Multiple pathways can bypass the essential role of fission yeast Hsk1 kinase in DNA replication initiation

Journal of Cell Biology

Volumn 195, Issue 3, 2011, Pages 387-401

  Matsumoto, Seiji ^a   Hayano, Motoshi ^a   Kanoh, Yutaka ^a   Masai, Hisao ^a  

^a TOKYO METROPOLITAN INSTITUTE OF MEDICAL SCIENCE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CELL CYCLE PROTEIN; CELL CYCLE PROTEIN 45; CELL CYCLE PROTEIN 7; DNA; HSK1 KINASE; HYDROXYUREA; MRC1 PROTEIN; PHOSPHOTRANSFERASE; PROTEIN; UNCLASSIFIED DRUG; CDC45 PROTEIN, S POMBE; DFP1 PROTEIN, S POMBE; DNA BINDING PROTEIN; FUNGAL DNA; HSK1 PROTEIN, S POMBE; MRC1 PROTEIN, S POMBE; NUCLEAR PROTEIN; PROTEIN KINASE; PROTEIN SERINE THREONINE KINASE; SCHIZOSACCHAROMYCES POMBE PROTEIN;

ARTICLE; CELL CYCLE M PHASE; CELL CYCLE S PHASE; CELL VIABILITY; CHROMATIN; CHROMOSOME; DNA REPLICATION; DNA SYNTHESIS; EUKARYOTE; HIGH TEMPERATURE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN FUNCTION; YEAST CELL; CYTOLOGY; DNA REPLICATION ORIGIN; ENZYMOLOGY; GENETICS; METABOLISM; SCHIZOSACCHAROMYCES; SIGNAL TRANSDUCTION; TEMPERATURE;

EUKARYOTA; SCHIZOSACCHAROMYCETACEAE;

CELL CYCLE PROTEINS; DNA REPLICATION; DNA, FUNGAL; DNA-BINDING PROTEINS; NUCLEAR PROTEINS; PROTEIN KINASES; PROTEIN-SERINE-THREONINE KINASES; REPLICATION ORIGIN; SCHIZOSACCHAROMYCES; SCHIZOSACCHAROMYCES POMBE PROTEINS; SIGNAL TRANSDUCTION; TEMPERATURE;

EID: 84855720100     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201107025     Document Type: Article

References (88)

1. Alcasabas, A.A., A.J. Osborn, J. Bachant, F. Hu, P.J. Werler, K. Bousset, K. Furuya, J.F. Diffley, A.M. Carr, and S.J. Elledge. 2001. Mrc1 transduces signals of DNA replication stress to activate Rad53. Nat. Cell Biol. 3:958-965. http://dx.doi.org/10.1038/ncb1101-958
2. Aparicio, O.M., A.M. Stout, and S.P. Bell. 1999. Differential assembly of Cdc45p and DNA polymerases at early and late origins of DNA replication. Proc. Natl. Acad. Sci. USA. 96:9130-9135. http://dx.doi.org/10.1073/pnas.96.16.9130
3. Arcangioli, B. 1998. A site- and strand-specific DNA break confers asymmetric switching potential in fission yeast. EMBO J. 17:4503-4510. http://dx.doi.org/10.1093/emboj/17.15.4503
4. Bailis, J.M., P. Bernard, R. Antonelli, R.C. Allshire, and S.L. Forsburg. 2003. Hsk1-Dfp1 is required for heterochromatin-mediated cohesion at centromeres. Nat. Cell Biol. 5:1111-1116. http://dx.doi.org/10.1038/ncb1069
5. Boddy, M.N., and P. Russell. 2001. DNA replication checkpoint. Curr. Biol. 11:R953-R956. http://dx.doi.org/10.1016/S0960-9822(01)00572-3
6. Bousset, K., and J.F. Diffley. 1998. The Cdc7 protein kinase is required for origin firing during S phase. Genes Dev. 12:480-490. http://dx.doi.org/10.1101/gad.12.4.480
7. Bramhill, D., and A. Kornberg. 1988. A model for initiation at origins of DNA replication. Cell. 54:915-918. http://dx.doi.org/10.1016/0092-8674(88)90102-X
8. Brown, G.W., and T.J. Kelly. 1999. Cell cycle regulation of Dfp1, an activator of the Hsk1 protein kinase. Proc. Natl. Acad. Sci. USA. 96:8443-8448. http://dx.doi.org/10.1073/pnas.96.15.8443
9. Burke, D.J., and D. Church. 1991. Protein synthesis requirements for nuclear division, cytokinesis, and cell separation in Saccharomyces cerevisiae. Mol. Cell. Biol. 11:3691-3698.
