Regulation of the G1 phase of the cell cycle by periodic stabilization and degradation of the p25(rum1) CDK inhibitor

EMBO Journal

Volumn 17, Issue 2, 1998, Pages 482-497

  Benito, Javier ^a   Martín Castellanos, Cristina ^a   Moreno, Sergio ^a  

^a Departamento de Microbiología y Genética   (Spain)

Author keywords

CDK inhibitor; Cyclin; Phosphorylation; Proteolysis; Rum 1

Indexed keywords

CYCLIN DEPENDENT KINASE INHIBITOR; CYCLINE; MUTANT PROTEIN; PROTEASOME; PROTEIN KINASE; UBIQUITIN; CYCLIN DEPENDENT KINASE; CYCLIN DEPENDENT KINASE 1; CYSTEINE PROTEINASE; FLAVODOXIN; FUNGAL PROTEIN; MULTIENZYME COMPLEX; OBR1 PROTEIN, S POMBE; RUM1 PROTEIN, S POMBE; SCHIZOSACCHAROMYCES POMBE PROTEIN;

ANAPHASE; ARTICLE; CELL CYCLE; CELL CYCLE G1 PHASE; CELL CYCLE S PHASE; CONTROLLED STUDY; DNA REPLICATION; MITOSIS; NONHUMAN; POLYPLOIDY; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN PHOSPHORYLATION; PROTEIN STABILITY; SCHIZOSACCHAROMYCES POMBE; DRUG ANTAGONISM; METABOLISM; PHOSPHORYLATION; PHYSIOLOGY; SCHIZOSACCHAROMYCES;

SCHIZOSACCHAROMYCES POMBE;

CDC2 PROTEIN KINASE; CELL CYCLE; CYCLIN-DEPENDENT KINASES; CYCLINS; CYSTEINE ENDOPEPTIDASES; FLAVODOXIN; FUNGAL PROTEINS; G1 PHASE; MULTIENZYME COMPLEXES; PHOSPHORYLATION; PROTEASOME ENDOPEPTIDASE COMPLEX; SCHIZOSACCHAROMYCES; SCHIZOSACCHAROMYCES POMBE PROTEINS; UBIQUITINS;

EID: 0032517963     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/17.2.482     Document Type: Article

References (105)

