Checkpoint responses to replication stalling: Inducing tolerance and preventing mutagenesis

Mutation Research - Fundamental and Molecular Mechanisms of Mutagenesis

Volumn 532, Issue 1-2, 2003, Pages 59-73

  Kai, Mihoko ^a   Wang, Teresa S F ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Cds1; Checkpoints; DinB; Mus81; Mutator phenotype; Rad17; Translesion synthesis

Indexed keywords

CYCLIN DEPENDENT KINASE 1; ENDONUCLEASE; HELICASE; NUCLEOTIDE; PROTEIN; PROTEIN RAD 60; UNCLASSIFIED DRUG;

CARCINOGENESIS; CELL DIVISION; CELL SURVIVAL; CHROMATIN; DNA DAMAGE; DNA REPAIR; DNA STRUCTURE; FRAMESHIFT MUTATION; GENE REPLICATION; MUTAGENESIS; MUTANT; NONHUMAN; PHENOTYPE; POINT MUTATION; PRIORITY JOURNAL; PROTEIN STABILITY; PROTEIN STRUCTURE; REGULATORY MECHANISM; REVIEW; SACCHAROMYCES; UPREGULATION; YEAST;

SCHIZOSACCHAROMYCES; SCHIZOSACCHAROMYCES POMBE;

EID: 0344741364     PISSN: 00275107     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mrfmmm.2003.08.010     Document Type: Review

References (140)

1. E.C. Friedberg, G.C. Walker, W. Siede, DNA Repair and Mutagenesis, ASM Press, Washington DC, 1995.
2. Hartwell L.H., Weinert T.A. Checkpoints: controls that ensure the order of cell cycle events. Science. 246:1989;629-634.
3. Prakash S., Sung P., Prakash L. DNA repair genes and proteins of Saccharomyces cerevisiae. Annu. Rev. Genet. 27:1993;33-70.
4. Elledge S.J. Cell cycle checkpoints: preventing an identity crisis. Science. 274:1996;1664-1672.
5. O'Connell M.J., Walworth N.C., Carr A.M. The G2-phase DNA damage checkpoint. Trends Cell Biol. 10:2000;296-303.
6. Zhou B.B., Elledge S.J. The DNA damage response: putting checkpoints in perspective. Nature. 408:2000;433-439.
7. Hoeijmakers J.H. Genome maintenance mechanisms for preventing cancer. Nature. 411:2001;366-374.
8. Nyberg K.A., Michelson R.J., Putnam C.W., Weinert T.A. Toward maintaining the genome: DNA damage and replication checkpoints. Annu. Rev. Genet. 36:2002;617-656.
9. Hartwell L.H., Kastan M.B. Cell cycle control and cancer. Science. 266:1994;1821-1828.
10. Lengauer C., Kinzler K.W., Vogelstein B. Genetic instabilities in human cancers. Nature. 396:1998;643-649.
11. Rhind N., Russell P. Mitotic DNA damage and replication checkpoints in yeast. Curr. Opin. Cell Biol. 10:1998;749-758.
12. Rhind N., Russell P. Chk1 and Cds1: linchpins of the DNA damage and replication checkpoint pathways. J. Cell Sci. 113:2000;3889-3896.
13. Abraham R.T. Cell cycle checkpoint signaling through the ATM and ATR kinases. Genes Dev. 15:2001;2177-2196.
14. Paulovich A.G., Margulies R.U., Garvik B.M., Hartwell L.H. RAD9, RAD17, and RAD24 are required for S phase regulation in Saccharomyces cerevisiae in response to DNA damage. Genetics. 145:1997;45-62.
15. Paulovich A.G., Armour C.D., Hartwell L.H. The Saccharomyces cerevisiae RAD9, RAD17, RAD24 and MEC3 genes are required for tolerating irreparable, ultraviolet-induced DNA damage. Genetics. 150:1998;75-93.
16. Datta A., Scheits J.L., Amin N.S., Lau P.J., Myung K., Kolodner R.D. Checkpoint-dependent activation of mutagenic repair in Saccharomyces cerevisiae pol3-01 mutants. Mol. Cell. 6:2000;593-603.
