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Cyclin B in Mouse Oocytes and Embryos: Importance for Human Reproduction and Aneuploidy

  • Zbigniew Polański
  • Hayden Homer
  • Jacek Z. KubiakEmail author
Chapter
Part of the Results and Problems in Cell Differentiation book series (RESULTS, volume 55)

Abstract

Oocyte maturation and early embryo development require precise coordination between cell cycle progression and the developmental programme. Cyclin B plays a major role in this process: its accumulation and degradation is critical for driving the cell cycle through activation and inactivation of the major cell cycle kinase, CDK1. CDK1 activation is required for M-phase entry whereas its inactivation leads to exit from M-phase. The tempo of oocyte meiotic and embryonic mitotic divisions is set by the rate of cyclin B accumulation and the timing of its destruction. By controlling when cyclin B destruction is triggered and by co-ordinating this with the completion of chromosome alignment, the spindle assembly checkpoint (SAC) is a critical quality control system important for averting aneuploidy and for building in the flexibility required to better integrate cell cycle progression with development. In this review we focus on cyclin B metabolism in mouse oocytes and embryos and illustrate how the cell cycle-powered clock (in fact cyclin B-powered clock) controls oocyte maturation and early embryo development, thereby providing important insight into human reproduction and potential causes of Down syndrome.

Keywords

Mouse Oocyte Spindle Assembly Checkpoint CDK1 Activity Meiotic Maturation Mammalian Oocyte 
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

While writing this article, JZK was supported by a grant from ARC. HH is supported by a Wellcome Trust Fellowship. ZP was supported by the Polish National Science Centre (grant N° DEC-2011/B/NZ3/00190).

References

  1. Baker DJ, Jeganathan KB, Cameron JD, Thompson M, Juneja S, Kopecka A, Kumar R, Jenkins RB, de Groen PC, Roche P, van Deursen JM (2004) BubR1 insufficiency causes early onset of aging-associated phenotypes and infertility in mice. Nat Genet 36:744–749PubMedGoogle Scholar
  2. Bergère M, Lombroso R, Gombault M, Wainer R, Selva J (2001) An idiopathic infertility with oocytes metaphase I maturation block: case report. Hum Reprod 16:2136–2138PubMedGoogle Scholar
  3. Brandeis M, Rosewell I, Carrington M, Crompton T, Jacobs MA, Kirk J, Gannon J, Hunt T (1998) Cyclin B2-null mice develop normally and are fertile whereas cyclin B1-null mice die in utero. Proc Natl Acad Sci USA 95:4344–4349PubMedGoogle Scholar
  4. Brunet S, Santa MA, Guillard P, Dujardin D, Kubiak JZ, Maro B (1999) Kinetochore fibers are not involved in the formation of the first meiotic spindle in mouse oocytes, but control the exit from the first meiotic M-phase. J Cell Biol 146(1):1–11PubMedGoogle Scholar
  5. Brunet S, Pahlavan G, Taylor S, Maro B (2003) Functionality of the spindle checkpoint during the first meiotic division of mammalian oocytes. Reproduction 126:443–450PubMedGoogle Scholar
  6. Cheeseman IM, Desai A (2008) Molecular architecture of the kinetochore-microtubule interface. Nat Rev Mol Cell Biol 9:33–46PubMedGoogle Scholar
  7. Chen J, Melton C, Suh N, Oh J, Horner K, Xie F, Sette C, Blelloch R, Conti M (2011) Genome-wide analysis of translation reveals a critical role for deleted in azoospermia-like (Dazl) at the oocyte-to-zygote transition. Genes Dev 25:755–766PubMedGoogle Scholar
