Multiple roles for kinases in DNA replication

EMBO Reports

Volumn 4, Issue 3, 2003, Pages 252-256

  Henneke, Ghislaine ^a   Koundrioukoff, Stéphane ^a   Hübscher, Ulrich ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

CALCINEURIN; CASEIN KINASE II; CELL CYCLE PROTEIN; CYCLIN A; CYCLIN B; CYCLIN DEPENDENT KINASE; CYCLIN DEPENDENT KINASE 1; CYCLIN DEPENDENT KINASE 2; CYCLIN DEPENDENT KINASE 4; CYCLIN DEPENDENT KINASE 6; CYCLIN E; CYCLINE; DEOXYRIBONUCLEASE I; DNA; DNA DIRECTED DNA POLYMERASE ALPHA; DNA DIRECTED DNA POLYMERASE DELTA; PHOSPHOTRANSFERASE; POLYDEOXYRIBONUCLEOTIDE SYNTHASE; PRIMER DNA; PRIMER RNA; PROTEIN SERINE THREONINE KINASE; REPLICATION FACTOR C; REPLICATION PROTEIN A; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; CYCLIN DEPENDENT KINASE 7; DUMB BELL FORMER 4 PROTEIN; PROTEIN; UNCLASSIFIED DRUG;

CELL CYCLE; CELL CYCLE G1 PHASE; CELL CYCLE G2 PHASE; CELL CYCLE S PHASE; COMPLEX FORMATION; DNA REPAIR; DNA REPLICATION; HOMOLOGOUS RECOMBINATION; METAPHASE; PHASE TRANSITION; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; REVIEW; CELL CYCLE REGULATION; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; NONHUMAN; PROTEIN ASSEMBLY; SACCHAROMYCES CEREVISIAE; SCHIZOSACCHAROMYCES POMBE;

ANIMALS; CELL CYCLE; CYCLIN-DEPENDENT KINASES; DNA POLYMERASE I; DNA POLYMERASE III; DNA REPLICATION; HUMANS; PHOSPHORYLATION; SIGNAL TRANSDUCTION;

EID: 0037366692     PISSN: 1469221X     EISSN: None     Source Type: Journal    
DOI: 10.1038/sj.embor.embor774     Document Type: Review

References (43)

