PP1 control of M phase entry exerted through 14-3-3-regulated Cdc25 dephosphorylation

EMBO Journal

Volumn 22, Issue 21, 2003, Pages 5734-5745

  Margolis, Seth S ^a   Walsh, Susan ^a   Weiser, Douglas C ^a   Yoshida, Minoru ^b   Shenolikar, Shirish ^a   Kornbluth, Sally ^c  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

^b RIKEN   (Japan)

^c NONE

Author keywords

14 3 3; Cdc25; Cdk2; PP1; Xenopus

Indexed keywords

CYCLIN DEPENDENT KINASE; PHOSPHOPROTEIN PHOSPHATASE 1; PROTEIN 14 3 3; PROTEIN KINASE; PROTEIN TYROSINE PHOSPHATASE; SERINE;

ANIMAL CELL; ARTICLE; CELL CYCLE M PHASE; CELL CYCLE PHASE; ENZYME INHIBITION; ENZYME SUBSTRATE; INTERPHASE; MEIOSIS; MITOSIS RATE; MOLECULAR RECOGNITION; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEPHOSPHORYLATION; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION;

14-3-3 PROTEINS; ANIMALS; BASE SEQUENCE; BINDING SITES; CDC2 PROTEIN KINASE; CDC2-CDC28 KINASES; CDC25 PHOSPHATASE; CYCLIN-DEPENDENT KINASE 2; DNA, COMPLEMENTARY; FEMALE; MITOSIS; MUTAGENESIS, SITE-DIRECTED; OOCYTES; PHOSPHOPROTEIN PHOSPHATASE; PHOSPHORYLATION; TYROSINE 3-MONOOXYGENASE; XENOPUS; XENOPUS PROTEINS;

ANIMALIA;

EID: 0242389822     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/cdg545     Document Type: Article

References (41)

