Cytostatic Arrest: Post-Ovulation Arrest until Fertilization in Metazoan Oocytes

Oogenesis: The Universal Process

Volumn , Issue , 2010, Pages 357-384

  Nishiyama, Tomoko ^a   Tachibana, Kazunori ^b   Kishimoto, Takeo ^b  

^a RESEARCH INSTITUTE OF MOLECULAR PATHOLOGY   (Austria)

^b TOKYO INSTITUTE OF TECHNOLOGY   (Japan)

Author keywords

Cell cycle; CSF; Cytostatic arrest; Fertilization; MAP kinase; Meiosis; Mos; Oocyte; Ovulation; Rsk

Indexed keywords

EID: 78649732927     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1002/9780470687970.ch14     Document Type: Chapter

References (113)

1. Abrieu, A., Lorca, T., Labbe, J.C. et al. (1996) MAP kinase does not inactivate, but rather prevents the cyclin degradation pathway from being turned on in Xenopus egg extracts. J. Cell Sci., 109(1), 239-246.
2. Abrieu, A., Fisher, D., Simon, M.N. et al. (1997)MAPKinactivation is required for the G2 to M-phase transition of the first mitotic cell cycle. EMBO J., 16, 6407-6413.
3. Adiyodi, K.G. and Adiyodi, R.G. (eds.) (1983) Reproductive Biology of Invertebrates, Vol I. Oogenesis, Oviposition, and Oosorption, John Wiley & Sons, Ltd, Chichester.
4. Amiel, A., Leclere, L., Robert, L. et al. (2009) Conserved functions for Mos in eumetazoan oocyte maturation revealed by studies in a cnidarian. Curr. Biol., 19, 305-311.
5. Bhatt, R.R. and Ferrell, J.E. Jr (1999) The protein kinase p90 rsk as an essential mediator of cytostatic factor activity. Science, 286, 1362-1365.
6. Bitangcol, J.C., Chau, A.S., Stadnick, E. et al. (1998) Activation of the p42 mitogen-activated protein kinase pathway inhibits Cdc2 activation and entry into M-phase in cycling Xenopus egg extracts. Mol. Biol. Cell, 9, 451-467.
7. Boveri, T. (1907) Zellenstudien VI. Die Entwicklung dispermer Seeigeleier. Ein Beitrag zur Befruchtungslehre und zur Theorie des Kerns, Gustav Fischer, Jena.
8. Brunet, S. and Maro, B. (2005) Cytoskeleton and cell cycle control during meiotic maturation of the mouse oocyte: integrating time and space. Reproduction, 130, 801-811.
9. Castro, A., Peter, M., Magnaghi-Jaulin, L. et al. (2001) Cyclin B/cdc2 induces c-Mos stability by direct phosphorylation in Xenopus oocytes. Mol. Biol. Cell, 12, 2660-2671.
10. Colledge, W.H., Carlton, M.B., Udy, G.B. and Evans, M.J. (1994) Disruption of c-mos causes parthenogenetic development of unfertilized mouse eggs. Nature, 370, 65-68.
11. Descombes, P. and Nigg, E.A. (1998) The polo-like kinase Plx1 is required for M phase exit and destruction of mitotic regulators in Xenopus egg extracts. EMBO J., 17, 1328-1335.
12. Dumont, J., Umbhauer, M., Rassinier, P. et al. (2005) p90Rsk is not involved in cytostatic factor arrest in mouse oocytes. J. Cell Biol., 169, 227-231.
13. Dunn, C.W., Hejnol, A., Matus, D.Q. et al. (2008) Broad phylogenomic sampling improves resolution of the animal tree of life. Nature, 452, 745-749.
14. Fenger, D.D., Carminati, J.L., Burney-Sigman, D.L. et al. (2000) PAN GU: a protein kinase that inhibits S phase and promotes mitosis is early Drosophila development. Development, 127, 4763-4774.
15. Fisher, D., Abrieu, A., Simon, M.N. et al. (1998) MAP kinase inactivation is required only for G2-M phase transition in early embryogenesis cell cycles of the starfishes Marthasterias glacialis and Astropecten aranciacus. Dev. Biol., 202, 1-13.
