Retinoblastoma tumor suppressor protein signals through inhibition of cyclin-dependent kinase 2 activity to disrupt PCNA function in S phase

Molecular and Cellular Biology

Volumn 21, Issue 12, 2001, Pages 4032-4045

  Sever Chroneos, Zvjezdana ^a,c   Angus, Steven P ^a   Fribourg, Anne F ^a   Wan, Huajing ^a   Todorov, Ivan ^b   Knudsen, Karen E ^a   Knudsen, Erik S ^a  

^a UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF TEXAS HEALTH CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN A; CYCLIN DEPENDENT KINASE 2; CYCLINE; RETINOBLASTOMA PROTEIN;

ANIMAL CELL; ARTICLE; CELL CYCLE S PHASE; CHROMATIN; DNA REPLICATION; ENZYME INHIBITION; GENE EXPRESSION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DNA BINDING; PROTEIN INDUCTION; SIGNAL TRANSDUCTION;

ANIMALS; BASE SEQUENCE; CDC2-CDC28 KINASES; CELL LINE; CHROMATIN; CYCLIN A; CYCLIN-DEPENDENT KINASE 2; CYCLIN-DEPENDENT KINASES; DNA PRIMERS; DNA REPLICATION; DNA-BINDING PROTEINS; PROLIFERATING CELL NUCLEAR ANTIGEN; PROTEIN-SERINE-THREONINE KINASES; RATS; REPLICATION PROTEIN A; RETINOBLASTOMA PROTEIN; S PHASE; SIGNAL TRANSDUCTION;

ANIMALIA;

EID: 0034996508     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.21.12.4032-4045.2001     Document Type: Article

References (65)