17. Myung K., Datta A., Kolodner R.D. Suppression of spontaneous chromosome rearrangements by S phase checkpoint functions in Saccharomyces cerevisiae. Cell. 104:2001;397-408.
18. Myung K., Kolodner R.D. Suppression of genome instability by redundant S-phase checkpoint pathways in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. U.S.A. 99:2002;4500-4507.
19. Kolodner R.D., Putnam C.D., Myung K. Maintenance of genome stability in Saccharomyces cerevisiae. Science. 297:2002;552-557.
20. Friedberg E.C., Wagner R., Radman M. Specialized DNA polymerases, cellular survival, and the genesis of mutations. Science. 296:2002;1627-1630.
21. Goodman M.F. Error-prone repair DNA polymerases in prokaryotes and eukaryotes. Annu. Rev. Biochem. 71:2002;17-50.
22. Morrison A., Johnson A.L., Johnston L.H., Sugino A. Pathway correcting DNA replication errors in Saccharomyces cerevisiae. EMBO J. 12:1993;1467-1473.
23. Morrison A., Sugino A. The 3′ → 5′ exonucleases of both DNA polymerases δ and ε participate in correcting errors of DNA replication in Saccharomyces cerevisiae. Mol. Gen. Genet. 242:1994;289-296.
24. Strand M., Prolla T.A., Liskay R.M., Petes T.D. Destabilization of tracts of simple repetitive DNA in yeast by mutations affecting DNA mismatch repair. Nature. 365:1993;274-276.
25. Kokoska R.J., Stefanovic L., Tran H.T., Resnick M.A., Gordenin D.A., Petes T.D. Destabilization of yeast micro- and minisatellite DNA sequences by mutations affecting a nuclease involved in Okazaki fragment processing (rad27) and DNA polymerase δ (pol3-t). Mol. Cell. Biol. 18:1998;2779-2788.
26. Kokoska R.J., Stefanovic L., DeMal J., Petes T.D. Increased rates of genomic deletions generated by mutations in the yeast gene encoding DNA polymerase δ or by decreases in the cellular levels of DNA polymerase δ Mol. Cell. Biol. 20:2000;7490-7504.
27. Tran H.T., Keen J.D., Kricker M., Resnick M.A., Gordenin D.A. Hypermutability of homonucleotide runs in mismatch repair and DNA polymerase proofreading yeast mutants. Mol. Cell. Biol. 17:1997;2859-2865.
28. Kirchner J.M., Tran H., Resnick M.A. A DNA polymerase e mutant that specifically causes +1 frameshift mutations withing homonucleotide runs in yeast. Genetics. 155:2000;1623-1632.
29. Gordenin D.A., Malkova A.L., Peterzen A., Kulikov V.N., Pavlov Y.I., Perkins E., Resnick M.A. Transposon Tn5 excision in yeast: influence of DNA polymerases α, δ, and ε and repair genes. Proc. Natl. Acad. Sci. U.S.A. 89:1992;3785-3789.
30. Tran H.T., Degtyareva N.P., Koloteva N.N., Sugino A., Msumoto H., Gordenin D.A., Resnick M.A. Replication slippage between distant short repeats in Saccharomyces cerevisiae depends on the direction of replication and the RAD50 and RAD52 genes. Mol. Cell. Biol. 15:1995;5607-5617.
31. Gutierrez P.J., Wang T.S.-F. Genomic instability induced by mutations in Saccharomyces cerevisiae POL1. Genetics. 165:2003;65-81.
32. Liu V.F., Bhaumik D., Wang T.S.-F. Mutator phenotype induced by aberrant replication. Mol. Cell. Biol. 19:1999;1126-1135.
33. Tishkoff D.X., Filosi N., Gaida G.M., Kolodner R.D. A novel mutation avoidance mechanism dependent on S. cerevisiae RAD27 is distinct from DNA mismatch repair. Cell. 88:1997;253-263.
