Phosphorylation by Cdc28 activates the Cdc20-dependent activity of the anaphase-promoting complex

Journal of Cell Biology

Volumn 149, Issue 7, 2000, Pages 1377-1390

  Rudner, Adam D ^a,b   Murray, Andrew W ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Budding yeast; Cdc5; Cks1; Mitosis; Pds1

Indexed keywords

CYCLIN DEPENDENT KINASE;

AMINO ACID SUBSTITUTION; ANAPHASE; ARTICLE; BINDING SITE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME BINDING; MITOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; YEAST;

ANAPHASE; BINDING SITES; CDC2-CDC28 KINASES; CELL CYCLE PROTEINS; FUNGAL PROTEINS; G1 PHASE; MITOSIS; MUTATION; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; RNA-BINDING PROTEINS; SACCHAROMYCES CEREVISIAE PROTEINS; SACCHAROMYCETALES; TIME FACTORS; UBIQUITIN-PROTEIN LIGASES;

SACCHAROMYCETALES;

EID: 0034717570     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.149.7.1377     Document Type: Article

References (77)

1. Amon, A. 1997. Regulation of B-type cyclin proteolysis by Cdc28-associated kinases in budding yeast. EMBO (Eur. Mol. Biol. Organ.) J. 16:2693-2702.
2. Biggins, S., F.F. Severin, N. Bhalla, I. Sassoon, A.A. Hyman, and A.W. Murray. 1999. The conserved protein kinase IpI1 regulates microtubule binding to kinetochores in budding yeast. Genes Dev. 13:532-544.
3. 2 cyclins. EMBO (Eur. Mol. Biol. Organ.) J. 12:3417-3426.
4. Brown, N.R., M.E. Noble, J.A. Endicott, and L.N. Johnson. 1999. The structural basis for specificity of substrate and recruitment peptides for cyclindependent kinases. Nat. Cell Biol. 1:438-443.
5. Charles, J., 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. 9:497-507.
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 Pds1p. Genes Dev. 10:3081-3093.
7. Descombes, P., and E.A. Nigg. 1998. The polo-like kinase Plx1 is required for M phase exit and destruction of mitotic regulators in Xenopus egg extracts. EMBO (Eur. Mol. Biol. Organ.) J. 17:1328-1335.
8. 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/GI transition in Saccharomyces cerevisiae. Genes Dev. 8:1640-1653.
9. Fang, G., H. Yu, and M.W. Kirschner. 1998a. The checkpoint protein MAD2 and the mitotic regulator CDC20 form a ternary complex with the anaphase-promoting complex to control anaphase initiation. Genes Dev. 12: 1871-1883.
10. Fang, G., H. Yu, and M.W. Kirschner. 1998b. Direct binding of CDC20 protein family members activates the anaphase-promoting complex in mitosis and G1. Mol. Cell. 2:163-171.
11. Funabiki, H., H. Yamano, K. Kumada, K. Nagao, T. Hunt, and M. Yanagida. 1996. Cut2 proteolysis required tor sister-chromatid separation in fission yeast. Nature. 381:438-441.
12. Funabiki, H., H. Yamano, K. Nagao, H. Tanaka, H. Yasuda, T. Hunt, and M. Yanagida. 1997. Fission yeast Cut2 required for anaphase has two destruction boxes. EMBO (Eur. Mol. Biol. Organ.) J. 16:5977-5987.
13. Ghiara, J.B., H.E. Richardson, K. Sugimoto, M. Henze, D.J. Lew, C. Witenberg, and S.I. Reed. 1991. A cyclin H homolog in S. cerevisiae: chronic activation of the Cdc28 protein kinase by cyclin prevents exit from mitosis. Cell. 65:163-174.
14. Glotzer, M., A.W. Murray, and M.W. Kirschner. 1991. Cyclin is degraded by the ubiquitin pathway. Nature. 349:132-138.
15. Grandin, N., and S.I Reed. 1993. Differential function and expression of Saccharomyces cerevisiae B-type cyclins in mitosis and meiosis. Mol. Cell. Biol. 13:2113-2125.
