Oscillations in Cdc14 release and sequestration reveal a circuit underlying mitotic exit

Journal of Cell Biology

Volumn 190, Issue 2, 2010, Pages 209-222

  Manzoni, Romilde ^a   Montani, Francesca ^b   Visintin, Clara ^b   Caudron, Fabrice ^c   Ciliberto, Andrea ^a   Visintin, Rosella ^b  

^a FIRC INSTITUTE OF MOLECULAR ONCOLOGY   (Italy)

^b EUROPEAN INSTITUTE OF ONCOLOGY   (Italy)

^c ETH ZURICH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN DEPENDENT KINASE; PHOSPHOPROTEIN PHOSPHATASE CDC14; POLO LIKE KINASE;

ARTICLE; BUDDING; CELL CYCLE REGULATION; CENTROSOME; CONTROLLED STUDY; ENZYME ACTIVATION; GENE DUPLICATION; MITOSIS; NEGATIVE FEEDBACK; NONHUMAN; OSCILLATION; PHENOTYPE; PRIORITY JOURNAL; YEAST;

CELL CYCLE PROTEINS; CYCLIN B; ENZYME ACTIVATION; MITOSIS; MODELS, BIOLOGICAL; NUCLEAR PROTEINS; PROTEIN KINASES; PROTEIN TYROSINE PHOSPHATASES; PROTEIN-SERINE-THREONINE KINASES; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SIGNAL TRANSDUCTION; UBIQUITIN-PROTEIN LIGASE COMPLEXES;

SACCHAROMYCETALES;

EID: 77954983991     PISSN: 00219525     EISSN: 00219525     Source Type: Journal    
DOI: 10.1083/jcb.201002026     Document Type: Article

References (56)