  8. Chesnel F, Eppig JJ (1995) Synthesis and accumulation of p34cdc2 and cyclin B in mouse oocytes during acquisition of competence to resume meiosis. Mol Reprod Dev 40:503–508PubMedGoogle Scholar
  9. Chesnel F, Vignaux F, Richard-Parpaillon L, Huguet A, Kubiak JZ (2005a) Differences in regulation of the first two M-phases in Xenopus laevis embryo cell-free extracts. Dev Biol 285:358–375PubMedGoogle Scholar
  10. Chesnel F, Gautier I, Richard-Parpaillon L, Kubiak JZ (2005b) Each mitosis can be different: how the cell cycle machinery modulates early embryonic M-phases. In: Tokumoto T (ed) New impact of protein modifications in the regulation of reproductive system. Research Signpost, Kerala, IndiaGoogle Scholar
  11. Chiang T, Duncan FE, Schindler K, Schultz RM, Lampson MA (2010) Evidence that weakened centromere cohesion is a leading cause of age-related aneuploidy in oocytes. Curr Biol 20:1522–1528PubMedGoogle Scholar
  12. Choi T, Aoki F, Mori M, Yamashita M, Nagahama Y, Kohmoto K (1991) Activation of p34cdc2 protein kinase activity in meiotic and mitotic cell cycles in mouse oocytes and embryos. Development 113:789–795PubMedGoogle Scholar
  13. Ciemerych MA, Kubiak JZ (1998) Cytostatic activity develops during meiosis I in oocytes of LT/Sv mice. Dev Biol 200:198–211PubMedGoogle Scholar
  14. Ciemerych MA, Tarkowski AK, Kubiak JZ (1998) Autonomous activation of histone H1 kinase, cortical activity and microtubule organization in one- and two-cell cycle mouse embryo. Biol Cell 90:557–564PubMedGoogle Scholar
  15. Ciemerych MA, Maro B, Kubiak JZ (1999) Control of duration of first two mitoses in a mouse embryo. Zygote 7:293–300PubMedGoogle Scholar
  16. Clarke HJ (2012) Post-transcriptional control of gene expression during mouse oogenesis. In: Kubiak JZ (ed) Mouse development, Results Probl Cell Differ. 55., 1–21. Springer, HeidelbergGoogle Scholar
  17. Courtois A, Hiiragi T (2012) Gradual meiosis-to-mitosis transition in the early mouse embryo. In: Kubiak JZ (ed) Mouse development, Results Probl Cell Differ. 55., 107–114. Springer, HeidelbergGoogle Scholar
  18. Devault A, Fesquet D, Cavadore JC, Garrigues AM, Labbé JC, Lorca T, Picard A, Philippe M, Dorée M (1992) Cyclin A potentiates maturation-promoting factor activation in the early Xenopus embryo via inhibition of the tyrosine kinase that phosphorylates cdc2. J Cell Biol 118:1109–1120PubMedGoogle Scholar
  19. Dumont J, Petri S, Pellegrin F, Terret ME, Bohnsack MT, Rassinier P, Georget V, Kalab P, Gruss OJ, Verlhac MH (2007) A centriole- and RanGTP-independent spindle assembly pathway in meiosis I of vertebrate oocytes. J Cell Biol 176:295–305PubMedGoogle Scholar
  20. Duncan FE, Chiang T, Schultz RM, Lampson MA (2009) Evidence that a defective spindle assembly checkpoint is not the primary cause of maternal age-associated aneuploidy in mouse eggs. Biol Reprod 81:768–776PubMedGoogle Scholar
  21. Eppig JJ (1978) Developmental potential of LT/Sv parthenotes derived from oocytes matured in vivo and in vitro. Dev Biol 65:244–249PubMedGoogle Scholar
  22. Fragouli E, Alfarawati S, Goodall NN, Sánchez-García JF, Colls P, Wells D (2011) The cytogenetics of polar bodies: insights into female meiosis and the diagnosis of aneuploidy. Mol Hum Reprod 118(3):381Google Scholar