16. Hardwick, K., and A.W. Murray. 1995. Madlp, a phosphoprotein component of the spindle assembly checkpoint in budding yeast. J. Cell Biol. 131:709-720.
17. Hardwick, K.G., E. Weiss, F.C. Luca, M. Winey, and A.W. Murray. 1996. Activation of the budding yeast spindle assembly checkpoint without mitotic spindle disruption. Science. 273:953-956.
18. Hardy, C.F., and A. Pautz. 1996. A novel role for Cdc5p in DNA replication. Mol. Cell. Biol. 16:6775-6782.
19. 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 protein kinase cdc2. J. Biol. Chem. 269: 4940-4946.
20. Holloway, S.L., M. Glotzer, R.W. King, and A.W. Murray. 1993. Anaphase is initiated by proteolysis rather than by the inactivation of MPF. Cell. 73: 1393-1402.
21. Hwang, L.H., and A.W. Murray. 1997. A novel yeast screen for mitotic arrest mutants identities DOC1, a new gene involved in cyclin proteolysis. Mol. Biol. Cell. 8:1877-1887.
22. 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.
23. Jaspersen, S.L., J.F. Charles, and D.O. Morgan. 1999. Inhibitory phosphorylation of the APC regulator Hetl is controlled by the kinase Cdc28 and the phosphatase Cdc14. Curr. Biol. 9:227-236.
24. 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.
25. Juang, Y.L., J. Huang, J.M. Peters, M.E. McLaughlin, C.Y. Tai, and D. Pellman. 1997. APC-mediated proteolysis of Asc1 and the morphogenesis of the mitotic spindle. Science. 275:1311-1314.
26. Kaiser, P., V. Moncollin, D.J. Clarke, M.H. Watson, B.L. Bertolaet, S.I. Reed, and E. Bailly. 1999. Cyclin-dependent kinase and Cks/Suc1 interact with the proteasome in yeast to control proteolysis of M-phase targets. Genes Dev. 13:1190-1202.
27. Kallio, M., J. Weinstein, J.R. Daum, D.J. Burke, and G.J. Gorbsky. 1998. Mammalian p55CDC mediates association of the spindle checkpoint protein Mad2 with the cyclosome/anaphase-promoting complex, and is involved in regulating anaphase onset and late mitolic events. J. Cell Biol. 141:1393-1406.
28. Kellogg, D.R., and A.W. Murray. 1995. NAP1 acts with Clb2 to perform mitotic functions and suppress polar bud growth in budding yeast. J. Cell Biol. 130: 675-685.
29. Kim, S.H., D.P. Lin, S. Matsumoto, A. Kitazano, and T. Matsumoto. 1998. Fission yeast slp1 - encodes the effector of the Mad2-dependent spindle checkpoint. Science. 279:1045-1047.
30. 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.
31. Kitada, K., A.L. Johnson, L.H. Johnston, and A. Sugino. 1993. A multicopy suppressor gene of the Saccharomyces cerevisiae G1 cell cycle mutant gene dbf4 encodes a protein kinase and is identified as CDC5. Mol. Cell. Biol. 13: 4445-4457.
32. Kitamura, K., H. Mackawa, and C. Shimoda. 1998. Fission yeast Ste9, a homolog of Het1/Cdh1 and Fizzy-related, is a novel negative regulator of cell cycle progression during G1-phase. Mol. Biol. Cell. 9:1065-1080.
33. Kotani, S., S. Tugendreich, M. Fujii, P.M. 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.
34. Kotani, S., H. Tanaka, H. Yasuda, and K. Todokoro. 1999. Regulation of APC activity by phosphorylation and regulatory factors. J. Cell Biol. 146:791-800.
35. Kramer, E.R., C. Gieffers, G. Holzl, M. Hengstschlager, and J.M. Peters. 1998. Activation of the human anaphase-promoting complex by proteins of the CDC20/Fizzy family. Curr. Biol. 8:1207-1210.
