Xenopus oocyte meiosis lacks spindle assembly checkpoint control

Journal of Cell Biology

Volumn 201, Issue 2, 2013, Pages 191-200

  Shao, Hua ^a   Li, Ruizhen ^a   Ma, Chunqi ^a   Chen, Eric ^a   Liu, X Johné ^a,b  

^a OTTAWA HOSPITAL RESEARCH INSTITUTE   (Canada)

^b UNIVERSITY OF OTTAWA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

AURORA B KINASE; NOCODAZOLE;

ANAPHASE; ANIMAL CELL; ARTICLE; CHROMOSOME; CONTROLLED STUDY; FEMALE; KARYOTYPING; M PHASE CELL CYCLE CHECKPOINT; MEIOSIS; METAPHASE; MICROTUBULE; NONHUMAN; OOCYTE; PRIORITY JOURNAL; XENOPUS LAEVIS;

ANAPHASE; ANIMALS; CDC42 GTP-BINDING PROTEIN; CELL POLARITY; CHROMOSOMES; CYCLIN B; CYSTEINE; DEMECOLCINE; ENZYME ACTIVATION; FEMALE; KARYOTYPING; M PHASE CELL CYCLE CHECKPOINTS; MEIOSIS; METAPHASE; MICROTUBULES; MITOTIC SPINDLE APPARATUS; NOCODAZOLE; OOCYTES; PROTEIN-SERINE-THREONINE KINASES; PROTEOLYSIS; TIME FACTORS; XENOPUS;

ANURA; MAMMALIA; VERTEBRATA; XENOPUS LAEVIS;

EID: 84876743943     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201211041     Document Type: Article

References (45)