1. Bartek, J., J. Bartkova, and J. Lukas. 1997. The retinoblastoma protein pathway in cell cycle control and cancer. Exp. Cell Res. 237:1-6.
2. Bashir, T., R. Horlein, J. Rommelaere, and K. Willwand. 2000. Cyclin A activates the DNA polymerase delta-dependent elongation machinery in vitro: a parvovirus DNA replication model. Proc. Natl. Acad. Sci. USA 97:5522-5527.
3. Bravo, R. 1986. Synthesis of the nuclear protein cyclin (PCNA) and its relationship with DNA replication. Exp. Cell Res. 163:287-293.
4. Brehm, A., E. A. Miska, D. J. McCance, J. L. Reid, A. J. Bannister, and T. Kouzarides. 1998. Retinoblastoma protein recruits histone deacetylase to repress transcription. Nature 391:597-601.
5. Bremner, R., B. L. Cohen, M. Sopta, P. A. Hamel, C. J. Ingles, B. L. Gallie, and R. A. Phillips. 1995. Direct transcriptional repression by pRB and its reversal hy specific cyclins. Mol. Cell. Biol. 15:3256-3265.
6. Brylawski, B. P., S. M. Cohen, J. L. Longmire, N. A. Doggett, M. Cordeiro-Stone, and D. G. Kaufman. 2000. Construction of a cosmid library of DNA replicated early in the S phase of normal human fibroblasts. J. Cell. Biochem. 78:509-517.
7. Bunch, R. T., and A. Eastman. 1997. 7-Hydroxystaurosporine (UCN-01) causes redistribution of proliferating cell nuclear antigen and abrogates cisplatin-induced S-phase arrest in Chinese hamster ovary cells. Cell Growth Differ. 8:779-788.
8. Chen, J., R. Peters, P. Saha, P. Lee, A. Theodoras, M. Pagano, G. Wagner, and A. Dutta. 1996. A 39 amino acid fragment of the cell cycle regulator p21 is sufficient to bind PCNA and partially inhibit DNA replication in vivo. Nucleic Acids Res. 24:1727-1733.
9. Chew, Y. P., M. Ellis, S. Wilkie, and S. Mittnacht. 1998. pRB phosphorylation mutants reveal role of pRB in regulating S phase completion by a mechanism independent of E2F. Oncogene 17:2177-2186.
10. Dimitrova, D. S., I. T. Todorov, T. Melendy, and D. M. Gilbert. 1999. Mcm2, but not RPA, is a component of the mammalian early G1-phase prereplication complex. J. Cell. Biol. 146:709-722.
11. Dimitrova, D. S., and D. M. Gilbert. 2000. Temporally coordientated assembly and disassembly of replication factories in the absence of DNA synthesis. Nat. Cell Biol. 2:686-694.
12. Donovan, S., and J. F. Diffley. 1996. Replication origins in eukaroytes. Curr. Opin. Genet. Dev. 6:203-207.
13. Dyson, N. 1998. The regulation of E2F by pRB-family proteins. Genes Dev. 12:2245-2262.
14. Findeisen, M., M. El-Denary, T. Kapitza, R. Graf, and U. Strausfeld. 1999. Cyclin A-dependent kinase activity affects chromatin binding of ORC, Cdc6, and MCM in egg extracts of Xenopus laevis. Eur. J. Biochem. 264:415-426.
15. Flores-Rozas, H., D. Clark, and R. D. Kolodner. 2000. Proliferating cell nuclear antigen and Msh2p-Msh6p interact to form an active mispair recognition complex. Nat. Genet. 26:375-378.
16. Fotedar, A., D. Cannella, P. Fitzgerald, T. Rousselle, S. Gupta, M. Doree, and R. Fotedar. 1996. Role for cyclin A-dependent kinase in DNA replication in human S phase cell extracts. J. Biol. Chem. 271:31627-31637.
17. Fotedar, R., and A. Fotedar. 1995. Cell cycle control of DNA replication. Prog. Cell Cycle Res. 1:73-89.
18. Fujita, M. 1999. Cell cycle regulation of DNA replication initiation proteins in mammalian cells. Front. Biosci. 4:D816-D823.
19. Fujita, M., T. Kiyono, Y. Hayashi, and M. Ishibashi. 1996. hCDC47, a human member of the MCM family: dissociation of the nucleus-bound form during S phase. J. Biol. Chem. 271:4349-4354.
20. Henricksen, L. A., and M. S. Wold. 1994. Replication protein A mutants lacking phosphorylation sites for p34cdc2 kinase support DNA replication J. Biol. Chem. 269:24203-24208.
21. Hinds, P. W., S. Mittnacht, V. Dulic, A. Arnold, S. I. Reed, and R. A. Weinberg. 1992. Regulation of retinoblastoma protein functions by ectopic expression of human cyclins. Cell 70:993-1006.