  23. Gerhart J, Wu M, Kirschner M (1984) Cell cycle dynamics of an M-phase-specific cytoplasmic factor in Xenopus laevis oocytes and eggs. J Cell Biol 98:1247–1255PubMedGoogle Scholar
  24. Greenwood J, Costanzo V, Robertson K, Hensey C, Gautier J (2001) Responses to DNA damage in Xenopus: cell death or cell cycle arrest. Novartis Found Symp 237:221–330; discussion 230–234PubMedGoogle Scholar
  25. Hached K, Xie SZ, Buffin E, Cladière D, Rachez C, Sacras M, Sorger PK, Wassmann K (2011) Mps1 at kinetochores is essential for female mouse meiosis I. Development 138:2261–2271PubMedGoogle Scholar
  26. Hamatani T, Carter MG, Sharov AA, Ko MS (2004) Dynamics of global gene expression changes during mouse preimplantation development. Dev Cell 6:117–131PubMedGoogle Scholar
  27. Hampl A, Eppig JJ (1995) Translational regulation of the gradual increase in histone H1 kinase activity in maturing mouse oocytes. Mol Reprod Dev 40:9–15PubMedGoogle Scholar
  28. Han SJ, Chen R, Paronetto MP, Conti M (2005) Wee1B is an oocyte-specific kinase involved in the control of meiotic arrest in the mouse. Curr Biol 15:1670–1676PubMedGoogle Scholar
  29. Harrison K, Sherrin D, Keeping J (2000) Repeated oocyte maturation block. J Assist Reprod Genet 17:231–233PubMedGoogle Scholar
  30. Hartwell LH, Weinert TA (1989) Checkpoints: controls that ensure the order of cell cycle events. Science 246:629–634PubMedGoogle Scholar
  31. Hassold T, Hunt P (2001) To err (meiotically) is human: the genesis of human aneuploidy. Nat Rev Genet 2:280–291PubMedGoogle Scholar
  32. Hauf S, Watanabe Y (2004) Kinetochore orientation in mitosis and meiosis. Cell 119:317–327PubMedGoogle Scholar
  33. Herbert M, Levasseur M, Homer H, Yallop K, Murdoch A, McDougall A (2003) Homologue disjunction in mouse oocytes requires proteolysis of securin and cyclin B1. Nat Cell Biol 5:1023–1025PubMedGoogle Scholar
  34. Hodgman R, Tay J, Mendez R, Richter JD (2001) CPEB phosphorylation and cytoplasmic polyadenylation are catalyzed by the kinase IAK1/Eg2 in maturing mouse oocytes. Development 128:2815–2822PubMedGoogle Scholar
  35. Hoffmann S, Tsurumi C, Kubiak JZ, Polanski Z (2006) Germinal vesicle material drives meiotic cell cycle of mouse oocyte through the 3′UTR-dependent control of cyclin B1 synthesis. Dev Biol 292:46–54PubMedGoogle Scholar
  36. Hoffmann S, Maro B, Kubiak JZ, Polanski Z (2011) A single bivalent efficiently inhibits cyclin B1 degradation and polar body extrusion in mouse oocytes indicating robust SAC during female meiosis I. PLoS One 6:e27143PubMedGoogle Scholar
  37. Holt JE, Weaver J, Jones KT (2010) Spatial regulation of APCCdh1-induced cyclin B1 degradation maintains G2 arrest in mouse oocytes. Development 137:1297–1304PubMedGoogle Scholar
  38. Homer H (2011) New insights into the genetic regulation of homologue disjunction in mammalian oocytes. Cytogenet Genome Res 133:209–222PubMedGoogle Scholar
  39. Homer HA, McDougall A, Levasseur M, Murdoch AP, Herbert M (2005a) Mad2 is required for inhibiting securin and cyclin B degradation following spindle depolymerisation in meiosis I mouse oocytes. Reproduction 130:829–843PubMedGoogle Scholar
  40. Homer HA, McDougall A, Levasseur M, Yallop K, Murdoch AP, Herbert M (2005b) Mad2 prevents aneuploidy and premature proteolysis of cyclin B and securin during meiosis I in mouse oocytes. Genes Dev 19:202–207PubMedGoogle Scholar
  41. Homer H, Gui L, Carroll J (2009) A spindle assembly checkpoint protein functions in prophase I arrest and prometaphase progression. Science 326:991–994PubMedGoogle Scholar
