Ordered assembly of Sld3, GINS and Cdc45 is distinctly regulated by DDK and CDK for activation of replication origins

EMBO Journal

Volumn 25, Issue 19, 2006, Pages 4663-4674

  Yabuuchi, Hayato ^a   Yamada, Yoshiki ^a,b   Uchida, Tomonori ^a   Sunathvanichkul, Tul ^a   Nakagawa, Takuro ^a   Masukata, Hisao ^a  

^a OSAKA UNIVERSITY   (Japan)

^b SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

CDK; Cell cycle; DDK; DNA replication; GINS

Indexed keywords

CYCLIN DEPENDENT KINASE ACTIVATING KINASE; PROTEIN CDC45; PROTEIN CUT5; PROTEIN DBF4; PROTEIN GINS; PROTEIN PSF2; PROTEIN PSF3; PROTEIN SLD3; PROTEIN SUBUNIT; UNCLASSIFIED DRUG;

ARTICLE; CHROMATIN IMMUNOPRECIPITATION; COMPLEX FORMATION; DNA FLANKING REGION; DNA REPLICATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ASSEMBLY; TEMPERATURE SENSITIVITY; YEAST;

CELL CYCLE PROTEINS; CHROMOSOMES, FUNGAL; CYCLIN-DEPENDENT KINASES; DNA-BINDING PROTEINS; MODELS, GENETIC; MULTIPROTEIN COMPLEXES; MUTATION; NUCLEAR PROTEINS; PROTEIN TRANSPORT; PROTEIN-SERINE-THREONINE KINASES; REPLICATION ORIGIN; S PHASE; SCHIZOSACCHAROMYCES; SCHIZOSACCHAROMYCES POMBE PROTEINS;

EUKARYOTA; SCHIZOSACCHAROMYCES POMBE;

EID: 33749345709     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/sj.emboj.7601347     Document Type: Article

References (54)

