Constant regulation of both the MPF amplification loop and the Greatwall-PP2A pathway is required for metaphase II arrest and correct entry into the first embryonic cell cycle

Journal of Cell Science

Volumn 123, Issue 13, 2010, Pages 2281-2291

  Lorca, Thierry ^a   Bernis, Cyril ^a,b   Vigneron, Suzanne ^a   Burgess, Andrew ^a   Brioudes, Estelle ^a   Labbé, Jean Claude ^a   Castro, Anna ^a  

^a Centre National de la Recherche Scientifique   (France)

^b SECTION OF CELL AND DEVELOPMENTAL BIOLOGY   (United States)

Author keywords

Cdc25; Greatwall; Mitosis; Myt1; PP2A; Wee1

Indexed keywords

CYCLIN A; CYCLIN B; MATURATION PROMOTING FACTOR; PHOSPHOPROTEIN PHOSPHATASE 2A; CELL CYCLE PROTEIN; CYCLIN DEPENDENT KINASE 1; GREATWALL PROTEIN, XENOPUS; MYT1 KINASE, XENOPUS; PHOSPHOPROTEIN PHOSPHATASE 2; PLK1 PROTEIN, XENOPUS; PROTEIN SERINE THREONINE KINASE; PROTEIN TYROSINE KINASE; PROTEIN TYROSINE PHOSPHATASE; WEE1 PROTEIN, XENOPUS; XENOPUS PROTEIN;

ARTICLE; CELL ACTIVATION; CELL CYCLE ARREST; CELL CYCLE G1 PHASE; CELL CYCLE G2 PHASE; CELL CYCLE M PHASE; CELL DIVISION; CELL MATURATION; EMBRYO CELL; INTERPHASE; METAPHASE; MITOSIS; MOLECULAR MECHANICS; NONHUMAN; OOCYTE; PHASE TRANSITION; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; ANIMAL; ANIMAL EMBRYO; CYTOLOGY; METABOLISM; PHYSIOLOGY; SIGNAL TRANSDUCTION; XENOPUS LAEVIS;

ANIMALS; CDC2 PROTEIN KINASE; CDC25 PHOSPHATASES; CELL CYCLE PROTEINS; CYCLIN A; CYCLIN B; EMBRYO, NONMAMMALIAN; MATURATION-PROMOTING FACTOR; METAPHASE; PROTEIN PHOSPHATASE 2; PROTEIN-SERINE-THREONINE KINASES; PROTEIN-TYROSINE KINASES; SIGNAL TRANSDUCTION; XENOPUS LAEVIS; XENOPUS PROTEINS;

EID: 77954355722     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.064527     Document Type: Article

References (53)