34. Kai M., Wang T.S.-F. Checkpoint activation regulates mutagenic translesion synthesis. Genes Dev. 1:2003;64-76.
35. Al-Khodairy F., Fotou E., Sheldrick K.S., Griffiths D.J., Lehmann A.R., Carr A.M. Identification and characterization of new elements involved in checkpoint and feedback controls in fission yeast. Mol. Biol. Cell. 5:1994;147-160.
36. Caspari T., Carr A.M. DNA structure checkpoint pathways in Schizosaccharomyces pombe. Biochemie. 81:1999;173-181.
37. Weinert T.A., Hartwell L.H. The Rad9 gene controls the cell cycle response to DNA damage in Saccharomyces cerevisiae. Science. 241:1988;317-322.
38. Green C.M., Lowndes N.F. Rad9 and Rad24 define two additive interacting branches of the DNA damage checkpoint pathway in budding yeast normally required for Rad53 modification and activation. EMBO J. 17:1998;2687-2698.
39. Tanaka K., Russell P. Mrc1 channels the DNA replication arrest signal to checkpoint kinase Cds1. Nat. Cell Biol. 3:2001;966-972.
40. Alcasabas A.A., Osborn A.J., Bachant J., Hu F., Werler P.J., Bousset K., Furuya K., Diffley J.F., Carr A.M., Elledge S.J. Mrc1 transduces signals of DNA replication stress to activate Rad53s. Nat. Cell Biol. 3:2001;958-965.
41. Kumagai A., Dunphy W.G. Claspin, a novel protein required for the activation of Chk1 during a DNA replication checkpoint response in Xenopus egg extracts. Mol. Cell. 6:2000;839-849.
42. Lee J., Kumagai A., Dunphy W.G. Claspin, a Chk1-regulatory protein, monitors DNA replication on chromatin independently of RPA, ATR, and Rad17. Mol. Cell. 11:2003;329-340.
43. Osborn A.J., Elledge S.J. Mrc1 is a replication fork component whose phosphorylation in response to DNA replication stress activates Rad53. Genes Dev. 17:2003;1755-1767.
44. Bentley N.J., Holtzman D.A., Flaggs G., Keegan K.S., DeMaggio A., Ford J.C., Hoekstra M., Carr A.M. The Schizosaccharomyces pombe rad3 checkpoint gene. EMBO J. 15:1996;6641-6651.
45. sp DNA structure checkpoint pathway. Curr. Opin. Genet. Dev. 7:1997;93-98.
46. Martinho R.G., Lindsay H.D., Flaggs G., DeMaggio A.J., Hoekstra M.F., Carr A.M., Bentley N.J. Analysis of Rad3 and Chk1 protetin kinases defines different checkpoint responses. EMBO J. 17:1998;7239-7249.
47. Melo J., Toczyski D. A unified view of the DNA-damage checkpoint. Curr. Opin. Cell Biol. 14:2002;237-245.
48. Edwards R.J., Bentley N.J., Carr A.M. A Rad3-Rad26 complex responds to DNA damage independently of other checkpoint proteins. Nat. Cell Biol. 1:1999;393-398.
49. Paciotti V., Clerici M., Luchinin G., Longhese P. The checkpoint protein Ddc2, functionally related to S pombe Rad26 interacts with Mec1 and is regulated by Mec1-dependent phosphorylation in budding yeast. Genes Dev. 14:2000;2046-2059.
50. Rouse J., Jackson S.P. LCD1: an essential gene involved in checkpoint control and regulation of the MEC1 signalling pathway in Saccharomyces cerevisiae. EMBO J. 19:2000;5801-5812.
51. Wakayama T., Kondo T., Ando S., Matsumoto K., Sugimoto K. Pie1, a protein interacting with Mec1, controls cell growth and checkpoint responses in Saccharomyces cerevisiae. Mol. Cell Biol. 21:2001;755-764.
52. Rouse J., Jackson S.P. Lcd1p recruits Mec1p to DNA lesions in vitro and in vivo. Mol. Cell. 9:2002;857-869.
53. Wolkow T.D., Enoch T. Fission yeast Rad26 is a regulatory subunit of the Rad3 checkpoint kinase. Mol. Biol. Cell. 13:2002;480-492.