1. Amon, A. 2002. Synchronization procedures. Methods Enzymol. 351:457-467. doi:10.1016/S0076-6879(02)51864-4
2. Azzam, R., S.L. Chen, W. Shou, A.S. Mah, G. Alexandru, K. Nasmyth, R.S. Annan, S.A. Carr, and R.J. Deshaies. 2004. Phosphorylation by cyclin B-Cdk underlies release of mitotic exit activator Cdc14 from the nucleolus. Science. 305:516-519. doi:10.1126/science.1099402
3. Bardin, A.J., M.G. Boselli, and A. Amon. 2003. Mitotic exit regulation through distinct domains within the protein kinase Cdc15. Mol. Cell. Biol. 23:5018-5030. doi:10.1128/MCB.23.14.5018-5030.2003
4. Bishop, A.C., O. Buzko, and K.M. Shokat. 2001. Magic bullets for protein kinases. Trends Cell Biol. 11:167-172. doi:10.1016/S0962-8924(01)01928-6
5. Cohen-Fix, O., J.M. Peters, M.W. Kirschner, and D. Koshland. 1996. Anaphase initiation in Saccharomyces cerevisiae is controlled by the APC-dependent degradation of the anaphase inhibitor Pds1p. Genes Dev. 10:3081-3093. doi:10.1101/gad.10.24.3081 (Pubitemid 27020537)
6. Darieva, Z., A. Pic-Taylor, J. Boros, A. Spanos, M. Geymonat, R.J. Reece, S.G. Sedgwick, A.D. Sharrocks, and B.A. Morgan. 2003. Cell cycle-regulated transcription through the FHA domain of Fkh2p and the coactivator Ndd1p. Curr. Biol. 13:1740-1745. doi:10.1016/j.cub.2003.08.053
7. Donovan, J.D., J.H. Toyn, A.L. Johnson, and L.H. Johnston. 1994. P40SDB25, a putative CDK inhibitor, has a role in the M/G1 transition in Saccharomyces cerevisiae. Genes Dev. 8:1640-1653. doi:10.1101/gad.8.14.1640
8. Elia, A.E., L.C. Cantley, and M.B. Yaffe. 2003a. Proteomic screen finds pSer/pThr-binding domain localizing Plk1 to mitotic substrates. Science. 299:1228-1231. doi:10.1126/science.1079079
9. Elia, A.E., P. Rellos, L.F. Haire, J.W. Chao, F.J. Ivins, K. Hoepker, D. Mohammad, L.C. Cantley, S.J. Smerdon, and M.B. Yaffe. 2003b. The molecular basis for phosphodependent substrate targeting and regulation of Plks by the Polo-box domain. Cell. 115:83-95. doi:10.1016/S0092-8674(03)00725-6
10. Geymonat, M., A. Spanos, P.A. Walker, L.H. Johnston, and S.G. Sedgwick. 2003. In vitro regulation of budding yeast Bfa1/Bub2 GAP activity by Cdc5. J. Biol. Chem. 278:14591-14594. doi:10.1074/jbc.C300059200
11. Haase, S.B., and S.I. Reed. 1999. Evidence that a free-running oscillator drives G1 events in the budding yeast cell cycle. Nature. 401:394-397.
12. Haase, S.B., M. Winey, and S.I. Reed. 2001. Multi-step control of spindle pole body duplication by cyclin-dependent kinase. Nat. Cell Biol. 3:38-42. doi:10.1038/35050543
13. Hu, F., and S.J. Elledge. 2002. Bub2 is a cell cycle regulated phospho-protein controlled by multiple checkpoints. Cell Cycle. 1:351-355.
14. Hu, F., Y. Wang, D. Liu, Y. Li, J. Qin, and S.J. Elledge. 2001. Regulation of the Bub2/Bfa1 GAP complex by Cdc5 and cell cycle checkpoints. Cell. 107:655-665. doi:10.1016/S0092-8674(01)00580-3
15. Jaspersen, S.L., J.F. Charles, R.L. Tinker-Kulberg, and D.O. Morgan. 1998. A late mitotic regulatory network controlling cyclin destruction in Saccharomyces cerevisiae. Mol. Biol. Cell. 9:2803-2817.
16. Jin, F., H. Liu, F. Liang, R. Rizkallah, M.M. Hurt, and Y. Wang. 2008. Temporal control of the dephosphorylation of Cdk substrates by mitotic exit pathways in budding yeast. Proc. Natl. Acad. Sci. USA. 105:16177-16182. doi:10.1073/pnas.0808719105
17. Jin, F., D. Richmond, and Y. Wang. 2009. The multilayer regulation of the metaphase-to-anaphase transition. Cell Cycle. 8:700-704.
18. König, C., H. Maekawa, and E. Schiebel. 2010. Mutual regulation of cyclindependent kinase and the mitotic exit network. J. Cell Biol. 188:351-368. doi:10.1083/jcb.200911128
19. Lee, K.S., T.Z. Grenfell, F.R. Yarm, and R.L. Erikson. 1998. Mutation of the polo-box disrupts localization and mitotic functions of the mammalian polo kinase Plk. Proc. Natl. Acad. Sci. USA. 95:9301-9306. doi:10.1073/pnas.95.16. 9301
