Pds1 and Esp1 control both anaphase and mitotic exit in normal cells and after DNA damage

Genes and Development

Volumn 13, Issue 15, 1999, Pages 1936-1949

  Tinker Kulbetg, Rachel L ^a   Morgan, David O ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

APC; Cyclin; DNA damage; Esp1; Mitotic exit; Pds1

Indexed keywords

CELL CYCLE PROTEIN; CYCLINE; INHIBITOR PROTEIN; INHIBITOR PROTEIN PDS1; PROTEIN; PROTEIN ESP1; UNCLASSIFIED DRUG;

ANAPHASE; ARTICLE; CYTOKINESIS; DNA DAMAGE; METAPHASE; MITOSIS; MITOSIS INHIBITION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; SISTER CHROMATID EXCHANGE; YEAST;

EID: 0033179736     PISSN: 08909369     EISSN: None     Source Type: Journal    
DOI: 10.1101/gad.13.15.1936     Document Type: Article

References (67)

1. Alexandria, G., W. Zachariae, A. Schleiffer, and K. Nasmyth. 1999. Sister chromatid separation and chromosome re-duplication are regulated by different mechanisms in response to spindle damage. EMBO J. 18: 2707-2721.
2. CDC28 tyrosine phosphorylation is not required for entry into mitosis in S. cerevisiae. Nature 355: 368-371.
3. Charles, J.F., S.L. Jaspersen, R.L. Tinker-Kulberg, L. Hwang, A. Szidon, and D.O. Morgan. 1998. The Polo-related kinase Cdc5 activates and is destroyed by the mitotic cyclin destruction machinery in S. cerevisiae. Curr. Biol. 8: 497-507.
4. Ciosk, R., W. Zachariae, C. Michaelis, A. Shevchenko, M. Mann, and K. Nasmyth. 1998. An ESP1/PDS1 complex regulates loss of sister chromatid cohesion at the metaphase to anaphase transition in yeast. Cell 93: 1067-1076.
5. Cohen-Fix, O. and D. Koshland. 1997. The anaphase inhibitor of Saccharomyces cerevisiae Pds1p is a target of the DNA damage checkpoint pathway. Proc. Natl. Acad. Sci. 94: 14361-14366.
6. 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 Pdslp. Genes & Dev. 10: 3081-3093.
7. SDB25, a putative CDK inhibitor, has a role in the M/G1 transition in Saccharomyces cerevisiae. Genes & Dev. 8: 1640-1653.
8. Elledge, S.J. 1996. Cell cycle checkpoints: Preventing an identity crisis. Science 274: 1664-1672.
9. Fang, G., H. Yu, and M.W. Kirschner. 1998. Direct binding of CDC20 protein family members activates the anaphase-promoting complex in mitosis and G1 Mol. Cell 2: 163-171.
10. Fesquet, D., P.J. Fitzpatrick, A.L. Johnson, K.M. Kramer, J.H. Toyn, and L.H. Johnston. 1999. A Bub2p-dependent spindle checkpoint pathway regulates the Dbf2 kinase in budding yeast. EMBO J. 18: 2424-2434.
11. Funabiki, H., K. Kumada, and M. Yanagida. 1996. Fission yeast Cut1 and Cut2 are essential for sister chromatid separation, concentrate along the metaphase spindle and form large complexes. EMBO J. 15: 6617-6628.
12. Gerber, M.R., A. Farrell, R. Deshaies, I. Herskowitz, and D.O. Morgan. 1995. Cdc37 is required for association of the protein kinase Cdc28 with Gl and mitotic cyclins. Proc. Natl. Acad. Sci. 92: 4651-4655.
13. Glotzer, M., A.W. Murray, and M.W. Kirschner. 1991. Cyclin is degraded by the ubiquitin pathway. Nature 349: 132-138.
14. Guthrie, C. and G.R. Fink, ed. 1991. Guide to yeast genetics and molecular biology. Methods in enzymology. Academic Press, San Diego, CA.
15. Hardwick, K.G. and A.W. Murray. 1995. Mad1p, a phosphoprotein component of the spindle assembly checkpoint in budding yeast. J. Cell Biol. 131: 709-720.
16. Hartwell, L.H. and T.A. Weinert. 1989. Checkpoints: Controls that ensure the order of cell cycle events. Science 246: 629-634.
17. Hershko, A. 1997. Roles of ubiquitin-mediated pioteolysis in cell cycle control, Curr. Opin. Cell Biol. 9: 788-799.
18. Hershko, A., D. Ganoth, V. Sudakin, A. Dahan, L.H. Cohen, F.C. Luca, J.V. Ruderman, and E. Eytan. 1994. Components of a system that ligates cyclin to ubiquitin and their regulation by the protein kinase cdc2. J. Biol. Chem. 269: 4940-4946.