54. Cortez D., Guntuku S., Qin J., Elledge S.J. ATR and ATRIP: partners in checkpoint signaling. Science. 294:2001;1713-1716.
55. Zou L., Elledge S.J. Sensing DNA damage through ATRIP recognition of RPA-ssDNA complexes. Science. 300:2003;1542-1548.
56. Kostrub C.F., Knudsen K., Subramani S., Enoch T. Hus1p, a conserved fission yeast checkpoint protein, interacts with Rad1p and is phosphorylated in response to DNA damage. EMBO J. 17:1998;2055-2066.
57. Aravind L., Walker D.R., Koonin E.V. Conserved domains in DNA repair proteins and evolution of repair systems. Nucleic Acids Res. 27:1999;1223-1242.
58. Venclovas C., Thelen M.P. Structure-based predictions of Rad1, Rad9, Hus1 and Rad17 participation in sliding clamp and clamp-loading complexes. Nucleic Acids Res. 28:2000;2481-2493.
59. Caspari T., Dahlen M., Kanter-Smoler G., Lindsay H.D., Hoffmann K., Papadimitriou K., Sunnerhagen P., Carr A.M. Characterization of Schizosaccharomyces pombe Hus1: a PCNA-related protein that associates with Rad1 and Rad9. Mol. Cell. Biol. 74:2000;1254-1262.
60. Griffiths D.J.F., Barbet N.C., McCready S., Lehmann A.R., Carr A.M. Fission yeast rad17: a homologue of budding yeast RAD24 that shares regions of sequence similarity with DNA polymerase accessory proteins. EMBO J. 14:1995;5812-5823.
61. Griffiths D., Uchiyama M., Nurse P., Wang T.S.-F. A novel allele of the chromatin-bound fission yeast checkpoint protein Rad17 separates the DNA structure checkpoints. J. Cell Sci. 113:2000;1075-1088.
62. Kai M., Tanaka H., Wang T.S.-F. Fission yeast Rad17 binds to chromatin in response to replication arrest or DNA damage. Mol. Cell. Biol. 21:2001;3289-3301.
63. Kondo T., Wakayama T., Naiki T., Matsumoto K., Sugimoto K. Recruitment of mec1 and ddc1 checkpoint proteins to double-strand breaks through distinct mechanisms. Science. 294:2001;867-870.
64. Melo J.A., Cohen J., Toczyski D.P. Two checkpoint complexes are independently recruited to sites of DNA damage in vivo. Genes Dev. 15:2001;2809-2821.
65. Zou L., Cortez D., Elledge S.J. Regulation of ATR substrate selection by Rad17-dependent loading of Rad9 complexes onto chromatin. Genes Dev. 16:2002;198-208.
66. Bermudez V.P., Lindsey-Boltz L.A., Cesare A.J., Maniwa Y., Griffith J.D., Hurwitz J., Sancar A. Loading of the human 9-1-1 checkpoint complex onto DNA by the checkpoint clamp loader hRad17-replication factor C complex in vitro. Proc. Natl. Acad. Sci. U.S.A. 100:2003;1633-1638.
67. Majka J., Burgers P.M. Yeast Rad17/Mec3/Ddc1: A sliding clamp for the DNA damage checkpoint. Proc. Natl. Acad. Sci. U.S.A. 100:2003;2249-2254.
68. Murakami H., Okayama H. A kinase from fission yeast responsible for blocking mitosis in S phase. Nature. 374:1995;817-819.
69. Lindsay H.D., Griffiths D.J.F., Edwards R., Murray J.M., Christensen P.U., Walworth N., Carr A.M. S-phase specific activation of Cds1 kinase defines a subpathway of the checkpoint response in S. pombe. Genes Dev. 12:1998;382-395.
70. Desany B.A., Alcasabas A.A., Bachant J.B., Elledge S.J. Recovery from DNA replicational stress is the essential function of the S-phase checkpoint pathway. Genes Dev. 12:1998;2956-2970.