10. Choo, K.H. 1997. Centromere DNA dynamics: latent centromeres and neocentromere formation. Am. J. Hum. Genet. 61:1225-1233. http://dx.doi.org/10.1086/301657
11. Costanzo, V., D. Shechter, P.J. Lupardus, K.A. Cimprich, M. Gottesman, and J. Gautier. 2003. An ATR- and Cdc7-dependent DNA damage checkpoint that inhibits initiation of DNA replication. Mol. Cell. 11:203-213. http://dx.doi.org/10.1016/S1097-2765(02)00799-2
12. Dolan, W.P., D.A. Sherman, and S.L. Forsburg. 2004. Schizosaccharomyces pombe replication protein Cdc45/Sna41 requires Hsk1/Cdc7 and Rad4/Cut5 for chromatin binding. Chromosoma. 113:145-156. http://dx.doi.org/10.1007/s00412-004-0302-8
13. Dolan, W.P., A.H. Le, H. Schmidt, J.P. Yuan, M. Green, and S.L. Forsburg. 2010. Fission yeast Hsk1 (Cdc7) kinase is required after replication initiation for induced mutagenesis and proper response to DNA alkylation damage. Genetics. 185:39-53. http://dx.doi.org/10.1534/genetics.109.112284
14. Donaldson, A.D., W.L. Fangman, and B.J. Brewer. 1998. Cdc7 is required throughout the yeast S phase to activate replication origins. Genes Dev. 12:491-501. http://dx.doi.org/10.1101/gad.12.4.491
15. Feng, W., D. Collingwood, M.E. Boeck, L.A. Fox, G.M. Alvino, W.L. Fangman, M.K. Raghuraman, and B.J. Brewer. 2006. Genomic mapping of singlestranded DNA in hydroxyurea-challenged yeasts identifies origins of replication. Nat. Cell Biol. 8:148-155. http://dx.doi.org/10.1038/ncb1358
16. Fletcher, R.J., B.E. Bishop, R.P. Leon, R.A. Sclafani, C.M. Ogata, and X.S. Chen. 2003. The structure and function of MCM from archaeal M. Thermoautotrophicum. Nat. Struct. Biol. 10:160-167. http://dx.doi.org/10.1038/nsb893
17. Geraghty, D.S., M. Ding, N.H. Heintz, and D.S. Pederson. 2000. Premature structural changes at replication origins in a yeast minichromosome maintenance (MCM) mutant. J. Biol. Chem. 275:18011-18021. http://dx.doi.org/10.1074/jbc.M909787199
18. Gérard, A., S. Koundrioukoff, V. Ramillon, J.-C. Sergère, N. Mailand, J.-P. Quivy, and G. Almouzni. 2006. The replication kinase Cdc7-Dbf4 promotes the interaction of the p150 subunit of chromatin assembly factor 1 with proliferating cell nuclear antigen. EMBO Rep. 7:817-823.