19. Holloway, S.L., M. Glotzer, R.W. King, and A.W. Murray. 1993. Anaphase is initiated by proteolysis rather than by the inactivation of maturation-promoting factor. Cell 73: 1393-1402.
20. Hwang, L.H., L.F. Lau, D.L. Smith, C.A. Mistrot, K.G. Hardwick, E.S. Hwang, A. Amon, and A.W. Murray. 1998. Budding yeast Cdc20: A target of the spindle checkpoint. Science 279: 1041-1044.
21. Irniger, S., S. Piatti, C. Michaelis, and K. Nasmyth. 1995. Genes involved in sister chromatid separation are needed for B-type cyclin proteolysis in budding yeast. Cell 81: 269-277.
22. 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.
23. Jaspersen, S.L., J.F. Charles, and D.O. Morgan. 1999. Inhibitory phosphorylation of the APC regulator Hct1 is controlled by the kinase Cdc28 and the phosphatase Cdc14. Curr. Biol. 9: 227-236.
24. Kaytor, M.D, and D.M. Livingston. 1994. Saccharomyces cerevisiae RAD52 alleles temperature-sensitive for the repair of DNA double-strand breaks. Genetics 137: 933-944.
25. Kim, S.H., D.P. Lin, S. Matsumoto, A. Kitazono, and T. Matsumoto. 1998. Fission yeast Slp1: An effector of the Mad2-dependent spindle checkpoint. Science 279: 1045-1047.
26. King, R.W., J.-M. Peters, S. Tugendreich, M. Rolfe, P. Hieter, and M.W. Kirschner. 1995. A 20S complex containing CDC27 and CDC16 catalyzes the mitosis-specific conjugation of ubiquitin to cyclin B. Cell 81: 279-288.
27. 1 cell cycle mutant gene dbf4 encodes a protein kinase and is identified as CDC5. Mol. Cell. Biol. 13: 4445-4457.
28. Kotani, S., S. Tugendreich, M. Fujii, P. Jorgensen, N. Watanabe, C. Hoog, P. Hieter, and K. Todokoro. 1998. PKA and MPF-activated Polo-like kinase regulate anaphase-promoting complex activity and mitosis progression. Mol. Cell 1: 371-380.
29. Lahav-Baratz, S., V. Sudakin, J.V. Ruderman, and A. Hershko. 1995. Reversible phosphorylation controls the activity of cyclosome-associated cyclin-ubiquitin ligase. Proc. Natl. Acad. Sci. 92: 9303-9307.
30. Li, R. 1999. Bifurcation of the mitotic checkpoint pathway in budding yeast. Proc. Natl. Acad. Sci. 96: 4989-4994.
31. Li, Y., C. Gorbea, D. Mahaffey, M. Rechsteiner, and R. Benezra. 1997. MAD2 associates with the cyclosome/anaphase-promoting complex and inhibits its activity. Proc. Natl. Acad. Sci. 94: 12431-12436.
32. 2/M checkpoint control to mitosis in Saccharomyces cerevisiae. Mol. & Gen. Genet. 253: 138-148.
33. Lim, H.H., P. Goh, and U. Surana. 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.
34. McGrew, J.T., L. Goetsch, B. Byers, and P. Baum. 1992. Requirement for ESP1 in the nuclear division of Saccharomyces cerevisiae. Mol. Biol. Cell 3: 1443-1454.
35. Moll, T., G. Tebb, U. Surana, H. Robitsch, and K. Nasmyth. 1991. The role of phosphorylation and the CDC28 protein kinase in the cell cycle-regulated nuclear import of the S. cerevisiae transcription factor SWI5. Cell 66: 743-758.
36. Morgan, D.O. 1999. Regulation of the APC and the exit from mitosis. Nature Cell Biol. 1: E47-E53.
37. Murray, A.W. 1994. The genetics of cell cycle checkpoints. Curr. Opin. Genet. Dev. 5: 5-11.
38. _. 1995. Cyclin ubiquitination: The destructive end of mitosis. Cell 81: 149-152.
39. New, J.H., T. Sugiyama, E. Zaitseva, and S.C. Kowalczykowski. 1998. Rad52 protein stimulates DNA strand exchange by Rad51 and rereplication protein A. Nature 391: 401-410.
40. Paulovich, A.G., R.U. Margulies, B.M. Garvik, and L.H. Hartwell. 1997. RAD9, RAD17, and RAD24 are required for S phase regulation in Saccharomyces cerevisiae in response to DNA damage. Genetics 145: 45-62.
41. Peters, J.-M. 1998. SCF and APC: The Yin and Yang of cell cycle regulated proteolysis. Cun. Opin. Cell Biol. 10: 759-768.
42. Prinz, S., E.S. Hwang, R. Visintin, and A. Amon. 1998. The regulation of Cdc20 proteolysis reveals a role for the APC components Cdc23 and Cdc27 during S phase and early mitosis. Curr. Biol. 8: 750-760.