22. Ishimi, Y., Y. Komamura-Kohno, Z. You, A. Omori, and M. Kitagawa. 2000. Inhibition of Mcm4,6,7 helicase activity by phosphorylation with cyclin A/Cdk2. J. Biol. Chem. 275:16235-16241.
23. Jiang, W., N. J. Wells, and T. Hunter. 1999. Multistep regulation of DNA replication by Cdk phosphorylation of HsCdc6. Proc. Natl. Acad. Sci. USA 96:6193-6198.
24. Kaelin, W. G., Jr. 1997. Recent insights into the functions of the retinoblastoma susceptibility gene product. Cancer Investig. 15:243-254.
25. Kearsey, S. E., D. Maiorano, E. C. Holmes, and I. T. Todorov. 1996. The role of MCM proteins in the cell cycle control of genome duplication. Bioessays 18:183-190.
26. Knudsen, E. S., C. Buckmaster, T. T. Chen, J. R. Feramisco, and J. Y. Wang. 1998. Inhibition of DNA synthesis by RB: effects on G1/S transition and S-phase progression. Genes Dev. 12:2278-2292.
27. Knudsen, E. S., and J. Y. Wang. 1996. Differential regulation of retinoblastoma protein function by specific Cdk phosphorylation sites. J. Biol. Chem. 271:8313-8320.
28. Knudsen, E. S., and J. Y. Wang. 1997. Dual mechanisms for the inhibition of E2F binding to RB by cyclin-dependent kinase-mediated RB phosphorylation. Mol. Cell. Biol. 17:5771-5783.
29. Knudsen, K. E., E. Weber, K. C., Arden, W. K., Cavenee, J. R. Feramisco, and E. S. Knudsen. 1999. RB inhibits cellular proliferation through two distinct mechanisms: inhibition of cell cycle progression and induction of cell death. Oncogene 20:345-349.
30. Knudsen, K. E., K. C. Arden, and W. K. Cavenee. 1998. Multiple G1 regulatory elements control the androgen-dependent proliferation of prostatic carcinoma cells. J. Biol. Chem. 273:20213-20222.
31. Knudsen, K. E., D. Booth, S. Naderi, Z. Sever-Chroneos, A. F. Fribourg, I. Hunton, J. R. Feramisco, J. Y. J. Wang, and E. S. Knudsen. 2000. RB-dependent S-phase response to DNA-damage. Mol. Cell. Biol. 20:7751-7763.
32. Knudsen, K. E., A. F. Fribourg, M. W. Strobeck, J. M. Blanchard, and E. S. Knudsen. 1999. Cyclin A is a functional target of retinoblastoma tumor suppressor protein-mediated cell cycle arrest. J. Biol. Chem. 274:27632-27641.
33. Komatsu, K., W. Wharton, H. Hang, C. Wu, S. Singh, H. B. Lieberman, W. J. Pledger, and H. G. Wang. 2000. PCNA interacts with hHus1/hRad9 in response to DNA damage and replication inhibition. Oncogene 19:5291-5297.
34. Krek, W., M. E. Ewen, S. Shirodkar, Z. Arany, W. G. Kaelin, Jr., and D. M. Livingston. 1994. Negative regulation of the growth-promoting transcription factor E2F-1 by a stably bound cyclin A-dependent protein kinase. Cell 78:161-172.
35. Krek, W., G. Xu, and D. M. Livingston. 1995. Cyclin A-kinase regulation of E2F-1 DNA binding function underlies suppression of an S phase checkpoint. Cell 83:1149-1158.
36. Levenson, V., and J. L. Hamlin. 1993. A general protocol for evaluating the specific effects of DNA replication inhibitors. Nucleic Acids Res. 21:3997-4004.
37. Lukas, C., C. S. Sorensen, E. Kramer, E. Santoni-Rugiu, C. Lindeneg, J. M. Peters, J. Bartek, and J. Lukas. 1999. Accumulation of cyclin B1 requires E2F and cyclin-A-dependent rearrangement of the anaphase-promoting complex. Nature 401:815-818.
38. Lukas, J., J. Bartkova, M. Rohde, M. Strauss, and J. Bartek. 1995. Cyclin D1 is dispensable for G1 control in retinoblastoma gene-deficient cells independently of cdk4 activity. Mol. Cell. Biol. 15:2600-2611.
39. Lukas, J., T. Herzinger, K. Hansen, M. C. Moroni, D. Resnitzky, K. Helin, S. I. Reed, and J. Bartek. 1997. Cyclin E-induced S phase without activation of the pRb/E2F pathway. Genes Dev. 11:1479-1492.
40. Lukas, J., D. Parry, L. Aagaard, D. J. Mann, J. Bartkova, M. Strauss, G. Peters, and J. Bartek. 1995. Retinoblastoma-protein-dependent cell-cycle inhibition by the tumour suppressor p16. Nature 375:503-506.
41. Lukas, J., C. S. Sorensen, C. Lukas, E. Santoni-Rugiu, and J. Bartek. 1999. p16INK4a, but not constitutively active pRb, can impose a sustained G1 arrest: molecular mechanisms and implications for oncogenesis. Oncogene 18:3930-3935.