1. Adachi, Y. and Laemmli, U.K. (1994) Study of the cell cycle-dependent assembly of the DNA pre-replication centres in Xenopus egg extracts. EMBO J., 13, 4153-4164.
2. 1 cyclins in the next cycle. Cell, 77, 1037-1050.
3. Bai, C., Sen, P., Hofman, K., Ma, L., Goebl, M., Harper, J.W. and Elledge, S.J. (1996) SKP1 connects cell cycle regulators to the ubiquitin proteolysis machinery through a novel motif, the F-Box. Cell, 86, 263-274.
4. Boyle, W.J, Van der Geer, P. and Hunter, T. (1991) Phosphopeptide mapping and phosphoamino acid analysis by two-dimensional separation on thin-layer cellulose plates. Methods Enzymol., 201, 110-149.
5. Booher, R.N., Alfa, C.E., Hyams, J.S. and Beach, D. (1989) The fission yeast cdc2/cdc13/suc1 protein kinase: regulation of catalytic activity and nuclear localization. Cell, 58, 485-497.
6. Brandeis, M. and Hunt, T. (1996) The proteolysis of mitotic cyclins in mammalian cells persist from the end of mitosis until the onset of S-phase. EMBO J., 15, 5280-5289.
7. cdc2 in establishing the dependency of S phase on mitosis. Nature, 349, 388-393.
8. Brown, K., Gerstberger, S., Carlson, L., Franzoso, G. and Sienblist, U. (1995) Control of IκB-α proteolysis by site specific, signal induced phosphorylation. Science, 267, 1485-1488.
9. Bueno, A., Richardson, H., Reed, S.I. and Russell, P. (1991) A fission yeast B-type cyclin functioning early in the cell cycle. Cell, 66, 149-160.
10. 1 cyclin, CLN2. Cell, 63, 999-1011.
11. Chen, Z., Hagler, J., Pallombella, V.J., Malandri, F., Scherer, D., Ballard, D. and Maniatis, T. (1995) Signal-induced site-specific phosphorylation targets IκB-α to the ubiquitin-proteasome pathway. Genes Dev., 9, 1586-1597.
12. Clurman, B.E., Sheaff, R.J., Thress, K., Groudine, M. and Roberts, J.M. (1996) Turnover of cyclinE by the ubiquitin-proteasome pathway is regulated by CDK2 binding and cyclin phosphorylation. Genes Dev., 10, 1979-1990.
13. Connelly, C. and Hieter, P. (1996) Budding yeast SKP1 encodes an evolutionary conserved kinetochore protein required for cell cycle progression. Cell, 86, 275-285.
14. cdc2 mitotic kinase. Cell, 83, 1001-1009.
15. 1 of the fission yeast cell cycle. EMBO J., 16, 4657-4664.
16. cdc25 during the cell cycle of the fission yeast Schizosaccharomyces pombe. J. Cell Sci., 109, 1647-1653.
17. Dahmann, C., Diffley, J.F.X. and Nasmyth, K. (1995) S-phase-promoting cyclin-dependent kinases prevent re-replication by inhibiting the transition of replication origins to a pre-replicative state. Curr. Biol., 5, 1257-1269.
18. Den Haese, G.J., Walworth, N., Carr, A.M. and Gould, K. (1995) The weel protein kinase regulates T14 phosphorylation of fission yeast cdc2. Mol. Biol. Cell., 6, 371-385.
19. Deshaies, R.J. (1995) The self-destructive personality of a cell cycle in transition. Curr. Opin. Cell Biol., 7, 781-789.
20. 1 cyclin Cln2 by a Cdc34-dependent pathway. EMBO J., 14, 303-312.
21. Diehl, J.A., Zindy, F. and Sherr, C.J. (1997) Inhibition of cyclin D1 phosphorylation on threonine-286 prevents its rapid degradation via the ubiquitin-proteasome pathway. Genes Dev., 11, 957-972.
22. Dirick, L., Bohm, T. and Nasmyth, K. (1995) Roles and regulation of Cln-Cdc28 kinases at the start of the cell cycle of Saccharomyces cerevisiae. EMBO J., 14, 4803-4813.
23. Dohadwala, M., Cruz e Silva, E.F., Hall, F.L., Williams, R.T., Carbonaro-Hall, D.A., Nairn, A.C., Greegard, P. and Berndt, N. (1994) Phosphorylation and inactivation of protein phosphatase 1 by cyclin-dependent kinases. Proc. Natl Acad. Sci. USA, 91, 6408-6412.
24. 1 transition in Saccharomyces cerevisiae. Genes Dev., 8, 1640-1653.
25. Elledge, S.J., Winston, J. and Harper, J.W. (1996) A question of balance: the role of cyclin-kinase inhibitors in development and tumorigenesis. Trends Cell Biol., 6, 388-392.