16. Goldman, D.S., Kiessling, A.A., Millette, C.F. and Cooper, G.M. (1987) Expression of c-mos RNA in germ cells of male and female mice. Proc. Natl. Acad. Sci. USA, 84, 4509-4513.
17. Gould, M.C. and Stephano, J.L. (1999) MAP kinase, meiosis, and sperm centrosome suppression in Urechis caupo. Dev. Biol., 216, 348-358.
18. Grimison, B., Liu, J., Lewellyn, A.L. and Maller, J.L. (2006) Metaphase arrest by cyclin E-Cdk2 requires the spindle-checkpoint kinase Mps1. Curr. Biol., 16, 1968-1973.
19. Haccard, O., Sarcevic, B., Lewellyn, A. et al. (1993) Induction of metaphase arrest in cleaving Xenopus embryos by MAP kinase. Science, 262, 1262-1265.
20. Hara, M., Mori, M., Wada, T. et al. (2009) Start of the embryonic cell cycle is dually locked in unfertilized starfish eggs. Development, 136, 1687-1696.
21. Harada, K., Oita, E. and Chiba, K. (2003) Metaphase I arrest of starfish oocytes induced via the MAP kinase pathway is released by an increase of intracellular pH. Development, 130, 4581-4586.
22. Hartwell, L.H. and Weinert, T.A. (1989) Checkpoints: controls that ensure the order of cell cycle events. Science, 246, 629-634.
23. Hashimoto, N.,Watanabe, N., Furuta, Y. et al. (1994) Parthenogenetic activation of oocytes in c-mosdeficient mice. Nature, 370, 68-71.
24. Hirao, Y. and Eppig, J.J. (1997) Parthenogenetic development of Mos-deficient mouse oocytes. Mol. Reprod. Dev., 48, 391-396.
25. Hwang, L.H., Lau, L.F., Smith, D.L. et al. (1998) Budding yeast Cdc20: a target of the spindle checkpoint. Science, 279, 1041-1044.
26. Inoue, D., Ohe, M., Kanemori, Y. et al. (2007) A direct link of the Mos-MAPK pathway to Erp1/Emi2 in meiotic arrest of Xenopus laevis eggs. Nature, 446, 1100-1104.
27. Ivanovska, I., Lee, E., Kwan, K.M. et al. (2004) The Drosophila MOS ortholog is not essential for meiosis. Curr. Biol., 14, 75-80.
28. Kashima, K., Kano, K. and Naito, K. (2007) Mos and the mitogen-activated protein kinase do not show cytostatic factor activity in early mouse embryos. J. Reprod. Dev., 53, 1175-1182.
29. Kearsey, S.E. and Cotterill, S. (2003) Enigmatic variations: Divergent modes of regulating eukaryotic DNA replication. Mol. Cell, 12, 1067-1075.
30. Kim, S.H., Lin, D.P., Matsumoto, S. et al. (1998) Fission yeast Slp1: an effector of the Mad2- dependent spindle checkpoint. Science, 279, 1045-1047.
31. King, R.W., Peters, J.M., Tugendreich, S. et al. (1995)A 20S complex containing CDC27 and CDC16 catalyzes the mitosis-specific conjugation of ubiquitin to cyclin B. Cell, 81, 279-288.
32. Kishimoto, T. (1998) Cell cycle arrest and release in starfish oocytes and eggs. Semin. Cell Dev. Biol., 9, 549-557.
33. Kishimoto, T. (2003) Cell-cycle control during meiotic maturation. Curr. Opin. Cell Biol., 15, 654-663.
34. Kishimoto, T. (2004) More than G1 or G2 arrest: useful starfish oocyte system for investigating skillful MAP kinase. Biol. Cell, 96, 241-244.
35. 2+ increase induces post-fertilization events viaMAP kinase dephosphorylation in eggs of the hydrozoan jellyfish Cladonema pacificum. Dev. Biol., 276, 228-241.
36. Kraft, C., Vodermaier, H.C., Maurer-Stroh, S. et al. (2005) The WD40 propeller domain of Cdh1 functions as a destruction box receptor for APC/C substrates. Mol. Cell, 18, 543-553.
37. Kubiak, J.Z., Weber, M., de Pennart, H. et al. (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, 3773-3778.
