Phosphorylation of mammalian CDC6 by cyclin A/CDK2 regulates its subcellular localization

EMBO Journal

Volumn 18, Issue 2, 1999, Pages 396-410

  Petersen, Birgit Otzen ^b   Lukas, Jiri ^a   Sørensen, Claus Storgaard ^a   Bartek, Jiri ^a   Helin, Kristian ^b  

^a DANISH CANCER SOCIETY RESEARCH CENTER   (Denmark)

^b EUROPEAN INSTITUTE OF ONCOLOGY   (Italy)

Author keywords

CDC6; Cyclin A; DNA replication; Phosphorylation

Indexed keywords

CYCLIN A; CYCLIN B; CYCLIN DEPENDENT KINASE; CYCLIN E;

ARTICLE; CELL CYCLE; CELL NUCLEUS; CELLULAR DISTRIBUTION; CYTOPLASM; DNA REPLICATION; ENZYME PHOSPHORYLATION; GENE EXPRESSION REGULATION; PRIORITY JOURNAL; PROTEIN DOMAIN; SEQUENCE ANALYSIS;

ANIMALS; BASE SEQUENCE; BINDING SITES; CDC2-CDC28 KINASES; CELL CYCLE; CELL CYCLE PROTEINS; CELL LINE; COS CELLS; CYCLIN A; CYCLIN-DEPENDENT KINASE 2; CYCLIN-DEPENDENT KINASES; DNA PRIMERS; HUMANS; NUCLEAR PROTEINS; PHOSPHORYLATION; PROTEIN KINASES; PROTEIN-SERINE-THREONINE KINASES; RATS; RECOMBINANT PROTEINS; S PHASE; SUBCELLULAR FRACTIONS; TRANSFECTION;

MAMMALIA;

EID: 0033556238     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/18.2.396     Document Type: Article

References (74)