36. Kumagai, A., and W.G. Dunphy. 1996. Purification and molecular cloning of Plx1, a Cdc25-regulatory kinase from Xenopus egg extracts. Science. 273: 1377-1380.
37. Kunkel, T.A. 1985. Rapid and efficient site-specific mutagenesis without phenotypic selection, Proc. Natl. Acad. Sci. USA. 82:488-492.
38. 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. USA. 92:9303-9307.
39. Lamb, J.R., W.A. Michaud, R.S Sikorski, and P.A. Hieter. 1994. Cdc16p, Cdc23p and Cdc27p form a complex essential for mitosis. EMBO (Eur. Mol. Biol. Organ.) J. 13:4321-4328.
40. Li, X., and M. Cai. 1997. Inactivation of the cyclin-dependent kinase Cdc28 abrogates cell cycle arrest induced by DNA damage and disassembly of mitotic spindles in Saccharomyces cerevisiae. Mol. Cell. Biol. 17:2723-2734.
41. Lim, H.H., and U. Surana. 1996. Cdc20, a beta-transducin homologue, links RAD9-mediated G2/M checkpoint control to mitosis in Saccharomyces cerevisiae. Mol. Gen. Genet. 253:138-148.
42. Longtine, M.S., A. McKenzie. 3rd, D.J. Demarini, N.G. Shah, A. Wach, A. Brachat, P. Philippsen, and J.R. Pringle. 1998. Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast. 14:953-961.
43. Lorca, T., A. Castro, A.M. Martinez, S. Vigneron, N. Morin, S. Sigrist, C. Lehner, M. Doree, and J.C. Labbe. 1998. Fizzy is required for activation of the APC/cyclosome in Xenopus egg extracts. EMBO (Eur. Mol. Biol. Organ.) J. 17:3565-3575.
44. Maniatis, T., E.F. Fritsch, and J. Sambrook. 1982. Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
45. CDC28 protein kinase activity from Saccharomyces cerevisiae. Science. 259:216-219.
46. Minshull, J., H. Sun, N.K. Tonks, and A.W. Murray. 1994. MAP-kinase dependent mitotic feedback arrest in Xenopus egg extracts. Cell. 79:475-486.
47. Patra, D., and W.G. Dunphy. 1996. Xe-p9, a Xenopus SUC1/CKS homolog, has multiple essential roles in cell cycle control. Genes Dev. 10:1503-1515.
48. Patra, D., and W.G. Dunphy. 1998. Xe-p9, a Xenopus Suc1/Cks protein, is essential for the Cdc2-dependent phosphorylation of the anaphase-promoting complex at mitosis. Genes Dev. 12:2549-2559.
49. Peters, J.M., R.W. King, C. Hoog, and M.W. Kirschner. 1996. Identification of BIME as a subunit of the anaphase-promoting complex. Science. 274:1199-1201.
50. Piggott, J.R., Rai, and B.L.A. Carter. 1982. A bifunctional gene involved in two phases of the yeast cell cycle. Nature. 298:391-394.
51. Prinz, S., E.S. Hwang, R. Visintin, and A. Amon. 1998. The regulation of Cdc20 proteolysis reveals a role for APC components Cdc23 and Cdc27 during S phase and early mitosis. Curr. Biol. 8:750-760.
52. Reed, S.I. 1980. The selection of S. cerevisiae mutants defective in the start event of cell division. Genetics. 95:561-577.
53. Rothblatt, J., and R. Schekman. 1989. A hitchhiker's guide to analysis of the secretory pathway in yeast. Methods Cell Biol. 32:3-36.
54. Rudner, A.D., K.G. Hardwick, and A.W. Murray. 2000. Cdc28 activates exit from mitosis in budding yeast. J. Cell Biol. 149:1361-1376.
55. Schwab, M., A.S. Lutum, and W. Seufert. 1997. Yeast Het1 is a regulator of Clb2 cyclin proteolysis. Cell. 90:683-693.
56. Sherman, F., G. Fink, and C. Lawrence. 1974. Methods in Yeast Genetics. Cold Spring Harbor Laboratory Press. Cold Spring Harbor, NY.
57. 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 (Eur. Mol. Biol. Organ.) J. 17:1336-1349.
58. Cdc20 promotes exit from mitosis by destroying the anaphase inhibitor Pds1 and cyclin Clb5. Nature. 402:203-207.