38. Kumano, M., Carroll, D.J., Denu, J.M. and Foltz, K.R. (2001) Calcium-mediated inactivation of the MAP kinase pathway in sea urchin eggs at fertilization. Dev. Biol., 236, 244-257.
39. Lapasset, L., Pradet-Balade, B., Verge, V. et al. (2008) Cyclin B synthesis and rapamycin-sensitive regulation of protein synthesis during starfish oocyte meiotic divisions. Mol. Reprod. Dev., 75, 1617-1626.
40. Lefebvre, C., Terret, M.E., Djiane, A. et al. (2002) Meiotic spindle stability depends on MAPKinteracting and spindle-stabilizing protein (MISS), a new MAPK substrate. J. Cell Biol., 157, 603-613.
41. Lillie, F.R. (1912) The fertilizing power of porations of the spermatozoon. J. Exp. Zool., 12, 427-476.
42. Liu, J. and Maller, J.L. (2005) Calcium elevation at fertilization coordinates phosphorylation of XErp1/Emi2 by Plx1 and CaMK II to release metaphase arrest by cytostatic factor. Curr. Biol., 15, 1458-1468.
43. Loeb, J. (1913) Artificial Parthenogenesis and Fertilization, Univ. Chicago Press, Chicago.
44. Masui, Y. (1974) A cytostatic factor in amphibian oocytes: its extraction and partial characterization. J. Exp. Zool., 187, 141-147.
45. Masui, Y. (1985) Meiotic arrest in animal oocytes, in Biology of Fertilization, Vol. 1 (eds C.B. Metz and A. Monroy), Academic Press, New York, pp. 189-219.
46. Masui, Y. (2000) The elusive cytostatic factor in the animal egg. Nat. Rev. Mol. Cell Biol., 1, 228-232.
47. Masui, Y. and Markert, C.L. (1971) Cytoplasmic control of nuclear behavior during meiotic maturation of frog oocytes. J. Exp. Zool., 177, 129-145.
48. McDougall, A. and Levasseur, M. (1998) Sperm-triggered calcium oscillations during meiosis in ascidian oocytes first pause, restart, then stop: correlations with cell cycle kinase activity. Development, 125, 4451-4459.
49. Meyerhof, P.G. and Masui, Y. (1977) Ca and Mg control of cytostatic factors from Rana pipiens oocytes which cause metaphase and cleavage arrest. Dev. Biol., 61, 214-229.
50. Miller, J.J., Summers, M.K., Hansen, D.V. et al. (2006) Emi1 stably binds and inhibits the anaphasepromoting complex/cyclosome as a pseudosubstrate inhibitor. Genes Dev., 20, 2410-2420.
51. Mori, M., Hara, M., Tachibana, K. and Kishimoto, T. (2006) p90Rsk is required for G1 phase arrest in unfertilized starfish eggs. Development, 133, 1823-1830.
52. Murakami, M.S. and Vande Woude, G.F. (1998) Analysis of the early embryonic cell cycles of Xenopus; regulation of cell cycle length by Xe-wee1 and Mos. Development, 125, 237-248.
53. Murakami, M.S., Copeland, T.D. andVandeWoude, G.F. (1999) Mos positively regulates Xe-Wee1 to lengthen the first mitotic cell cycle of Xenopus. Genes Dev., 13, 620-631.
54. Musacchio, A. and Salmon, E.D. (2007) The spindle-assembly checkpoint in space and time. Nat. Rev. Mol. Cell Biol., 8, 379-393.
55. Mutter, G.L. and Wolgemuth, D.J. (1987) Distinct developmental patterns of c-mos protooncogene expression in female and male mouse germ cells. Proc. Natl. Acad. Sci. USA, 84, 5301-5305.
56. Nagano, H., Hirai, S., Okano, K. and Ikegami, S. (1981) Achromosomal cleavage of fertilized starfish eggs in the presence of aphidicolin. Dev. Biol., 85, 409-415.
57. Nebreda, A.R. and Hunt, T. (1993) The c-mos proto-oncogene protein kinase turns on and maintains the activity of MAP kinase, but not MPF, in cell-free extracts of Xenopus oocytes and eggs. EMBO J., 12, 1979-1986.