  42. Hsieh M, Lee D, Panigone S, Horner K, Chen R, Theologis A, Lee DC, Threadgill DW, Conti M (2007) Luteinizing hormone-dependent activation of the epidermal growth factor network is essential for ovulation. Mol Cell Biol 27:1914–1924PubMedGoogle Scholar
  43. Huo LJ, Fan HY, Zhong ZS, Chen DY, Schatten H, Sun QY (2004) Ubiquitin-proteasome pathway modulates mouse oocyte meiotic maturation and fertilization via regulation of MAPK cascade and cyclin B1 degradation. Mech Dev 121:1275–1287PubMedGoogle Scholar
  44. Huo LJ, Yu LZ, Liang CG, Fan HY, Chen DY, Sun QY (2005) Cell-cycle-dependent subcellular localization of cyclin B1, phosphorylated cyclin B1 and p34cdc2 during oocyte meiotic maturation and fertilization in mouse. Zygote 13:45–53PubMedGoogle Scholar
  45. Hupalowska A, Kalaszczynska I, Hoffmann S, Tsurumi C, Kubiak JZ, Polanski Z, Ciemerych MA (2008) Metaphase I arrest in LT/Sv mouse oocytes involves the spindle assembly checkpoint. Biol Reprod 79(6):1102–1110PubMedGoogle Scholar
  46. Iwabuchi M, Ohsumi K, Yamamoto TM, Sawada W, Kishimoto T (2000) Residual Cdc2 activity remaining at meiosis I exit is essential for meiotic M-M transition in Xenopus oocyte extracts. EMBO J 19:4513–4523PubMedGoogle Scholar
  47. Kalab P, Kubiak JZ, Verlhac MH, Colledge WH, Maro B (1996) Activation of p90rsk during meiotic maturation and first mitosis in mouse oocytes and eggs: MAP kinase-independent and -dependent activation. Development 122:1957–1964PubMedGoogle Scholar
  48. Kallio M, Eriksson JE, Gorbsky GJ (2000) Differences in spindle association of the mitotic checkpoint protein Mad2 in mammalian spermatogenesis and oogenesis. Dev Biol 225:112–123PubMedGoogle Scholar
  49. Kanatsu-Shinohara M, Schultz RM, Kopf GS (2000) Acquisition of meiotic competence in mouse oocytes: absolute amounts of p34(cdc2), cyclin B1, cdc25C, and wee1 in meiotically incompetent and competent oocytes. Biol Reprod 63:1610–1616PubMedGoogle Scholar
  50. Kitajima TS, Ohsugi M, Ellenberg J (2011) Complete kinetochore tracking reveals error-prone homologous chromosome biorientation in mammalian oocytes. Cell 146:568–581PubMedGoogle Scholar
  51. Kraft C, Herzog F, Gieffers C, Mechtler K, Hagting A, Pines J, Peters JM (2003) Mitotic regulation of the human anaphase-promoting complex by phosphorylation. EMBO J 22:6598–6609PubMedGoogle Scholar
  52. Kubiak JZ, Ciemerych MA (2001) Cell cycle regulation in early mouse embryos. Novartis Found Symp 237:79–89; discussion 89–99PubMedGoogle Scholar
  53. Kubiak JZ, Weber M, Géraud G, Maro B (1992) Cell cycle modification during the transitions between meiotic M-phases in mouse oocytes. J Cell Sci 102:457–467PubMedGoogle Scholar
  54. Kubiak JZ, Weber M, de Pennart H, Winston NJ, Maro B (1993) The metaphase II arrest in mouse oocytes is controlled through microtubule-dependent destruction of cyclin B in the presence of CSF. EMBO J 12:3773–3778PubMedGoogle Scholar
  55. Kubiak JZ, Ciemerych MA, Hupalowska A, Sikora-Polaczek M, Polanski Z (2008) On the transition from the meiotic to mitotic cell cycle during early mouse development. Int J Dev Biol 52:201–217PubMedGoogle Scholar
  56. Ledan E, Polanski Z, Terret ME, Maro B (2001) Meiotic maturation of the mouse oocyte requires an equilibrium between cyclin B synthesis and degradation. Dev Biol 232:400–413PubMedGoogle Scholar
