Mitotic exit in the absence of separase activity

Molecular Biology of the Cell

Volumn 20, Issue 5, 2009, Pages 1576-1591

  Lu, Ying ^a   Cross, Frederick ^a  

^a ROCKEFELLER UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COHESIN; PHOSPHOPROTEIN PHOSPHATASE CDC14; SEPARASE;

ARTICLE; CHROMATID; ENZYME ACTIVITY; MICROTUBULE; MITOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION;

CELL CYCLE PROTEINS; CHROMATIDS; CHROMOSOMAL PROTEINS, NON-HISTONE; CYCLIN-DEPENDENT KINASES; ENDOPEPTIDASES; MITOSIS; MITOTIC SPINDLE APPARATUS; NUCLEAR PROTEINS; PROTEIN TRANSPORT; PROTEIN TYROSINE PHOSPHATASES; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

SACCHAROMYCETALES;

EID: 65249101389     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E08-10-1042     Document Type: Article

References (73)

1. Alexandria, G., Zachariae, W., Schleiffer, A., and Nasmyth, K. (1999). Sister chromatid separation and chromosome re-duplication are regulated by different mechanisms in response to spindle damage. EMBO J. 18, 2707-2721.
2. Asakawa, K., and Toh-e, A. (2002). A defect of Kap104 alleviates the requirement of mitotic exit network gene functions in Saccharomyces cerevisiae. Genetics 162, 1545-1556.
3. Azzam, R., Chen, S. L., Shou, W., Mah, A. S., Alexandru, G., Nasmyth, K., Annan, R. S., Carr, S. A., and Deshaies, R. J. (2004). Phosphorylation by cyclin
4. B-Cdk underlies release of mitotic exit activator Cdc14 from the nucleolus. Science 305, 516-519.
5. Bachant, J., Jessen, S. R., Kavanaugh, S. E., and Fielding, C. S. (2005). The yeast S phase checkpoint enables replicating chromosomes to bi-orient and restrain spindle extension during S phase distress. J. Cell Biol. 168, 999-1012.
6. Bardin, A. J., Visintin, R., and Amon, A. (2000). A mechanism for coupling exit from mitosis to partitioning of the nucleus. Cell 102, 21-31.
7. Bean, J. M., Siggia, E. D., and Cross, F. R. (2006). Coherence and timing of cell cycle start examined at single-cell resolution. Mol. Cell 21, 3-14.
8. Bembenek, J., Kang, J., Kurischko, C., Li, B., Raab, J. R., Belanger, K. D., Luca, F. C., and Yu, H. (2005). Crm1-mediated nuclear export of Cdc14 is required for the completion of cytokinesis in budding yeast. Cell Cycle 4, 961-971.
9. Bi, E., Maddox, P., Lew, D. J., Salmon, E. D., McMillan, J. N., Yeh, E., and Pringle, J. R. (1998). Involvement of an actomyosin contractile ring in Saccha- romyces cerevisiae cytokinesis. J Cell Biol. 142, 1301-1312.
10. Charvin, G., Cross, F. R., and Siggia, E. D. (2008). A microfluidic device for temporally controlled gene expression and long-term fluorescent imaging in unperturbed dividing yeast cells. PLoS ONE 3, e1468.
11. Chen, C. T., Feoktistova, A., Chen, J. S., Shim, Y. S., Clifford, D. M., Gould, K. L., and McCollum, D. (2008). The SIN kinase Sid2 regulates cytoplasmic retention of the S. pombe Cdc14-like phosphatase Clp1. Curr. Biol. 18, 1594-1599.
12. Cohen-Fix, O., Peters, J. M., Kirschner, M. W., and Koshland, D. (1996). Anaphase initiation in Saccharomyces cerevisiae is controlled by the APC- dependent degradation of the anaphase inhibitor Pds1p. Genes Dev. 10, 3081-3093.
13. D'Amours, D., Stegmeier, F., and Amon, A. (2004). Cdc14 and condensin control the dissolution of cohesin-independent chromosome linkages at repeated DNA. Cell 117, 455-469.
14. Eluere, R., Offner, N., Varlet, I., Motteux, O., Signon, L., Picard, A., Bailly, E., and Simon, M. N. (2007). Compartmentalization of the functions and regulation of the mitotic cyclin Clb2 in S. cerevisiae. J. Cell Sci. 120, 702-711.