58. Nishiyama, T., Ohsumi, K. and Kishimoto, T. (2007a) Phosphorylation of Erp1 by p90rsk is required for cytostatic factor arrest in Xenopus laevis eggs. Nature, 446, 1096-1099.
59. Nishiyama, T., Yoshizaki, N., Kishimoto, T. and Ohsumi, K. (2007b) Transient activation of calcineurin is essential to initiate embryonic development in Xenopus laevis. Nature, 449, 341-345.
60. Nishizawa, M., Furuno, N., Okazaki, K. et al. (1993) Degradation of Mos by the N-terminal proline (Pro2)-dependent ubiquitin pathway on fertilization of Xenopus eggs: possible significance of natural selection for Pro2 in Mos. EMBO J., 12, 4021-4027.
61. Ohsumi, K., Koyanagi, A., Yamamoto, T.M. et al. (2004) Emi1-mediated M-phase arrest in Xenopus eggs is distinct from cytostatic factor arrest. Proc. Natl. Acad. Sci. USA, 101, 12531-12536.
62. Okano-Uchida, T., Sekiai, T., Lee, K. et al. (1998) In vivo regulation of cyclin A/Cdc2 and cyclin B/ Cdc2 through meiotic and early cleavage cycles in starfish. Dev. Biol., 197, 39-53.
63. Okano-Uchida, T., Okumura, E., Iwashita, M. et al. (2003) Distinct regulators for Plk1 activation in starfish meiotic and early embryonic cycles. EMBO J., 22, 5633-5642.
64. Oskarsson, M., Mcclements, W.L., Blair, D.G. et al. (1980) Properties of a normal mouse cell DNA sequence (sarc) homologous to the src sequence of Moloney sarcoma virus. Science, 207, 1222-1224.
65. Page, A.W. and Orr-Weaver, T.L. (1997) Stopping and starting the meiotic cell cycle. Curr. Opin. Genet. Dev., 7, 23-31.
66. Peters, J.M. (2006) The anaphase promoting complex/cyclosome: a machine designed to destroy. Nat. Rev. Mol. Cell Biol., 7, 644-656.
67. Picard, A., Galas, S., Peaucellier, G. and Doree, M. (1996) Newly assembled cyclin B-cdc2 kinase is required to suppressDNAreplication between meiosis I and meiosis II in starfish oocytes.EMBOJ., 15, 3590-3598.
68. Posada, J., Yew, N., Ahn, N.G. et al. (1993) Mos stimulates MAP kinase in Xenopus oocytes and activates a MAP kinase kinase in vitro. Mol. Cell Biol., 13, 2546-2553.
69. Propst, F. and Vande Woude, G.F. (1985) Expression of c-mos proto-oncogene transcripts in mouse tissues. Nature, 315, 516-518.
70. Propst, F., Rosenberg, M.P., Iyer, A. et al. (1987) c-mos proto-oncogene RNA transcripts in mouse tissues: structural features, developmental regulation, and localization in specific cell types. Mol. Cell Biol., 7, 1629-1637.
71. Rauh, N.R., Schmidt, A., Bormann, J. et al. (2005) Calcium triggers exit from meiosis II by targeting the APC/C inhibitor XErp1 for degradation. Nature, 437, 1048-1052.
72. Reimann, J.D. and Jackson, P.K. (2002) Emi1 is required for cytostatic factor arrest in vertebrate eggs. Nature, 416, 850-854.
73. Russo, G.L.,Wilding, M., Marino, M. and Dale, B. (1998) Ins and outs of meiosis in ascidians. Semin. Cell Dev. Biol., 9, 559-567.
74. Russo, G.L., Bilotto, S., Ciarcia, G. and Tosti, E. (2009) Phylogenetic conservation of cytostatic factor related genes in the ascidian Ciona intestinalis. Gene, 429, 104-111.
75. Sadler, K.C. and Ruderman, J.V. (1998) Components of the signaling pathway linking the 1-methyladenine receptor to MPF activation and maturation in starfish oocytes. Dev. Biol., 197, 25-38.
76. Sagata, N. (1996) Meiotic metaphase arrest in animal oocytes: its mechanisms and biological significance. Trends Cell Biol., 6, 22-28.