1. Adachi, Y. & 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. Allende, J.E. & Allende, C.C. (1995) Protein kinases. 4. Protein kinase CK2: an enzyme with multiple substrates and a puzzling regulation. FASEB J., 9, 313-323.
3. Bell, S.P. & Dutta, A. (2002) DNA replication in eukaryotic cells. Annu. Rev. Biochem., 71, 333-374.
4. Cardoso, M.C., Leonhardt, H. & Nadal-Ginard, B. (1993) Reversal of terminal differentiation and control of DNA replication: cyclin A and Cdk2 specifically localize at subnuclear sites of DNA replication. Cell, 74, 979-992.
5. Desdouets, C., Santocanale, C., Drury, L.S., Perkins, G., Foiani, M., Plevani, P. & Diffley, J.F. (1998) Evidence for a Cdc6p-independent mitotic resetting event involving DNA polymerase α. EMBO J., 17, 4139-4146.
6. Dimitrova, D.S. & Gilbert, D.M. (2000) Temporally coordinated assembly and disassembly of replication factories in the absence of DNA synthesis. Nature Cell Biol., 2, 686-694.
7. Din, S., Brill, S.J., Fairman, M.P. & Stillman, B. (1990) Cell-cycle-regulated phosphorylation of DNA replication factor A from human and yeast cells. Genes Dev., 4. 968-977.
8. Ducoux, M., Urbach, S., Baldacci, G., Hubscher, U., Koundrioukoff, S., Christensen, J. & Hughes, P. (2001) Mediation of proliferating cell nuclear antigen (PCNA)-dependent DNA replication through a conserved p21(Cip1)-like PCNA-binding motif present in the third subunit of human DNA polymerase δ. J. Biol. Chem., 276, 49258-49266.
9. Dutta, A. & Stillman, B. (1992) Cdc2 family kinases phosphorylate a human cell DNA replication factor, RPA, and activate DNA replication. EMBO J., 11, 2189-2199.
10. Foiani, M., Liberi, G., Lucchini, G. & Plevani, P. (1995) Cell cycle-dependent phosphorylation and dephosphorylation of the yeast DNA polymerase α-primase B subunit. Mol. Cell. Biol., 15, 883-891.
11. Fotedar, R. & Roberts, J.M. (1991) Association of p34cdc2 with replicating DNA. Cold Spring Harb. Symp. Quant. Biol., 56, 325-333.
12. Fotedar, R. & Roberts, J.M. (1992) Cell cycle regulated phosphorylation of RPA-32 occurs within the replication initiation complex. EMBO J., 11, 2177-2187.
13. Frouin, I., Montecucco, A., Biamonti, G., Hübscher, U., Spadari, S. & Maga, G. (2002) Cell cycle-dependent dynamic association of cyclin/Cdk complexes with human DNA replication proteins. EMBO J., 21, 2485-2495.
14. Henricksen, L.A., Umbricht, C.B. & Wold, M.S. (1994) Recombinant replication protein A: expression, complex formation, and functional characterization. J. Biol. Chem., 269, 11121-11132.
15. Jallepalli, P.V. & Kelly, T.J. (1997) Cyclin-dependent kinase and initiation at eukaryotic origins: a replication switch? Curr. Opin. Cell Biol., 9, 358-363.
16. Jares, P., Donaldson, A. & Blow, J.J. (2000) The Cdc7/Dbf4 protein kinase: target of the S phase checkpoint? EMBO Rep., 1, 319-322.
17. Jaumot, M., Grana, X., Giordano, A., Reddy, P.V., Agell, N. & Bachs, O. (1994) Cyclin/cdk2 complexes in the nucleus of HeLa cells. Biochem. Biophys. Res. Commun., 203, 1527-1534.
18. Kawabe, T., Suganuma, M., Ando, T., Kimura, M., Hori, H. & Okamoto, T. (2002) Cdc25C interacts with PCNA at G2/M transition. Oncogene, 21, 1717-1726.
19. Koundrioukoff, S., Jonsson, Z.O., Hasan, S., de Jong, R.N., van der Vliet, P.C., Hottiger, M.O. & Hübscher, U. (2000) A direct interaction between proliferating cell nuclear antigen (PCNA) and Cdk2 targets PCNA-interacting proteins for phosphorylation. J. Biol. Chem., 275, 22882-22887.
20. Leonhardt, H., Rahn, H.P., Weinzierl, R, Sporbert, A., Cremer, T., Zink, D. & Cardoso, M.C. (2000) Dynamics of DNA replication factories in living cells. J. Cell Biol., 149, 271-280.
21. Litchfield, D.W., Luscher, B., Lozeman, F.J., Eisenman, R.N. & Krebs, E.G. (1992) Phosphorylation of casein kinase II by p34cdc2 in vitro and at mitosis. J. Biol. Chem., 267, 13943-13951.
22. 2+/calmodulin-dependent protein kinase II inhibits DNA synthesis. Biochemistry, 36, 5300-5310.
23. Mcllwraith, M.J., Van Dyck, E., Masson, J.Y., Stasiak, A.Z., Stasiak, A. & West, S.C. (2000) Reconstitution of the strand invasion step of double-strand break repair using human Rad5l Rad52 and RPA proteins. J. Mol. Biol., 304, 151-164.
