Cdc7p-Dbf4p kinase binds to chromatin during S phase and is regulated by both the APC and the RAD53 checkpoint pathway

EMBO Journal

Volumn 18, Issue 19, 1999, Pages 5334-5346

  Weinreich, Michael ^a   Stillman, Bruce ^a  

^a Howard Hughes Medical Institute Cold Spring Harbor Laboratory Cold Spring Harbor   (United States)

Author keywords

Cdc7p Dbf4p kinase; Cell cycle; Chromatin binding; DNA replication; Saccharomyces cerevisiae

Indexed keywords

CELL PROTEIN; CYCLIN DEPENDENT KINASE; HYDROXYUREA; PROTEIN DBF4P; PROTEIN SUBUNIT; RECOMBINANT PROTEIN; UNCLASSIFIED DRUG;

ADAPTATION; ANAPHASE; ARTICLE; AUTOPHOSPHORYLATION; CELL CYCLE G1 PHASE; CELL CYCLE S PHASE; CELL DIVISION; CHROMATIN; CHROMOSOME DUPLICATION; CONTROLLED STUDY; DNA REPLICATION; ENZYME ACTIVITY; FUNGUS MUTANT; GENE MUTATION; MINICHROMOSOME; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN PHOSPHORYLATION; PROTEIN PURIFICATION; REGULATOR GENE; SACCHAROMYCES CEREVISIAE; TEMPERATURE;

CELL CYCLE PROTEINS; CHROMATIN; DNA POLYMERASE I; DNA PRIMASE; FUNGAL PROTEINS; GENES, APC; HYDROXYUREA; PHOSPHOPROTEINS; PROTEIN BINDING; PROTEIN KINASES; PROTEIN-SERINE-THREONINE KINASES; S PHASE; SACCHAROMYCES CEREVISIAE PROTEINS; SUBSTRATE SPECIFICITY;

EUKARYOTA; FUNGI; SACCHAROMYCES CEREVISIAE;

EID: 0033215306     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/18.19.5334     Document Type: Article

References (73)