1. Batiha, O., and A. Swan. 2012. Evidence that the spindle assembly checkpoint does not regulate APC(Fzy) activity in Drosophila female meiosis. Genome. 55:63-67. http://dx.doi.org/10.1139/g11-079
2. Bayaa, M., R.A. Booth, Y. Sheng, and X.J. Liu. 2000. The classical progesterone receptor mediates Xenopus oocyte maturation through a nongenomic mechanism. Proc. Natl. Acad. Sci. USA. 97:12607-12612. http://dx.doi.org/10.1073/pnas.220302597
3. Belloc, E., and R. Méndez. 2008. A deadenylation negative feedback mechanism governs meiotic metaphase arrest. Nature. 452:1017-1021. http://dx.doi.org/10.1038/nature06809
4. Benink, H.A., and W.M. Bement. 2005. Concentric zones of active RhoA and Cdc42 around single cell wounds. J. Cell Biol. 168:429-439. http://dx.doi.org/10.1083/jcb.200411109
5. Brunet, S., A.S. Maria, P. Guillaud, D. Dujardin, J.Z. Kubiak, and B. Maro. 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. 146:1-12. http://dx.doi.org/10.1083/jcb.146.1.1
6. Clark-Maguire, S., and P.E. Mains. 1994. Localization of the mei-1 gene product of Caenorhaditis elegans, a meiotic-specific spindle component. J. Cell Biol. 126:199-209. http://dx.doi.org/10.1083/jcb.126.1.199
7. Clute, P., and Y. Masui. 1995. Regulation of the appearance of division asynchrony and microtubule-dependent chromosome cycles in Xenopus laevisembryos. Dev. Biol. 171:273-285. http://dx.doi.org/10.1006/dbio.1995.1280
8. Eichenlaub-Ritter, U., and I. Boll. 1989. Nocodazole sensitivity, age-related aneuploidy, and alterations in the cell cycle during maturation of mouse oocytes. Cytogenet. Cell Genet. 52:170-176. http://dx.doi.org/10.1159/000132871
9. Ferrell, J.E. Jr., and E.M. Machleder. 1998. The biochemical basis of an all-or-none cell fate switch in Xenopus oocytes. Science. 280:895-898. http://dx.doi.org/10.1126/science.280.5365.895
10. Furuno, N., M. Nishizawa, K. Okazaki, H. Tanaka, J. Iwashita, N. Nakajo, Y. Ogawa, and N. Sagata. 1994. Suppression of DNA replication via Mos function during meiotic divisions in Xenopus oocytes. EMBO J. 13:2399-2410.
11. Gall, J.G., and Z. Wu. 2010. Examining the contents of isolated Xenopus germinal vesicles. Methods. 51:45-51. http://dx.doi.org/10.1016/j.ymeth.2009.12.010
12. Gerhart, J., M. Wu, and M. Kirschner. 1984. Cell cycle dynamics of an M-phase-specific cytoplasmic factor in Xenopus laevis oocytes and eggs. J. Cell Biol. 98:1247-1255. http://dx.doi.org/10.1083/jcb.98.4.1247
13. Graf, J.-D., and H.R. Kobel. 1991. Genetics of Xenopus laevis. Methods Cell Biol. 36:19-34. http://dx.doi.org/10.1016/S0091-679X(08)60270-8
14. Hara, K., P. Tydeman, and M. Kirschner. 1980. A cytoplasmic clock with the same period as the division cycle in Xenopus eggs. Proc. Natl. Acad. Sci. USA. 77:462-466. http://dx.doi.org/10.1073/pnas.77.1.462
15. Hodges, C.A., and P.A. Hunt. 2002. Simultaneous analysis of chromosomes and chromosome-associated proteins in mammalian oocytes and embryos. Chromosoma. 111:165-169. http://dx.doi.org/10.1007/s00412-002-0195-3
16. Homer, H.A., A. McDougall, M. Levasseur, A.P. Murdoch, and M. Herbert. 2005. Mad2 is required for inhibiting securin and cyclin B degradation following spindle depolymerisation in meiosis I mouse oocytes. Reproduction. 130:829-843. http://dx.doi.org/10.1530/rep.1.00856
17. Hu, C.K., M. Coughlin, C.M. Field, and T.J. Mitchison. 2008. Cell polarization during monopolar cytokinesis. J. Cell Biol. 181:195-202. http://dx.doi.org/10.1083/jcb.200711105
18. Kolano, A., S. Brunet, A.D. Silk, D.W. Cleveland, and M.H. Verlhac. 2012. Error-prone mammalian female meiosis from silencing the spindle assembly checkpoint without normal interkinetochore tension. Proc. Natl. Acad. Sci. USA. 109:E1858-E1867. http://dx.doi.org/10.1073/pnas.1204686109
19. Leblanc, J., X. Zhang, D. McKee, Z.B. Wang, R. Li, C. Ma, Q.Y. Sun, and X.J. Liu. 2011. The small GTPase Cdc42 promotes membrane protrusion during polar body emission via ARP2-nucleated actin polymerization. Mol. Hum. Reprod. 17:305-316. http://dx.doi.org/10.1093/molehr/gar026
20. LeMaire-Adkins, R., K. Radke, and P.A. Hunt. 1997. Lack of checkpoint control at the metaphase/anaphase transition: a mechanism of meiotic nondisjunction in mammalian females. J. Cell Biol. 139:1611-1619. http://dx.doi.org/10.1083/jcb.139.7.1611
21. Liu, X.S., and X.J. Liu. 2006. Oocyte isolation and enucleation. Methods Mol. Biol. 322:31-41. http://dx.doi.org/10.1007/978-1-59745-000-3_3
22. Ma, C., C. Cummings, and X.J. Liu. 2003. Biphasic activation of Aurora-A kinase during the meiosis I- meiosis II transition in Xenopus oocytes. Mol. Cell. Biol. 23:1703-1716. http://dx.doi.org/10.1128/MCB.23.5.1703-1716.2003
23. Ma, C., H.A. Benink, D. Cheng, V. Montplaisir, L. Wang, Y. Xi, P.P. Zheng, W.M. Bement, and X.J. Liu. 2006. Cdc42 activation couples spindle positioning to first polar body formation in oocyte maturation. Curr. Biol. 16: 214-220. http://dx.doi.org/10.1016/j.cub.2005.11.067