1. Bulavin, D.V. et al. (2003) Dual phosphorylation controls Cdc25 phosphatases and mitotic entry. Nat. Cell Biol., 5, 545-551.
2. Cohen, P.T. (2002) Protein phosphatase 1-targeted in many directions. J. Cell Sci., 115, 241-256.
3. Coleman, T.R. and Dunphy, W.G. (1994) Cdc2 regulatory factors. Curr. Opin. Cell Biol., 6, 877-882.
4. Connor, J.H., Quan, H., Oliver, C. and Shenolikar, S. (1998) Inhibitor-1, a regulator of protein phosphatase 1 function. Methods Mol. Biol., 93, 41-58.
5. 2 arrest in Xenopus oocytes depends on phosphorylation of cdc25 by protein kinase A. Proc. Natl Acad. Sci. USA, 99, 16794-16799.
6. Egloff, M.P., Johnson, D.F., Moorhead, G., Cohen, P.T., Cohen, P. and Barford, D. (1997) Structural basis for the recognition of regulatory subunits by the catalytic subunit of protein phosphatase 1. EMBO J., 16, 1876-1887.
7. Finidori-Lepicard, J., Schorderet-Slatkíne, S., Hanoune, J. and Baulieu, E.E. (1981) Progesterone inhibits membrane-bound adenylate cyclase in Xenopus laevis oocytes. Nature, 292, 255-257.
8. Furnari, B., Rhind, N. and Russell, P. (1997) Cdc25 mitotic inducer targeted by chk1 DNA damage checkpoint kinase. Science, 277, 1495-1497.
9. Furnari, B., Blasina, A., Boddy, M.N., McGowan, C.H. and Russell, P. (1999) Cdc25 inhibited in vivo and in vitro by checkpoint kinases Cds1 and Chk1. Mol. Biol. Cell, 10, 833-845.
10. Graves, P.R., Lovly, C.M., Uy, G.L. and Piwnica-Worms, H. (2001) Localization of human Cdc25C is regulated both by nuclear export and 14-3-3 protein binding. Oncogene, 20, 1839-1851.
11. Guadagno, T.M. and Newport, J.W. (1996) Cdk2 kinase is required for entry into mitosis as a positive regulator of Cdc2-cyclin B kinase activity. Cell, 84, 73-82.
12. 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.
13. Huchon, D., Ozon, R. and Demaille, J.G. (1981a) Protein phosphatase-1 is involved in Xenopus oocyte maturation. Nature, 294, 358-359.
14. Huchon, D., Ozon, R., Fischer, E.H. and Demaille, J.G. (1981b) The pure inhibitor of cAMP-dependent protein kinase initiates Xenopus laevis meiotic maturation. A 4-step scheme for meiotic maturation. Mol. Cell. Endocrinol., 22, 211-222.
15. Hutchins, J.R., Dikovskaya, D. and Clarke, P.R. (2002) Dephosphorylation of the inhibitory phosphorylation site S287 in Xenopus Cdc25C by protein phosphatase-2A is inhibited by 14-3-3 binding. FEBS Lett., 528, 267-271.
16. Izumi, T. and Maller, J.L. (1993) Elimination of cdc2 phosphorylation sites in the cdc25 phosphatase blocks initiation of M-phase. Mol. Biol. Cell, 4, 1337-1350.
17. 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.
18. Karaiskou, A., Cayla, X., Haccard, O., Jessus, C. and Ozon, R. (1998) MPF amplification in Xenopus oocyte extracts depends on a two-step activation of cdc25 phosphatase. Exp. Cell Res., 244, 491-500.
19. 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.
20. Kumagai, A., Guo, Z., Emami, K.H., Wang, S.X. and Dunphy, W.G. (1998a) The Xenopus Chk1 protein kinase mediates a caffeine-sensitive pathway of checkpoint control in cell-free extracts. J. Cell Biol., 142, 1559-1569.
21. Kumagai, A., Yakowec, P.S. and Dunphy, W.G. (1998b) 14-3-3 proteins act as negative regulators of the mitotic inducer Cdc25 in Xenopus egg extracts. Mol. Biol. Cell, 9, 345-354.
22. Kumagai, A. and Dunphy, W.G. (1999) Binding of 14-3-3 proteins and nuclear export control the intracellular localization of the mitotic inducer Cdc25. Genes Dev., 13, 1067-1072.
23. Lew, D.J. and Kornbluth, S. (1996) Regulatory roles of cyclin dependent kinase phosphorylation in cell cycle control. Curr. Opin. Cell Biol., 8, 795-804.
24. Maller, J.L., Butcher, F.R. and Krebs, E.G. (1979) Early effect of progesterone on levels of cyclic adenosine 3′:5′-monophosphate in Xenopus oocytes. J. Biol. Chem., 254, 579-582.
25. Moore, J.D., Kirk, J.A. and Hunt T. (2003) Unmasking the S-phase-promoting potential of cyclin B1. Science, 300, 987-990.
26. Mulner, O., Huchon, D., Thibier, C. and Ozon, R. (1979) Cyclic AMP synthesis in Xenopus laevis oocytes: inhibition by progesterone. Biochim. Biophys Acta, 582, 179-184.
27. 2 checkpoint control: regulation of 14-3-3 protein binding by phosphorylation of Cdc25c on serine-216. Science, 277, 1501-1504.
28. Peng, C.Y., Graves, P.R., Ogg, S., Thoma, R.S., Byrnes, M.J., 3rd, Wu, Z., Stephenson, M.T. and Piwnica-Worms, H. (1998) C-TAK1 protein kinase phosphorylates human Cdc25C on serine 216 and promotes 14-3-3 protein binding. Cell Growth Differ., 9, 197-208.
29. Pinna, L.A. and Donella-Deana, A. (1994) Phosphorylated synthetic peptides as tools for studying protein phosphatases. Biochim. Biophys Acta, 1222, 415-431.
30. 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.
31. Sadler, S.E. and Maller, J.L. (1981) Progesterone inhibits adenylate cyclase in Xenopus oocytes. Action on the guanine nucleotide regulatory protein. J. Biol. Chem., 256, 6368-6373.
32. Sanchez, Y., Wong, C., Thoma, R.S., Richman, R., Wu, Z., Piwnica-Worms, H. and Elledge, S.J. (1997) Conservation of the Chk1 checkpoint pathway in mammals: linkage of DNA damage to Cdk regulation through Cdc25. Science, 277, 1497-1501.
33. Sheppeck, J.E., 2nd, Gauss, C.M. and Chamberlin, A.R. (1997) Inhibition of the Ser-Thr phosphatases PP1 and PP2A by naturally occurring toxins. Bioorg. Med. Chem., 5, 1739-1750.
34. Smythe, C. and Newport, J.W. (1991) Systems for the study of nuclear assembly, DNA replication and nuclear breakdown in Xenopus laevis egg extracts. Methods Cell Biol., 35, 449-468.
35. Terry-Lorenzo, R.T., Inoue, M., Connor, J.H., Haystead, T.A., Armbruster, B.N., Gupta, R.P., Oliver, C.J. and Shenolikar, S. (2000) Neurofilament-L is a protein phosphatase-1-binding protein associated with neuronal plasma membrane and post-synaptic density. J. Biol. Chem., 275, 2439-2446.
36. Wakula, P., Beullens, M., Ceulemans, H., Stalmans, W. and Bollen, M. (2003) Degeneracy and function of the ubiquitous RVXF motif that mediates binding to protein phosphatase-1. J. Biol. Chem., 278, 18817-18823.
37. Walsh, A.H., Cheng, A. and Honkanen, R.E. (1997) Fostriecin, an antitumor antibiotic with inhibitory activity against serine/threonine protein phosphatases types 1 (PP1) and 2A (PP2A), is highly selective for PP2A. FEBS Lett., 416, 230-234.
38. Walsh, S., Margolis, S.S. and Kornbluth, S. (2003) Phosphorylation of the cyclin b1 cytoplasmic retention sequence by mitogen-activated protein kinase and plx. Mol. Cancer Res., 1, 280-289.
39. Yaffe, M.B., Rittinger, K., Volinia, S., Caron, P.R., Aitken, A., Leffers, H., Gamblin, S.J., Smerdon, S.J. and Cantley, L.C. (1997) The structural basis for 14-3-3: phosphopeptide binding specificity. Cell, 91, 961-971.
40. 2 arrest in the Xenopus oocyte: a role for 14-3-3-mediated inhibition of Cdc25 nuclear import. EMBO J., 18, 2174-2183.
41. Zeng, Y., Forbes, K.C., Wu, Z., Moreno, S., Piwnica-Worms, H. and Enoch, T. (1998) Replication checkpoint requires phosphorylation of the phosphatase Cdc25 by Cds1 or Chk1. Nature, 395, 507-510.