77. Sagata, N., Watanabe, N., Vande Woude, G.F. and Ikawa, Y. (1989) The c-mos proto-oncogene product is a cytostatic factor responsible for meiotic arrest in vertebrate eggs. Nature, 342, 512-518.
78. Schmidt, A., Duncan, P.I., Rauh, N.R. et al. (2005) Xenopus polo-like kinase Plx1 regulates XErp1, a novel inhibitor of APC/C activity. Genes Dev., 19, 502-513.
79. Schmidt, M., Oskarsson, M.K., Dunn, J.K. et al. (1988) Chicken homolog of the mos proto-oncogene. Mol. Cell Biol., 8, 923-929.
80. Schwab, M.S., Roberts, B.T., Gross, S.D. et al. (2001) Bub1 is activated by the protein kinase p90(Rsk) during Xenopus oocyte maturation. Curr. Biol., 11, 141-150.
81. Shibuya, E.K. and Masui, Y. (1988) Stabilization and enhancement of primary cytostatic factor (CSF) by ATP and NaF in amphibian egg cytosols. Dev. Biol., 129, 253-264.
82. Shibuya, E.K. and Masui, Y. (1989) Molecular characteristics of cytostatic factors in amphibian egg cytosols. Development, 106, 799-808.
83. Shibuya, E.K. and Ruderman, J.V. (1993) Mos induces the in vitro activation of mitogen-activated protein kinases in lysates of frog oocytes and mammalian somatic cells. Mol. Biol. Cell, 4, 781-790.
84. Shibuya, E.K., Boulton, T.G., Cobb, M.H. and Ruderman, J.V. (1992) Activation of p42 MAP kinase and the release of oocytes from cell cycle arrest. EMBO J., 11, 3963-3975.
85. Shirato, Y., Tamura, M., Yoneda, M. and Nemoto, S. (2006) Centrosome destined to decay in starfish oocytes. Development, 133, 343-350.
86. Shoji, S., Yoshida, N., Amanai, M. et al. (2006) Mammalian Emi2 mediates cytostatic arrest and transduces the signal for meiotic exit via Cdc20. EMBO J., 25, 834-845.
87. Standart, N., Minshull, J., Pines, J. and Hunt, T. (1987) Cyclin synthesis, modification and destruction during meiotic maturation of the starfish oocyte. Dev. Biol., 124, 248-258.
88. Sudakin, V., Ganoth, D., Dahan, A. et al. (1995) The cyclosome, a large complex containing cyclinselective ubiquitin ligase activity, targets cyclins for destruction at the end of mitosis. Mol. Biol. Cell, 6, 185-197.
89. Tachibana, K., Machida, T., Nomura, Y. and Kishimoto, T. (1997) MAP kinase links the fertilization signal transduction pathway to the G1/S-phase transition in starfish eggs.EMBOJ., 16, 4333-4339.
90. Tachibana, K., Tanaka, D., Isobe, T. and Kishimoto, T. (2000) c-Mos forces the mitotic cell cycle to undergo meiosis II to produce haploid gametes. Proc. Natl. Acad. Sci. USA, 97, 14301-14306.
91. Tachibana, K., Hara, M., Hattori, Y. and Kishimoto, T. (2008) Cyclin B-Cdk1 controls pronuclear union in interphase. Curr. Biol., 18, 1308-1313.
92. Tachibana, K., Mori, M., Matsuhira, T. et al. (2010) Initiation of DNA replication by fertilization is regulated by p90Rsk at pre-RC/pre-IC transition in starfish eggs. Proc. Natl. Acad. Sci. USA, in press.
93. Tamura, M. and Nemoto, S. (2001) Reproductive maternal centrosomes are cast off into polar bodies during maturation division in starfish oocytes. Exp. Cell Res., 269, 130-139.
94. Tang,W.,Wu, J.Q., Guo, Y. et al. (2008) Cdc2 and Mos regulate Emi2 stability to promote the meiosis I-meiosis II transition. Mol. Biol. Cell, 19, 3536-3543.
95. Terret, M.E., Lefebvre, C., Djiane, A. et al. (2003) DOC1R: a MAP kinase substrate that control microtubule organization of metaphase II mouse oocytes. Development, 130, 5169-5177.
96. Thibier, C., De Smedt, V., Poulhe, R. et al. (1997) In vivo regulation of cytostatic activity in Xenopus metaphase II-arrested oocytes. Dev. Biol., 185, 55-66.