26. Fisher, D. and Nurse, P. (1995) Cyclins of the fission yeast Schizosaccharomyces pombe. Semin. Cell Biol., 6, 73-78.
27. 1 cyclins. EMBO J., 15, 850-860
28. 1-type cyclin puc1 in the fission yeast Schizosaccharomyces pombe. Nature, 351, 245-248.
29. Forsburg, S.L. and Nurse, P. (1994) Analysis of Schizosaccharomyces pombe cyclin puc1: evidence for a role in cell cycle exit. J. Cell Sci., 107, 601-613.
30. Funabiki, H., Yamano, H., Kumada, K., Nagao, K., Hunt, T. and Yanagida, M. (1996) Cut2 proteolysis required for sister-chromatid separation in fission yeast. Nature, 381, 438-441.
31. Glotzer, M., Murray, A.W. and Kirschner, M.W. (1991) Cyclin is degraded by the ubiquitin pathway. Nature, 349, 132-138.
32. Goebl, M.G., Yochem, J., Jentsch, S., McGrath, J.P., Varshavsky, A. and Byers, B. (1988) The yeast cell cycle gene CDC34 encodes a ubiquitin-conjugating enzyme. Science, 241, 1331-1335.
33. Gordon, C., McGurk, G., Wallace, M. and Hastie, N.D. (1996) A conditional lethal mutant in the fission yeast 26S protease subunit mts3 is defective in metaphase to anaphase transition. J. Biol. Chem., 271, 5704-5711.
34. Gould, K.L and Nurse, P. (1989) Tyrosine phosphorylation of the fission yeast cdc2 protein kinase regulates entry into mitosis. Nature, 342, 39-45.
35. cdc2 function. EMBO J., 10, 3297-3309.
36. Hartwell, L.H., Culotti, J., Pringle, J. and Reid, B.J. (1974) Genetic control of the cell division cycle in yeast. Science, 183, 46-51.
37. cdc2 tyrosine phosphorylation. EMBO J., 14, 2760-2771.
38. cdc2-mitotic B cyclin complex. Cell, 78, 813-822.
39. Hershko, A., Ganoth, D., Pehrson, J., Palazzo, R.E. and Cohen, L.H. (1991) Methylated ubiquitin inhibits cyclin degradation in clam embryo extracts. J. Biol. Chem., 266, 16376-16379.
40. Hershko, A., Ganoth, D., Sudakin, V., Dhan, A., Cohen, L.H., Luca, F.C., Ruderman, J.V. and Eytan, E. (1994) Components of a system that ligates cyclin to ubiquitin and their regulation by the protein kinase cdc2. J. Biol. Chem., 266, 16376-16370.
41. + that encodes a nuclear scaffold-like protein blocks spindle elongation in mitotic anaphase. J.Cell Biol., 106, 1171-1183.
42. Irniger, S., Piatti, S., Michaelis, C. and Nasmyth, K. (1995) Genes involved in sister chromatid separation are needed for B-type cyclin proteolysis in budding yeast. Cell, 81, 269-277.
43. Jallepalli, P.V. and Kelly, T.J. (1996) rum1 and cdc18 link inhibition of cyclin-dependent kinase to the initiation of DNA replication in Schizosaccharomyces pombe. Genes Dev., 10, 541-552.
44. + gene product couples S-phase to Start and mitosis. Cell, 74, 371-382.
45. King, R.W., Peters, J.M., Tugendreich, S., Rolfe, M., Hieter, P. and Kirschner, M.W. (1995) A 20S complex containing CDC27 and CDC16 catalyzes the mitosis-specific conjugation of ubiquitin to cyclin B. Cell, 81, 279-288.
46. Kipreos, E.T., Lander, L.E., Wing, J.P., He, W.W. and Hedgecock, E.M. (1996) cul-1 is required for cell cycle exit in C.elegans and identifies a novel gene family. Cell, 85, 829-839.
47. Kominami, K. and Toda, T. (1997) Fission yeast WD-repeat protein pop1 regulates genome ploidy through ubiquitin-proteasome-mediated degradation of the CDK inhibitor rum1 and the S-phase initiator cdc18. Genes Dev., 11, 1548-1560.
48. 1 progression in fission yeast. Trends Cell Biol., 5, 62-66.
49. Labib, K., Moreno, S. and Nurse, P. (1995) Interaction of cdc2 and rum1 regulates Start and S-phase in fission yeast. J. Cell Sci., 108, 3285-3294.
50. 1 cyclin Cln2 induced by CDK-dependent phosphorylation. Science, 271, 1597-1601.
51. rum1 CDK inhibitor. EMBO J., 15, 839-849.
52. 1-to-S phase transition and identifies a conserved family of proteins. Mol. Cell. Biol., 16, 6634-6643.