  57. Lefebvre C, Terret ME, Djiane A, Rassinier P, Maro B, Verlhac MH (2002) Meiotic spindle stability depends on MAPK-interacting and spindle-stabilizing protein (MISS), a new MAPK substrate. J Cell Biol 157:603–613PubMedGoogle Scholar
  58. LeMaire-Adkins R, Radke K, Hunt PA (1997) Lack of checkpoint control at the metaphase/anaphase transition: a mechanism of meiotic nondisjunction in mammalian females. J Cell Biol 139:1611–1619PubMedGoogle Scholar
  59. Lister LM, Kouznetsova A, Hyslop LA, Kalleas D, Pace SL, Barel JC, Nathan A, Floros V, Adelfalk C, Watanabe Y, Jessberger R, Kirkwood TB, Höög C, Herbert M (2010) Age-related meiotic segregation errors in mammalian oocytes are preceded by depletion of cohesin and Sgo2. Curr Biol 20:1511–1521PubMedGoogle Scholar
  60. Liu L, Keefe DL (2008) Defective cohesin is associated with age-dependent misaligned chromosomes in oocytes. Reprod Biomed Online 16:103–112PubMedGoogle Scholar
  61. Liu D, Matzuk MM, Sung WK, Guo Q, Wang P, Wolgemuth DJ (1998) Cyclin A1 is required for meiosis in the male mouse. Nat Genet 20:377–380PubMedGoogle Scholar
  62. Maciejewska Z, Polanski Z, Kisiel K, Kubiak JZ, Ciemerych MA (2009) Spindle assembly checkpoint-related failure perturbs early embryonic divisions and reduces reproductive performance of LT/Sv mice. Reproduction 137:931–942PubMedGoogle Scholar
  63. Madgwick S, Jones KT (2007) How eggs arrest at metaphase II: MPF stabilisation plus APC/C inhibition equals Cytostatic Factor. Cell Div 2:4PubMedGoogle Scholar
  64. Madgwick S, Levasseur M, Jones KT (2005) Calmodulin-dependent protein kinase II, and not protein kinase C, is sufficient for triggering cell-cycle resumption in mammalian eggs. J Cell Sci 118:3849–3859PubMedGoogle Scholar
  65. Madgwick S, Hansen DV, Levasseur M, Jackson PK, Jones KT (2006) Mouse Emi2 is required to enter meiosis II by reestablishing cyclin B1 during interkinesis. J Cell Biol 174:791–801PubMedGoogle Scholar
  66. Marangos P, Carroll J (2004) The dynamics of cyclin B1 distribution during meiosis I in mouse oocytes. Reproduction 128:153–62PubMedGoogle Scholar
  67. Masui Y, Clarke HJ (1979) Oocyte maturation. Int Rev Cytol 57:185–282PubMedGoogle Scholar
  68. Masui Y, Markert CL (1971) Cytoplasmic control of nuclear behavior during meiotic maturation of frog oocytes. J Exp Zool 177:129–145PubMedGoogle Scholar
  69. McGuinness BE, Anger M, Kouznetsova A, Gil-Bernabé AM, Helmhart W, Kudo NR, Wuensche A, Taylor S, Hoog C, Novak B, Nasmyth K (2009) Regulation of APC/C activity in oocytes by a Bub1-dependent spindle assembly checkpoint. Curr Biol 19:369–380PubMedGoogle Scholar
  70. Mehlmann LM, Jones TL, Jaffe LA (2002) Meiotic arrest in the mouse follicle maintained by a Gs protein in the oocyte. Science 297:1343–1345PubMedGoogle Scholar
  71. Mehlmann LM, Saeki Y, Tanaka S, Brennan TJ, Evsikov AV, Pendola FL, Knowles BB, Eppig JJ, Jaffe LA (2004) The Gs-linked receptor GPR3 maintains meiotic arrest in mammalian oocytes. Science 306:1947–1950PubMedGoogle Scholar
  72. Minshull J, Sun H, Tonks NK, Murray AW (1994) A MAP kinase-dependent spindle assembly checkpoint in Xenopus egg extracts. Cell 79:475–486PubMedGoogle Scholar
  73. Morris SA, Zernicka-Goetz M (2012) Formation of distinct cell types in the mouse blastocyst. In: Kubiak JZ (ed) Mouse development, Results Probl Cell Differ. 55., 203–217. Springer, HeidelbergGoogle Scholar
