Interplay between S-cyclin-dependent kinase and Dbf4-dependent kinase in controlling DNA replication through phosphorylation of yeast Mcm4 N-terminal domain

Molecular Biology of the Cell

Volumn 19, Issue 5, 2008, Pages 2267-2277

  Devault, Alain ^a,b   Gueydon, Elisabeth ^a   Schwob, Etienne ^a  

^a CNRS   (France)

^b Centre National de la Recherche Scientifique   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE; CYCLIN DEPENDENT KINASE; HYDROXYUREA; MINICHROMOSOME MAINTENANCE PROTEIN 4; PROTEIN CLB2; PROTEIN CLB3; PROTEIN CLB4; PROTEIN CLB5; PROTEIN KINASE; PROTEIN KINASE DBF4; REPLISOME;

AMINO TERMINAL SEQUENCE; ARTICLE; BOB1 GENE; CELL CYCLE S PHASE; CLB5 GENE; CLB6 GENE; CONTROLLED STUDY; DNA REPLICATION; DNA SYNTHESIS; ENZYME ACTIVATION; EUKARYOTE; FUNGAL GENE; GENE MUTATION; IN VIVO STUDY; MCM4 GENE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; TEMPERATURE; YEAST;

AMINO ACID SEQUENCE; CELL CYCLE PROTEINS; CYCLIN-DEPENDENT KINASES; DNA, FUNGAL; DNA-BINDING PROTEINS; MITOSIS; MOLECULAR SEQUENCE DATA; MUTATION; PHENOTYPE; PHOSPHORYLATION; PROTEIN STRUCTURE, TERTIARY; REPLICATION ORIGIN; S PHASE; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SEQUENCE ALIGNMENT;

EUKARYOTA; SACCHAROMYCETALES;

EID: 48249129062     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E07-06-0614     Document Type: Article

References (54)