97. Tsurumi, C., Hoffmann, S., Geley, S. et al. (2004) The spindle assembly checkpoint is not essential for CSF arrest of mouse oocytes. J. Cell Biol., 167, 1037-1050.
98. Tunquist, B.J., Eyers, P.A., Chen, L.G. et al. (2003) Spindle checkpoint proteins Mad1 and Mad2 are required for cytostatic factor-mediated metaphase arrest. J. Cell Biol., 163, 1231-1242.
99. Tunquist, B.J., Schwab, M.S., Chen, L.G. and Maller, J.L. (2002) The spindle checkpoint kinase bub1 and cyclin e/cdk2 both contribute to the establishment of meiotic metaphase arrest by cytostatic factor. Curr. Biol., 12, 1027-1033.
100. Usui, K., Hirohashi, N. and Chiba, K. (2008) Involvement of mitogen-activating protein kinase and intracellular pH in the duration of the metaphase I (MI) pause of starfish oocytes after spawning. Develop. Growth Differ., 50, 357-364.
101. Vardy, L. and Orr-Weaver, T.L. (2007a) The Drosophila PNG kinase complex regulates the translation of cyclin B. Dev. Cell, 12, 157-166.
102. Vardy, L. and Orr-Weaver, T.L. (2007b) Regulating translation of maternal messages: multiple repression mechanisms. Trends Cell Biol., 17, 547-554.
103. Verlhac, M.H., Kubiak, J.Z.,Weber,M. et al. (1996) Mos is required for MAP kinase activation and is involved in microtubule organization during meiotic maturation in the mouse. Development, 122, 815-822.
104. Verlhac, M.H., Lefebvre, C., Kubiak, J.Z. et al. (2000) Mos activates MAP kinase in mouse oocytes through two opposite pathways. EMBO J., 19, 6065-6074
105. Walter, S.A., Guadagno, T.M. and Ferrell, J.E. Jr (1997) Induction of a G2-phase arrest in Xenopus egg extracts by activation of p42 mitogen-activated protein kinase. Mol. Biol. Cell, 8, 2157-2169.
106. Walter, S.A., Guadagno, S.N. and Ferrell, J.E. Jr (2000) Activation ofWee1 by p42MAPKin vitro and in cycling Xenopus egg extracts. Mol. Biol. Cell, 11, 887-896.
107. Watanabe, N., Hunt, T., Ikawa, Y. and Sagata, N. (1991) Independent inactivation of MPF and cytostatic factor (Mos) upon fertilization of Xenopus eggs. Nature, 352, 247-248.
108. Winston, N.J., McGuinness, O., Johnson, M.H. and Maro, B. (1995) The exit of mouse oocytes from meiotic M-phase requires an intact spindle during intracellular calcium release. J. Cell Sci., 108, 143-151.
109. Wu, Q., Guo, Y., Yamada, A. et al. (2007) A role for Cdc2- and PP2A-mediated regulation of Emi2 in the maintenance of CSF arrest. Curr. Biol., 17, 213-224.
110. Yamada, H., Hirai, S., Ikegami, S. et al. (1985) The fate of DNA originally existing in the zygote nucleus during achromosomal cleavage of fertilized echinoderm eggs in the presence of aphidicolin: Microscopic studies with anti-DNA antibody. J. Cell Physiol., 124, 9-12.
111. Yamamoto, D.S., Tachibana, K., Sumitani, M. et al. (2008) Involvement of Mos-MEK-MAPK pathway in cytostatic factor (CSF) arrest in eggs of the parthenogenetic insect, Athalia rosae. Mech. Dev., 125, 996-1008.
112. Yamamoto, T.M., Iwabuchi, M., Ohsumi, K. and Kishimoto, T. (2005) APC/C-Cdc20-mediated degradation of cyclin B participates in CSF arrest in unfertilized Xenopus eggs. Dev. Biol., 279, 345-355.
113. Yamano, H., Gannon, J., Mahbubani, H. and Hunt, T. (2004) Cell cycle-regulated recognition of the destruction box of cyclin B by the APC/C in Xenopus egg extracts. Mol. Cell, 13, 137-147.