20. Lee, K.S., S. Song, and R.L. Erikson. 1999. The polo-box-dependent induction of ectopic septal structures by a mammalian polo kinase, plk, in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA. 96:14360-14365. doi:10.1073/pnas.96.25.14360
21. Lu, Y., and F.R. Cross. 2010. Periodic cyclin-Cdk activity entrains an autonomous Cdc14 release oscillator. Cell. 141:268-279. doi:10.1016/j.cell.2010. 03.021
22. Mah, A.S., A.E. Elia, G. Devgan, J. Ptacek, M. Schutkowski, M. Snyder, M.B. Yaffe, and R.J. Deshaies. 2005. Substrate specificity analysis of protein kinase complex Dbf2-Mob1 by peptide library and proteome array screening. BMC Biochem. 6:22. doi:10.1186/1471-2091-6-22
23. McCleland, M.L., and P.H. O'Farrell. 2008. RNAi of mitotic cyclins in Drosophila uncouples the nuclear and centrosome cycle. Curr. Biol. 18:245-254. doi:10.1016/j.cub.2008.01.041
24. Mendenhall, M.D. 1993. An inhibitor of p34CDC28 protein kinase activity from Saccharomyces cerevisiae. Science. 259:216-219. doi:10.1126/science.8421781 (Pubitemid 23041796)
25. Mohl, D.A., M.J. Huddleston, T.S. Collingwood, R.S. Annan, and R.J. Deshaies. 2009. Dbf2-Mob1 drives relocalization of protein phosphatase Cdc14 to the cytoplasm during exit from mitosis. J. Cell Biol. 184:527-539. doi:10.1083/jcb.200812022
26. Morgan, D.O. 2007. The Cell Cycle: Principles of Control. New Science Press/Oxford University Press, London/Sunderland, MA. 297 pp.
27. Mountain, H.A., and C. Korch. 1991. TDH2 is linked to MET3 on chromosome X of Saccharomyces cerevisiae. Yeast. 7:873-880. doi:10.1002/yea.320070814
28. Nasmyth, K. 1996. At the heart of the budding yeast cell cycle. Trends Genet. 12:405-412. doi:10.1016/0168-9525(96)10041-X (Pubitemid 26336483)
29. Nguyen, V.Q., C. Co, and J.J. Li. 2001. Cyclin-dependent kinases prevent DNA re-replication through multiple mechanisms. Nature. 411:1068-1073. doi:10.1038/35082600
30. Novák, B., and J.J. Tyson. 2008. Design principles of biochemical oscillators. Nat. Rev. Mol. Cell Biol. 9:981-991. doi:10.1038/nrm2530
31. Pereira, G., C. Manson, J. Grindlay, and E. Schiebel. 2002. Regulation of the Bfa1p-Bub2p complex at spindle pole bodies by the cell cycle phosphatase Cdc14p. J. Cell Biol. 157:367-379. doi:10.1083/jcb.200112085 (Pubitemid 34839802)
32. Peters, J.M. 2002. The anaphase-promoting complex: proteolysis in mitosis and beyond. Mol. Cell. 9:931-943. doi:10.1016/S1097-2765(02)00540-3
33. Peters, J.M. 2006. The anaphase promoting complex/cyclosome: a machine designed to destroy. Nat. Rev. Mol. Cell Biol. 7:644-656. doi:10.1038/nrm1988
34. Queralt, E., and F. Uhlmann. 2008. Cdk-counteracting phosphatases unlock mitotic exit. Curr. Opin. Cell Biol. 20:661-668. doi:10.1016/j.ceb.2008.09.003
35. Queralt, E., C. Lehane, B. Novak, and F. Uhlmann. 2006. Downregulation of PP2A(Cdc55) phosphatase by separase initiates mitotic exit in budding yeast. Cell. 125:719-732. doi:10.1016/j.cell.2006.03.038
36. Rock, J.M., and A. Amon. 2009. The FEAR network. Curr. Biol. 19:R1063-R1068. doi:10.1016/j.cub.2009.10.002
37. Schwab, M., A.S. Lutum, and W. Seufert. 1997. Yeast Hct1 is a regulator of Clb2 cyclin proteolysis. Cell. 90:683-693. doi:10.1016/S0092-8674(00)80529-2 (Pubitemid 27357960)
38. Schwob, E., T. Böhm, M.D. Mendenhall, and K. Nasmyth. 1994. The B-type cyclin kinase inhibitor p40SIC1 controls the G1 to S transition in S. cerevisiae. Cell. 79:233-244. doi:10.1016/0092-8674(94)90193-7
39. Shirayama, M., W. Zachariae, R. Ciosk, and K. Nasmyth. 1998. The Pololike kinase Cdc5p and the WD-repeat protein Cdc20p/fizzy are regulators and substrates of the anaphase promoting complex in Saccharomyces cerevisiae. EMBO J. 17:1336-1349. doi:10.1093/emboj/17.5.1336 (Pubitemid 28105513)