71. Lopes M., Cotta-Ramusino C., Pellicioli A., Liberi G., Plevani P., Muzi-Falconi M., Newlon C.S., Foiani M. The DNA replication checkpoint response stabilizes stalled replication forks. Nature. 412:2001;557-561.
72. Sogo J.M., Lopes M., Foiani M. Fork reversal and ssDNA accumulation at stalled replication forks owing to checkpoint defects. Science. 297:2002;599-602.
73. Santocanale S., Diffley J.F.X. A Mec1- and Rad53-dependent checkpoint controls late-firing origins of DNA replication. Nature. 395:1998;615-618.
74. Shirahige K., Hori Y., Shirishi K., Yamashita M., Takahashi K., Obuse C., Tsurimoto T., Yoshikawa H. Regulation of DNA-replication origins during cell-cycle progression. Nature. 395:1998;618-621.
75. Kim S.M., Huberman J.A. Regulation of replication timing in fission yeast. EMBO J. 20:2001;6115-6126.
76. Tercero J.A., Longhese M.P., Diffley J.F.X. A central role for DNA replication forks in checkpoint activation and response. Mol. Cell. 11:2003;1323-1336.
77. Sun Z., Hsiao J., Fay D.S., Stern D.F. Rad53 FHA domain associated with phosphorylated Rad9 in the DNA checkpoint. Science. 281:1998;272-274.
78. Boddy M.N., Russell P. DNA replication checkpoint. Curr. Biol. 11:2001;R953-R956.
79. Boddy M.N., Lopez-Girona A., Shanahan P., Interthal H., Heyer W.D., Russell P. Damage tolerance protein Mus81 associates with the FHA1 domain of checkpoint kinase Cds1. Mol. Cell. Biol. 20:2000;8758-8766.
80. M.N. Boddy, P. Shanahan, W.H. McDonald, A. Lopez-Girona, E. Noguchi, J.R.Yates III, P. Russell, Replication checkpoint kinase Cds1 regulates recombinational repair protein Rad60, Mol. Cell. Biol. 23 (2003) 5939-5946.
81. Sutton M.D., Smith B.T., Godoy V.G., Walker G.C. The SOS response: recent insights into umuDC-dependent mutagenesis and DNA damage tolerance. Annu. Rev. Genet. 34:2000;479-497.
82. Wagner J., Gruz P., Kim S.R., Yamada M., Matsui K., Fuchs R.P., Nohmi T., coli DNA polymerase E. DNA pol IV, involved in mutagenesis. Mol. Cell. 4:1999;281-286.
83. Ohmori H., Friedberg E.C., Fuchs R.P., Goodman M.F., Hanaoka F., Hinkle D., Kunkel T.A., Lawrence C.W., Livneh Z., Nohmi T., Prakash L., Prakash S., Todo T., Walker G.C., Wang Z., Woodgate R. The Y-family of DNA polymerases. Mol. Cell. 8:2001;7-8.
84. Wang Z. Translesion synthesis by the UmuC family of DNA polymerases. Mutat. Res. 486:2001;59-70.
85. Johnson R.E., Prakash S., Prakash L. Efficient bypass of a thymine-thymine dimer by yeast DNA polymerase. Polym. Sci. 283:1999;1001-1004.
86. Masutani C., Kusumoto R., Yamada A., Dohmae M., Yokoi M., Yuasa M., Araki M., Iwai S., Takio K., Hanaoka F. The XPV (xeroderma pigmentosum variant) gene encodes human DNA polymerase η Nature. 399:1999;700-704.
87. Johnson R.E., Washington M.T., Prakash S., Prakash L. Fidelity of human DNA polymerase η J. Biol. Chem. 275:2000;7447-7450.
88. Matsuda T., Bebenek K., Masutani C., Rogozin I.B., Hanaoka F., Kunkel T.A. Error rate and specificity of human and murine DNA polymerase η J. Mol. Biol. 312:2001;335-346.
89. Washington M.T., Johnson R.E., Prakash L., Prakash S. Accuracy of lesion bypass by yeast and human DNA polymerase η Proc. Natl. Acad. Sci. U.S.A. 98:2001;8355-8360.