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. Bishop, A. C. et al. (2000). A chemical switch for inhibitor-sensitive alleles of any protein kinase. Nature 407, 395-401.
3. Blow, J. J., and Dutta, A. (2005). Preventing re-replication of chromosomal DNA. Nat. Rev. Mol. Cell Biol. 6, 476-486.
4. Chong, J. P., Hayashi, M. K., Simon, M. N., Xu, R. M., and Stillman, B. (2000). A double-hexamer archaeal minichromosome maintenance protein is an ATP-dependent DNA helicase. Proc. Natl. Acad. Sci. USA 97, 1530-1535.
5. Cross, F. R., Yuste-Rojas, M., Gray, S., and Jacobson, M. D. (1999). Specialization and targeting of B-type cyclins. Mol. Cell 4, 11-19.
6. Diffley, J. F. (2004). Regulation of early events in chromosome replication. Curr. Biol. 14, R778-R786.
7. Findeisen, M., El-Denary, M., Kapitza, T., Graf, R., and Strausfeld, U. (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.
8. Fletcher, R. J., and Chen, X. S. (2006). Biochemical activities of the BOB1 mutant in Methanobacterium thermoautotrophicum MCM. Biochemistry 45, 462-467.
9. Gambus, A., Jones, R. C., Sanchez-Diaz, A., Kanemaki, M., van Deursen, F., Edmondson, R. D., and Labib, K. (2006). GINS maintains association of Cdc45 with MCM in replisome progression complexes at eukaryotic DNA replication forks. Nat. Cell Biol. 8, 358-366.
10. Gari, E., Piedrafita, L., Aldea, M., and Herrero, E. (1997). A set of vectors with a tetracycline-regulatable promoter system for modulated gene expression in Saccharomyces cerevisiae. Yeast 13, 837-848.
11. Hardy, C. F., Dryga, O., Seematter, S., Pahl, P. M., and Sclafani, R. A. (1997). mcm5/cdc46-bob1 bypasses the requirement for the S phase activator Cdc7p. Proc. Natl. Acad. Sci. USA 94, 3151-3155.
12. 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.
13. Hu, F., and Aparicio, O. M. (2005). Swe1 regulation and transcriptional control restrict the activity of mitotic cyclins toward replication proteins in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 102, 8910-8915.
14. Ishimi, Y., and Komamura-Kohno, Y. (2001). Phosphorylation of Mcm4 at specific sites by cyclin-dependent kinase leads to loss of Mcm4,6,7 helicase activity. J. Biol. Chem. 276, 34428-34433.
15. Ishimi, Y., Komamura-Kohno, Y., You, Z., Omori, A., and Kitagawa, M. (2000). Inhibition of Mcm4,6,7 helicase activity by phosphorylation with cyclin A/Cdk2. J. Biol. Chem. 275, 16235-16241.
16. Janke, C. et al. (2004). A versatile toolbox for PCR-based tagging of yeast genes: new fluorescent proteins, more markers and promoter substitution cassettes. Yeast 21, 947-962.
17. Kamimura, Y., Tak, Y. S., Sugino, A., and Araki, H. (2001). Sld3, which interacts with Cdc45 (Sld4), functions for chromosomal DNA replication in Saccharomyces cerevisiae. EMBO J. 20, 2097-2107.
18. Kanemaki, M., and Labib, K. (2006). Distinct roles for Sld3 and GINS during establishment and progression of eukaryotic DNA replication forks. EMBO J. 25, 1753-1763.
19. Kelman, Z., Lee, J. K., and Hurwitz, J. (1999). The single minichromosome maintenance protein of Methanobacterium thermoautotrophicum DeltaH contains DNA helicase activity. Proc. Natl. Acad. Sci. USA 96, 14783-14788.
20. Kesti, T., McDonald, W. H., Yates, J. R., 3rd, and Wittenberg, C. (2004). Cell cycle-dependent phosphorylation of the DNA polymerase epsilon subunit, Dpb2, by the Cdc28 cyclin-dependent protein kinase. J. Biol. Chem. 279, 14245-14255.
21. Kinoshita, E., Kinoshita-Kikuta, E., Takiyama, K., and Koike, T. (2006). Phosphate-binding tag, a new tool to visualize phosphorylated proteins. Mol. Cell Proteomics 5, 749-757.
22. Knop, M., Siegers, K., Pereira, G., Zachariae, W., Winsor, B., Nasmyth, K., and Schiebel, E. (1999). Epitope tagging of yeast genes using a PCR-based strategy: more tags and improved practical routines. Yeast 15, 963-972.
23. Komamura-Kohno, Y., Karasawa-Shimizu, K., Saitoh, T., Sato, M., Hanaoka, F., Tanaka, S., and Ishimi, Y. (2006). Site-specific phosphorylation of MCM4 during the cell cycle in mammalian cells. FEBS J. 273, 1224-1239.
24. Labib, K., Tercero, J. A., and Diffley, J. F. (2000). Uninterrupted MCM2-7 function required for DNA replication fork progression. Science 288, 1643-1647.
25. Lee, J. K., and Hurwitz, J. (2001). Processive DNA helicase activity of the minichromosome maintenance proteins 4, 6, and 7 complex requires forked DNA structures. Proc. Natl. Acad. Sci. USA 98, 54-59.
26. Lengronne, A., Pasero, P., Bensimon, A., and Schwob, E. (2001). Monitoring S phase progression globally and locally using BrdU incorporation in TK(+) yeast strains. Nucleic Acids Res. 29, 1433-1442.
27. Liku, M. E., Nguyen, V. Q., Rosales, A. W., Irie, K., and Li, J. J. (2005). CDK Phosphorylation of a novel NLS-NES module distributed between two subunits of the Mcm2-7 complex prevents chromosomal rereplication. Mol. Biol. Cell. 16, 5026-5039.
28. Loog, M., and Morgan, D. O. (2005). Cyclin specificity in the phosphorylation of cyclin-dependent kinase substrates. Nature 434, 104-108.
29. Lundgren, M., Andersson, A., Chen, L., Nilsson, P., and Bernander, R. (2004). Three replication origins in Sulfolobus species: synchronous initiation of chromosome replication and asynchronous termination. Proc. Natl. Acad. Sci. USA 101, 7046-7051.