1. Aparicio OM, Stout AM, Bell SP (1999) Differential assembly of Cdc45p and DNA polymerases at early and late origins of DNA replication. Proc Natl Acad Sci USA 96: 9130-9135
2. Araki H, Leem SH, Phongdara A, Sugino A (1995) Dpb11, which interacts with DNA polymerase II(ε) in Saccharomyces cerevisiae, has a dual role in S-phase progression and at a cell cycle checkpoint. Proc Natl Acad Sci USA 92: 11791-11795
3. Bell SP, Dutta A (2002) DNA replication in eukaryotic cells. Annu Rev Biochem 71: 333-374
4. Booher RN, Alfa CE, Hyams JS, Beach DH (1989) The fission yeast cdc2/cdc13/suc1 protein kinase: regulation of catalytic activity and nuclear localization. Cell 58: 485-497
5. Dai J, Chuang RY, Kelly TJ (2005) DNA replication origins in the Schizosaccharomyces pombe genome. Proc Natl Acad Sci USA 102: 337-342
6. De Antoni A, Gallwitz D (2000) A novel multi-purpose cassette for repeated integrative epitope tagging of genes in Saccharomyces cerevisiae. Gene 246: 179-185
7. Diffley JF, Cocker JH, Dowell SJ, Rowley A (1994) Two steps in the assembly of complexes at yeast replication origins in vivo. Cell 78: 303-316
8. Feng W, D'Urso G (2001) Schizosaccharomyces pombe cells lacking the amino-terminal catalytic domains of DNA polymerase epsilon are viable but require the DNA damage checkpoint control. Mol Cell Biol 21: 4495-4504
9. Friedman KL, Brewer BJ, Fangman WL (1997) Replication profile of Saccharomyces cerevisiae chromosome VI. Genes Cells 2: 667-678
10. Gambus A, Jones RC, Sanchez-Diaz A, Kanemaki M, van Deursen F, Edmondson RD, 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
11. Gilbert DM (2001) Making sense of eukaryotic DNA replication origins. Science 294: 96-100
12. Hardy CF, Dryga O, Seematter S, Pahl PM, Sclafani RA (1997) mcm5/cdc46-bob1 bypasses the requirement for the S phase activator Cdc7p. Proc Natl Acad Sci USA 94: 3151-3155
13. Hashimoto Y, Takisawa H (2003) Xenopus Cut5 is essential for a CDK-dependent process in the initiation of DNA replication. EMBO J 22: 2526-2535
14. Hiraoka Y, Toda T, Yanagida M (1984) The NDA3 gene of fission yeast encodes β-tubulin: a cold-sensitive nda3 mutation reversibly blocks spindle formation and chromosome movement in mitosis. Cell 39: 349-358
15. Huang HK, Bailis JM, Leverson JD, Gomez EB, Forsburg SL, Hunter T (2005) Suppressors of Bir1p (Survivin) identify roles for the chromosomal passenger protein Pic1p (INCENP) and the replication initiation factor Psf2p in chromosome segregation. Mol Cell Biol 25: 9000-9015
16. Ishiai M, Sanchez JP, Amin AA, Murakami Y, Hurwitz J (1996) Purification, gene cloning, and reconstitution of the heterotrimeric single-stranded DNA-binding protein from Schizosaccharomyces pombe. J Biol Chem 271: 20868-20878
17. Kamimura Y, Masumoto H, Sugino A, Araki H (1998) Sld2, which interacts with Dpb11 in Saccharomyces cerevisiae, is required for chromosomal DNA replication. Mol Cell Biol 18: 6102-6109
18. Kamimura Y, Tak YS, Sugino A, Araki H (2001) Sld3, which interacts with Cdc45 (Sld4), functions for chromosomal DNA replication in Saccharomyces cerevisiae. EMBO J 20: 2097-2107
19. Kanemaki M, Labib K (2006) Distinct roles for Sld3 and GINS during establishment and progression of eukaryotic DNA replication forks. EMBO J 25: 1753-1763
20. Kanemaki M, Sanchez-Diaz A, Gambus A, Labib K (2003) Functional proteomic identification of DNA replication proteins by induced proteolysis in vivo. Nature 423: 720-724
21. Kearsey SE, Cotterill S (2003) Enigmatic variations: divergent modes of regulating eukaryotic DNA replication. Mol Cell 12: 1067-1075
22. Kim SM, Huberman JA (2001) Regulation of replication timing in fission yeast. EMBO J 20: 6115-6126
23. Kubota Y, Takase Y, Komori Y, Hashimoto Y, Arata T, Kamimura Y, Araki H, Takisawa H (2003) A novel ring-like complex of Xenopus proteins essential for the initiation of DNA replication. Genes Dev 17: 1141-1152
24. Lei M, Kawasaki Y, Young MR, Kihara M, Sugino A, Tye BK (1997) Mcm2 is a target of regulation by Cdc7-Dbf4 during the initiation of DNA synthesis. Genes Dev 11: 3365-3374
25. Masai H, Arai K (2002) Cdc7 kinase complex: a key regulator in the initiation of DNA replication. J Cell Physiol 190: 287-296
26. Masuda T, Mimura S, Takisawa H (2003) CDK- and Cdc45-dependent priming of the MCM complex on chromatin during S-phase in Xenopus egg extracts: possible activation of MCM helicase by association with Cdc45. Genes Cells 8: 145-161
27. Masumoto H, Muramatsu S, Kamimura Y, Araki H (2002) S-Cdk-dependent phosphorylation of Sld2 essential for chromosomal DNA replication in budding yeast. Nature 415: 651-655