19. Gilbert, D.M. 2007. Replication origin plasticity, Taylor-made: inhibition vs recruitment of origins under conditions of replication stress. Chromosoma. 116:341-347. http://dx.doi.org/10.1007/s00412-007-0105-9
20. Hansen, R.S., S. Thomas, R. Sandstrom, T.K. Canfield, R.E. Thurman, M. Weaver, M.O. Dorschner, S.M. Gartler, and J.A. Stamatoyannopoulos. 2010. Sequencing newly replicated DNA reveals widespread plasticity in human replication timing. Proc. Natl. Acad. Sci. USA. 107:139-144. http://dx.doi.org/10.1073/pnas.0912402107
21. Hardy, C.F., O. Dryga, S. Seematter, P.M. Pahl, and R.A. Sclafani. 1997. mcm5/cdc46-bob1 bypasses the requirement for the S phase activator Cdc7p. Proc. Natl. Acad. Sci. USA. 94:3151-3155. http://dx.doi.org/10.1073/pnas.94.7.3151
22. Hartwell, L.H. 1973. Three additional genes required for deoxyribonucleic acid synthesis in Saccharomyces cerevisiae. J. Bacteriol. 115:966-974.
23. Hartwell, L.H. 1974. Saccharomyces cerevisiae cell cycle. Bacteriol. Rev. 38:164-198.
24. Hayano, M., Y. Kanoh, S. Matsumoto, and H. Masai. 2011. Mrc1 marks early-firing origins and coordinates timing and efficiency of initiation in fission yeast. Mol. Cell. Biol. 31:2380-2391. http://dx.doi.org/10.1128/MCB.01239-10
25. Hayashi, M., Y. Katou, T. Itoh, A. Tazumi, Y. Yamada, T. Takahashi, T. Nakagawa, K. Shirahige, and H. Masukata. 2007. Genome-wide localization of pre-RC sites and identification of replication origins in fission yeast. EMBO J. 26:1327-1339. http://dx.doi.org/10.1038/sj.emboj.7601585
26. Hayashi, M.T., T.S. Takahashi, T. Nakagawa, J. Nakayama, and H. Masukata. 2009. The heterochromatin protein Swi6/HP1 activates replication origins at the pericentromeric region and silent mating-type locus. Nat. Cell Biol. 11:357-362. http://dx.doi.org/10.1038/ncb1845
27. Heichinger, C., C.J. Penkett, J. Bähler, and P. Nurse. 2006. Genome-wide characterization of fission yeast DNA replication origins. EMBO J. 25:5171-5179. http://dx.doi.org/10.1038/sj.emboj.7601390
28. Hiratani, I., and D.M. Gilbert. 2009. Replication timing as an epigenetic mark. Epigenetics. 4:93-97. http://dx.doi.org/10.4161/epi.4.2.7772
29. Hiratani, I., T. Ryba, M. Itoh, T. Yokochi, M. Schwaiger, C.-W. Chang, Y. Lyou, T.M. Townes, D. Schübeler, and D.M. Gilbert. 2008. Global reorganization of replication domains during embryonic stem cell differentiation. PLoS Biol. 6:e245. http://dx.doi.org/10.1371/journal.pbio.0060245
30. Ishii, K., Y. Ogiyama, Y. Chikashige, S. Soejima, F. Masuda, T. Kakuma, Y. Hiraoka, and K. Takahashi. 2008. Heterochromatin integrity affects chromosome reorganization after centromere dysfunction. Science. 321: 1088-1091. http://dx.doi.org/10.1126/science.1158699
31. Jackson, A.L., P.M. Pahl, K. Harrison, J. Rosamond, and R.A. Sclafani. 1993. Cell cycle regulation of the yeast Cdc7 protein kinase by association with the Dbf4 protein. Mol. Cell. Biol. 13:2899-2908.
32. Jares, P., and J.J. Blow. 2000. Xenopus cdc7 function is dependent on licensing but not on XORC, XCdc6, or CDK activity and is required for XCdc45 loading. Genes Dev. 14:1528-1540.