24. Matthews, L.R., P. Carter, D. Thierry-Mieg, and K. Kemphues. 1998. ZYG-9, a Caenorhabditis elegans protein required for microtubule organization and function, is a component of meiotic and mitotic spindle poles. J. Cell Biol. 141:1159-1168. http://dx.doi.org/10.1083/jcb.141.5.1159
25. Murray, A.W., and M.W. Kirschner. 1989. Dominoes and clocks: the union of two views of the cell cycle. Science. 246:614-621. http://dx.doi.org/10.1126/science.2683077
26. Musacchio, A., and E.D. Salmon. 2007. The spindle-assembly checkpoint in space and time. Nat. Rev. Mol. Cell Biol. 8:379-393. http://dx.doi.org/10.1038/nrm2163
27. Nagaoka, S.I., C.A. Hodges, D.F. Albertini, and P.A. Hunt. 2011. Oocytespecific differences in cell-cycle control create an innate susceptibility to meiotic errors. Curr. Biol. 21:651-657. http://dx.doi.org/10.1016/j.cub.2011.03.003
28. Ohan, N., Y. Agazie, C. Cummings, R. Booth, M. Bayaa, and X.J. Liu. 1999. RHO-associated protein kinase ? potentiates insulin-induced MAP kinase activation in Xenopus oocytes. J. Cell Sci. 112:2177-2184.
29. Ohsumi, K., W. Sawada, and T. Kishimoto. 1994. Meiosis-specific cell cycle regulation in maturing Xenopus oocytes. J. Cell Sci. 107:3005-3013.
30. Peter, M., A. Castro, T. Lorca, C. Le Peuch, L. Magnaghi-Jaulin, M. Dorée, and J.C. Labbé. 2001. The APC is dispensable for first meiotic anaphase in Xenopus oocytes. Nat. Cell Biol. 3:83-87. http://dx.doi.org/10.1038/35050607
31. Pines, J. 2006. Mitosis: a matter of getting rid of the right protein at the right time. Trends Cell Biol. 16:55-63. http://dx.doi.org/10.1016/j.tcb.2005.11.006
32. Rieder, C.L., A. Schultz, R. Cole, and G. Sluder. 1994. Anaphase onset in vertebrate somatic cells is controlled by a checkpoint that monitors sister kinetochore attachment to the spindle. J. Cell Biol. 127:1301-1310. http://dx.doi.org/10.1083/jcb.127.5.1301
33. Rieder, C.L., R.W. Cole, A. Khodjakov, and G. Sluder. 1995. The checkpoint delaying anaphase in response to chromosome monoorientation is mediated by an inhibitory signal produced by unattached kinetochores. J. Cell Biol. 130:941-948. http://dx.doi.org/10.1083/jcb.130.4.941
34. Schultz, R.M., and P.M. Wassarman. 1977. Biochemical studies of mammalian oogenesis: Protein synthesis during oocyte growth and meiotic maturation in the mouse. J. Cell Sci. 24:167-194.
35. Shao, H., C. Ma, X. Zhang, R. Li, A.L. Miller, W.M. Bement, and X.J. Liu. 2012. Aurora B regulates spindle bipolarity in meiosis in vertebrate oocytes. Cell Cycle. 11:2672-2680. http://dx.doi.org/10.4161/cc.21016
36. Skoufias, D.A., S. DeBonis, Y. Saoudi, L. Lebeau, I. Crevel, R. Cross, R.H. Wade, D. Hackney, and F. Kozielski. 2006. S-trityl-L-cysteine is a reversible, tight binding inhibitor of the human kinesin Eg5 that specifically blocks mitotic progression. J. Biol. Chem. 281:17559-17569. http://dx.doi.org/10.1074/jbc.M511735200
37. Sluder, G. 1979. Role of spindle microtubules in the control of cell cycle timing. J. Cell Biol. 80:674-691. http://dx.doi.org/10.1083/jcb.80.3.674
38. Soewarto, D., H. Schmiady, and U. Eichenlaub-Ritter. 1995. Consequences of non-extrusion of the first polar body and control of the sequential segregation of homologues and chromatids in mammalian oocytes. Hum. Reprod. 10:2350-2360.
39. Taieb, F.E., S.D. Gross, A.L. Lewellyn, and J.L. Maller. 2001. Activation of the anaphase-promoting complex and degradation of cyclin B is not required for progression from Meiosis I to II in Xenopus oocytes. Curr. Biol. 11:508-513. http://dx.doi.org/10.1016/S0960-9822(01)00145-2
40. Tian, J., S. Kim, E. Heilig, and J.V. Ruderman. 2000. Identification of XPR-1, a progesterone receptor required for Xenopus oocyte activation. Proc. Natl. Acad. Sci. USA. 97:14358-14363. http://dx.doi.org/10.1073/pnas.250492197
41. Verlhac, M.H., C. Lefebvre, P. Guillaud, P. Rassinier, and B. Maro. 2000. Asymmetric division in mouse oocytes: with or without Mos. Curr. Biol. 10:1303-1306. http://dx.doi.org/10.1016/S0960-9822(00)00753-3
42. von Dassow, G., K.J. Verbrugghe, A.L. Miller, J.R. Sider, and W.M. Bement. 2009. Action at a distance during cytokinesis. J. Cell Biol. 187:831-845. http://dx.doi.org/10.1083/jcb.200907090
43. Wassarman, P.M., W.J. Josefowicz, and G.E. Letourneau. 1976. Meiotic maturation of mouse oocytes in vitro: inhibition of maturation at specific stages of nuclear progression. J. Cell Sci. 22:531-545.
44. Zhang, X., C. Ma, A.L. Miller, H.A. Katbi, W.M. Bement, and X.J. Liu. 2008. Polar body emission requires a RhoA contractile ring and Cdc42- mediated membrane protrusion. Dev. Cell. 15:386-400. http://dx.doi.org/10.1016/j.devcel.2008.07.005
45. Zou, H., T.J. McGarry, T. Bernal, and M.W. Kirschner. 1999. Identification of a vertebrate sister-chromatid separation inhibitor involved in transformation and tumorigenesis. Science. 285:418-422. http://dx.doi.org/10.1126/science.285.5426.418