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. Aparicio, O.M., Weinstein, D.M. and Bell, S.P. (1997) Components and dynamics of DNA replication in S.cerevisiae: Redistribution of MCM proteins and Cdc45p duing S phase. Cell, 90, 59-69.
3. Bartek, J., Bartkova, J. and Lukas, J. (1996) The retinoblastoma protein pathway and the restriction point. Curr. Opin. Cell Biol., 8, 805-814.
4. Botchan, M. (1996) Coordinating DNA replication with cell division: Current status of the licensing concept. Proc. Natl Acad. Sci. USA, 93, 9997-10000.
5. 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.
6. Bravo, R. and Macdonald-Bravo, H. (1987) Existence of two populations of cyclin/proliferating cell nuclear antigen during the cell cycle: association with DNA replication sites. J. Cell Biol., 105, 1549-1554.
7. Broek, D., Bartlett, R., Crawford, K. and Nurse, P. (1991) Involvement of p34cdc2 in establishing the dependency of S phase on mitosis. Nature, 349, 388-393.
8. 1 expression and multistage dynamics of cyclin A in human osteosarcoma cells. Oncogene, 8, 1649-1659.
9. Carpenter, P.B., Mueller, P.R. and Dunphy, W.G. (1996) Role for a Xenopus Orc2-related protein in controlling DNA replication. Nature, 379, 357-360.
10. Chen, J., Saha, P., Kornbluth, S., Dynlacht, B.D. and Dutta, A. (1996) Cyclin-binding motifs are essential for the function of p21CIP1. Mol. Cell. Biol., 16, 4673-4682.
11. Chong, J.P.J., Mahbubani, M.H., Khoo, C.-Y. and Blow, J.J. (1995) Purification of an Mcm-containing complex as a component of the DNA replication licensing system. Nature, 375, 418-421.
12. Cocker, J.H., Piatti, S., Santocanale, C., Nasmyth, K. and Diffley, J.F. (1996) An essential role for the Cdc6 protein in forming prereplicative complexes of budding yeast. Nature, 379, 180-182.
13. Coleman, T.R., Carpenter, P.B. and Dunphy, W.G. (1996) The Xenopus Cdc6 proteins is essential for the initiation of a single round of DNA replication in cell-free extracts. Cell, 87, 53-63.
14. Dahmann, C., Diffley, J.F.X. and Nasmyth, K.A. (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.
15. Dalton, S. and Whitbread, L. (1995) Cell cycle regulated nuclear import and export of Cdc47, a protein essential for initiation of DNA replication in budding yeast. Proc. Natl Acad. Sci. USA, 92, 2514-2518.
16. Diffley, J.F.X. (1996) Once and once only upon a time: specifying and regulating origins of DNA replication in eukaryotic cells. Genes Dev., 10, 2819-2830.
17. Diffley, J.F.X., Cocker, J.H., Dowell, S.J. and Rowley, A. (1994) Two steps in the assembly of complexes at yeast replication origins in vivo. Cell, 78, 303-316.
18. Donovan, S., Harwood, J., Drury, L.S. and Diffley, J.F.X. (1997) Cdc6p-dependent loading of Mcm proteins onto pre-replicative chromatin in budding yeast. Proc. Nutl Acad. Sci. USA, 94, 5611-5616.
19. 1-S phase protein kinase. Science, 257, 1958-1961.
20. Dutta, A. and Bell, S.P. (1997) Initiation of DNA replication in eukaryotic cells. Annu. Rev. Cell Dev. Biol., 13, 293-332.
21. Elsasser, S., Lou, F., Wang, B., Campbell, J.L. and Jong, A. (1996) Interaction between yeast Cdc6 protein and B-type cyclin/Cdc28 kinases. Mol. Biol. Cell, 7, 1723-1735.
22. Ewen, M., Faha, B., Harlow, E. and Livingston, D. (1992) Interaction of p107 with cyclin A independent of complex formation with viral oncoproteins. Science, 255, 85-87.
23. Faha, B.F., Harlow, E. and Lees, E.M. (1993) The adenovirus E1A-associated kinase consists of cyclin E/p33cdk2 and cyclin A/p33cdk2. J. Virol., 67, 2456-2465.
24. Field, J., Nikawa, J.-I., Broek, D., MacDonald, B., Rodgers, L., Wilson, I.A., Lerner, R.A. and Wigler, M. (1988) Purification of a RAS-responsive adenylyl cyclase complex from Saccharomyces cerevisiae by use of an epitope addition method. Mol. Cell. Biol., 8, 2159-2165.