33. Katis, V.L., J.J. Lipp, R. Imre, A. Bogdanova, E. Okaz, B. Habermann, K. Mechtler, K. Nasmyth, and W. Zachariae. 2010. Rec8 phosphorylation by casein kinase 1 and Cdc7-Dbf4 kinase regulates cohesin cleavage by separase during meiosis. Dev. Cell. 18:397-409. http://dx.doi.org/10.1016/j.devcel.2010.01.014
34. Katou, Y., Y. Kanoh, M. Bando, H. Noguchi, H. Tanaka, T. Ashikari, K. Sugimoto, and K. Shirahige. 2003. S-phase checkpoint proteins Tof1 and Mrc1 form a stable replication-pausing complex. Nature. 424:1078-1083. http://dx.doi.org/10.1038/nature01900
35. Kim, J.M., N. Takemoto, K. Arai, and H. Masai. 2003. Hypomorphic mutation in an essential cell-cycle kinase causes growth retardation and impaired spermatogenesis. EMBO J. 22:5260-5272. http://dx.doi.org/10.1093/emboj/cdg497
36. Kim, J.M., N. Kakusho, M. Yamada, Y. Kanoh, N. Takemoto, and H. Masai. 2008. Cdc7 kinase mediates Claspin phosphorylation in DNA replication checkpoint. Oncogene. 27:3475-3482. http://dx.doi.org/10.1038/sj.onc.1210994
37. Koren, A., I. Soifer, and N. Barkai. 2010. MRC1-dependent scaling of the budding yeast DNA replication timing program. Genome Res. 20:781-790. http://dx.doi.org/10.1101/gr.102764.109
38. Liu, C.L., S.L. Schreiber, and B.E. Bernstein. 2003. Development and validation of a T7 based linear amplification for genomic DNA. BMC Genomics. 4:19. http://dx.doi.org/10.1186/1471-2164-4-19
39. Liu, P., L.R. Barkley, T. Day, X. Bi, D.M. Slater, M.G. Alexandrow, H.P. Nasheuer, and C. Vaziri. 2006. The Chk1-mediated S-phase checkpoint targets initiation factor Cdc45 via a Cdc25A/Cdk2-independent mechanism. J. Biol. Chem. 281:30631-30644. http://dx.doi.org/10.1074/jbc.M602982200
40. Lopez-Mosqueda, J., N.L. Maas, Z.O. Jonsson, L.G. Defazio-Eli, J. Wohlschlegel, and D.P. Toczyski. 2010. Damage-induced phosphorylation of Sld3 is important to block late origin firing. Nature. 467:479-483. http://dx.doi.org/10.1038/nature09377
41. Masai, H., and K.-I. Arai. 2002. Cdc7 kinase complex: a key regulator in the initiation of DNA replication. J. Cell. Physiol. 190:287-296. http://dx.doi.org/10.1002/jcp.10070
42. +, a Schizosaccharomyces pombe gene related to Saccharomyces cerevisiae CDC7, is required for chromosomal replication. EMBO J. 14:3094-3104.
43. Masai, H., C. Taniyama, K. Ogino, E. Matsui, N. Kakusho, S. Matsumoto, J.-M. Kim, A. Ishii, T. Tanaka, T. Kobayashi, et al. 2006. Phosphorylation of MCM4 by Cdc7 kinase facilitates its interaction with Cdc45 on the chromatin. J. Biol. Chem. 281:39249-39261. http://dx.doi.org/10.1074/jbc.M608935200
44. Masai, H., S. Matsumoto, Z. You, N. Yoshizawa-Sugata, and M. Oda. 2010. Eukaryotic chromosome DNA replication: where, when, and how? Annu. Rev. Biochem. 79:89-130. http://dx.doi.org/10.1146/annurev.biochem.052308.103205
45. Matos, J., J.J. Lipp, A. Bogdanova, S. Guillot, E. Okaz, M. Junqueira, A. Shevchenko, and W. Zachariae. 2008. Dbf4-dependent CDC7 kinase links DNA replication to the segregation of homologous chromosomes in meiosis I. Cell. 135:662-678. http://dx.doi.org/10.1016/j.cell.2008.10.026