90. Trincao J., Johnson R.E., Escalante C.R., Prakash S., Prakash L., Aggarwal A.K. Structure of the catalytic core of S cerevisiae DNA polymerase η: implications for translesion DNA synthesis. Mol. Cell. 8:2001;417-426.
91. Prakash S., Prakash L. Translesion DNA synthesis in eukaryotes: a one- or two-polymerase affair. Genes Dev. 16:2002;1872-1883.
92. Tanaka K., Yonekawa T., Kawasaki Y., Kai M., Furuya K., Iwasaki M., Murakami H., Yanagida M., Okayama H. Fission yeast Eso1p is required for establishing sister chromatid cohesion during S phase. Mol. Cell. Biol. 20:2000;3459-3469.
93. Madril A.C., Johnson R.E., Washington M.T., Prakash L., Prakash S. Fidelity and damage bypass ability of Schizosaccharomyces pombe Eso1 protein, comprised of DNA polymerase η and sister chromatid cohesion protein Ctf7. J. Biol. Chem. 276:2001;42857-42862.
94. Ohashi E., Bebenek K., Matsuda T., Feaver W.J., Gerlach V.L., Friedberg E.C., Ohmori H., Kunkel T.A. Fidelity and processivity of DNA synthesis by DNA polymerase κ, the product of the human DINB1 gene. J. Biol. Chem. 275:2000a;39678-39684.
95. Ohashi E., Ogi T., Kusumoto R., Iwai S., Masutani C., Hanaoka F., Ohmori H. Error-prone bypass of certain DNA lesions by the human DNA polymerase κ Genes Dev. 14:2000b;1589-1594.
96. Washington M.T., Johnson R.E., Prakash L., Prakash S. Human DINB1-encoded DNA polymerase kappa is a promiscuous extender of mispaired primer termini. Proc. Natl. Acad. Sci. USA. 99:2002;1910-1914.
97. Courcelle J., Hanawalt P.C. RecQ and RecJ process blocked replication forks prior to the resumption of replication in UV-irradiated Escherichia coli. Mol. Gen. Genet. 262:1999;543-551.
98. Courcelle J., Donaldson J.R., Chow K.H., Courcelle C.T. DNA damage-induced replication fork regression and processing in Escherichia coli. Science. 299:2003;1064-1067.
99. Doe C.L., Dixon J., Osman F., Whitby M.C. Partial suppression of the fission yeast rqh1(-) phenotype by expression of a bacterial Holliday junction resolvase. EMBO J. 19:2000;2751-2762.
100. Doe C.L., Ahn J.S., Dixon J., Whitby M.C. Mus81-Eme1 and rqh1 involvement in processing stalled and collapsed replication forks. J. Biol. Chem. 277:2002;32753-32759.
101. Boddy M.N., Gaillard P.H., McDonald W.H., Shanahan P., Yates J.R., Russell P. Mus81-Eme1 are essential components of a Holliday junction resolvase. Cell. 107:2001;537-548.
102. Stewart E., Chapman C.R., Al-Khodairy F., Carr A.M., Enoch T. rqh1+: a fission yeast gene related to the Bloom's and Werner's syndrome genes, is required for reversible S phase arrest. EMBO J. 16:1997;2682-2692.
103. Murray J.M., Lindsay H.D., Munday C.A., Carr A.M. Role of Schizosaccharomyces pombe RecQ homolog, recombination, and checkpoint genes in UV damage tolerance. Mol. Cell. Biol. 17:1997;6868-6875.
104. Chakraverty R.K., Hickson I.D. Defending genome integrity during DNA replication: a proposed role for RecQ family helicases. Bioessays. 21:1999;286-294.
105. Hickson I.D., Davies S.L., Li J.L., Levitt N.C., Mohaghegh P., North P.S., Wu L. Role of the Bloom's syndrome helicase in maintenance of genome stability. Biochem. Soc. Trans. 29:2001;201-204.
106. Frei C., Gasser S.M. RecQ-like helicases: the DNA replication checkpoint connection. J. Cell Sci. 113:2000;2641-2646.