  74. Murray AW (2004) Recycling the cell cycle: cyclins revisited. Cell 116:221–234PubMedGoogle Scholar
  75. Musacchio A, Salmon ED (2007) The spindle-assembly checkpoint in space and time. Nat Rev Mol Cell Biol 8:379–393PubMedGoogle Scholar
  76. Nagaoka SI, Hodges CA, Albertini DF, Hunt PA (2011) Oocyte-specific differences in cell-cycle control create an innate susceptibility to meiotic errors. Curr Biol 21(8):651–657PubMedGoogle Scholar
  77. Nasmyth K (2002) Segregating sister genomes: the molecular biology of chromosome separation. Science 297:559–565PubMedGoogle Scholar
  78. Nguyen TB, Manova K, Capodieci P, Lindon C, Bottega S, Wang XY, Refik-Rogers J, Pines J, Wolgemuth DJ, Koff A (2002) Characterization and expression of mammalian cyclin b3, a prepachytene meiotic cyclin. J Biol Chem 277:41960–41969PubMedGoogle Scholar
  79. Niault T, Hached K, Sotillo R, Sorger PK, Maro B, Benezra R, Wassmann K (2007) Changing Mad2 levels affects chromosome segregation and spindle assembly checkpoint control in female mouse meiosis I. PLoS One 2(11):e1165PubMedGoogle Scholar
  80. Nixon VL, Levasseur M, McDougall A, Jones KT (2002) Ca(2+) oscillations promote APC/C-dependent cyclin B1 degradation during metaphase arrest and completion of meiosis in fertilizing mouse eggs. Curr Biol 12:746–750PubMedGoogle Scholar
  81. Norris RP, Ratzan WJ, Freudzon M, Mehlmann LM, Krall J, Movsesian MA, Wang H, Ke H, Nikolaev VO, Jaffe LA (2009) Cyclic GMP from the surrounding somatic cells regulates cyclic AMP and meiosis in the mouse oocyte. Development 136:1869–1878PubMedGoogle Scholar
  82. O’Neill GT, Kaufman MH (1987) Ovulation and fertilization of primary and secondary oocytes in LT/Sv strain mice. Gamete Res 18:27–36PubMedGoogle Scholar
  83. Pan H, Ma P, Zhu W, Schultz RM (2008) Age-associated increase in aneuploidy and changes in gene expression in mouse eggs. Dev Biol 316:397–407PubMedGoogle Scholar
  84. Park JY, Su YQ, Ariga M, Law E, Jin SL, Conti M (2004) EGF-like growth factors as mediators of LH action in the ovulatory follicle. Science 303:682–684PubMedGoogle Scholar
  85. Peng XR, Hsueh AJ, LaPolt PS, Bjersing L, Ny T (1991) Localization of luteinizing hormone receptor messenger ribonucleic acid expression in ovarian cell types during follicle development and ovulation. Endocrinology 129:3200–3207PubMedGoogle Scholar
  86. Pesin JA, Orr-Weaver TL (2008) Regulation of APC/C activators in mitosis and meiosis. Annu Rev Cell Dev Biol 24:475–499PubMedGoogle Scholar
  87. Peters JM (2006) The anaphase promoting complex/cyclosome: a machine designed to destroy. Nat Rev Mol Cell Biol 7:644–656PubMedGoogle Scholar
  88. Petronczki M, Siomos MF, Nasmyth K (2003) Un ménage à quatre: the molecular biology of chromosome segregation in meiosis. Cell 112:423–440PubMedGoogle Scholar
  89. Pirino G, Wescott MP, Donovan PJ (2009) Protein kinase A regulates resumption of meiosis by phosphorylation of Cdc25B in mammalian oocytes. Cell Cycle 8:665–670PubMedGoogle Scholar
  90. Polański Z (1986) In-vivo and in-vitro maturation rate of oocytes from two strains of mice. J Reprod Fertil 78:103–109PubMedGoogle Scholar
  91. Polanski Z (1997) Strain difference in the timing of meiosis resumption in mouse oocytes: involvement of a cytoplasmic factor(s) acting presumably upstream of the dephosphorylation of p34cdc2 kinase. Zygote 5:105–109PubMedGoogle Scholar
