Computational modelling of mitotic exit in budding yeast: The role of separase and Cdc14 endocycles

Journal of the Royal Society Interface

Volumn 8, Issue 61, 2011, Pages 1128-1141

  Vinod, P K ^a   Freire, Paula ^a,b   Rattani, Ahmed ^a   Ciliberto, Andrea ^c   Uhlmann, Frank ^d   Novak, Bela ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b INSTITUTO GULBENKIAN DE CIÊNCIA   (Portugal)

^c FIRC INSTITUTE OF MOLECULAR ONCOLOGY   (Italy)

^d CRUK London Research Institute   (United Kingdom)

Author keywords

Budding yeast; Endocycles; Mathematical model; Mitotic exit; Oscillation

Indexed keywords

BUDDING YEAST; COMPLEX REGULATORY NETWORK; COMPREHENSIVE SYSTEM; COMPUTATIONAL MODELLING; CRITICAL NODE; CYCLIN-DEPENDENT KINASE; ENDOCYCLES; EUKARYOTIC CELL CYCLE; INTUITIVE REASONING; MATHEMATICAL MODELLING; MITOTIC EXIT; OPERATING PRINCIPLES; OSCILLATION; REGULATORY NETWORK; SYSTEMATIC ANALYSIS;

NUMERICAL ANALYSIS; YEAST;

MATHEMATICAL MODELS;

CELL CYCLE PROTEIN 20; CYCLIN B2; CYCLIN DEPENDENT KINASE; PHOSPHOPROTEIN PHOSPHATASE CDC14; SEPARASE;

ARTICLE; ENZYME ACTIVITY; EUKARYOTIC CELL; GENE REGULATORY NETWORK; MATHEMATICAL COMPUTING; MATHEMATICAL MODEL; MITOSIS; OSCILLATION; PROTEIN DEGRADATION; PROTEIN FUNCTION; YEAST;

BIOLOGICAL CLOCKS; CELL CYCLE PROTEINS; ENDOPEPTIDASES; MITOSIS; MODELS, BIOLOGICAL; PROTEIN TYROSINE PHOSPHATASES; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EUKARYOTA; SACCHAROMYCETALES;

EID: 79960078600     PISSN: 17425689     EISSN: 17425662     Source Type: Journal    
DOI: 10.1098/rsif.2010.0649     Document Type: Article

References (46)

