Phosphorylation-dependent degradation of the cyclin-dependent kinase inhibitor p27(Kip1)

EMBO Journal

Volumn 16, Issue 17, 1997, Pages 5334-5344

  Vlach, Jaromir ^a   Hennecke, Silke ^a   Amati, Bruno ^a  

^a SWISS INST FOR EXP CANCER RESEARCH   (Switzerland)

Author keywords

CDK; CKI; Cyclin; p27; Proteasome

Indexed keywords

CELL CYCLE PROTEIN; CYCLINE; PROTEASOME; PROTEIN KINASE INHIBITOR;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; CELL CYCLE G1 PHASE; COMPLEX FORMATION; GENE MUTATION; GENETIC CONSERVATION; NONHUMAN; POINT MUTATION; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN DEGRADATION; PROTEIN PHOSPHORYLATION; RAT; RETROVIRUS;

AMINO ACID SEQUENCE; ANIMALS; CDC2-CDC28 KINASES; CELL CYCLE PROTEINS; CELLS, CULTURED; CYCLIN E; CYCLIN-DEPENDENT KINASE 2; CYCLIN-DEPENDENT KINASE INHIBITOR P27; CYCLIN-DEPENDENT KINASES; CYSTEINE ENDOPEPTIDASES; ENZYME INHIBITORS; G1 PHASE; MICROTUBULE-ASSOCIATED PROTEINS; MOLECULAR SEQUENCE DATA; MULTIENZYME COMPLEXES; PHOSPHOPROTEINS; PHOSPHORYLATION; POINT MUTATION; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN BINDING; PROTEIN-SERINE-THREONINE KINASES; RATS; SEQUENCE HOMOLOGY, AMINO ACID; TUMOR SUPPRESSOR PROTEINS;

ANIMALIA; UNIDENTIFIED RETROVIRUS;

EID: 0030847760     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/16.17.5334     Document Type: Article

References (71)