107. Wu L., Hickson I.D. RecQ helicases and cellular responses to DNA damage. Mutat. Res. 509:2002;35-47.
108. Laursen L.V., Ampatzidou E., Andersen A.H., Murray J.M. Role for the fission yeast RecQ Helicase in DNA repair in G(2). Mol. Cell. Biol. 23:2003;3692-3705.
109. Myung K., Datta A., Chen C., Kolodner R.D. SGS1, the Saccharomyces cerevisiae homologue of BLM and WRN, suppresses genome instability and homologous recombination. Nat. Genet. 27:2001;113-116.
110. Constantinou A., Tarsounas M., Karow J.K., Brosh R.M., Bohr V.A., Hickson I.D., West S.C. Werner's syndrome protein (WRN) migrates Holliday junctions and co- localizes with RPA upon replication arrest. EMBO Rep. 1:2000;80-84.
111. Karow J.K., Constantinou A., Li J.L., West S.C., Hickson I.D. The Bloom's syndrome gene product promotes branch migration of Holliday junctions. Proc. Natl. Acad. Sci. U.S.A. 97:2000;6504-6508.
112. Fabre F., Chan A., Heyer W.D., Gangloff S. Alternate pathways involving Sgs1/Top3, Mus81/Mms4, and Srs2 prevent formation of toxic recombination intermediates from single-stranded gaps created by DNA replication. Proc. Natl. Acad. Sci. U.S.A. 99:2002;16887-16892.
113. Osborn A.J., Elledge S.J., Zou L. Checking on the fork: the DNA-replication stress-response pathway. Trends Cell Biol. 12:2002;509-516.
114. Frei C., Gasser S.M. The yeast Sgs1p helicase acts upstream of Rad53p in the DNA replication checkpoint and colocalizes with Rad53p in S-phase-specific foci. Genes Dev. 14:2000;81-96.
115. Versini G., Comet I., Wu M., Hoopes L., Schwob E., Pasero P. The yeast Sgs1 helicase is differentially required for genomic and ribosomal DNA replication. EMBO J. 22:2003;1939-1949.
116. Cobb J.A., Bjergbaek L., Shimada K., Frei C., Gasser S.M. DNA polymerase stabilization at stalled replication forks requires Mec1 and the RecQ helicase Sgs1. EMBO J. 22:2003;4325-4336.
117. Kaliraman V., Mullen J.R., Fricke W.M., Bastin-Shanower S.A., Brill S.J. Functional overlap between Sgs1-Top3 and the Mms4-Mus81 endonuclease. Genes Dev. 15:2001;2730-2740.
118. Chen X.B., Melchionna R., Denis C.M., Gaillard P.H., Blasina A., Van de Weyer I., Boddy M.N., Russell P., Vialard J., McGowan C.H. Human Mus81-associated endonuclease cleaves Holliday Junctions in vitro. Mol. Cell. 8:2001;1117-1127.
119. Bastin-Shanower S.A., Fricke W.M., Mullen J.R., Brill S.J. The mechanism of Mus81-MMS4 cleavage site selection distinguishes it from the homologous endonuclease rad1-rad10. Mol. Cell Biol. 23:2003;3487-3496.
120. Whitby M.C., Osman F., Dixon J. Cleavage of model replication forks by fission yeast Mus81-Eme1 and budding yeast Mus81-MMS4. J. Biol. Chem. 278:2003;6928-6935.
121. Constantinou A., Chen X.B., McGowan C.H., West S.C. Holliday junction resolution in human cells: two junction endonucleases with distinct substrate specificities. EMBO J. 21:2002;5577-5585.
122. Ciccia A., Constantinou A., West S.C. Identification and characterization of the human Mus81-Eme1 endonuclease. J. Biol. Chem. 278:2003;25172-25178.
123. Interthal H., Heyer W.D. MUS81 encodes a novel helix-hairpin-helix protein involved in the response to UV- and methylation-induced DNA damage in Saccharomyces cerevisiae. Mol. Gen. Genet. 263:2000;812-827.
124. Mullen J.R., Kaliraman V., Ibrahim S.S., Brill S.J. Requirement for three novel protein complexes in the absence of the Sgs1 DNA helicase in Saccharomyces cerevisiae. Genetics. 157:2001;103-118.