15. Epstein, C. B., and Cross, F. R. (1992). CLB 5, a novel B cyclin from budding yeast with a role in S phase. Genes Dev. 6, 1695-1706.
16. Fitch, I., Dahmann, C., Surana, U., Amon, A., Nasmyth, K., Goetsch, L., Byers, B., and Futcher, B. (1992). Characterization of four B-type cyclin genes of the budding yeast Saccharomyces cerevisiae. Mol. Biol. Cell 3, 805-818.
17. Gadal, O., Strauss, D., Kessl, J., Trumpower, B., Tollervey, D., and Hurt, E. (2001). Nuclear export of 60s ribosomal subunits depends on Xpo1p and requires a nuclear export sequence-containing factor, Nmd3p, that associates with the large subunit protein Rpl10p. Mol. Cell. Biol. 21, 3405-3415.
18. Higuchi, T., and Uhlmann, F. (2005). Stabilization of microtubule dynamics at anaphase onset promotes chromosome segregation. Nature 433, 171-176.
19. Hirano, T., Funahashi, S. I., Uemura, T., and Yanagida, M. (1986). Isolation and characterization of Schizosaccharomyces pombe cutmutants that block nuclear division but not cytokinesis. EMBO J. 5, 2973-2979.
20. Hofken, T., and Schiebel, E. (2002). A role for cell polarity proteins in mitotic exit. EMBO J. 21, 4851-4862.
21. Holt, L. J., Krutchinsky, A. N., and Morgan, D. O. (2008). Positive feedback sharpens the anaphase switch. Nature 454, 353-357.
22. Hwang,L. H.,Lau,L. F.,Smith,D. L.,Mistrot,C. A.,Hardwick,K. G.,Hwang, E. S., Amon, A., and Murray, A. W. (1998). Budding yeast Cdc 20, a target of the spindle checkpoint. Science 279, 1041-1044.
23. Jaspersen, S. L., Charles, J. F., and Morgan, D. O. (1999). Inhibitory phosphor- ylation of the APC regulator Hct1 is controlled by the kinase Cdc28 and the phosphatase Cdc14. Curr. Biol. 9, 227-236.
24. Jaspersen, S. L., Charles, J. F., Tinker-Kulberg, R. L., and Morgan, D. O. (1998). A late mitotic regulatory network controlling cyclin destruction in Saccharo- myces cerevisiae. Mol. Biol. Cell 9, 2803-2817.
25. Jaspersen, S. L., and Morgan, D. O. (2000). Cdc14 activates cdc15 to promote mitotic exit in budding yeast. Curr. Biol. 10, 615-618.
26. Jensen, S., Segal, M., Clarke, D. J., and Reed, S. I. (2001). A novel role of the budding yeast separin Esp1 in anaphase spindle elongation: evidence that proper spindle association of Esp1 is regulated by Pds1. J. Cell Biol. 152, 27-40.
27. Khmelinskii, A., Lawrence, C., Roostalu, J., and Schiebel, E. (2007). Cdc14- regulated midzone assembly controls anaphase B. J. Cell Biol. 177, 981-993.
28. Kim, S. H., Lin, D. P., Matsumoto, S., Kitazono, A., and Matsumoto, T. (1998). Fission yeast Slp 1, an effector of the Mad2-dependent spindle checkpoint. Science 279, 1045-1047.
29. Koch, C., and Nasmyth, K. (1994). Cell cycle regulated transcription in yeast. Curr. Opin. Cell Biol. 6, 451-459.
30. Lew, D. J., and Reed, S. I. (1993). Morphogenesis in the yeast cell cycle: regulation by Cdc28 and cyclins. J. Cell Biol. 120, 1305-1320.
31. Lim, H. H., Goh, P. Y., and 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.
32. Menssen, R., Neutzner, A., and Seufert, W. (2001). Asymmetric spindle pole localization of yeast Cdc15 kinase links mitotic exit and cytokinesis. Curr. Biol. 11, 345-350.
33. Michaelis, C., Ciosk, R., and Nasmyth, K. (1997). Cohesins: chromosomal proteins that prevent premature separation of sister chromatids. Cell 91, 35-45.
34. Molk, J. N., Schuyler, S. C., Liu, J. Y., Evans, J. G., Salmon, E. D., Pellman, D., and Bloom, K. (2004). The differential roles of budding yeast Tem1p, Cdc15p, and Bub2p protein dynamics in mitotic exit. Mol. Biol. Cell 15, 1519-1532.