1. Abrieu, A., Brassac, T., Galas, S., Fisher, D., Labbe, J. C. and Doree, M. (1998). The Polo-like kinase Plx1 is a component of the MPF amplification loop at the G2/M-phase transition of the cell cycle in Xenopus eggs. J. Cell Sci. 111, 1751-1757. (Pubitemid 28330561)
2. Archambault, V., Zhao, X., White-Cooper, H., Carpenter, A. T. and Glover, D. M. (2007). Mutations in Drosophila Greatwall/Scant reveal its roles in mitosis and meiosis and interdependence with Polo kinase. PLoS Genet. 3, e200.
3. Bernis, C., Vigneron, S., Burgess, A., Labbe, J. C., Fesquet, D., Castro, A. and Lorca, T. (2007). Pin1 stabilizes Emi1 during G2 phase by preventing its association with SCF(betatrcp). EMBO Rep. 8, 91-98.
4. Castilho, P. V., Williams, B. C., Mochida, S., Zhao, Y. and Goldberg, M. L. (2009). The M phase kinase Greatwall (Gwl) promotes inactivation of PP2A/B55delta, a phosphatase directed against CDK phosphosites. Mol. Biol. Cell 20, 4777-4789.
5. Castro, A., Peter, M., Magnaghi-Jaulin, L., Vigneron, S., Galas, S., Lorca, T. and Labbe, J. C. (2001). Cyclin B/cdc2 induces c-Mos stability by direct phosphorylation in Xenopus oocytes. Mol. Biol. Cell 12, 2660-2671.
6. Clarke, P. R., Leiss, D., Pagano, M. and Karsenti, E. (1992). Cyclin A- and cyclin B-dependent protein kinases are regulated by different mechanisms in Xenopus egg extracts. EMBO J. 11, 1751-1761.
7. Clarke, P. R., Hoffmann, I., Draetta, G. and Karsenti, E. (1993). Dephosphorylation of cdc25-C by a type-2A protein phosphatase: specific regulation during the cell cycle in Xenopus egg extracts. Mol. Biol. Cell 4, 397-411. (Pubitemid 23122127)
8. D'Amours, D. and Amon, A. (2004). At the interface between signaling and executing anaphase-Cdc14 and the FEAR network. Genes Dev. 18, 2581-2595.
9. Draetta, G. and Beach, D. (1988). Activation of cdc2 protein kinase during mitosis in human cells: cell cycle-dependent phosphorylation and subunit rearrangement. Cell 54, 17-26.
10. Felix, M. A., Cohen, P. and Karsenti, E. (1990). Cdc2 H1 kinase is negatively regulated by a type 2A phosphatase in the Xenopus early embryonic cell cycle: evidence from the effects of okadaic acid. EMBO J. 9, 675-683. (Pubitemid 20080598)
11. Gautier, J., Solomon, M. J., Booher, R. N., Bazan, J. F. and Kirschner, M. W. (1991). cdc25 is a specific tyrosine phosphatase that directly activates p34cdc2. Cell 67, 197-211. (Pubitemid 121001436)
12. Glotzer, M., Murray, A. W. and Kirschner, M. W. (1991). Cyclin is degraded by the ubiquitin pathway. Nature 349, 132-138.
13. Gould, K. L. and Nurse, P. (1989). Tyrosine phosphorylation of the fission yeast cdc2+ protein kinase regulates entry into mitosis. Nature 342, 39-45.
14. Hoffmann, I., Clarke, P. R., Marcote, M. J., Karsenti, E. and Draetta, G. (1993). Phosphorylation and activation of human cdc25-C by cdc2-cyclin B and its involvement in the self-amplification of MPF at mitosis. EMBO J. 12, 53-63.
15. Izumi, T., Walker, D. H. and Maller, J. L. (1992). Periodic changes in phosphorylation of the Xenopus cdc25 phosphatase regulate its activity. Mol. Biol. Cell 3, 927-939.
16. Kinoshita, N., Ohkura, H. and Yanagida, M. (1990). Distinct, essential roles of type 1 and 2A protein phosphatases in the control of the fission yeast cell division cycle. Cell 63, 405-415. (Pubitemid 120035307)
17. Kinoshita, N., Yamano, H., Niwa, H., Yoshida, T. and Yanagida, M. (1993). Negative regulation of mitosis by the fission yeast protein phosphatase ppa2. Genes Dev. 7, 1059-1071.
18. Krek, W. and Nigg, E. A. (1991). Differential phosphorylation of vertebrate p34cdc2 kinase at the G1/S and G2/M transitions of the cell cycle: identification of major phosphorylation sites. EMBO J. 10, 305-316.
19. Kumagai, A. and Dunphy, W. G. (1991). The cdc25 protein controls tyrosine dephosphorylation of the cdc2 protein in a cell-free system. Cell 64, 903-914. (Pubitemid 121001178)
20. Kumagai, A. and Dunphy, W. G. (1996). Purification and molecular cloning of Plx1, a Cdc25-regulatory kinase from Xenopus egg extracts. Science 273, 1377-1380. (Pubitemid 26296523)
21. Lorca, T., Fesquet, D., Zindy, F., Le Bouffant, F., Cerruti, M., Brechot, C., Devauchelle, G. and Doree, M. (1991). An okadaic acid-sensitive phosphatase negatively controls the cyclin degradation pathway in amphibian eggs. Mol. Cell. Biol. 11, 1171-1175.
22. Lorca, T., Labbe, J. C., Devault, A., Fesquet, D., Strausfeld, U., Nilsson, J., Nygren, P. A., Uhlen, M., Cavadore, J. C. and Doree, M. (1992). Cyclin A-cdc2 kinase does not trigger but delays cyclin degradation in interphase extracts of amphibian eggs. J. Cell Sci. 102, 55-62.
23. Lorca, T., Castro, A., Martinez, A. M., Vigneron, S., Morin, N., Sigrist, S., Lehner, C., Doree, M. and Labbe, J. C. (1998). Fizzy is required for activation of the APC/cyclosome in Xenopus egg extracts. EMBO J. 17, 3565-3575.
24. Lundgren, K., Walworth, N., Booher, R., Dembski, M., Kirschner, M. and Beach, D. (1991). mik1 and wee1 cooperate in the inhibitory tyrosine phosphorylation of cdc2. Cell 64, 1111-1122. (Pubitemid 121001198)