43. Rose, M.D., F. Winston, and P. Hieter. 1990. Methods in yeast genetics - A laboratory course manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
44. Rudner, A.D. and A.W. Murray. 1996. The spindle assembly checkpoint. Curr. Opin. Cell Biol. 8: 773-780.
45. Schwab, M., A.S. Lutum, and W. Seufert. 1997. Yeast Hct1 is a regulator of Clb2 cyclin proteolysis. Cell 90: 683-693.
46. Schweitzer, B. and P. Philippsen. 1991. CDC15, an essential cell cycle gene in Saccharomyces cerevisiae, encodes a protein kinase domain. Yeast 7: 265-273.
47. Shirayama, M., Y. Matsui, and A. Toh-e. 1994. The yeast TEM1 gene, which encodes a GTP-binding protein, is involved in termination of M phase. Mol. Cell. Biol. 14: 7476-7482.
48. _. 1996. Dominant mutant alleles of yeast protein kinase gene CDC15 suppress the Ite1 defect in termination of M phase and genetically interact with CDC14. Mol. Gen. & Genet. 251: 176-185.
49. Shirayama, M., W. Zachariae, R. Ciosk, and K. Nasmyth. 1998. The Polo-like 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.
50. Skowyra, D., K.L. Craig, M. Tyers, S.J. Elledge, and J.W. Harper. 1997. F-box proteins are receptors that recruit phosphorylated substrates to the SCF ubiquitin-ligase complex. Cell 91: 209-219.
51. cdc28 Nature 355; 365-368.
52. Sudakin, V., D. Ganoth, A. Dahan, H. Heller, J. Hershko, F.C. Luca, J.V. Ruderman, and A. Hershko. 1995. The cyclosome, a large complex containing cyclin-selective ubiquitin-ligase activity, targets cyclins for destruction at the end of mitosis. Mol. Biol. Cell 6: 185-198.
53. 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.
54. Taylor, G.S., Y. Liu, C. Baskerville, and H. Charbonneau. 1997. The activity of Cdc14p, an oligomeric dual specificity protein phosphatase from Saccharomyces cerevisiae, is required for cell cycle progression. J. Biol. Chem. 272: 24054-24063.
55. Toyn, J.H., A.L. Johnson, J.D. Donovan, W.M. Toone, and L.H. Johnston. 1996. 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.
56. Verma, R., R.S. Annan, M.J. Huddleston, S.A. Carr, G. Reynard, and R.J. Deshaies. 1997. Phosphorylation of Siclp by G1 Cdk required for its degradation and entry into S phase. Science 278: 455-460.
57. 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.
58. Visintin, R., K. Craig, E.S. Hwang, S. Prinz, M. Tyers, and A. Amon. 1998. The phosphatase Cdcl4 triggers mitotic exit by reversal of Cdk-dependent phosphorylation. Mol. Cell 2: 709-718.
59. Wan, J., H. Xu, and M. Grunstein. 1992. CDC14 of Saccharomyces cerevisiae. J. Biol. Chem. 267: 11274-11280.
60. Weinert, T. 1998. DNA damage checkpoints update: Getting molecular. Curr. Opin. Genet. Dev. 8: 185-193.
61. Weinert, T.A. and L.H. Hartwell. 1988. The RAD9 gene controls the cell cycle response to DNA damage in Saccharomyces cerevisiae. Science 241: 317-322.
62. _. 1990. Characterization of RAD9 of Saccharomyces cerevisiae and evidence that its function acts posttranslationally in cell cycle arrest after DNA damage. Mol. Cell. Biol. 10: 6554-6564.
63. Yamamoto, A., V. Guacci, and D. Koshland. 1996a. Pds1p is required for the faithful execution of anaphase in yeast. J. Cell Biol. 133: 85-97.
64. _. 1996b. Pds1, an inhibitor of anaphase in budding yeast, plays a critical role in the APC and checkpoint pathway(s). J. Cell Biol. 133: 99-110.
65. Yang, S.S., E. Yeh, E.D. Salmon, and K. Bloom. 1997. Identification of a mid-anaphase checkpoint in budding yeast. J. Cell Biol. 136: 345-354.
66. Zachariae, W. and K. Nasmyth. 1996. TPR proteins required for anaphase progression mediate ubiquitination of mitotic B-type cyclins in yeast. Mol Biol. Cell 7: 791-801.
67. 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.