1. Adams, P.D., Sellers, W.R., Sharma, S.K., Wu, A.D., Nalin, C.M. and Kaelin, W.G. (1996) Identification of a cyclin-cdk2 recognition motif present in substrates and p21-like cyclin-dependent kinase inhibitors. Mol. Cell. Biol., 16, 6623-6633.
2. Agrawal, D., Hauser, P., McPherson, F., Dong, F., Garcia, A. and Pledger, W.J. (1996) Repression of p27kip1 synthesis by platelet-derived growth factor in BALB/c 3T3 cells. Mol. Cell. Biol., 16, 4327-4336.
3. 1 cyclins in the next cycle. Cell, 77, 1037-1050.
4. Bai, C., Sen, P., Hofmann, 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.
5. 1 cyclins in yeast. Nature, 384, 279-282.
6. Brandeis, M. and Hunt, T. (1996) The proteolysis of mitotic cyclins in mammalian cells persists from the end of mitosis until the onset of S phase. EMBO J., 15, 5280-5289.
7. Catzavelos, C. et al. (1997) Decreased levels of the cell-cycle inhibitor p27Kip1 protein: Prognostic implications in primary breast cancer. Nature Med., 3, 227-230.
8. Ciechanover, A. (1994) The ubiquitin-proteasome proteolytic pathway. Cell, 79, 13-21.
9. Clurman, B.E., Sheaff, R.J., Thress, K., Groudine, M. and Roberts, J.M. (1996) Turnover of cyclin E by the ubiquitin-proteasome pathway is regulated by cdk2 binding and cyclin phosphorylation. Genes Dev., 10, 1979-1990.
10. Coats, S., Flanagan, W.M., Nourse, J. and Roberts, J.M. (1996) Requirement of p27(kip1) for restriction point control of the tibroblast cell cycle. Science, 272, 877-880.
11. 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.
12. de Nooij, J.C., Letendre, M.A. and Hariharan, I.K. (1996) A cyclin-dependent kinase inhibitor, dacapo, is necessary for timely exit from the cell cycle during Drosophila embryogenesis. Cell, 87, 1237-1247.
13. 1 cyclin Cln2p by a Cdc34p-dependent pathway. EMBO J., 14, 303-312.
14. Dynlacht, B.D., Flores, O., Lees, J.A. and Harlow, E. (1994) Differential regulation of E2F transactivation by cyclin/cdk2 complexes. Genes Dev., 8, 1772-1786.
15. Fero, M.L., Rivkin, M., Tasch, M., Porter, P., Carow, C.E., Firpo, E., Polyak, K., Tsai, L.H., Broudy, V. Perlmutter, R.M., Kaushansky, K. and Roberts, J.M. (1996) A syndrome of multiorgan hyperplasia with features of gigantism, tumorigenesis, and female sterility in p27(kip1)-deficient mice. Cell, 85, 733-744.
16. Fotedar, R., Fitzgerald, P., Rousselle, T., Cannella, D., Doree, M., Messier, H. and Fotedar, A. (1996) p21 contains independent binding sites for cyclin and cdk2: both sites are required to inhibit cdk2 kinase activity. Oncogene, 12, 2155-2164.
17. Fredersdorf, S. et al. ( 1997) High level expression of p27Kip1 and cyclin D1 in some human breast cancer cells: Inverse correlation between the expression of p27Kip1 and degree of malignancy in human breast and colorectal cancers. Proc. Natl Acad. Sci. USA, 94, 6380-6385.
18. Goubin, F. and Ducommun, B. (1995) Identification of binding domains on the p21Cip1 cyclin-dependent kinase inhibitor. Oncogene, 10, 2281-2287.
19. Halevy, O., Novitch, B.G., Spicer, D.B., Skapek, S.X., Rhee, J., Hannon, G.J., Beach, D. and Lassar, A.B. (1995) Correlation of terminal cell cycle arrest of skeletal muscle with induction of p21 by MyoD. Science, 267, 1018-1021.
20. Harper, J.W. and Elledge, S.J. (1996) Cdk inhibitors in development and cancer. Curr. Opin. Genet. Dev., 6, 56-64.
21. Hengst, L. and Reed, S.I. (1996) Translational control of p27Kip1 accumulation during the cell cycle. Science, 271, 1861-1864.
22. Hengst, L., Dulic, V. Slingerland, J.M., Lees, E. and Reed, S.I. (1994) A cell cycle-regulated inhibitor of cyclin-dependent kinases. Proc. Natl Acad. Sci. USA, 91, 5291-5295.
23. Hershko, A. and Ciechanover, A. (1992) The ubiquitin system for protein degradation. Annu. Rev. Biochem., 61, 761-807.
24. Isaksson, A., Musti, A.M. and Bohmann, D. (1996) Ubiquitin in signal transduction and cell transformation. Biochim. Biophys. Acta, 1288, F21-F29.