  92. Polanski Z, Ledan E, Brunet S, Louvet S, Verlhac MH, Kubiak JZ, Maro B (1998) Cyclin synthesis controls the progression of meiotic maturation in mouse oocytes. Development 125:4989–4997PubMedGoogle Scholar
  93. Refik-Rogers J, Manova K, Koff A (2006) Misexpression of cyclin B3 leads to aberrant spermatogenesis. Cell Cycle 5:1966–1973PubMedGoogle Scholar
  94. Reis A, Chang HY, Levasseur M, Jones KT (2006) APCcdh1 activity in mouse oocytes prevents entry into the first meiotic division. Nat Cell Biol 8:539–540PubMedGoogle Scholar
  95. Reis A, Madgwick S, Chang HY, Nabti I, Levasseur M, Jones KT (2007) Prometaphase APCcdh1 activity prevents non-disjunction in mammalian oocytes. Nat Cell Biol 9:1192–1198PubMedGoogle Scholar
  96. Revenkova E, Herrmann K, Adelfalk C, Jessberger R (2010) Oocyte cohesin expression restricted to predictyate stages provides full fertility and prevents aneuploidy. Curr Biol 20:1529–1533PubMedGoogle Scholar
  97. Rieder CL, Cole RW, Khodjakov A, Sluder G (1995) The checkpoint delaying anaphase in response to chromosome monoorientation is mediated by an inhibitory signal produced by unattached kinetochores. J Cell Biol 130:941–948PubMedGoogle Scholar
  98. Schindler K, Schultz RM (2009) CDC14B acts through FZR1 (CDH1) to prevent meiotic maturation of mouse oocytes. Biol Reprod 80:795–803PubMedGoogle Scholar
  99. Schmiady H, Neitzel H (2002) Arrest of human oocytes during meiosis I in two sisters of consanguineous parents: first evidence for an autosomal recessive trait in human infertility: Case report. Hum Reprod 17:2556–2559PubMedGoogle Scholar
  100. Shonn MA, McCarroll R, Murray AW (2002) Spo13 protects meiotic cohesin at centromeres in meiosis I. Genes Dev 16:1659–1671PubMedGoogle Scholar
  101. Sikora-Polaczek M, Hupalowska A, Polanski Z, Kubiak JZ, Ciemerych MA (2006) The first mitosis of the mouse embryo is prolonged by transitional metaphase arrest. Biol Reprod 74:734–743PubMedGoogle Scholar
  102. Solc P, Schultz RM, Motlik J (2010) Prophase I arrest and progression to metaphase I in mouse oocytes: comparison of resumption of meiosis and recovery from G2-arrest in somatic cells. Mol Hum Reprod 16:654–664PubMedGoogle Scholar
  103. Steuerwald N, Cohen J, Herrera RJ, Sandalinas M, Brenner CA (2001) Association between spindle assembly checkpoint expression and maternal age in human oocytes. Mol Hum Reprod 7:49–55PubMedGoogle Scholar
  104. Steuerwald NM, Bermúdez MG, Wells D, Munné S, Cohen J (2007) Maternal age-related differential global expression profiles observed in human oocytes. Reprod Biomed Online 14:700–708PubMedGoogle Scholar
  105. Suwinska A (2012) Preimplantation mouse embryo: developmental fate and potency of blastomeres. In: Kubiak JZ (ed) Mouse development, Results Probl Cell Differ. 55., 141–164. Springer, HeidelbergGoogle Scholar
  106. Sweeney C, Murphy M, Kubelka M, Ravnik SE, Hawkins CF, Wolgemuth DJ, Carrington M (1996) A distinct cyclin A is expressed in germ cells in the mouse. Development 122:53–64PubMedGoogle Scholar
  107. Tachibana-Konwalski K, Godwin J, van der Weyden L, Champion L, Kudo NR, Adams DJ, Nasmyth K (2010) Rec8-containing cohesin maintains bivalents without turnover during the growing phase of mouse oocytes. Genes Dev 24:2505–2516PubMedGoogle Scholar
  108. Tanaka TU (2010) Kinetochore-microtubule interactions: steps towards bi-orientation. EMBO J 29:4070–4082PubMedGoogle Scholar
  109. Tarkowski AK (1959) Experiments on the development of isolated blastomers of mouse eggs. Nature 184:1286–1287PubMedGoogle Scholar
