G1-phase and B-type cyclins exclude the DNA-replication factor Mcm4 from the nucleus

Nature Cell Biology

Volumn 1, Issue 7, 1999, Pages 415-422

  Labib, Karim ^a   Diffley, John F X ^a   Kearsey, Stephen E ^b  

^a IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

^b UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

SACCHAROMYCETALES;

CDC54 PROTEIN, S CEREVISIAE; CDC6 PROTEIN, S CEREVISIAE; CELL CYCLE PROTEIN; CYCLIN DEPENDENT KINASE; CYCLIN DEPENDENT KINASE 1; CYCLINE; DNA BINDING PROTEIN; FUNGAL PROTEIN; HYBRID PROTEIN; SACCHAROMYCES CEREVISIAE PROTEIN;

ARTICLE; CELL CYCLE; CELL CYCLE G1 PHASE; CELL CYCLE S PHASE; CELL NUCLEUS; CHROMATIN; CYTOLOGY; DNA REPLICATION; GENETICS; METABOLISM; PHYSIOLOGY; REPORTER GENE; SACCHAROMYCES CEREVISIAE;

CDC28 PROTEIN KINASE, S CEREVISIAE; CELL CYCLE; CELL CYCLE PROTEINS; CELL NUCLEUS; CHROMATIN; CYCLIN-DEPENDENT KINASES; CYCLINS; DNA REPLICATION; DNA-BINDING PROTEINS; FUNGAL PROTEINS; G1 PHASE; GENES, REPORTER; RECOMBINANT FUSION PROTEINS; S PHASE; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 0033224310     PISSN: 14657392     EISSN: None     Source Type: Journal    
DOI: 10.1038/15649     Document Type: Article

References (48)