35. Mumberg, D., Muller, R., and Funk, M. (1994). Regulatable promoters of Saccharomyces cerevisiae: comparison of transcriptional activity and their use for heterologous expression. Nucleic Acids Res. 22, 5767-5768.
36. Padmashree, C. G., and Surana, U. (2001). Cdc28-Clb mitotic kinase negatively regulates bud site assembly in the budding yeast. J. Cell Sci. 114, 207-218.
37. Palmer, R. E., Koval, M., and Koshland, D. (1989). The dynamics of chromosome movement in the budding yeast Saccharomyces cerevisiae. J. Cell Biol. 109, 3355-3366.
38. Pereira, G., Manson, C., Grindlay, J., and Schiebel, E. (2002). Regulation of the Bfa1p-Bub2p complex at spindle pole bodies by the cell cycle phosphatase Cdc14p. J. Cell Biol. 157, 367-379.
39. Pereira, G., and Schiebel, E. (2003). Separase regulates INCENP-Aurora B anaphase spindle function through Cdc14. Science 302, 2120-2124.
40. Queralt, E., Lehane, C., Novak, B., and Uhlmann, F. (2006). Downregulation of PP2A(Cdc55) phosphatase by separase initiates mitotic exit in budding yeast. Cell 125, 719-732.
41. Rahal, R., and Amon, A. (2008). Mitotic CDKs control the metaphase- anaphase transition and trigger spindle elongation. Genes Dev. 22, 1534-1548.
42. Rodrigues, F., van Hemert, M., Steensma, H. Y., Corte-Real, M., and Leao, C. (2001). Red fluorescent protein (DsRed) as a reporter in Saccharomyces cerevisiae. J. Bacteriol. 183, 3791-3794.
43. Ross, K. E., and Cohen-Fix, O. (2004). A role for the FEAR pathway in nuclear positioning during anaphase. Dev. Cell 6, 729 -735.
44. Schwab, M., Lutum, A. S., and Seufert, W. (1997). Yeast Hct1 is a regulator of Clb2 cyclin proteolysis. Cell 90, 683-693.
45. Schwob, E.,Bohm,T.,Mendenhall,M. D.,and Nasmyth, K. (1994). The B-type cyclin kinase inhibitor p40SIC1 controls the G1 to S transition in S. cerevisiae. Cell 79, 233-244.
46. Severin, F., Hyman, A. A., and Piatti, S. (2001). Correct spindle elongation at the metaphase/anaphase transition is an APC-dependent event in budding yeast. J. Cell Biol. 155, 711-718.
47. Shirayama, M., Toth, A., Galova, M., and Nasmyth, K. (1999). APC(Cdc20) promotes exit from mitosis by destroying the anaphase inhibitor Pds1 and cyclin Clb5. Nature 402, 203-207.
48. Shou, W., and Deshaies, R. J. (2002). Multiple telophase arrest bypassed (tab) mutants alleviate the essential requirement for Cdc15 in exit from mitosis in S. cerevisiae. BMC Genet. 3,4.
49. Shou,W.,Seol,J. H.,Shevchenko,A.,Baskerville,C.,Moazed,D.,Chen,Z. W., Jang, J., Shevchenko, A., Charbonneau, H., and Deshaies, R. J. (1999). Exit from mitosis is triggered by Tem1-dependent release of the protein phosphatase Cdc14 from nucleolar RENT complex. Cell 97, 233-244.
50. Skotheim, J. M., Di Talia, S., Siggia, E. D., and Cross, F. R. (2008). Positive feedback of G1 cyclins ensures coherent cell cycle entry. Nature 454, 291-296.
51. Spellman, P. T., Sherlock, G., Zhang, M. Q., Iyer, V. R., Anders, K., Eisen, M. B., Brown, P. O., Botstein, D., and Futcher, B. (1998). Comprehensive identification of cell cycle-regulated genes of the yeast Saccharomyces cerevisiae by microarray hybridization. Mol. Biol. Cell 9, 3273-3297.
52. Stegmeier, F., and Amon, A. (2004). Closing mitosis: the functions of the Cdc14 phosphatase and its regulation. Annu. Rev. Genet. 38, 203-232.
53. Stegmeier, F., Visintin, R., and 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.