1. Morgan, D. O. 2007 The cell cycle: principles of control. London, UK: New Science Press.
2. Bloom, J. & Cross, F. R. 2007 Multiple levels of cyclin specificity in cell-cycle control. Nat. Rev. Mol. Cell. Biol. 8, 149-160. (doi:10.1038/nrm2105)
3. Mortensen, E. M., Haas, W., Gygi, M., Gygi, S. P. & Kellogg, D. R. 2005 Cdc28-dependent regulation of the Cdc5/Polo kinase. Curr. Biol. 15, 2033-2037. (doi:10.1016/j.cub.2005.10.046)
4. Queralt, E. & Uhlmann, F. 2008 Cdk-counteracting phosphatases unlock mitotic exit. Curr. Opin. Cell. Biol. 20, 661-668. (doi:10.1016/j.ceb.2008.09. 003)
5. D'Amours, D. & Amon, A. 2004 At the interface between signaling and executing anaphase-Cdc14 and the FEAR network. Genes Dev. 18, 2581-2595. (doi:10.1101/gad.1247304)
6. Bardin, A. J., Visintin, R. & Amon, A. 2000 A mechanism for coupling exit from mitosis to partitioning of the nucleus. Cell 102, 21-31. (doi:10.1016/S0092-8674(00)00007-6)
7. Stegmeier, F., Visintin, R. & Amon, A. 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)
8. Sullivan, M. & Uhlmann, F. 2003 A non-proteolytic function of separase links the onset of anaphase to mitotic exit. Nat. Cell. Biol. 5, 249-254. (doi:10.1038/ncb940)
9. Pereira, G., Hofken, T., Grindlay, J., Manson, C. & Schiebel, E. 2000 The Bub2p spindle checkpoint links nuclear migration with mitotic exit. Mol. Cell. 6, 1-10. (doi:10.1016/S1097-2765(00)00002-2)
10. Uhlmann, F., Wernic, D., Poupart, M. A., Koonin, E. V. & Nasmyth, K. 2000 Cleavage of cohesin by the CD clan protease separin triggers anaphase in yeast. Cell 103, 375-386. (doi:10.1016/S0092-8674(00)00130-6)
11. Queralt, E., Lehane, C., Novak, B. & Uhlmann, F. 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)
12. Toth, A., Queralt, E., Uhlmann, F. & Novak, B. 2007 Mitotic exit in two dimensions. J. Theor. Biol. 248, 560-573. (doi:10.1016/j.jtbi.2007.06.014)
13. Lu, Y. & Cross, F. R. 2010 Periodic cyclin-Cdk activity entrains an autonomous Cdc14 release oscillator. Cell 141, 268-279. (doi:10.1016/j.cell. 2010.03.021)
14. Manzoni, R., Montani, F., Visintin, C., Ciliberto, A. & Visintin, R. 2010 Oscillations in Cdc14 release and sequestration reveal the circuit underlying mitotic exit. J. Cell. Biol. 190, 209-222. (doi:10.1083/jcb. 201002026)
15. Knapp, D., Bhoite, L., Stillman, D. J. & Nasmyth, K. 1996 The transcription factor Swi5 regulates expression of the cyclin kinase inhibitor p40SIC1. Mol. Cell. Biol. 16, 5701-5707.
16. Toyn, J. H., Johnson, A. L., Donovan, J. D., Toone, W. M. & Johnston, L. H. 1997 The Swi5 transcription factor of Saccharomyces cerevisiae has a role in exit from mitosis through induction of the cdk-inhibitor Sic1 in telophase. Genetics 145, 85-96.
17. Moll, T., Tebb, G., Surana, U., Robitsch, H. & Nasmyth, K. 1991 The role of phosphorylation and the CDC28 protein kinase in cell cycle-regulated nuclear import of the S. cerevisiae transcription factor SWI5. Cell 66, 743-758. (doi:10.1016/0092-8674(91)90118-I)
18. Verma, R., Annan, R. S., Huddleston, M. J., Carr, S. A., Reynard, G. & Deshaies, R. J. 1997 Phosphorylation of Sic1p by G1 Cdk required for its degradation and entry into S phase. Science 278, 455-460. (doi:10.1126/science. 278.5337.455)
19. Donovan, J. D., Toyn, J. H., Johnson, A. L. & Johnston, L. H. 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)
20. Schwob, E., Bohm, T., Mendenhall, M. D. & Nasmyth, K. 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)
21. Mendenhall, M. D., al-Jumaily, W. & Nugroho, T. T. 1995 The Cdc28 inhibitor p40SIC1. Prog. Cell Cycle Res. 1, 173-185.
22. Shirayama, M., Toth, A., Galova, M. & Nasmyth, K. 1999 APC(Cdc20) promotes exit from mitosis by destroying the anaphase inhibitor Pds1 and cyclin Clb5. Nature 402, 203-207. (doi:10.1038/46080)
23. Amon, A., Tyers, M., Futcher, B. & Nasmyth, K. 1993 Mechanisms that help the yeast cell cycle clock tick: G2 cyclins transcriptionally activate G2 cyclins and repress G1 cyclins. Cell 74, 993-1007. (doi:10.1016/0092-8674(93) 90722-3)