125. de los Santos T., Loidl J., Larkin B., Hollingsworth N.M. A role for MMS4 in the processing of recombination intermediates during meiosis in Saccharomyces cerevisiae. Genetics. 159:2001;1511-1525.
126. Morishita T., Tsutsui Y., Iwasaki H., Shinagawa H. The Schizosaccharomyces pombe rad60 gene is essential for repairing double-strand DNA breaks spontaneously occurring during replication and induced by DNA-damaging agents. Mol. Cell. Biol. 22:2002;3537-3548.
127. Lee S.K., Johnson R.E., Yu S.L., Prakash L., Prakash S. Requirement of yeast SGS1 and SRS2 genes for replication and transcription. Science. 286:1999;2339-2342.
128. Broomfield S., Xiao W. Suppression of genetic defects within the RAD6 pathway by srs2 is specific for error-free post-replication repair but not for damage-induced mutagenesis. Nucleic Acids Res. 30:2002;732-739.
129. Broomfield S., Hryciw T., Xiao W. DNA postreplication repair and mutagenesis in Saccharomyces cerevisiae. Mutat. Res. 486:2001;167-184.
130. Vaze M.B., Pellicioli A., Lee S.E., Ira G., Liberi G., Arbel-Eden A., Foiani M., Haber J.E. Recovery from checkpoint-mediated arrest after repair of a double-strand break requires Srs2 helicase. Mol. Cell. 10:2002;373-385.
131. Veaute X., Jeusset J., Soustelle C., Kowalczykowshi S.C., Cam E.L., Fabre F. The Srs2 helicase prevents recombination by disrupting Rad51 nucleoprotein filaments. Nature. 423:2003;309-312.
132. Krejcl L., Komen S.V., Li Y., Villemin J., Reddy M.S., klein H., Elleberger T., Sung P. DNA helicase Srs2 disrupts the Rad51 presynptic filament. Nature. 423:2003;305-309.
133. Wang S.W., Goodwin A., Hickson I.D., Norbury C.J. Involvement of Schizosaccharomyces pombe Srs2 in cellular responses to DNA damage. Nucleic Acids Res. 29:2001;2963-2972.
134. Maftahi M., Hope J.C., Delgado-Cruzata L., Han C.S., Freyer G.A. The severe slow growth of Δsrs2 Δrqh1 in Schizosaccharomyces pombe is suppressed by loss of recombination and checkpoint genes. Nucleic Acids Res. 30:2002;4781-4792.
135. Bhaumik D., Wang T.S.-F. Mutational effect of fission yeast Polα on cell cycle events. Mol. Biol. Cell. 9:1998;2107-2123.
136. Tanaka K., Boddy M.N., Chen X.B., McGowan C.H., Russell P. Threonine-11, phosphorylated by Rad3 and ATM in vitro, Is required for activation of fission yeast checkpoint kinase Cds1. Mol. Cell. Biol. 21:2001;3398-3404.
137. O'Neill T., Dwyer A.J., Ziv Y., Chan D.W., Lees-Miller S.P., Abraham R.H., Lai J.H., Hill D., Shiloh Y., Cantley L.C., Rathbun G.A. Utilization of oriented peptide libraries to identify substrate motifs selected by ATM. J. Biol. Chem. 275:2000;22719-22727.
138. Kim S.T., Lim D.S., Canman C.E., Kastan M.B. Substrate specificities and identification of putative substrates of ATM kinase family members. J. Biol. Chem. 274:1999;37538-37543.
139. Tercero J.A., Diffley J.F. Regulation of DNA replication fork progression through damaged DNA by the Mec1/Rad53 checkpoint. Nature. 412:2001;553-557.
140. Lehmann A.R., Walicka M., Griffths D.J.F., Murray J.M., Watts F.Z., McCready S., Carr A.M. The rad18 gene of Schizosaccharomyces pombe defines a new subgroup of the SMC superfamily involved in DNA repair. Mol. Cell Biol. 15:1995;7067-7080.