28. Mimura S, Masuda T, Matsui T, Takisawa H (2000) Central role for Cdc45 in establishing an initiation complex of DNA replication in Xenopus egg extracts. Genes Cells 5: 439-452
29. Miyake S, Yamashita S (1998) Identification of sna41 gene, which is the suppressor of nda4 mutation and is involved in DNA replication in Schizosaccharomyces pombe. Genes Cells 3: 157-166
30. Moreno S, Klar A, Nurse P (1991) Molecular genetic analysis of fission yeast Schizosaccharomyces pombe. Methods Enzymol 194: 795-823
31. Nakajima R, Masukata H (2002) SpSld3 is required for loading and maintenance of SpCdc45 on chromatin in DNA replication in fission yeast. Mol Biol Cell 13: 1462-1472
32. Noguchi E, Shanahan P, Noguchi C, Russell P (2002) CDK phosphorylation of Drc1 regulates DNA replication in fission yeast. Curr Biol 12: 599-605
33. Norden C, Mendoza M, Dobbelaere J, Kotwaliwale CV, Biggins S, Barral Y (2006) The NoCut pathway links completion of cytokinesis to spindle midzone function to prevent chromosome breakage. Cell 125: 85-98
34. Nougarede R, Della Seta F, Zarzov P, 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
35. Nurse P, Thuriaux P (1980) Regulatory genes controlling mitosis in the fission yeast Schizosaccharomyces pombe. Genetics 96: 627-637
36. Obuse C, Okuno Y, Okazaki T, Masukata H (1996) A replication-enhancing element with transcriptional silencer activity in autonomously replicating human chromosomal fragments. Mol Biol Cell 7: 43-55
37. Ogawa Y, Takahashi T, Masukata H (1999) Association of fission yeast Orp1 and Mcm6 proteins with chromosomal replication origins. Mol Cell Biol 19: 7228-7236
38. Patel PK, Arcangioli B, Baker SP, Bensimon A, Rhind N (2006) DNA replication origins fire stochastically in fission yeast. Mol Biol Cell 17: 308-316
39. Saka Y, Fantes P, Sutani T, McInerny C, Creanor J, Yanagida M (1994) Fission yeast cut5 links nuclear chromatin and M phase regulator in the replication checkpoint control. EMBO J 13: 5319-5329
40. Segurado M, de Luis A, Antequera F (2003) Genome-wide distribution of DNA replication origins at A+T-rich islands in Schizosaccharomyces pombe. EMBO Rep 4: 1048-1053
41. Seki T, Akita M, Kamimura Y, Muramatsu S, Araki H, Sugino A (2006) GINS is a DNA polymerase ε accessory factor during chromosomal DNA replication in budding yeast. J Biol Chem 281: 21422-21432
42. Tak YS, Tanaka Y, Endo S, Kamimura Y, Araki H (2006) A CDK-catalysed regulatory phosphorylation for formation of the DNA replication complex Sld2-Dpb11. EMBO J 25: 1987-1996
43. Takahashi T, Masukata H (2001) Interaction of fission yeast ORC with essential adenine/thymine stretches in replication origins. Genes Cells 6: 837-849
44. Takayama Y, Kamimura Y, Okawa M, Muramatsu S, Sugino A, Araki H (2003) GINS, a novel multiprotein complex required for chromosomal DNA replication in budding yeast. Genes Dev 17: 1153-1165
45. Takeda DY, Dutta A (2005) DNA replication and progression through S phase. Oncogene 24: 2827-2843
46. Takeda T, Ogino K, Tatebayashi K, Ikeda H, Arai K, Masai H (2001) Regulation of initiation of S phase, replication checkpoint signaling, and maintenance of mitotic chromosome structures during S phase by Hsk1 kinase in the fission yeast. Mol Biol Cell 12: 1257-1274
47. Tanaka T, 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
48. goa1, a novel mutation causing G1/S arrest in fission yeast, is defective in a CDC45 homolog and interacts genetically with polα. Mol Genet Genomics 265: 1039-1049
49. Walter JC (2000) Evidence for sequential action of cdc7 and cdk2 protein kinases during initiation of DNA replication in Xenopus egg extracts. J Biol Chem 275: 39773-39778
50. Weinreich M, Stillman B (1999) Cdc7p-Dbf4p kinase binds to chromatin during S phase and is regulated by both the APC and the RAD53 checkpoint pathway. EMBO J 18: 5334-5346
51. Yamada Y, Nakagawa T, Masukata H (2004) A novel intermediate in initiation complex assembly for fission yeast DNA replication. Mol Biol Cell 15: 3740-3750
52. Yamashita M, Hori Y, Shinomiya T, Obuse C, Tsurimoto T, Yoshikawa H, Shirahige K (1997) The efficiency and timing of initiation of replication of multiple replicons of Saccharomyces cerevisiae chromosome VI. Genes Cells 2: 655-665
53. Yompakdee C, Huberman JA (2004) Enforcement of late replication origin firing by clusters of short G-rich DNA sequences. J Biol Chem 279: 42337-42344
54. Zou L, 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