24. Chen, K. C., Csikasz-Nagy, A., Gyorffy, B., Val, J., Novak, B. & Tyson, J. J. 2000 Kinetic analysis of a molecular model of the budding yeast cell cycle. Mol. Biol. Cell 11, 369-391.
25. Chen, K. C., Calzone, L., Csikasz-Nagy, A., Cross, F. R., Novak, B. & Tyson, J. J. 2004 Integrative analysis of cell cycle control in budding yeast. Mol. Biol. Cell 15, 3841-3862. (doi:10.1091/mbc.E03-11-0794)
26. Shou, W. et al. 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)
27. Visintin, R., Hwang, E. S. & Amon, A. 1999 Cfi1 prevents premature exit frommitosis by anchoring Cdc14 phosphatase in the nucleolus. Nature 398, 818-823. (doi:10.1038/19775)
28. Azzam, R., Chen, S. L., Shou, W., Mah, A. S., Alexandru, G., Nasmyth, K., Annan, R. S., Carr, S. A. & Deshaies, R. J. 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)
29. Lu, Y. & Cross, F. 2009 Mitotic exit in the absence of separase activity. Mol. Biol. Cell. 20, 1576-1591. (doi:10.1091/mbc.E08-10-1042)
30. Mohl, D. A., Huddleston, M. J., Collingwood, T. S., Annan, R. S. & Deshaies, R. J. 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)
31. Goldbeter, A. & Koshland Jr, D. E. 1981 An amplified sensitivity arising from covalent modification in biological systems. Proc. Natl Acad. Sci. USA 78, 6840-6844. (doi:10.1073/pnas.78.11.6840)
32. Nasmyth, K., Peters, J. M. & Uhlmann, F. 2000 Splitting the chromosome: cutting the ties that bind sister chromatids. Science 288, 1379-1385. (doi:10.1126/science.288.5470.1379)
33. Visintin, R., Craig, K., Hwang, E. S., Prinz, S., Tyers, M. & Amon, A. 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)
34. Stegmeier, F. & Amon, A. 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)
35. Drapkin, B. J., Lu, Y., Procko, A. L., Timney, B. L. & Cross, F. R. 2009 Analysis of the mitotic exit control system using locked levels of stable mitotic cyclin. Mol. Syst. Biol. 5, 328. (doi:10.1038/msb.2009.78)
36. Yeong, F. M., Lim, H. H., Padmashree, C. G. & Surana, U. 2000 Exit from mitosis in budding yeast: biphasic inactivation of the Cdc28-Clb2 mitotic kinase and the role of Cdc20. Mol. Cell. 5, 501-511. (doi:10.1016/S1097-2765(00) 80444-X)
37. Schwab, M., Lutum, A. S. & Seufert, W. 1997 Yeast Hct1 is a regulator of Clb2 cyclin proteolysis. Cell 90, 683-693. (doi:10.1016/S0092-8674(00)80529- 2)
38. Wasch, R. & Cross, F. R. 2002 APC-dependent proteolysis of the mitotic cyclin Clb2 is essential for mitotic exit. Nature 418, 556-562. (doi:10.1038/nature00856)
39. Lim, H. H., Goh, P. Y. & Surana, U. 1998 Cdc20 is essential for the cyclosome-mediated proteolysis of both Pds1 and Clb2 during M phase in budding yeast. Curr. Biol. 8, 231-234. (doi:10.1016/S0960-9822(98)70088-0)
40. Thornton, B. R. & Toczyski, D. P. 2003 Securin and B-cyclin/CDK are the only essential targets of the APC. Nat. Cell. Biol. 5, 1090-1094. (doi:10.1038/ncb1066)
41. Jaspersen, S. L., Charles, J. F., Tinker-Kulberg, R. L. & Morgan, D. O. 1998 A late mitotic regulatory network controlling cyclin destruction in Saccharomyces cerevisiae. Mol. Biol. Cell 9, 2803-2817.
42. Jaspersen, S. L. & Morgan, D. O. 2000 Cdc14 activates cdc15 to promote mitotic exit in budding yeast. Curr. Biol. 10, 615-618. (doi:10.1016/S0960-9822(00)00491-7)
43. Cohen-Fix, O. & Koshland, D. 1999 Pds1p of budding yeast has dual roles: inhibition of anaphase initiation and regulation of mitotic exit. Genes Dev. 13, 1950-1959. (doi:10.1101/gad.13.15.1950)
44. Sullivan, M., Holt, L. & Morgan, D. O. 2008 Cyclin-specific control of ribosomal DNA segregation. Mol. Cell. Biol. 28, 5328-5336. (doi:10.1128/MCB.00235-08)
45. Tyson, J. J. & Novak, B. 2008 Temporal organization of the cell cycle. Curr. Biol. 18, R759-R768. (doi:10.1016/j.cub.2008.07.001)
46. Visintin, C., Tomson, B. N., Rahal, R., Paulson, J., Cohen, M., Taunton, J., Amon, A. & Visintin, R. 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)