1. Aparicio, O.M., Weinstein, D.M. and Bell, S.P. (1997) Components and dynamics of DNA replication complexes in S. cerevisiae: redistribution of MCM proteins and Cdc45p during S phase. Cell, 91, 59-69.
2. Bousset, K. and Diffley, J.F.X. (1998) The Cdc7 protein kinase is required for origin firing during S phase. Genes Dev., 12, 480-490.
3. Brown, G.W. and Kelly, T.J. (1998) Purification of Hsk1, a minichromosome maintenance protein kinase from fission yeast. J. Biol. Chem., 273, 22083-22090.
4. Buck, V., White, A. and Rosamond, J. (1991) CDC7 protein kinase activity is required for mitosis and meiosis in Saccharomyces cerevisiae. Mol. Gen. Genet., 227, 452-457.
5. Chapman, J.W. and Johnston, L.H. (1989) The yeast gene, DBF4, essential for entry into S-phase is cell cycle regulated. Exp. Cell Res., 180, 419-428.
6. Cheng, L., Collyer, T. and Hardy, C.F. (1999) Cell cycle regulation of DNA replication initiator factor Dbf4p. Mol. Cell. Biol., 19, 4270-4278.
7. Chong, J.P.J., Thommes, P. and Blow, J.J. (1996) The role of MCM/P1 proteins in the licensing of DNA replication. Trends Biochem. Sci., 21, 102-106.
8. 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.
9. Desdouets, C., Santocanale, C., Drury, L.S., Perkins, G., Foiani, M., Plevani, P. and Diffley, J.F. (1998) Evidence for a Cdc6p-independent mitotic resetting event involving DNA polymerase α. EMBO J., 17, 4139-4146.
10. 1 phase. J. Cell Sci., 110, 753-763.
11. Diffley, J.F.X. (1996) Once and only once upon a time: specifying and regulating origins of DNA replication in eukaryotic cells. Genes Dev., 10, 2819-2830.
12. Dohrmann, P.R., Oshiro, G., Tecklenburg, M. and Sclafani, R.A. (1999) RAD53 regulates DBF4 independently of checkpoint function in Saccharomyces cerevisiae. Genetics, 151, 965-977.
13. Donaldson, A.D., Fangman, W.L. and Brewer, B.J. (1998a) Cdc7 is required throughout the yeast S phase to activate replication origins. Genes Dev., 12, 491-501.
14. Donaldson, A.D., Raghuraman, M.K., Friedman, K.L., Cross, F.R., Brewer, B.J. and Fangman, W.L. (1998b) CLB5-dependent activation of late replication origins in S.cerevisiae. Mol. Cell, 2, 173-182.
15. Donovan, S., Harwood, J., Drury, L.S. and Diffley, J.F.X. (1997) Cdc6p-dependent loading of Mem proteins onto pre-replicative chromatin in budding yeast. Proc. Natl Acad. Sci. USA, 94, 5611-5616.
16. Dowell, S.J., Romanowski, P. and Diffley, J.F.X. (1994) Interaction of Dbf4, the Cdc7 protein kinase regulatory subunit, with yeast replication origins in vivo. Science, 265, 1243-1246.
17. Dutta, A. and Bell, S.P. (1997) Initiation of DNA replication in eukaryotic cells. Annu. Rev. Cell Dev. Biol., 13, 293-332.
18. Elledge, S.J. (1996) Cell cycle checkpoints: preventing an identity crisis. Science, 274, 1664-1672.
19. Foiani, M., Liberi, G., Lucchini, G. and Plevani, P. (1995) Cell cycle-dependent phosphorylation and dephosphorylation of the yeast DNA polymerase α-primase B subunit. Mol. Cell. Biol., 15, 883-891.
20. Foiani, M., Lucchini, G. and Plevani, P. (1997) The DNA polymerase α-primase complex couples DNA replication, cell-cycle progression and DNA-damage response. Trends Biochem. Sci., 22, 424-427.
21. Fujita, M., Kiyono, T., Hayashi, Y. and Ishibashi, M. (1997) In vivo interaction of human MCM heterohexameric complexes with chromatin. J. Biol. Chem., 272, 10928-10935.
22. Fujita, M., Yamada, C., Tsurumi, T., Hanaoka, F., Matsuzawa, K. and Inagaki, M. (1998) Cell cycle- and chromatin binding state-dependent phosphorylation of human MCM heterohexameric complexes. J. Biol. Chem., 273, 17095-17101.
23. Hanks, S.K., Quinn, A.M. and Hunter, T. (1988) The protein kinase family: conserved features and deduced phylogeny of the catalytic domains. Science, 241, 42-52.
24. Hardy, C.F.J., Dryga, O., Seematter, S., Pahl, P.M.B. and Sclafani, R.A. (1997) mcm5/cdc46-bobI bypasses the requirement for the S phase activator Cdc7p. Proc. Natl Acad. Sci. USA, 94, 3151-3155.