30. Masai, H., Matsui, E., You, Z., Ishimi, Y., Tamai, K., and Arai, K. (2000). Human Cdc7-related kinase complex. In vitro phosphorylation of MCM by concerted actions of Cdks and Cdc7 and that of a critical threonine residue of Cdc7 by Cdks. J. Biol. Chem. 275, 29042-29052.
31. Masai, H. et al. (2006). Phosphorylation of MCM4 by Cdc7 kinase facilitates its interaction with Cdc45 on the chromatin. J. Biol. Chem. 281, 39249-39261.
32. Masumoto, H., Muramatsu, S., Kamimura, Y., and Araki, H. (2002). S-Cdk-dependent phosphorylation of Sld2 essential for chromosomal DNA replication in budding yeast. Nature 415, 651-655.
33. Montagnoli, A., Valsasina, B., Brotherton, D., Troiani, S., Rainoldi, S., Tenca, P., Molinari, A., and Santocanale, C. (2006). Identification of Mcm2 phosphorylation sites by S-phase-regulating kinases. J. Biol. Chem. 281, 10281-10290.
34. Nguyen, V. Q., Co, C., and Li, J. J. (2001). Cyclin-dependent kinases prevent DNA re-replication through multiple mechanisms. Nature 411, 1068-1073.
35. Nougarede, R., Della Seta, F., Zarzov, P., and Schwob, E. (2000). Hierarchy of S-phase-promoting factors: yeast Dbf4-Cdc7 kinase requires prior S-phase cyclin-dependent kinase activation. Mol. Cell Biol. 20, 3795-3806.
36. Pacek, M., and Walter, J. C. (2004). A requirement for MCM7 and Cdc45 in chromosome unwinding during eukaryotic DNA replication. EMBO J. 23, 3667-3676.
37. Pereverzeva, I., Whitmire, E., Khan, B., and Coue, M. (2000). Distinct phosphoisoforms of the Xenopus Mcm4 protein regulate the function of the Mcm complex. Mol. Cell Biol. 20, 3667-3676.
38. Raghuraman, M. K., Winzeler, E. A., Collingwood, D., Hunt, S., Wodicka, L., Conway, A., Lockhart, D. J., Davis, R. W., Brewer, B. J., and Fangman, W. L. (2001). Replication dynamics of the yeast genome. Science 294, 115-121.
39. Schwob, E., and Nasmyth, K. (1993). CLB5 and CLB6, a new pair of B cyclins involved in DNA replication in Saccharomyces cerevisiae. Genes Dev. 7, 1160-1175.
40. Sclafani, R. A., Tecklenburg, M., and Pierce, A. (2002). The mcm5-bob1 bypass of Cdc7p/Dbf4p in DNA replication depends on both Cdk1-independent and Cdk1-dependent steps in Saccharomyces cerevisiae. Genetics 161, 47-57.
41. Sheu, Y. J., and Stillman, B. (2006). Cdc7-Dbf4 phosphorylates MCM proteins via a docking site-mediated mechanism to promote S phase progression. Mol. Cell 24, 101-113.
42. Shin, J. H., Jiang, Y., Grabowski, B., Hurwitz, J., and Kelman, Z. (2003). Substrate requirements for duplex DNA translocation by the eukaryal and archaeal minichromosome maintenance helicases. J. Biol. Chem. 278, 49053-49062.
43. Tak, Y. S., Tanaka, Y., Endo, S., Kamimura, Y., and Araki, H. (2006). A CDK-catalysed regulatory phosphorylation for formation of the DNA replication complex Sld2-Dpb11. EMBO J. 25, 1987-1996.
44. Takahashi, T. S., and Walter, J. C. (2005). Cdc7-Drf1 is a developmentally regulated protein kinase required for the initiation of vertebrate DNA replication. Genes Dev. 19, 2295-2300.
45. Takayama, Y., Kamimura, Y., Okawa, M., Muramatsu, S., Sugino, A., and Araki, H. (2003). GINS, a novel multiprotein complex required for chromosomal DNA replication in budding yeast. Genes Dev. 17, 1153-1165.
46. Takeda, D. Y., and Dutta, A. (2005). DNA replication and progression through S phase. Oncogene 24, 2827-2843.
47. Tanaka, S., Umemori, T., Hirai, K., Muramatsu, S., Kamimura, Y., and Araki, H. (2007). CDK-dependent phosphorylation of Sld2 and Sld3 initiates DNA replication in budding yeast. Nature 445, 328-332.
48. Tanaka, T., and Nasmyth, K. (1998). Association of RPA with chromosomal replication origins requires an mcm protein, and is regulated by rad53, and cyclin- and Dbf4-dependent kinases. EMBO J. 17, 5182-5191.
49. Tercero, J. A., Labib, K., and Diffley, J. F. (2000). DNA synthesis at individual replication forks requires the essential initiation factor Cdc45p. EMBO J. 19, 2082-2093.
50. Vas, A., Mok, W., and Leatherwood, J. (2001). Control of DNA rereplication via Cdc2 phosphorylation sites in the origin recognition complex. Mol. Cell Biol. 21, 5767-5777.
51. Wan, L., Niu, H., Futcher, B., Zhang, C., Shokat, K. M., Boulton, S. J., and Hollingsworth, N. M. (2008). Cdc28-Clb5 (CDK-S) and Cdc7-Dbf4 (DDK) collaborate to initiate meiotic recombination in yeast. Genes Dev. 22, 386-397.
52. Wilmes, G. M., Archambault, V., Austin, R. J., Jacobson, M. D., Bell, S. P., and Cross, F. R. (2004). Interaction of the S-phase cyclin Clb5 with an "RXL" docking sequence in the initiator protein Orc6 provides an origin-localized replication control switch. Genes Dev. 18, 981-991.
53. Zegerman, P., and Diffley, J. F. (2007). Phosphorylation of Sld2 and Sld3 by cyclin-dependent kinases promotes DNA replication in budding yeast. Nature 445, 281-285.
54. Zou, L., and Stillman, B. (2000). Assembly of a complex containing Cdc45p, replication protein A, and Mcm2p at replication origins controlled by S-phase cyclin-dependent kinases and Cdc7p-Dbf4p kinase. Mol. Cell Biol. 20, 3086-3096.