46. Matsumoto, S., K. Ogino, E. Noguchi, P. Russell, and H. Masai. 2005. Hsk1-Dfp1/Him1, the Cdc7-Dbf4 kinase in Schizosaccharomyces pombe, associates with Swi1, a component of the replication fork protection complex. J. Biol. Chem. 280:42536-42542. http://dx.doi.org/10.1074/jbc.M510575200
47. Matsumoto, S., M. Shimmoto, N. Kakusho, M. Yokoyama, Y. Kanoh, M. Hayano, P. Russell, and H. Masai. 2010. Hsk1 kinase and Cdc45 regulate replication stress-induced checkpoint responses in fission yeast. Cell Cycle. 9:4627-4637. http://dx.doi.org/10.4161/cc.9.23.13937
48. Nakamura, T., M. Nakamura-Kubo, T. Nakamura, and C. Shimoda. 2002. Novel fission yeast Cdc7-Dbf4-like kinase complex required for the initiation and progression of meiotic second division. Mol. Cell. Biol. 22:309-320. http://dx.doi.org/10.1128/MCB.22.1.309-320.2002
49. Noguchi, E., C. Noguchi, W.H. McDonald, J.R. Yates III, and P. Russell. 2004. Swi1 and Swi3 are components of a replication fork protection complex in fission yeast. Mol. Cell. Biol. 24:8342-8355. http://dx.doi.org/10.1128/MCB.24.19.8342-8355.2004
50. Ogino, K., K. Hirota, S. Matsumoto, T. Takeda, K. Ohta, K. Arai, and H. Masai. 2006. Hsk1 kinase is required for induction of meiotic dsDNA breaks without involving checkpoint kinases in fission yeast. Proc. Natl. Acad. Sci. USA. 103:8131-8136. http://dx.doi.org/10.1073/pnas.0602498103
51. Okuno, Y., T. Okazaki, and H. Masukata. 1997. Identification of a predominant replication origin in fission yeast. Nucleic Acids Res. 25:530-537. http://dx.doi.org/10.1093/nar/25.3.530
52. Osborn, A.J., and S.J. Elledge. 2003. Mrc1 is a replication fork component whose phosphorylation in response to DNA replication stress activates Rad53. Genes Dev. 17:1755-1767. http://dx.doi.org/10.1101/gad.1098303
53. Patel, P.K., B. Arcangioli, S.P. Baker, A. Bensimon, and N. Rhind. 2006. DNA replication origins fire stochastically in fission yeast. Mol. Biol. Cell. 17:308-316. http://dx.doi.org/10.1091/mbc.E05-07-0657
54. Patel, P.K., N. Kommajosyula, A. Rosebrock, A. Bensimon, J. Leatherwood, J. Bechhoefer, and N. Rhind. 2008. The Hsk1(Cdc7) replication kinase regulates origin efficiency. Mol. Biol. Cell. 19:5550-5558. http://dx.doi.org/10.1091/mbc.E08-06-0645
55. Pessoa-Brandão, L., and R.A. Sclafani. 2004. CDC7/DBF4 functions in the translesion synthesis branch of the RAD6 epistasis group in Saccharomyces cerevisiae. Genetics. 167:1597-1610. http://dx.doi.org/10.1534/genetics.103.021675
56. Petermann, E., T. Helleday, and K.W. Caldecott. 2008. Claspin promotes normal replication fork rates in human cells. Mol. Biol. Cell. 19:2373-2378. http://dx.doi.org/10.1091/mbc.E07-10-1035
57. Pfaffle, P., and V. Jackson. 1990. Studies on rates of nucleosome formation with DNA under stress. J. Biol. Chem. 265:16821-16829.