40. Shirayama, M., A. Tóth, M. Gálová, and K. Nasmyth. 1999. APC(Cdc20) promotes exit from mitosis by destroying the anaphase inhibitor Pds1 and cyclin Clb5. Nature. 402:203-207. doi:10.1038/46080
41. Shou, W., J.H. Seol, A. Shevchenko, C. Baskerville, D. Moazed, Z.W. Chen, J. Jang, A. Shevchenko, H. Charbonneau, and R.J. Deshaies. 1999. Exit from mitosis is triggered by Tem1-dependent release of the protein phosphatase Cdc14 from nucleolar RENT complex. Cell. 97:233-244. doi:10.1016/S0092-8674(00)80733-3 (Pubitemid 29194274)
42. Snead, J.L., M. Sullivan, D.M. Lowery, M.S. Cohen, C. Zhang, D.H. Randle, J. Taunton, M.B. Yaffe, D.O. Morgan, and K.M. Shokat. 2007. A coupled chemical-genetic and bioinformatic approach to Polo-like kinase pathway exploration. Chem. Biol. 14:1261-1272. doi:10.1016/j.chembiol.2007.09.011
43. Stegmeier, F., and A. Amon. 2004. Closing mitosis: the functions of the Cdc14 phosphatase and its regulation. Annu. Rev. Genet. 38:203-232. doi:10.1146/annurev.genet.38.072902.093051
44. Stegmeier, F., R. Visintin, and A. Amon. 2002. Separase, polo kinase, the kinetochore protein Slk19, and Spo12 function in a network that controls Cdc14 localization during early anaphase. Cell. 108:207-220. doi:10.1016/S0092- 8674(02)00618-9 (Pubitemid 34161141)
45. Sullivan, M., and D.O. Morgan. 2007. Finishing mitosis, one step at a time. Nat. Rev. Mol. Cell Biol. 8:894-903. doi:10.1038/nrm2276
46. Surana, U., A. Amon, C. Dowzer, J. McGrew, B. Byers, and K. Nasmyth. 1993. Destruction of the CDC28/CLB mitotic kinase is not required for the metaphase to anaphase transition in budding yeast. EMBO J. 12:1969-1978. (Pubitemid 23157713)
47. Tollervey, D., H. Lehtonen, M. Carmo-Fonseca, and E.C. Hurt. 1991. The small nucleolar RNP protein NOP1 (fibrillarin) is required for pre-rRNA processing in yeast. EMBO J. 10:573-583. (Pubitemid 21905510)
48. Tomson, B.N., R. Rahal, V. Reiser, F. Monje-Casas, K. Mekhail, D. Moazed, and A. Amon. 2009. Regulation of Spo12 phosphorylation and its essential role in the FEAR network. Curr. Biol. 19:449-460. doi:10.1016/j.cub.2009.02.024
49. Visintin, R., S. Prinz, and A. Amon. 1997. CDC20 and CDH1: a family of substrate-specific activators of APC-dependent proteolysis. Science. 278:460-463. doi:10.1126/science.278.5337.460 (Pubitemid 27454429)
50. Visintin, R., K. Craig, E.S. Hwang, S. Prinz, M. Tyers, and A. Amon. 1998. The phosphatase Cdc14 triggers mitotic exit by reversal of Cdk-dependent phosphorylation. Mol. Cell. 2:709-718. doi:10.1016/S1097-2765(00)80286-5
51. Visintin, R., E.S. Hwang, and A. Amon. 1999. Cfi1 prevents premature exit from mitosis by anchoring Cdc14 phosphatase in the nucleolus. Nature. 398:818-823. doi:10.1038/19775
52. Visintin, R., F. Stegmeier, and A. Amon. 2003. The role of the polo kinase Cdc5 in controlling Cdc14 localization. Mol. Biol. Cell. 14:4486-4498. doi:10.1091/mbc.E03-02-0095
53. Visintin, C., B.N. Tomson, R. Rahal, J. Paulson, M. Cohen, J. Taunton, A. Amon, and R. Visintin. 2008. APC/C-Cdh1-mediated degradation of the Polo kinase Cdc5 promotes the return of Cdc14 into the nucleolus. Genes Dev. 22:79-90. doi:10.1101/gad.1601308
54. Yoshida, S., and A. Toh-e. 2002. Budding yeast Cdc5 phosphorylates Net1 and assists Cdc14 release from the nucleolus. Biochem. Biophys. Res. Commun. 294:687-691. doi:10.1016/S0006-291X(02)00544-2
55. Zachariae, W., M. Schwab, K. Nasmyth, and W. Seufert. 1998. Control of cyclin ubiquitination by CDK-regulated binding of Hct1 to the anaphase promoting complex. Science. 282:1721-1724. doi:10.1126/science.282.5394.1721
56. Zhang, C., D.M. Kenski, J.L. Paulson, A. Bonshtien, G. Sessa, J.V. Cross, D.J. Templeton, and K.M. Shokat. 2005. A second-site suppressor strategy for chemical genetic analysis of diverse protein kinases. Nat. Methods. 2:435-441. doi:10.1038/nmeth764