  110. Tarkowski AK (1961) Mouse chimaeras developed from fused eggs. Nature 190:857–860PubMedGoogle Scholar
  111. Tay J, Hodgman R, Richter JD (2000) The control of cyclin B1 mRNA translation during mouse oocyte maturation. Dev Biol 221:1–9PubMedGoogle Scholar
  112. Terret ME, Lefebvre C, Djiane A, Rassinier P, Moreau J, Maro B, Verlhac MH (2003) DOC1R: a MAP kinase substrate that control microtubule organization of metaphase II mouse oocytes. Development 130:5169–5177PubMedGoogle Scholar
  113. Tsurumi C, Hoffmann S, Graeser R, Geley S, Polanski Z (2004) The spindle assembly checkpoint is not essential for CSF arrest of mouse oocytes. J Cell Biol 167:1037–1050PubMedGoogle Scholar
  114. Vaccari S, Weeks JL 2nd, Hsieh M, Menniti FS, Conti M (2009) Cyclic GMP signaling is involved in the luteinizing hormone-dependent meiotic maturation of mouse oocytes. Biol Reprod 81:595–604PubMedGoogle Scholar
  115. Verlhac M-H, 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
  116. Verlhac M-H, 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 organisation during mouse meiosis. Development 122:815–822PubMedGoogle Scholar
  117. Wassmann K, Niault T, Maro B (2003) Metaphase I arrest upon activation of the Mad2-dependent spindle checkpoint in mouse oocytes. Curr Biol 13:1596–1608PubMedGoogle Scholar
  118. Winston NJ (1997) Stability of cyclin B protein during meiotic maturation and the first mitotic cell division in mouse oocytes. Biol Cell 89:211–219PubMedGoogle Scholar
  119. Winston N, Bourgain-Guglielmetti F, Ciemerych MA, Kubiak JZ, Senamaud-Beaufort C, Carrington M, Bréchot C, Sobczak-Thépot J (2000) Early development of mouse embryos null mutant for the cyclin A2 gene occurs in the absence of maternally derived cyclin A2 gene products. Dev Biol 223:139–153PubMedGoogle Scholar
  120. Wolgemuth DJ (2011) Function of the A-type cyclins during gametogenesis and early embryogenesis. Results Probl Cell Differ 53:391–413PubMedGoogle Scholar
  121. 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 13:1252–1258PubMedGoogle Scholar
  122. Zhang Y, Zhang Z, Xu XY, Li XS, Yu M, Yu AM, Zong ZH, Yu BZ (2008) Protein kinase A modulates Cdc25B activity during meiotic resumption of mouse oocytes. Dev Dyn 237:3777–3786PubMedGoogle Scholar
  123. Zheng W, Liu K (2012) Maternal control of mouse preimplantation development. In: Kubiak JZ (ed) Mouse development, Results Probl Cell Differ. 55., 115–139. Springer, HeidelbergGoogle Scholar

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© Springer-Verlag Berlin Heidelberg 2012

Authors and Affiliations

  • Zbigniew Polański
    • 1
  • Hayden Homer
    • 2
    • 3
  • Jacek Z. Kubiak
    • 4
    • 5
    Email author
  1. 1.Department of Genetics and Evolution, Institute of ZoologyJagiellonian UniversityKrakówPoland
  2. 2.Mammalian Oocyte and Embryo Research Laboratory, Institute for Women’s HealthUniversity College London and University College London Hospitals NHS Foundation TrustLondonUK
  3. 3.Department of Obstetrics and Gynaecology, Institute for Women’s HealthUniversity College London and University College London Hospitals NHS Foundation TrustLondonUK
  4. 4.Institut de Génétique et Développement de RennesCNRS, UMR 6290RennesFrance
  5. 5.IFR 140, Faculté de MédecineUniversité Rennes 1, UEBRennesFrance

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