53. Maundrell, K. (1989) nmt1 of fission yeast: a highly transcribed gene completely repressed by thiamine. J. Biol. Chem., 265, 10857-10864.
54. Mirabito, P.M. and Morris, N.R. (1993) BIMA, a TPR-containing protein required for mitosis, localizes to the spindle pole body in Aspergillus nidulans. J. Cell Biol., 120, 959-968.
55. Monderset, O., McGowan, C.H. and Russell, P. (1996) Cig2, a B-type cyclin, promotes the onset of S in Schizosaccharomyces pombe. Mol. Cell. Biol., 16, 1527-1533.
56. cdc2: in vivo veritas? Cell, 61, 549-551.
57. + gene. Nature, 367, 236-242.
58. cdc2 protein kinase during mitosis. Cell, 58, 361-372.
59. Moreno, S., Klar, A. and Nurse, P. (1991) Molecular genetic analysis of fission yeast Schizosaccharomyces pombe. Methods Enzymol., 194, 793-823.
60. + gene. J. Cell Sci. Suppl., 18, 63-68.
61. Murray, A.W. (1995) Cyclin ubiquitination: the destructive end of mitosis. Cell, 81, 149-152.
62. Murray, A.W. and Kirschner, M.W. (1989) Cyclin synthesis drives the early embryonic cell cycle. Nature, 339, 275-280.
63. Murray, A.W., Solomon, M.J. and Kirschner, M.W. (1989) The role of cyclin synthesis and degradation in the control of maturation promoting factor activity. Nature, 339, 280-286.
64. Musti, A.M., Treier, M., Peverali, F.A. and Bohman, D. (1986) Differential regulation of c-Jun and JunD by ubiquitin-dependent protein degradation. Biol. Chem., 377, 619-624.
65. Nasmyth, K. (1993) Control of the yeast cell cycle by the Cdc28 protein kinase. Curr. Opin.Cell Biol., 5, 166-179.
66. Nasmyth, K. (1996) At the heart of the budding yeast cell cycle. Trends Genet., 12, 405-412.
67. Nugroho, T.T. and Mendenhall, M.D. (1994) An inhibitor of yeast cyclin-dependent protein kinase plays an important role in ensuring the genomic integrity of daughter cells. Mol. Cell. Biol., 14, 3320-3328.
68. Nurse, P. (1975) Genetic control of cell size at cell division in yeast. Nature, 256, 547-551.
69. Nurse, P. (1994) Ordering S-phase and M-phase in the cell cycle. Cell, 79, 547-550.
70. 2 for control of mitosis in fission yeast. Nature, 292, 558-560.
71. Obara-Ishihara, T. and Okayama, H. (1994) A B-type cyclin negatively regulates conjugation via interacting with cell cycle 'start' genes in fission yeast. EMBO J., 13, 1863-1872.
72. O'Donnell, K.L., Osmani, A.H., Osmani, S.A. and Morris, N.R. (1991) bimA encodes a member of the tretratricopeptide repeat family of proteins and is required for the completion of mitosis in Aspergillus nidulans. J. Cell Sci., 99, 711-719.
73. Pagano, M., Tam, S.W., Theodoras, A.M., Beer-Romero, P. Del Sal, G., Chau, V., Yew, P.R., Draetta, G.F. and Rolfe, M. (1995) Role of the ubiquitin-proteasome pathway in regulating abundance of the cyclin-dependent kinase inhibitor p27. Science, 269, 682-685.
74. Pahl, H.L. and Baeuerle, P.A. (1996) Control of gene expression by proteolysis. Curr. Opin. Cell Biol., 8, 340-347.
75. Pardee, A. (1974) A restriction point for control of normal animal cell proliferation. Proc. Natl Acad. Sci. USA, 71, 1286-1290.
76. Peter, M. and Herskowitz, I. (1994) Direct inhibition of the yeast cyclin-dependent kinase cdc28-cln by Far1. Science. 265, 1228-1231.
77. Peter, M., Gartner, A., Horecka, J., Ammerer, G. and Herskowitz, I. (1993) FAR1 links the signal transduction pathway to the cell cycle machinery in yeast. Cell. 73, 747-760.
78. Picard, A., Galas, S., Peaucellier, G. and Dorée, M. (1996) Newly assembled cyclinB-cdc2 kinase is required to suppress DNA replication between meiosis I and meiosis II is starfish oocyles. EMBO J., 15, 3590-3598.
79. Piggott, J. R., Rai, R. and Carter, B.L.A. (1982) A bifunctional product involved in two phases of the yeast cell cycle. Nature, 298, 391-393.