58. Pope, B.D., I. Hiratani, and D.M. Gilbert. 2010. Domain-wide regulation of DNA replication timing during mammalian development. Chromosome Res. 18:127-136. http://dx.doi.org/10.1007/s10577-009-9100-8
59. Randell, J.C., A. Fan, C. Chan, L.I. Francis, R.C. Heller, K. Galani, and S.P. Bell. 2010. Mec1 is one of multiple kinases that prime the Mcm2-7 helicase for phosphorylation by Cdc7. Mol. Cell. 40:353-363. http://dx.doi.org/10.1016/j.molcel.2010.10.017
60. Santocanale, C., and J.F. Diffley. 1998. A Mec1- and Rad53-dependent checkpoint controls late-firing origins of DNA replication. Nature. 395:615-618. http://dx.doi.org/10.1038/27001
61. Sasanuma, H., K. Hirota, T. Fukuda, N. Kakusho, K. Kugou, Y. Kawasaki, T. Shibata, H. Masai, and K. Ohta. 2008. Cdc7-dependent phosphorylation of Mer2 facilitates initiation of yeast meiotic recombination. Genes Dev. 22:398-410. http://dx.doi.org/10.1101/gad.1626608
62. Sclafani, R.A. 2000. Cdc7p-Dbf4p becomes famous in the cell cycle. J. Cell Sci. 113:2111-2117.
63. Sclafani, R.A., M. Patterson, J. Rosamond, and W.L. Fangman. 1988. Differential regulation of the yeast CDC7 gene during mitosis and meiosis. Mol. Cell. Biol. 8:293-300.
64. Scorah, J., and C.H. McGowan. 2009. Claspin and Chk1 regulate replication fork stability by different mechanisms. Cell Cycle. 8:1036-1043. http://dx.doi.org/10.4161/cc.8.7.8040
65. Sheu, Y.-J., and B. Stillman. 2006. Cdc7-Dbf4 phosphorylates MCM proteins via a docking site-mediated mechanism to promote S phase progression. Mol. Cell. 24:101-113. http://dx.doi.org/10.1016/j.molcel.2006.07.033
66. Sheu, Y.J., and B. Stillman. 2010. The Dbf4-Cdc7 kinase promotes S phase by alleviating an inhibitory activity in Mcm4. Nature. 463:113-117. http://dx.doi.org/10.1038/nature08647
67. Shimmoto, M., S. Matsumoto, Y. Odagiri, E. Noguchi, P. Russell, and H. Masai. 2009. Interactions between Swi1-Swi3, Mrc1 and S phase kinase, Hsk1 may regulate cellular responses to stalled replication forks in fission yeast. Genes Cells. 14:669-682. http://dx.doi.org/10.1111/j.1365-2443.2009.01300.x
68. Shirahige, K., Y. Hori, K. Shiraishi, M. Yamashita, K. Takahashi, C. Obuse, T. Tsurimoto, and H. Yoshikawa. 1998. Regulation of DNA-replication origins during cell-cycle progression. Nature. 395:618-621. http://dx.doi.org/10.1038/27007
69. Snaith, H.A., G.W. Brown, and S.L. Forsburg. 2000. Schizosaccharomyces pombe Hsk1p is a potential cds1p target required for genome integrity. Mol. Cell. Biol. 20:7922-7932. http://dx.doi.org/10.1128/MCB.20.21.7922-7932.2000
70. Sommariva, E., T.K. Pellny, N. Karahan, S. Kumar, J.A. Huberman, and J.Z. Dalgaard. 2005. Schizosaccharomyces pombe Swi1, Swi3, and Hsk1 are components of a novel S-phase response pathway to alkylation damage. Mol. Cell. Biol. 25:2770-2784. http://dx.doi.org/10.1128/MCB.25.7.2770-2784.2005
71. Szyjka, S.J., C.J. Viggiani, and O.M. Aparicio. 2005. Mrc1 is required for normal progression of replication forks throughout chromatin in S. cerevisiae. Mol. Cell. 19:691-697. http://dx.doi.org/10.1016/j.molcel.2005.06.037
72. Takayama, Y., Y.M. Mamnun, M. Trickey, S. Dhut, F. Masuda, H. Yamano, T. Toda, and S. Saitoh. 2010. Hsk1- and SCF(Pof3)-dependent proteolysis of S. pombe Ams2 ensures histone homeostasis and centromere function. Dev. Cell. 18:385-396. http://dx.doi.org/10.1016/j.devcel.2009.12.024
73. Takeda, T., K. Ogino, E. Matsui, M.K. Cho, H. Kumagai, T. Miyake, K. Arai, and H. Masai. 1999. A fission yeast gene, him1(+)/dfp1(+), encoding a regulatory subunit for Hsk1 kinase, plays essential roles in S-phase initiation as well as in S-phase checkpoint control and recovery from DNA damage. Mol. Cell. Biol. 19:5535-5547.
