:1431–1436CrossRefPubMedPubMedCentralGoogle Scholar
  64. Schuh M, Ellenberg J (2008) A new model for asymmetric spindle positioning in mouse oocytes. Curr Biol 18:1986–1992CrossRefPubMedGoogle Scholar
  65. Sela-Abramovich S, Edry I, Galiani D, Nevo N, Dekel N (2006) Disruption of gap junctional communication within the ovarian follicle induces oocyte maturation. Endocrinology 147:2280–2286CrossRefPubMedGoogle Scholar
  66. Simerly C, Nowak G, de Lanerolle P, Schatten G (1998) Differential expression and functions of cortical myosin IIA and IIB isotypes during meiotic maturation, fertilization, and mitosis in mouse oocytes and embryos. Mol Biol Cell 9:2509–2525CrossRefPubMedPubMedCentralGoogle Scholar
  67. Stewart MP, Helenius J, Toyoda Y, Ramanathan SP, Muller DJ, Hyman AA (2011) Hydrostatic pressure and the actomyosin cortex drive mitotic cell rounding. Nature 469:226–230CrossRefPubMedGoogle Scholar
  68. Sun S-C, Wang Z-B, Xu Y-N, Lee S-E, Cui X-S, Kim N-H (2011a) Arp2/3 complex regulates asymmetric division and cytokinesis in mouse oocytes. PLoS One 6:e18392CrossRefPubMedPubMedCentralGoogle Scholar
  69. Sun S-C, Xu Y-N, Li Y-H, Lee S-E, Jin Y-X, Cui X-S, Kim N-H (2011b) WAVE2 regulates meiotic spindle stability, peripheral positioning and polar body emission in mouse oocytes. Cell Cycle 10:1853–1860CrossRefPubMedGoogle Scholar
  70. Szollosi D, Calarco P, Donahue RP (1972) Absence of centrioles in the first and second meiotic spindles of mouse oocytes. J Cell Sci 11:521–541PubMedGoogle Scholar
  71. Théry M, Jiménez-Dalmaroni A, Racine V, Bornens M, Jülicher F (2007) Experimental and theoretical study of mitotic spindle orientation. Nature 447:493–496CrossRefPubMedGoogle Scholar
  72. Verlhac MH, de Pennart H, Maro B, Cobb MH, Clarke HJ (1993) MAP kinase becomes stably activated at metaphase and is associated with microtubule-organizing centers during meiotic maturation of mouse oocytes. Dev Biol 158:330–340CrossRefPubMedGoogle Scholar
  73. Verlhac MH, Kubiak JZ, Clarke HJ, Maro B (1994) Microtubule and chromatin behavior follow MAP kinase activity but not MPF activity during meiosis in mouse oocytes. Development 120:1017–1025PubMedGoogle Scholar
  74. Verlhac MH, Kubiak JZ, Weber M, Géraud G, Colledge WH, Evans MJ, Maro B (1996) Mos is required for MAP kinase activation and is involved in microtubule organization during meiotic maturation in the mouse. Development 122:815–822PubMedGoogle Scholar
  75. Verlhac M-H, Lefebvre C, Guillaud P, Rassinier P, Maro B (2000) Asymmetric division in mouse oocytes: with or without Mos. Curr Biol 10:1303–1306CrossRefPubMedGoogle Scholar
  76. Vinot S, Le T, Maro B, Louvet-Vallée S (2004) Two PAR6 proteins become asymmetrically localized during establishment of polarity in mouse oocytes. Curr Biol 14:520–525CrossRefPubMedGoogle Scholar
  77. Weber M, Kubiak JZ, Arlinghaus RB, Pines J, Maro B (1991) c-mos proto-oncogene product is partly degraded after release from meiotic arrest and persists during interphase in mouse zygotes. Dev Biol 148:393–397CrossRefPubMedGoogle Scholar
  78. Wolinsky H (2007) A mythical beast. Increased attention highlights the hidden wonders of chimeras. EMBO Rep 8:212–214CrossRefPubMedPubMedCentralGoogle Scholar
  79. Wühr M, Tan ES, Parker SK, Detrich HW, Mitchison TJ (2010) A model for cleavage plane determination in early amphibian and fish embryos. Curr Biol 20:2040–2045CrossRefPubMedPubMedCentralGoogle Scholar
  80. Yamagata K, FitzHarris G (2013) 4D imaging reveals a shift in chromosome segregation dynamics during mouse pre-implantation development. Cell Cycle 12:157–165CrossRefPubMedPubMedCentralGoogle Scholar
  81. Yanez LZ, Han J, Behr BB, Pera RAR, Camarillo DB (2016) Human oocyte developmental potential is predicted by mechanical properties within hours after fertilization. Nat Commun 7:10809CrossRefPubMedPubMedCentralGoogle Scholar
  82. Yi K, Unruh JR, Deng M, Slaughter BD, Rubinstein B, Li R (2011) Dynamic maintenance of asymmetric meiotic spindle position through Arp2/3-complex-driven cytoplasmic streaming in mouse oocytes. Nat Cell Biol 13:1252–1258CrossRefPubMedPubMedCentralGoogle Scholar
  83. Yi K, Rubinstein B, Unruh JR, Guo F, Slaughter BD, Li R (2013) Sequential actin-based pushing forces drive meiosis I chromosome migration and symmetry breaking in oocytes. J Cell Biol 200:567–576CrossRefPubMedPubMedCentralGoogle Scholar
  84. Yoo H, Roth-Johnson EA, Bor B, Quinlan ME (2015) Drosophila Cappuccino alleles provide insight into formin mechanism and role in oogenesis. Mol Biol Cell 26:1875–1886CrossRefPubMedPubMedCentralGoogle Scholar
  85. Yu X-J, Yi Z, Gao Z, Qin D, Zhai Y, Chen X, Ou-Yang Y, Wang Z-B, Zheng P, Zhu M-S et al (2014) The subcortical maternal complex controls symmetric division of mouse zygotes by regulating F-actin dynamics. Nat Commun 5:4887CrossRefPubMedGoogle Scholar
  86. Zhao T, Graham OS, Raposo A, St Johnston D (2012) Growing microtubules push the oocyte nucleus to polarize the Drosophila dorsal-ventral axis. Science 336:999–1003CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer International Publishing AG 2017

Authors and Affiliations

  • Agathe Chaigne
    • 1
    • 2
  • Marie-Emilie Terret
    • 3
  • Marie-Hélène Verlhac
    • 3
    Email author
  1. 1.MRC Laboratory for Molecular Cell BiologyUCLLondonUK
  2. 2.Institute for the Physics of Living SystemsUCLLondonUK
  3. 3.CIRB, Collège de France, CNRS-UMR7241, INSERM-U1050ParisFrance

Personalised recommendations