25. Millar, J. B., McGowan, C. H., Lenaers, G., Jones, R. and Russell, P. (1991). p80cdc25 mitotic inducer is the tyrosine phosphatase that activates p34cdc2 kinase in fission yeast. EMBO J. 10, 4301-4309.
26. Minshull, J., Straight, A., Rudner, A. D., Dernburg, A. F., Belmont, A. and Murray, A. W. (1996). Protein phosphatase 2A regulates MPF activity and sister chromatid cohesion in budding yeast. Curr. Biol. 6, 1609-1620.
27. Mochida, S., Ikeo, S., Gannon, J. and Hunt, T. (2009). Regulated activity of PP2A-B55 delta is crucial for controlling entry into and exit from mitosis in Xenopus egg extracts. EMBO J. 28, 2777-2785.
28. Mueller, P. R., Coleman, T. R. and Dunphy, W. G. (1995a). Cell cycle regulation of a Xenopus Wee1-like kinase. Mol. Biol. Cell 6, 119-134.
29. Mueller, P. R., Coleman, T. R., Kumagai, A. and Dunphy, W. G. (1995b). Myt1: a membrane-associated inhibitory kinase that phosphorylates Cdc2 on both threonine-14 and tyrosine-15. Science 270, 86-90.
30. 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.
31. Murray, A. W. and Kirschner, M. W. (1991). What controls the cell cycle? Sci. Am. 264, 56-63.
32. Murray, A. W., Solomon, M. J. and Kirschner, M. W. (1989). The role of cyclin synthesis and degradation in the control of maturation promoting factor activity. Nature 339, 280-286.
33. Nakajima, H., Toyoshima-Morimoto, F., Taniguchi, E. and Nishida, E. (2003). Identification of a consensus motif for Plk (Polo-like kinase) phosphorylation reveals Myt1 as a Plk1 substrate. J. Biol. Chem. 278, 25277-25280.
34. Nurse, P. (1990). Universal control mechanism regulating onset of M-phase. Nature 344, 503-508.
35. Okano-Uchida, T., Okumura, E., Iwashita, M., Yoshida, H., Tachibana, K. and Kishimoto, T. (2003). Distinct regulators for Plk1 activation in starfish meiotic and early embryonic cycles. EMBO J. 22, 5633-5642.
36. Parker, L. L. and Piwnica-Worms, H. (1992). Inactivation of the p34cdc2-cyclin B complex by the human WEE1 tyrosine kinase. Science 257, 1955-1957.
37. Potapova, T. A., Daum, J. R., Byrd, K. S. and Gorbsky, G. J. (2009). Fine tuning the cell cycle: activation of the Cdk1 inhibitory phosphorylation pathway during mitotic exit. Mol. Biol. Cell 20, 1737-1748.
38. Qian, Y. W., Erikson, E., Li, C. and Maller, J. L. (1998). Activated polo-like kinase Plx1 is required at multiple points during mitosis in Xenopus laevis. Mol. Cell. Biol. 18, 4262-4271. (Pubitemid 28287949)
39. Qian, Y. W., Erikson, E. and Maller, J. L. (1999). Mitotic effects of a constitutively active mutant of the Xenopus polo-like kinase Plx1. Mol. Cell. Biol. 19, 8625-8632. (Pubitemid 30414055)
40. Qian, Y. W., Erikson, E., Taieb, F. E. and Maller, J. L. (2001). The polo-like kinase Plx1 is required for activation of the phosphatase Cdc25C and cyclin B-Cdc2 in Xenopus oocytes. Mol. Biol. Cell 12, 1791-1799.
41. Russell, P. and Nurse, P. (1987a). Negative regulation of mitosis by wee1+, a gene encoding a protein kinase homolog. Cell 49, 559-567.
42. Russell, P. and Nurse, P. (1987b). The mitotic inducer nim1+ functions in a regulatory network of protein kinase homologs controlling the initiation of mitosis. Cell 49, 569-576.
43. Smythe, C. and Newport, J. W. (1992). Coupling of mitosis to the completion of S phase in Xenopus occurs via modulation of the tyrosine kinase that phosphorylates p34cdc2. Cell 68, 787-797.
44. Solomon, M. J., Glotzer, M., Lee, T. H., Philippe, M. and Kirschner, M. W. (1990). Cyclin activation of p34cdc2. Cell 63, 1013-1024.
45. Stegmeier, F. and Amon, A. (2004). Closing mitosis: the functions of the Cdc14 phosphatase and its regulation. Annu. Rev. Genet. 38, 203-232.
46. Strausfeld, U., Labbe, J. C., Fesquet, D., Cavadore, J. C., Picard, A., Sadhu, K., Russell, P. and Doree, M. (1991). Dephosphorylation and activation of a p34cdc2/cyclin B complex in vitro by human CDC25 protein. Nature 351, 242-245.
47. Trautmann, S. and McCollum, D. (2002). Cell cycle: new functions for Cdc14 family phosphatases. Curr. Biol. 12, R733-R735.
48. Vigneron, S., Brioudes, E., Burgess, A., Labbe, J. C., Lorca, T. and Castro, A. (2009). Greatwall maintains mitosis through regulation of PP2A. EMBO J. 28, 2786-2793.
49. Walter, S. A., Guadagno, S. N. and Ferrell, J. E., Jr (2000). Activation of Wee1 by p42 MAPK in vitro and in cycling xenopus egg extracts. Mol. Biol. Cell 11, 887-896.
50. Watanabe, N., Arai, H., Nishihara, Y., Taniguchi, M., Hunter, T. and Osada, H. (2004). M-phase kinases induce phospho-dependent ubiquitination of somatic Wee1 by SCFbeta-TrCP. Proc. Natl. Acad. Sci. USA 101, 4419-4424.
51. 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.
52. Yu, J., Zhao, Y., Li, Z., Galas, S. and Goldberg, M. L. (2006). Greatwall kinase participates in the Cdc2 autoregulatory loop in Xenopus egg extracts. Mol. Cell 22, 83-91.
53. Zhang, Y., Yao, B., Delikat, S., Bayoumy, S., Lin, X. H., Basu, S., McGinley, M., Chan-Hui, P. Y., Lichenstein, H. and Kolesnick, R. (1997). Kinase suppressor of Ras is ceramide-activated protein kinase. Cell 89, 63-72.