25. Fox, C.A., Loo, S., Dillin, A. and Rine, J. (1995) The origin recognition complex has essential functions in transcriptional silencing and chromosomal replication. Genes Dev., 9, 911-924.
26. Girard, F., Strausfeld, U., Fernandez, A. and Lamb, N. (1991) Cyclin A is required for the onset of DNA replication in mammalian fibroblasts. Cell, 67, 1169-1179.
27. Graham, F.L. and Van der Eb, A.J. (1973) A new technique for the assay of infectivity of human adenovirus. Virology, 52, 456-467.
28. Grallert, B. and Nurse, P. (1996) The ORC1 homolog orp1 in fission yeast plays a key role in regulating onset of S phase. Genes Dev., 10, 2644-2654.
29. Hateboer, G., Wobst, A., Petersen, B.O., Le Cam, L., Vigo, E., Sardet, C. and Helin, K. (1998) Cell-cycle regulated expression of mammalian CDC6 is dependent on E2F. Mol. Cell. Biol., 18, 6679-6697.
30. Hayles, J., Fisher, D., Woolard, A. and Nurse, P. (1994) Temporal order of S phase and mitosis in fission yeast is determined by the state of the p34cdc2/mitotic cyclin B complex. Cell, 78, 813-822.
31. Helin, K. (1998) Regulation of cell proliferation by the E2F transcription factors. Curr. Opin. Genet. Dev., 8, 28-35.
32. Hennesy, K.M., Lee, A., Chen, E. and Botstein, D. (1991) A group of interacting yeast DNA replication genes. Genes Dev., 5, 958-969.
33. Hinds, P.W., Mittnacht, S., Dulic, V., Arnold, A., Reed, S.I. and Weinberg, R.A. (1992) Regulation of retinoblastoma protein functions by ectopic expression of human cyclins. Cell, 70, 993-1006.
34. Jallepalli, P.V., Brown, G.W., Muzi-Falconi, M., Tien, D. and Kelly, T.J. (1997) Regulation of the replication initiation protein p65cdc18 by CDK phosphorylation. Genes Dev., 11, 2767-2779.
35. Kelly, T.J., Martin, G.S., Forsburg, S.L., Stephen, R.J., Russo, A. and Nurse, P. (1993) The fission yeast cdc18+ gene product couples S phase to START and mitosis. Cell, 74, 371-382.
36. Klemm, R.D., Austin, R.J. and Bell, S.P. (1997) Coordinate binding of ATP and origin DNA regulates the ATPase activity of the origin recognition complex. Cell, 88, 493-502.
37. Kubota, Y., Mimura, S., Nishimoto, S., Takisawa, H. and Nojima, H. (1995) Identification of yeast MCM3-related protein as a component of Xenopus DNA replication licensing factor. Cell, 81, 601-609.
38. Leatherwood, J., Lopez-Girona, A. and Russel, P. (1996) Interaction of Cdc2 and Cdc18 with a fission yeast ORC2-like protein. Nature, 379, 360-363.
39. Liang, C. and Stillman, B. (1997) Persistent initiation of DNA replication and chromatin-bound MCM proteins during the cell cycle in cdc6 mutants. Genes Dev., 11, 3375-3386.
40. Liang, C., Weinreich, M. and Stillman, B. (1995) ORC and Cdc6p interact and determine the frequency of initiation of DNA replication in the genome. Cell, 81, 667-676.
41. Lukas, J., Petersen, B.O., Holm, K., Bartek, J. and Helin, K. (1996) Deregulated expression of E2F family members induces S-phase entry and overcomes p16INK4A-mediated growth suppression. Mol. Cell. Biol., 16, 1047-1057.
42. Madine, M.A., Khoo, C.-Y., Mills, A.D. and Laskey, R.A. (1995) MCM3 complex required for cell cycle regulation of DNA replication in vertebrate cells. Nature, 375, 421-424.
43. 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.
44. 1 kinase activity for cdk6, a novel cyclin D partner. Mol. Cell. Biol., 14, 2077-2086.
45. 1 phase of the cell cycle by the ruml + gene. Nature, 367, 236-242.
46. Morgan, D.O. (1997) Cyclin-dependent kinases: engines, clocks and microprocessors. Annu. Rev. Cell. Dev. Biol., 13, 261-291.
47. Muzi-Falconi, M. and Kelly, T.J. (1995) Orp1, a member of the Cdc18/ Cdc6 family of S-phase regulators is homologous to a component of the origin recognition complex. Proc. Natl Acad. Sci. USA, 92, 12475-12479.
48. Muzi-Falconi, M., Brown, G.W. and Kelly, T.J. (1996a) cdc18+ regulates initiation of DNA replication in Schizosaccharomyces pombe. Proc. Natl Acad. Sci. USA, 93, 1666-1670.