25. Jackson, P.K. (1996) Cull and destroy. Curr. Biol., 6, 1209-1212.
26. Jentsch, S. (1992) The ubiquitin-conjugation system. Annu. Rev. Genet., 26, 179-207.
27. 1 phase arrest mediated by an inhibitor (p27Kip1) of cyclin-dependent kinase 4 activation. Cell, 79, 487-496.
28. King, R.W., Deshaies, R.J., Peters, J.-M. and Kirschner, M.W. (1996) How proteolysis drives the cell cycle. Science, 274, 1652-1652.
29. Kiyokawa, H., Kineman, R.D., Manovatodorova, K.O., Soares, V.C., Hoffman, E.S., Ono, M., Khanam, D., Hayday, A.C., Frohman, L.A. and Koff, A. (1996) Enhanced growth of mice lacking the cyclin-dependent kinase inhibitor function of p27(kip1). Cell, 85, 721-732.
30. Kiek, W., Ewen, M.E., Shirodkar, S., Arany, Z., Kaelin, W.J. and Livingston, D.M. (1994) Negative regulation of the growth-promoting transcription factor E2F-1 by a stably bound cyclin A-dependent protein kinase. Cell. 78, 161-172.
31. Lane, M.E., Sauer, K., Wallace, K., Jan, Y.N., Lehner, C.F. and Vaessm, H. (1996) Dacapo, a cyclin-dependent kinase inhibitor, stops cell proliferation during drosophila development. Cell, 87, 1225-1235.
32. 1 cyclin Cln2 induced by CDK-dependent phosphorylation. Science, 271, 1597-1601.
33. Lee, M.H., Reynisdottir, I. and Massague, J. (1995) Cloning of p57KIP2, a cyclin-dependent kinase inhibitor with unique domain structure and tissue distribution. Genes Dev., 9, 639-649.
34. Lin, J., Reichner, C., Wu, X. and Levine, A.I. (1996) Analysis of wild-type and mutant p21WAF-1 gene activities. Mol. Cell. Biol., 16, 1786-93.
35. Loda, M., Cukor, B., Tam, S.W., Lavin, P., Fiorentino, M., Draetta, G.F., Jessup, J.M. and Pagano, M. (1997) Increased proteasome-dependent degradation of the cylin-dependent kina inhibitor p27 in aggressive colorectal carcinomas. Nature Med., 3, 231-234.
36. Luo, Y., Hurwitz, J. and Massague, J. (1995) Cell-cycle inhibition by independent CDK and PCNA binding domains in p21Cip1. Nature, 375, 159-161.
37. Mathias, N., Johnson, S.L., Winey, M., Adams, A., Goetsch, L., Pringle, J.R., Byers, B. and Goebl, M.G. (1996) Cdc53p acts in concert with Cdc4p and Cdc34p to control the G(1)-to-S-phase transition and identifies a conserved family of proteins. Mol. Cell. Biol. 16, 6634-6643.
38. Matsuoka, S., Edwards, M.C., Bai, C., Parker, S., Zhang, P., Baldmi, A., Harper, J.W. and Elledge, S.J. (1995) p57KIP2, a structurally distinct member of the p21CIP1 Cdk inhibitor family, is a candidate tumor suppressor gene. Genes Dev., 9, 650-662.
39. Matsushime, H., Quelle, D.E., Shurtleff, S.A., Shibuya, M., Sherr, C.J. and Kato, J.Y. (1994) D-type cyclin-dependent kinase activity in mammalian cells. Mol. Cell. Biol., 14, 2066-2076.
40. Meijer, L. (1996) Chemical inhibitors of cyclin-dependent kinases. Trends Cell Biol., 6, 393-397.
41. Morgan, D.O. (1995) Principles of CDK regulation. Nature, 374, 131-134.
42. Nakanishi, M., Robetorye, R.S., Adami, G.R., Pereira-Smith, O.M. and Smith, J.R. (1995) Identification of the active region of the DNA synthesis inhibitory gene p21Sdi1/CIP1/WAF1. EMBO J., 14, 555-563.
43. Nakayama, K., Ishida, N., Shirane, M., Inomata, A., Inoue, T., Shishido, N., Hori, I., Loh, D.Y. and Nakayama, K. (1996) Mice lacking p27(kip1) display increased body size, multiple organ hyperplasia, retinal dysplasia, and pituitary tumors. Cell, 85, 707-720.
44. Nasmyth, K. (1996) At the heart of the yeast cell cycle. Trends Genet., 12, 405-413.
45. Nourse, J., Firpo, E., Flanagan, W.M., Coats, S., Polyak, K., Lee, M.H., Massagué, J., Crabtree, G. and Roberts, J. (1994) Interleukin-2-mediated elimination of p27 Kip1 cyclin-dependent kinase inhibitor prevented by rapamycin. Nature, 372, 570-573.
46. 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.