54. Sullivan, M., Higuchi, T., Katis, V. L., and Uhlmann, F. (2004). Cdc14 phosphatase induces rDNA condensation and resolves cohesin-independent cohesion during budding yeast anaphase. Cell 117, 471-482.
55. Sullivan, M., and Uhlmann, F. (2003). A non-proteolytic function of separase links the onset of anaphase to mitotic exit. Nat. Cell Biol. 5, 249-254.
56. Thornton, B. R., and Toczyski, D. P. (2003). Securin and B-cyclin/CDK are the only essential targets of the APC. Nat. Cell Biol. 5, 1090-1094.
57. Tinker-Kulberg, R. L., and Morgan, D. O. (1999). Pds1 and Esp1 control both anaphase and mitotic exit in normal cells and after DNA damage. Genes Dev. 13, 1936-1949.
58. Trautmann, S., Wolfe, B. A., Jorgensen, P., Tyers, M., Gould, K. L., and McCollum, D. (2001). Fission yeast Clp1p phosphatase regulates G2/M transition and coordination of cytokinesis with cell cycle progression. Curr. Biol. 11, 931-940.
59. Uhlmann, F., Lottspeich, F., and Nasmyth, K. (1999). Sister-chromatid separation at anaphase onset is promoted by cleavage of the cohesin subunit Scc1. Nature 400, 37-42.
60. Uhlmann, F., Wernic, D., Poupart, M. A., Koonin, E. V., and Nasmyth, K. (2000). Cleavage of cohesin by the CD clan protease separin triggers anaphase in yeast. Cell 103, 375-386.
61. Verma, R., Annan, R. S., Huddleston, M. J., Carr, S. A., Reynard, G., and Deshaies, R. J. (1997). Phosphorylation of Sic1p by G1 Cdk required for its degradation and entry into S phase. Science 278, 455-460.
62. Visintin, C., Tomson, B. N., Rahal, R., Paulson, J., Cohen, M., Taunton, J., Amon, A., and 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.
63. Visintin, R., Prinz, S., and Amon, A. (1997). CDC20 and CDH1: a family of substrate-specific activators of APC-dependent proteolysis. Science 278, 460-463.
64. Visintin, R., Craig, K., Hwang, E. S., Prinz, S., Tyers, M., and Amon, A. (1998). The phosphatase Cdc14 triggers mitotic exit by reversal of Cdk-dependent phosphorylation. Mol. Cell 2, 709-718.
65. Visintin, R., Hwang, E. S., and Amon, A. (1999). Cfi1 prevents premature exit from mitosis by anchoring Cdc14 phosphatase in the nucleolus. Nature 398, 818-823.
66. Visintin, R., Stegmeier, F., and Amon, A. (2003). The role of the polo kinase Cdc5 in controlling Cdc14 localization. Mol. Biol. Cell 14, 4486-4498.
67. Wasch, R., and Cross, F. R. (2002). APC-dependent proteolysis of the mitotic cyclin Clb2 is essential for mitotic exit. Nature 418, 556-562.
68. Wirth, K. G., et al. (2006). Separase: a universal trigger for sister chromatid disjunction but not chromosome cycle progression. J. Cell Biol. 172, 847- 860.
69. Yamamoto, A., Guacci, V., and Koshland, D. (1996). Pds1p, an inhibitor of anaphase in budding yeast, plays a critical role in the APC and checkpoint pathway(s). J. Cell Biol. 133, 99-110.
70. Yeh, E., Skibbens, R. V., Cheng, J. W., Salmon, E. D., and Bloom, K. (1995). Spindle dynamics and cell cycle regulation of dynein in the budding yeast, Saccharomyces cerevisiae. J. Cell Biol. 130, 687-700.
71. Yeong, F. M., Lim, H. H., Padmashree, C. G., and 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.
72. Yoshida, S., Asakawa, K., and Toh-e, A. (2002). Mitotic exit network controls the localization of Cdc14 to the spindle pole body in Saccharomyces cerevisiae. Curr. Biol. 12, 944-950.
73. Zeng, X., Kahana, J. A., Silver, P. A., Morphew, M. K., Mcintosh, J. R., Fitch, I. T., Carbon, J., and Saunders, W. S. (1999). Slk19p is a centromere protein that functions to stabilize mitotic spindles. J. Cell Biol. 146, 415-425.