74. Takeda, T., K. Ogino, K. Tatebayashi, H. Ikeda, Arai Ki, and H. Masai. 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.
75. Tanaka, K. 2010. Multiple functions of the S-phase checkpoint mediator. Biosci. Biotechnol. Biochem. 74:2367-2373. http://dx.doi.org/10.1271/bbb.100583
76. Tanaka, K., and P. Russell. 2001. Mrc1 channels the DNA replication arrest signal to checkpoint kinase Cds1. Nat. Cell Biol. 3:966-972. http://dx.doi.org/10.1038/ncb1101-966
77. Tanaka, K., and P. Russell. 2004. Cds1 phosphorylation by Rad3-Rad26 kinase is mediated by forkhead-associated domain interaction with Mrc1. J. Biol. Chem. 279:32079-32086. http://dx.doi.org/10.1074/jbc.M404834200
78. Tanaka, T., M. Yokoyama, S. Matsumoto, R. Fukatsu, Z. You, and H. Masai. 2010. Fission yeast Swi1-Swi3 complex facilitates DNA binding of Mrc1. J. Biol. Chem. 285:39609-39622. http://dx.doi.org/10.1074/jbc.M110.173344
79. Taylor, J.H. 1977. Increase in DNA replication sites in cells held at the beginning of S phase. Chromosoma. 62:291-300. http://dx.doi.org/10.1007/BF00327029
80. Tourrière, H., G. Versini, V. Cordón-Preciado, C. Alabert, and P. Pasero. 2005. Mrc1 and Tof1 promote replication fork progression and recovery independently of Rad53. Mol. Cell. 19:699-706. http://dx.doi.org/10.1016/j.molcel.2005.07.028
81. Warburton, P.E. 2004. Chromosomal dynamics of human neocentromere formation. Chromosome Res. 12:617-626. http://dx.doi.org/10.1023/B:CHRO.0000036585.44138.4b
82. Weintraub, H., H. Beug, M. Groudine, and T. Graf. 1982. Temperaturesensitive changes in the structure of globin chromatin in lines of red cell precursors transformed by ts-AEV. Cell. 28:931-940. http://dx.doi.org/10.1016/0092-8674(82)90072-1
83. Wu, P.-Y.J., and P. Nurse. 2009. Establishing the program of origin firing during S phase in fission Yeast. Cell. 136:852-864. http://dx.doi.org/10.1016/j.cell.2009.01.017
84. Xu, Y.J., M. Davenport, and T.J. Kelly. 2006. Two-stage mechanism for activation of the DNA replication checkpoint kinase Cds1 in fission yeast. Genes Dev. 20:990-1003. http://dx.doi.org/10.1101/gad.1406706
85. Yabuuchi, H., Y. Yamada, T. Uchida, T. Sunathvanichkul, T. Nakagawa, and H. Masukata. 2006. Ordered assembly of Sld3, GINS and Cdc45 is distinctly regulated by DDK and CDK for activation of replication origins. EMBO J. 25:4663-4674. http://dx.doi.org/10.1038/sj.emboj.7601347
86. Zegerman, P., and J.F. Diffley. 2010. Checkpoint-dependent inhibition of DNA replication initiation by Sld3 and Dbf4 phosphorylation. Nature. 467:474-478. http://dx.doi.org/10.1038/nature09373
87. Zhao, H., K. Tanaka, E. Nogochi, C. Nogochi, and P. Russell. 2003. Replication checkpoint protein Mrc1 is regulated by Rad3 and Tel1 in fission yeast. Mol. Cell. Biol. 23:8395-8403. http://dx.doi.org/10.1128/MCB.23.22.8395-8403.2003
88. Zou, L., and B. Stillman. 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. http://dx.doi.org/10.1128/MCB.20.9.3086-3096.2000