47. Pagano, M., Tam, S.W., Theodoras, A.M., Beer, R.P, Del, S.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.
48. Pahl, H.L. and Baeuerle, P.A. (1996) Control of gene expression by proteolysis. Curr. Opin. Cell Biol., 8, 340-347.
49. Peter, M. and Herskowitz, I. (1994) Joining the complex: cyclin-dependent kinase inhibitory proteins and the cell cycle. Cell, 79, 181-184.
50. Polyak, K., Kato, J.Y., Solomon, M.J., Sherr, C.J., Massague, J., Roberts, J.M. and Koff, A. (1994a) p27Kip1, a cyclin-Cdk inhibitor, links transforming growth factor-beta and contact inhibition to cell cycle arrest. Genes Dev., 8, 9-22.
51. Polyak, K., Lee, M.H., Erdjument, B.H., Koff, A., Roberts, J.M., Tempst, P. and Massague, J. (1994b) Cloning of p27Kip1, a cyclin-dependent kinase inhibitor and a potential mediator of extracellular antimitogenic signals. Cell, 78, 59-66.
52. Poon, R.Y.C., Toyoshima, H. and Hunter, T. (1995) Redistribution of the CDK inhibitor p27 between different cyclin-CDK complexes in the mouse fibroblast cell cycle and in cells arrested with lovastatin and ultraviolet irradiation. Mol. Biol. Cell. 6, 1197-1213.
53. Porter, P.L., Malone, K.E., Heagerty, P.J., Alexander, G.M., Gatti, L.A., Firpo, E.J., Daling, J.R. and Roberts, J.M. (1997) Expression of cell-cycle regulators p27(kip1) and cyclin E, alone and in combination, correlate with survival in young breast cancer patients. Nature Med., 3, 222-225.
54. Reynisdottir, I., Polyak, K., Iavarone, A. and Massague, J. (1995) Kip/Cip and Ink4 Cdk inhibitors cooperate to induce cell cycle arrest in response to TGF-beta. Genes Dev., 9, 1831-1845.
55. 0 state) on fibroblasts. J. Biol. Chem., 271, 18337-18341.
56. Rock, K.L., Gramm, C., Rothstein, L., Clark, K., Stein, R., Dick, L., Hwang, D. and Goldberg, A.L. (1994) Inhibitors of the proteasome block the degradation of most cell proteins and the generation of peptides presented on MHC class I molecules. Cell, 78, 761-771.
57. Kip1 cyclin-dependent kinase inhibitor bound to the cyclin A-Cdk2 complex. Nature, 382, 325-331.
58. 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.
59. 1 to S transition in S. cerevisiae. Cell, 79, 233-244.
60. Sheaff, R.J., Groudine, M., Gordon, M., Roberts, J.M. and Clurman, B.E. (1997) Cyclin E-CDK2 is a regulator of p27Kip1. Genes Dev., 11, 1464-1478.
61. 1 cyclin-dependent kinases. Genes Dev., 9, 1149-1163.
62. Slingerland, J.M., Hengst, L., Pan, C.H., Alexander, D., Stampfer, M.R. and Reed, S.I. (1994) A novel inhibitor of cyclin-Cdk activity detected in transforming growth factor beta-arrested epithelial cells. Mol. Cell. Biol., 14, 3683-3694.
63. Soos, T.J., Kiyokawa, H., Yan, J.S., Rubin, M.S., Giordano, A., DeBlasio, A., Bottega, S., Wong, B., Mendelsohn, J. and Koff, A. (1996) Formation of p27-CDK complexes during the human mitotic cell cycle. Cell Growth Differ., 7, 135-146.
64. Su, J.Y., Rempel, R.E., Erikson, E. and Maller, J.L. (1995) Cloning and characterization of the Xenopus cyclin-dependent kinase inhibitor p27XIC1. Proc. Natl Acad. Sci. USA, 92, 10187-10191.
65. 1 cyclin-Cdk protein kinase activity, is related to p21. Cell, 78, 67-74.
66. 1 cyclin function at Start. Proc. Natl Acad. Sci. USA, 93, 7772-7776.
67. kip1 is abrogated by c-Myc. EMBO J., 15, 6595-6604.
68. 1 cyclins for degradation by the ubiquitin proteolytic pathway. Cell, 86, 453-463.
69. Won, K.-A. and Reed, S.I. (1996) Activation of cyclin E-CDK2 is coupled to site-specific autophosphorylation and ubiquitin-dependent degradation of cyclin E. EMBO J., 15, 4182-4193.
70. Yaglom, J., Linskens, M.H., Sadis, S., Rubin, D.M., Futcher, B. and Finley, D. (1995) p34Cdc28-mediated control of Cln3 cyclin degradation. Mol. Cell. Biol., 15, 731-741.
71. Zhu, L., Harlow, E. and Dynlacht, B.D. (1995) p107 uses a p21CIP1-related domain to bind cyclin/cdk2 and regulate interactions with E2F. Genes Dev., 9, 1740-1752.