49. Muzi-Falconi, M., Brown, G.W. and Kelly, T.J. (1996b) DNA replication: Controlling initiation during the cell cycle. Curr. Biol., 6, 229-233.
50. Nasmyth, K. (1996) Putting the cell cycle in order. Science, 274, 1643-1645.
51. Nishitani, H. and Nurse, P. (1995) p65cdc 18 plays a major role controlling the initiation of DNA replication in fission yeast. Cell, 83, 397-405.
52. 1,-to-S phase transition. Mol. Cell. Biol., 15, 2612-2624.
53. Pagano, M., Pepperkok, R., Verde, F., Ansorge, W. and Draetta, G. (1992) Cyclin A is required at two points in the human cell cycle. EMBO J., 11, 961-971.
54. Pagano, M., Pepperkok, R., Lukas, J., Baldin, V., Ansorge, W., Bartek, J. and Draetta, G. (1993) Regulation of the cell cycle by the cdk2 protein kinase in cultured human fibroblasts. J. Cell Biol., 121, 101-111.
55. 1 is important for the onset of S phase and for preventing a 'reductional' anaphase in the budding yeast Saccharomyces cerevisiae. EMBO J., 14, 3788-3799.
56. 1 defines a 'point of no return' after which Cdc6 synthesis cannot promote DNA replication in yeast. Genes Dev., 10, 1516-1531.
57. Pines, J. and Hunter, T. (1990) Human cyclin A is adenovirus E1A-associated protein p60 and behaves differently from cyclin B. Nature, 346, 760-763.
58. 1/S phase transition by expression of cyclins D1 and E with an inducible system. Mol. Cell. Biol., 14, 1669-1679.
59. Rowles, A. and Blow, J.J. (1997) Chromatin proteins in the initiation of DNA replication. Curr. Opin. Gen. Dev., 7, 152-157.
60. Rowles, A., Chong, J.P.J., Brown, L., Howell, M. Evan, G.I. and Blow, J.J. (1996) Interaction between the origin recognition complex and the replication licencing system in Xenopus. Cell, 87, 287-296.
61. Saha, P., Chen, J., Thome, K.C., Lawlis, S.J., Hou, Z.-H., Hendricks, M., Parvin, J.D. and Dutta, A. (1998) Human CDC6/Cdc18 associates with Orc1 and cyclin-cdk and is selectively eliminated from the nucleus at the onset of S phase. Mol. Cell. Biol., 18, 2758-2767.
62. Santocanale, C. and Diffley, J.F.X. (1996) ORC- and Cdc6-dependent complexes at active and inactive chromosomal replication origins in Saccharomyces cerevisiae. EMBO J., 15, 6671-6679.
63. 1 to S transition in S.cerevisiae. Cell, 79, 233-244.
64. Sherr, C.J. (1996) Cancer cell cycles. Science, 274, 1672-1677.
65. Stillman, B. (1996) Cell cycle control of DNA replication. Science, 274, 1659-1664.
66. Tanaka, T., Knapp, D. and Nasmyth, K. (1997) Loading of an Mcm protein onto DNA replication origins is regulated by Cdc6p and CDKs. Cell, 90, 649-660.
67. 1-to-S transition in mammalian cells. Oncogene, 8, 1593-1602.
68. Williams, R.S., Shohet, R.V. and Stillman, B. (1997) A human protein related to yeast Cdc6p. Proc. Natl Acad. Sci. USA, 94, 142-147.
69. Wuarin, J. and Nurse, P. (1996) Regulating S phase: CDKs, licencing and proteolysis. Cell, 85, 785-787.
70. Yan, H., Mercham, A.M. and Tye, B.-K. (1993) Cell cycle-regulated nuclear localization of MCM2 and MCM3, which are required for initiation of DNA synthesis at chromosomal replication origins in yeast. Genes Dev., 7, 2149-2160.
71. Yan, Z., DeGregori, J., Shohet, R., Leone, G., Stillman, B., Nevins, J.R. and Williams, R.S. (1998) Cdc6 is regulated by E2F and is essential for DNA replication in mammalian cells. Proc. Natl Acad. Sci. USA, 95, 3603-3608.
72. Zerfass-Thome, K., Schulze, A., Zwershke, W., Vogt, B., Helin, K., Bartek, J., Henglein, B. and Jansen-Dürr, P. (1997) p27KIP1 blocks cyclin E-dependent transactivation of cyclin A gene expression. Mol. Cell. Biol., 17, 407-415.
73. 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.
74. Zindy, F., Lamas, E., Chenivesse, X., Sobczak, J., Wang, J., Fesquet, D., Henglein, B. and Brechot, C. (1992) Cyclin A is required in S phase in normal epithelial cells. Biochem. Biophys. Res. Commun., 182, 1144-1154.