24. Montecucco, A., Rossi, R., Levin, D.S., Gary, R., Park, M.S., Motycka, T.A., Ciarrocchi, G., Villa, A., Biamonti, G. & Tomkinson, A.E. (1998) DNA ligase I is recruited to sites of DNA replication by an interaction with proliferating cell nuclear antigen: identification of a common targeting mechanism for the assembly of replication factories. EMBO J., 17, 3786-3795.
25. Montecucco, A., Rossi, R., Ferrari, G., Scovassi, A.I., Prosperi, F. & Biamonti, G. (2001) Etoposide induces the dispersal of DNA ligase I from replication factories. Mol. Biol. Cell, 12, 2109-2118.
26. Morris, T.A., DeLorenzo, R. J. & Tombes, R. M. (1998) CaMK-II inhibition reduces cyclin D1 levels and enhances the association of p27kip1 with Cdk2 to cause G1 arrest in NIH 3T3 cells. Exp. Cell Res., 240, 218-227.
27. Nasheuer, H.P., Moore, A., Wahl, A.F. & Wang, T.S. (1991) Cell cycle-dependent phosphorylation of human DNA polymerase α. J. Biol. Chem., 266, 7893-7903.
28. Nigg, E.A. (1995) Cyclin-dependent protein kinases: key regulators of the eukaryotic cell cycle. Bioessays, 17, 471-480.
29. Norbury, C.J. & Hickson, I.D. (2001) Cellular responses to DNA damage. Annu. Rev. Pharmacol. Toxicol., 41, 367-401.
30. Pan, Z.Q., Park, C.H., Amin, A.A., Hurwitz, J. & Sancar, A. (1995) Phosphorylated and unphosphorylated forms of human single-stranded DNA-binding protein are equally active in simian virus 40 DNA replication and in nucleotide excision repair. Proc. Natl Acad. Sci. USA, 92, 4636-4640.
31. Park, H., Davis, R. & Wang, T.S. (1995) Studies of Schizosaccharomyces pombe DNA polymerase α at different stages of the cell cycle. Nucleic Acids Res., 23, 4337-4344.
32. Philipova, D., Mullen, J.R., Maniar, H.S., Lu, J., Gu, C. & Brill, S.J. (1996) A hierarchy of SSB protomers in replication protein A. Genes Dev., 10, 2222-2233.
33. Prigent, C., Lasko, D.D., Kodama, K., Woodgett, J.R. & Lindahl, T. (1992) Activation of mammalian DNA ligase I through phosphorylation by casein kinase II. EMBO J., 11, 2925-2933.
34. Rasmussen, G. & Rasmussen, C. (1995) Calmodulin-dependent protein kinase II is required for G1/S progression in HeLa cells. Biochem. Cell Biol., 73, 201-207.
35. Rossi, R., Villa, A., Negri, C., Scovassi, I., Ciarrocchi, G., Biamonti, G. & Montecucco, A. (1999) The replication factory targeting sequence/PCNA-binding site is required in G(1) to control the phosphorylation status of DNA ligase I. EMBO J., 18, 5745-5754.
36. Russo, G.L., Vandenberg, M.T., Yu, I.J., Bae, Y.S., Franza, B.R. Jr & Marshak, D.R. (1992) Casein kinase II phosphorylates p34cdc2 kinase in G1 phase of the HeLa cell division cycle. J. Biol. Chem., 267, 20317-20325.
37. Schub, O., Rohaly, G., Smith, R.W., Schneider, A., Dehde, S., Dornreiter, I. & Nasheuer, H.P. (2001) Multiple phosphorylation sites of DNA polymerase α-primase cooperate to regulate the initiation of DNA replication in vitro. J. Biol. Chem., 276, 38076-38083.
38. Smith, G.C. & Jackson, S.P. (1999) The DNA-dependent protein kinase. Genes Dev., 13, 916-934.
39. Treuner, K., Findeisen, M., Strausfeld, U. & Knippers, R. (1999) Phosphorylation of replication protein A middle subunit (RPA32) leads to a disassembly of the RPA heterotrimer. J. Biol. Chem., 274, 15556-15561.
40. Voitenleitner, C., Fanning, E. & Nasheuer, H.P. (1997) Phosphorylation of DNA polymerase α-primase by cyclin A-dependent kinases regulates initiation of DNA replication in vitro. Oncogene, 14, 1611-1615.
41. Voitenleitner, C., Rehfuess, C., Hilmes, M., O'Rear, L., Liao, P.C., Gage, D.A., Ott, R., Nasheuer, H.P. & Fanning, E. (1999) Cell cycle-dependent regulation of human DNA polymerase α-primase activity by phosphorylation. Mol. Cell. Biol., 19, 646-656.
42. Xiong, Y., Zhang, H. & Beach, D. (1992) D type cyclins associate with multiple protein kinases and the DNA replication and repair factor PCNA. Cell, 71, 505-514.
43. Zeng, X.R., Hao, H., Jiang, Y. & Lee, M.Y. (1994) Regulation of human DNA polymerase δ during the cell cycle. J. Biol. Chem., 269, 24027-24033.