42. Magnaghi-Jaulin, L., R. Groisman, I. Naguibneva, P. Robin, S. Lorain, J. P. Le Villain, F. Troalen, D. Trouche, and A. Harel-Bellan. 1998. Retinoblastoma protein represses transcription by recruiting a histone deacetylase. Nature 391:601-605.
43. Mittnacht, S. 1998. Control of pRB phosphorylation. Curr. Opin. Genet. Dev. 8:21-27.
44. Nevins, J. R. 1998. Toward an understanding of the functional complexity of the E2F and retinoblastoma families. Cell Growth Differ. 9:585-593.
45. Ogryzko, V. V., P. Wong, and B. H. Howard. 1997. WAF1 retards S-phase progression primarily by inhibition of cyclin-dependent kinases. Mol. Cell. Biol. 17:4877-4882.
46. 1-to-S phase transition. Mol. Cell. Biol. 15:2612-2624.
47. Pelizon, C., M. A. Madine, P. Romanowski, and R. A. Laskey. 2000. Unphosphorylatable mutants of cdc6 disrupt its nuclear export but still support DNA replication once per cell cycle. Genes Dev. 14:2526-2533.
48. Petersen, B. O., J. Lukas, C. S. Sorensen, J. Bartek, and K. Helin. 1999. Phosphorylation of mammalian CDC6 by cyclin A/CDK2 regulates its subcellular localization. EMBO J. 18:396-410.
49. Prelich, G., M. Kostura, D. R. Marshak, M. B. Mathews, and B. Stillman. 1987. The cell-cycle regulated proliferating cell nuclear antigen is required for SV40 DNA replication in vitro Nature 326:471-475.
50. Prosperi, E. 1997. Multiple roles of the proliferating cell nuclear antigen: DNA replication, repair and cell cycle control. Prog. Cell Cycle Res. 3:193-210.
51. Prosperi, E., A. I. Scovassi, L. A. Stivala, and L. Bianchi. 1994. Proliferating cell nuclear antigen bound to DNA synthesis sites: phosphorylation and association with cyclin D1 and cyclin A. Exp. Cell Res. 215:257-262.
52. Roussel, M. F. 1998. Key effectors of signal transduction and G1 progression. Advances in Cancer Res. 74:1-24.
53. Saudan, P., J. Vlach, and P. Beard. 2000. Inhibition of S-phase progression by adeno-associated virus rep78 protein is mediated by hypophosphorylated pRb. EMBO J. 19:4351-4361.
54. Sherr, C. J. 1996. Cancer cell cycles. Science 274:1672-1677.
55. Shivji, M. K., S. J. Grey, U. P. Strausfeld, R. D. Wood, and J. J. Blow. 1994. Cip1 inhibits DNA replication but not PCNA-dependent nucleotide excision-repair. Curr. Biol. 4:1062-1068.
56. Stillman, B. 1996. Cell cycle control of DNA replication. Science 274:1659-1664.
57. Strobeck, M. W., M. DeCristafaro, A. F. Fribourg, K. E. Knudsen, B. Weissman, A. N. Imbalzano, and E. S. Knudsen. 2000. Brg-1 is required for RB-mediated arrest. Proc. Natl. Acad. Sci. USA 57:3475-3480.
58. Todorov, I. T., A. Attaran, and S. E. Kearsey. 1995. BM28, a human member of the MCM2-3-5 family, is displaced from chromatin during DNA replication. J. Cell. Biol. 129:1433-1445.
59. Toschi, L., and R. Bravo. 1988. Changes in cyclin/proliferating cell nuclear antigen distribution during DNA repair synthesis. J. Cell. Biol. 107:1623-1628.
60. Waga, S., G. J. Hannon, D. Beach, and B. Stillman. 1994. The p21 inhibitor of cyclin-dependent kinases controls DNA replication by interaction with PCNA. Nature 369:574-578.
61. Waga, S., and B. Stillman. 1998. The DNA replication fork in eukaryotic cells. Annu. Rev. Biochem. 67:721-751.
62. Wang, J. Y., E. S. Knudsen, and P. J. Welch. 1994. The retinoblastoma tumor suppressor protein. Adv. Cancer Res. 64:25-85.
63. Weinberg, R. A. 1995. The retinoblastoma protein and cell cycle control. Cell 81:323-330.
64. Welch, P. J., and J. Y. Wang. 1993. A C-terminal protein-binding domain in the retinoblastoma protein regulates nuclear c-Abl tyrosine kinase in the cell cycle. Cell 75:779-790.
65. Zhang, H. S., M. Gavin, A. Dahiya, A. A. Postigo, D. Ma, R. X. Luo, J. W. Harbour, and D. C. Dean. 2000. Exit from G1 and S phase of the cell cycle is regulated hy repressor complexes containing HDAC-Rb-hSWI/SNF and Rb-hSWI/SNF. Cell 101:79-89.