59. Shteinberg, M., and A. Hershko. 1999. Role of Suc1 in the activation of the cyclosome by protein kinase Cdk1/cyclin B. Biochem. Biophys. Res. Comm. 257:12-18.
60. Shteinberg, M., Y. Protopopov, T. Listovsky, M. Brandeis, and A. Hershko. 1999. Phosphorylation of the cyclosome is required for its stimulation by Fizzy/cdc20. Biochem. Biophys. Res. Comm. 260:193-198.
61. Straight, A.F., A.S. Belmont, C.C. Robinett, and A.W. Murray. 1996. GFP tagging of budding yeast chromosomes reveals that protein-protein interactions can mediate sister chromatid cohesion. Curr. Biol. 6:1599-1608.
62. Sudakin, V., D. Ganoth, A. Dahan, H. Heller, J. Hersko, F. Luca, J.V. Ruderman, and A. Hershko. 1995. The cyclosome, a large complex containing cyclin-selective ubiquitination ligase activity, targets cyclins for destruction at the end of mitosis. Mol. Biol. Cell. 6:185-198.
63. Sudakin, V., M. Shteinberg, D. Ganoth, J. Hershko, and A. Hershko. 1997. Binding of activated cyclosome to pl3(suc1). Use for affinity purification. J. Biol. Chem. 272:18051-18059.
64. Surana, U., H. Robitsch, C. Price, T. Schuster, I. Fitch, A.B. Futcher, and K. Nasmyth. 1991. The role of CDC28 and cyclins during mitosis in the budding yeast S. cerevisiae. Cell. 65:145-161.
65. Tang, Y., and S.I. Reed. 1993. The Cdk-associated protein Cks1 functions both in G1 and G2 in Saccharomyces cerevisiae. Dev. 7:822-832.
66. Visintin, R., S. Prinz, and A. Amon. 1997. CDC20 and CDII1: a family of substrate-specific activators of APC-dependent proteolysis. Science. 278:460-463.
67. 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.
68. Vorlaufer, E., and J.M. Peters. 1998. Regulation of the cyclin B degradation system by an inhibitor of mitotic proteolysis. Mol. Biol. Cell. 9:1817-1831.
69. Weinstein, J. 1997. Cell cycle-regulated expression, phosphorylation, and degradation of p55Cdc. A mammalian homolog of CDC20/Fizzy/slp1. J. Biol. Chem. 272:28501-28511.
70. Westendorf, J.M., P.N. Rao, and L. Gerace. 1994. Cloning of cDNAs for M-phase phosphoproteins recognized by the MPM2 monoclonal antibody and determination of the phosphorylated epitope. Proc. Natl. Acad. Sci. USA. 91:714-718.
71. Yamada, H., K. Kumada, and M. Yanagida. 1997. Distinct subunit functions and cell cycle regulated phosphorylation of 20S APC/cyclosome required for anaphase in fission yeast. J. Cell Sci. 110:1793-1804.
72. Yamamoto, A., V. Guacci. and D. Koshland. 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.
73. Yamano, H., J. Gannon, and T. Hunt. 1996. The role of proteolysis in cell cycle progression in Schizosaccharomyces pombe. EMBO (Eur. Mol. Biol. Organ.) J. 15:5268-5279.
74. Yamashita, Y.M., Y. Nakaseko, I. Samejima, K. Kumada, H. Yamada, D. Michaelson, and M. Yanagida. 1996. 20S cyclosome complex formation and proteolylic activity inhibited by the cAMP/PKA pathway. Nature. 384:276-279.
75. Yeong, M.F., H.H. Lim, P.C.G., and U. Surana. 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.
76. Zachariae, W., T.H. Shin, M. Galova, B. Obermaier, and K. Nasmyth. 1996. Identification of subunits of the anaphase-promoting complex of Saccharomyces cerevisiae. Science. 274:1201-1204.
77. Zachariae, W., M. Schwab, K. Nasmyth, and W. Seufert. 1998. Control of cyclin ubiquitination by CDK-regulated binding of Het1 to the anaphase promoting complex. Science. 282:1721-1724.