25. Hartwell, L.H. (1973) Three additional genes required for deoxyribonucleic acid synthesis in Saccharomyces cerevisiae. J. Bacteriol., 115, 966-974.
26. Hendrickson, M., Madine, M., Dalton, S. and Gautier, J. (1996) Phosphorylation of MCM4 by cdc2 protein kinase inhibits the activity of the minichromosome maintenance complex. Proc. Natl Acad. Sci. USA, 93, 12223-12228.
27. Hereford, L.M. and Hartwell, L.H. (1974) Sequential gene function in the initiation of Saccharomyces cerevisiae DNA synthesis. J. Mol. Biol., 84, 445-461.
28. Hess, G.F., Drong, R.F., Weiland, K.L., Slightom, J.L., Sclafani, R.A. and Hollingsworth, R.E. (1998) A human homolog of the yeast CDC7 gene is overexpressed in some tumors and transformed cell lines. Gene, 211, 133-140.
29. Hollingsworth, R.E. and Sclafani, R.A. (1990) DNA metabolism gene CDC7 from yeast encodes a serine (threonine) protein kinase. Proc. Natl Acad. Sci. USA, 87, 6272-6276.
30. cdk2. J. Biol. Chem., 271, 25240-25246.
31. Hu, B., Burkhart, R., Schulte, D., Musahl, C. and Knippers, R. (1993) The P1 family: a new class of nuclear mammalian proteins related to the yeast Mcm replication proteins. Nucleic Acids Res., 21, 5289-5293.
32. Jackson, A.L., Pahl, P.M.B., Harrison, K., Rosamond, J. and Sclafani, R.A. (1993) Cell cycle regulation of the yeast Cdc7 protein kinase by association with the Dbf4 protein. Mol. Cell. Biol., 13, 2899-2908.
33. Jiang, W. and Hunter, T. (1997) Identification and characterization of a human protein kinase related to budding yeast Cdc7p. Proc. Natl Acad. Sci USA, 94, 14320-14325.
34. Johnson, L.N., Noble, M.E.M. and Owen, D.J. (1996) Active and inactive protein kinases: structural basis for regulation. Cell, 85, 149-158.
35. Johnston, L.H. and Thomas, A.P. (1982) A further two mutants defective in initiation of the S phase in the yeast Saccharomyces cerevisiae. Mol. Gen. Genet., 186, 445-448.
36. 1/S transition. J. Biol. Chem., 273, 23248-23257.
37. Kimura, H., Nozaki, N. and Sugimoto, K. (1994) DNA polymerase a associated P1 protein, a murine homologue of yeast MCM3, changes its intranuclear distribution during the DNA synthetic period. EMBO J., 13, 4311-4320.
38. King, R.W., Deshaies, R.J., Peters, J.-M. and Kirschner, M.W. (1996) How proteolysis drives the cell cycle. Science, 274, 1652-1659.
39. 1/S cell cycle transition. Genetics, 131, 21-29.
40. Lei, M., Kawasaki, Y., Young, M.R., Kihara, M., Sugino, A. and Tye, B.K. (1997) Mcm2 is a target of regulation by Cdc7-Dbf4 during the initiation of DNA synthesis. Genes Dev., 11, 3365-3374.
41. 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.
42. 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.
43. + a Schizosaccharomyces pombe gene related to Saccharomyces cerevisiae CDC7, is required for chromosomal replication. EMBO J., 14, 3094-3104.
44. Morgan, D.O. (1995) Principles of CDK regulation. Nature, 374, 131-134.
45. Nasheuer, H.-P., Moore, A., Wahl, A.F. and Wang, T.S.-F. (1991) Cell cycle-dependent phosphorylation of human DNA polymerase α. J. Biol. Chem., 266, 7893-7903.
46. Neuwald, A.F., Aravind, L., Spouge, J.L. and Koonin, E.V. (1999) AAA+: A class of chaperone-like ATPases associated with the assembly, operation and disassembly of protein complexes. Genome Res., 9, 27-43.
47. cdc2 and its companion cyclin-dependent kinases. Trends Cell Biol., 3, 296-301.
48. Oshiro, G., Owens, J.C., Shellman, Y., Sclafani, R.A. and Li, J.J. (1999) Cell cycle control of Cdc7p kinase activity through regulation of Dbf4p stability. Mol. Cell. Biol., 19, 4888-4896.
49. Owens, J.C., Detweiler, C.S. and Li, J.J. (1997) CDC45 is required in conjunction with CDC7/DBF4 to trigger the initiation of DNA replication. Proc. Natl Acad. Sci. USA, 94, 12521-12526.
50. Patterson, M., Sclafani, R.A., Fangman, W.L. and Rosamond, J. (1986) Molecular characterization of cell cycle gene CDC7 from Saccharomyces cerevisiae. Mol. Cell. Biol., 6, 1590-1598.