80. Reed, S.I and Wittenberg, C. (1990) Mitotic role for the Cdc28 protein kinase of Saccharomyces cerevisiae. Proc. Natl Acad. Sci. USA, 87, 5697-5701.
81. Rogers, S., Wells, R. and Rechsteiner, M. (1986) Amino acid sequences common to rapidly degraded proteins: the PEST hypothesis. Science, 234, 364-368.
82. + to initiate anaphase. J. Cell. Biol., 127, 1655-1670.
83. Sauer, K., Knoblich, J.A., Richardson, H. and Lehner, C.F. (1995) Distinct modes of cyclinE/cdc2c kinase regulation and S-phase control in mitotic and endoreduplication cycles of Drosophila embryogenesis. Genes Dev., 9, 1327-1339.
84. Sazer, S. and Sherwood, S.W. (1990) Mitochondrial growth and DNA synthesis occur in the absence of nuclear DNA replication in fission yeast. J. Cell Sci., 97, 509-516.
85. 1 cyclin-dependent kinases. Genes Dev., 9, 1149-1163.
86. Schneider, B.L., Yang, Q.-H. and Futcher, A.B. (1996) Linkage of replication to Start by the Cdk inhibitor Sic1. Science, 272, 560-562.
87. 1 to S transition in S.cereviasiae. Cell, 79, 233-244.
88. Stern, B. and Nurse, P. (1996) A quantitative model for the cdc2 control of S-phase and mitosis in fission yeast. Trends Genet., 12, 345-350.
89. Stuart, D. and Wittenberg, C. (1995) CLN3, not positive feedback, determines the timing of CLN2 transcription in cycling cells. Genes Dev., 9, 2780-2794.
90. Sudakin, V., Ganoth, D., Dahan, A., Heller, H., Hershko, J., Luca, F.C., Ruderman, J.V. and Hershko, A. (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, 185-197.
91. Thanos, D. and Maniatis, T. (1995) NF-κB: a lesson in family values. Cell, 80, 529-532.
92. Traenkner, E.B.-H., Pahl, H.L., Henkel., T., Schmidt, K.N., Wilk, S. and Baeuerle, P. (1995) Phosphorylation of human IκB-α on serine 32 and 36 controls IκB-α proteolysis and NF-κB activation in response to diverse stimuli. EMBO J., 14, 2876-2883.
93. Treier, M., Staszewski, L.M. and Bohman, D. (1994) Ubiquitin-dependent c-Jun degradation in vivo is mediated by the ¶ domain. Cell, 78, 787-798.
94. Tugendreich, S., Tomkiel, J.W., Earnshaw, J. and Hieter, P. (1995) CDC27Hs colocalizes with CDC16Hs to the centrosome and mitotic spindle and is essential for the metaphase to anaphase transition. Cell, 81, 261-268.
95. Tyers, M., Tokiwa, G., Nash, R. and Futcher, B. (1992) The Cln3-Cdc28 kinase complex of S.cerevisiae is regulated by proteolysis and phosphorylation. EMBO J., 11, 1773-1784.
96. Van der Geer, P. and Hunter, T. (1994) Phosphopeptide mapping and phosphoamino acid analysis by electrophoresis and chromatography on thin-layer cellulose plates. Electrophoresis, 15, 544-554.
97. Verma, R., Feldman, R.M.R. and Deshaies, R.J. (1997) SIC1 is ubiquitinated in vitro by a pathway that requires CDC4, CDC34 and cyclin/CDK activities. Mol. Biol. Cell, 8, 1427-1437.
98. 1 cyclins for the degradation by the ubiquitin proteolytic pathway. Cell, 86, 453-463.
99. CDC28 protein kinase. Cell, 62, 225-237.
100. Won, K.-A. and Reed, S.I. (1996) Activation of cyclinE/CDK2 is coupled to site-specific autophosphorylation and ubiquitin-dependent degradation of cyclin E. EMBO J., 15, 37-44.
101. Wuarin, J. and Nurse, P. (1996) Regulating S phase: CDKs, licensing and proteolysis. Cell, 85, 785-787.
102. Cdc28-mediated control of Cln3 cyclin degradation. Mol. Cell. Biol., 15, 731-741.
103. Yamano, H., Ishii, K. and Yanagida, M. (1994) Phosphorylation of dis2 protein phosphatase at the C-terminal cdc2 consensus and its potential role in cell cycle regulation. EMBO J., 13, 5310-5318.
104. Yamano, H., Gannon, J. and Hunt, T. (1996) The role of proteolysis in cell cycle progression in Schizosaccharomyces pombe. EMBO J., 15, 5268-5279.
105. Yochem, J. and Byers, B. (1987) Structural comparison of the yeast cell division cycle gene CDC4 and a related pseudogene. J. Mol. Biol., 195, 233-245.