1. Bell, S. P. & Stillman, B. Nucleotide dependent recognition of chromosomal origins of DNA replication by a multi-protein complex. Nature 357, 128-134 (1992).
2. Diffley, J. F. X. & Cocker, J. H. Protein-DNA interactions at a yeast replication origin. Nature 357, 169-172 (1992).
3. Diffley, J. F. X., Cocker, J. H., Dowell, S. J. & Rowley, A. Two steps in the assembly of complexes at yeast replication origins in vivo. Cell 78, 303-316 (1994).
4. Santocanale, C. & Diffley, J. F. X. ORC- and Cdc6-dependent complexes at active and inactive chromosomal replication origins in Saccharomyces cerevisiae. EMBO J. 15, 6671-6679 (1996).
5. Aparicio, O. M., Weinstein, D. M. & Bell, S. P. Components and dynamics of DNA replication complexes in S. cerevisiae: redistribution of MCM complexes and Cdc45p during S phase. Cell 91, 59-69 (1997).
6. Tanaka, T., Knapp, D. & Nasmyth, K. Loading of an Mcm protein onto DNA-replication origins is regulated by Cdc6p and CDKs. Cell 90, 649-660 (1997).
7. Cocker, J. H., Piatti, S., Santocanale, C., Nasmyth, K. & Diffley, J. F. X. An essential role for the Cdc6 protein in forming the pre-replicative complexes of budding yeast. Nature 379, 180-182 (1996).
8. Piatti, S., Lengauer, C. & Nasmyth, K. Cdc6 is an unstable protein whose de novo synthesis in G1 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 (1995).
9. Drury, L. S., Perkins, G. & Diffley, J. F. X. The Cdc4/34/53 pathway targets Cdc6p for proteolysis in budding yeast. EMBO J. 16, 5966-5976 (1997).
10. Kearsey, S. E. & Labib, K. MCM proteins: evolution, properties, and role in DNA replication. Biochim. Biophys. Acta 1398, 113-136 (1998).
11. Tye, B. K. Mcm proteins in DNA replication. Annu. Rev. Biochem. 68, 649-686 (1999).
12. Yan, H., Merchant, A. M. & Tye, B.-K. Cell cycle-regulated nuclear localisation of MCM2 and MCM3, which are required for the initiation of DNA synthesis at chromosomal replication origins in yeast. Genes Dev. 7, 2149-2160 (1993).
13. Donovan, S., Harwood, J., Drury, L. S. & Diffley, J. F. X. Cdc6-dependent loading of Mcm proteins onto pre-replicative chromatin in budding yeast. Proc. Natl Acad. Sci. USA 94, 5611-5616 (1997).
14. Liang, C. & Stillman, B. Persistent initiation of DNA replication and chromatin-bound MCM proteins during the cell cycle in cdc6 mutants. Genes Dev. 11, 3375-3386 (1997).
15. Young, M. R. & Tye, B. K. 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 (1997).
16. Weinreich, M., Liang, C. & Stillman, B. The Cdc6p nucleotide-binding motif is required for loading Mcm proteins onto chromatin. Proc. Natl Acad. Sci. USA 96, 441-446 (1999).
17. Donaldson, A. D. et al. CLB5-dependent activation of late replication origins in S. cerevisiae. Mol. Cell 2, 173-183 (1998).
18. Dahmann, C., Diffley, J. F. X. & Nasmyth, K. A. S-phase-promoting cyclin-dependent kinases prevent re-replication by inhibiting the transition of origins to a pre-replicative state. Curr. Biol. 5, 1257-1269 (1995).
19. Detweiler, C. S. & Li, J. J. Ectopic induction of Clb2 in early G1 phase is sufficient to block prereplicative complex formation in Saccharomyces cerevisiae. Proc. Natl Acad. Sci. USA 95, 2384-2389 (1998).
20. cdc2 in establishing the dependency of S phase on mitosis. Nature 349, 388-393 (1991).
21. cdc2-mitotic B cyclin complex. Cell 78, 813-822 (1994).
22. Moreno, S. & Nurse, P. Regulation of progression through the G1 phase of the cell-cycle by the rum1 gene. Nature 367, 236-242 (1994).
23. Labib, K., Moreno, S. & Nurse, P. Interaction of cdc2 and rum1 regulates Start and S-phase in fission yeast. J. Cell Sci. 108, 3285-3294 (1995).
24. Itzhaki, J. E., Gilbert, C. S. & Porter, A. C. Construction by gene targeting in human cells of a "conditional" CDC2 mutant that rereplicates its DNA. Nature Genet. 15, 258-265 (1997).
25. cdc18 plays a major role controlling the initiation of DNA replication in fission yeast. Cell 83, 397-405 (1995).
26. cdc18 by CDK phosphorylation. Genes Dev. 11, 2767-2779 (1997).
27. Lopez-Girona, A., Mondesert, O., Leatherwood, J. & Russell, P. Negative regulation of cdc18 DNA replication protein by cdc2. Mol. Biol. Cell 9, 63-73 (1998).
28. Sánchez, M. M., Calzada, J. A. & Bueno, A. Functionally homologous DNA replication genes in fission and budding yeast. J. Cell Sci. 112, 2381-2390 (1999).
29. Hennessy, K. M., Clark, C. D. & Botstein, D. Subcellular localization of yeast CDC46 varies with the cell cycle. Genes Dev. 4, 2252-2263 (1990).
30. Dalton, S. & Whitbread, L. 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 (1995).
31. Amon, A., Irniger, S. & Nasmyth, K. Closing the cell cycle circle in yeast: G2 cyclin proteolysis initiated at mitosis persists until the activation of G1 cyclins in the next cycle. Cell 77, 1037-1050 (1994).
32. SIC1 imposes the requirement for C1n G1 cyclin function at Start. Proc. Natl Acad. Sci. USA 93, 7772-7776 (1996).
33. Verma, R., Feldman, R. M. & Deshaies, R. J. SIC1 is ubiquitinated in vitro by a pathway that requires CDC4, CDC34, and cyclin/CDK activities. Mol. Biol. Cell 8, 1427-1437 (1997).
34. Desdouets, C. et al. Evidence for a Cdc6p-independent mitotic resetting event involving DNA polymerase α. EMBO J. 17, 4139-4146 (1998).
35. Surana, U. et al. Destruction of the CDC28/CLB mitotic kinase is not required for the metaphase to anaphase transition in budding yeast. EMBO J. 12, 1969-1978 (1993).
36. Piatti, S., Bohm, T., Cocker, J. H., Diffley, J. F. X. & Nasmyth, K. Activation of S-phase promoting CDKs in late G1 defines a "point of no return" after which Cdc6 synthesis cannot promote DNA replication in yeast. Genes Dev. 10, 1516-1531 (1996).
37. Amon, A., Tyers, M., Futcher, B. & Nasmyth, K. Mechanisms that help the yeast cell cycle clock tick: G2 cyclins transcriptionally activate G2 cyclins and repress G1 cyclins. Cell 74, 993-1007 (1993).
38. Dohmen, R. J., Wu, P. & Varshavsky, A. Heat-inducible degron: a method for constructing temperature-sensitive mutants. Science 263, 1273-1276 (1994).
39. Zwerschke, W., Rottjakob, H.-W. & Küntzel, H. The Saccharomyces cerevisiae CDC6 gene is transcribed at late mitosis and encodes a ATP/GTPase controlling S phase initiation. J. Biol. Chem. 269, 23351-23356 (1994).
40. McInerny, C. J., Partridge, J. F., Mikesell, G. E., Creemer, D. P. & Breeden, L. L. A novel Mcm1-dependent element in the SWI4, CLN3, CDC6, and CDC47 promoters activates M/G1-specific transcription. Genes Dev. 11, 1277-1288 (1999).
41. Blow, J. J. & Laskey, R. A. A role for the nuclear envelope in controlling DNA replication within the cell cycle. Nature 332, 546-548 (1988).
42. Thommes, P., Kubota, Y., Takisawa, H. & Blow, J. J. The RLF-M component of the replication licensing system forms complexes containing all six MCM/P1 polypeptides. EMBO J. 16, 3312-3319 (1997).
43. Hua, X. H., Yan, H. & Newport, J. A role for Cdk2 kinase in negatively regulating DNA replication during S phase of the cell cycle. J. Cell. Biol. 137, 183-192 (1997).
44. Sanders Williams, R., Shohet, R. V. & Stillman, B. A human protein related to yeast Cdc6p. Proc. Natl Acad. Sci. USA 94, 142-147 (1997).
45. Saha, P. et al. 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 (1998).
46. Jiang, W., Wells, N. J. & Hunter, T. Multistep regulation of DNA regulation by Cdk phosphorylation of HsCdc6. Proc. Natl Acad. Sci. USA 96, 6193-6198 (1999).
47. Peterson, B. O., Lukas, J., Sorenson, C. S., Bartek, J. & Helin, K. Phosphorylation of mammalian CDC6 by Cyclin A/CDK2 regulates its subcellular localization. EMBO J. 18, 396-410 (1999).
48. Sikorski, R. S. & Hieter, P. A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics 122, 19-27 (1989).