51. Perkins, G. and Diffley, J.F.X. (1998) Nucleotide-dependent prereplicative complex assembly by Cdc6p, a homolog of eukaryotic and prokaryotic clamp-loaders. Mol. Cell, 2, 23-32.
52. Peters, J.M., King, R.W., Hoog, C. and Kirschner, M.W. (1996) Identification of BIME as a subunit of the anaphase-promoting complex. Science, 274, 1199-1201.
53. Piatti, S. (1997) Cell cycle regulation of S phase entry in Saccharomyces cerevisiae. Progr. Cell Cycle Res., 3, 143-156.
54. 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.
55. 1 defines a 'point of no return' after which Cdc6 synthesis cannot promote DNA replication in yeast. Genes Dev., 10, 1516-1531.
56. Plevani, P., Foiani, P., Valsasnini, G., Badaracco, R., Cheriathundam, R. and Chang, L.M.S. (1985) Polypeptide structure of DNA primase from a yeast DNA polymerase-primase complex. J. Biol. Chem., 260, 7102-7107.
57. Sato, N., Arai, K. and Masai, H. (1997) Human and Xenopus cDNAs encoding budding yeast Cdc7-related kinases: in vitro phosphorylation of MCM subunits by a putative human homologue of Cdc7. EMBO J., 16, 4340-4351.
58. 1 to S transition in S.cerevisiae. Cell, 79, 233-244.
59. Sclafani, R.A., Patterson, M., Rosamond, J. and Fangman, W.L. (1988) Differential regulation of the yeast CDC7 gene during mitosis and meiosis. Mol. Cell. Biol., 8, 293-300.
60. Songyang, Z., Blechner, S., Hoagland, N., Hoekstra, M.F, Piwnica-Worms, H. and Cantley, L.C. (1994) Use of an oriented peptide library to determine the optimal substrates of protein kinases. Curr. Biol., 4, 973-982.
61. Stillman, B. (1996) Cell cycle control of DNA replication. Science, 274, 1659-1663.
62. Tanaka, T. and Nasmyth, K. (1998) Association of RPA with chromosomal replication origins requires an Mem protein and is regulated by Ra-d53 and cyclin- and Dbf4-dependent kinases. EMBO J., 17, 5182-5191.
63. Tanaka, T., Knapp, D. and Nasmyth, K. (1997) Loading of an Mem protein onto DNA replication origins is regulated by Cdc6p and CDKs. Cell, 90, 649-660.
64. Thomas, B.J. and Rothstein, R. (1989) Elevated recombination rates in transcriptionally active DNA. Cell, 56, 619-630.
65. Thommes, P., Kubota, Y., Takisawa, H. and Blow, J.J. (1997) The RLF-M component of the replication licensing system forms complexes containing all six MCM/P1 polypeptides. EMBO J., 16, 3312-3319.
66. Todorov, I.T., Attaran, A. and Kearsey, S.E. (1995) BM28, a human member of the MCM2-3-5 family, is displaced from chromatin during DNA replication. J. Cell Biol., 129, 1433-1445.
67. Waga, S. and Stillman, B. (1998) The DNA replication fork in eukaryotic cells. Annu. Rev. Biochem., 67, 721-751.
68. Weinreich, M., Liang, C. and Stillman, B. (1999) The Cdc6p nucleotide-binding motif is required for loading Mcm proteins onto chromatin. Proc. Natl Acad. Sci. USA, 96, 441-446.
69. Yamano, H., Tsurumi, C., Cannon, J. and Hunt, T. (1998) The role of the destruction box and its neighbouring lysine residues in cyclin B for anaphase ubiquitin-dependent proteolysis in fission yeast: defining the D-box receptor. EMBO J., 17, 5670-5678.
70. Yoon, H.-J., Loo, S. and Campbell, J.L. (1993) Regulation of Saccharomyces cerevisiae CDC7 function during the cell cycle. Mol. Biol. Cell, 4, 195-208.
71. Young, M.R. and Tye, B.K. (1997) Mcm2 and Mcm3 are constitutive nuclear proteins that exhibit distinct isoforms and bind chromatin during specific cell cycle stages of Saccharomyces cerevisiae. Mol. Biol. Cell, 8, 1587-1601.
72. Zhao, X., Muller, E.G.D. and Rothstein, R. (1998) A suppressor of two essential checkpoint genes identifies a novel protein that negatively affects dNTP pools. Mol. Cell, 2, 329-340.
73. Zou, L. and Stillman, B. (1998) Formation of a preinitiation complex by S-phase cyclin CDK-dependent loading of Cdc45p onto chromatin. Science, 280, 593-596.