Checkpoint activation regulates mutagenic translesion synthesis

Genes and Development

Volumn 17, Issue 1, 2003, Pages 64-76

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

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Cds1; Checkpoint response; DinB; Mutagenic translesion synthesis; Mutator phenotype; Rad17

Indexed keywords

CHECKPOINT KINASE 2; DNA POLYMERASE; POL PROTEIN; PROTEIN DERIVATIVE; PROTEIN DINB; PROTEIN RAD17; UNCLASSIFIED DRUG;

ARTICLE; CELL DIVISION; CONTROLLED STUDY; DNA DAMAGE; DNA REPLICATION; DNA SYNTHESIS; GENE DELETION; GENE MUTATION; GENOME; MOLECULAR INTERACTION; MUTAGENESIS; NONHUMAN; PHENOTYPE; POINT MUTATION; PRIORITY JOURNAL; PROTEIN EXPRESSION;

EID: 0037224965     PISSN: 08909369     EISSN: None     Source Type: Journal    
DOI: 10.1101/gad.1043203     Document Type: Article

References (59)

1. Al-Khodairy, F., Fotou, E., Sheldrick, K.S., Griffiths, D.J., Lehmann, A.R., and Carr, A.M. 1994. Identification and characterization of new elements involved in checkpoint and feedback controls in fission yeast. Mol. Biol. Cell. 5: 147-160.
2. Bahler, J., Wu, J.Q., Longtine, M.S., Shah III, N.G., Steever, A.B., Wach, A., Philippsen, P., and Pringle, J.R. 1998. Heterologous modules for efficient and versatile PCR-based gene targeting in Schizosaccharomyces pombe. Yeast 14: 943-951.
3. Bhaumik, D. and Wang, T.S.F. 1998. Mutational effect of fission yeast Polα on cell cycle events. Mol. Biol. Cell 9: 2107-2123.
4. Boddy, M.N., Gaillard, P.H., McDonald, W.H., Shanahan, P., Yates, J.R., and Russell, P. 2001. Mus81-Eme1 are essential components of a Holliday junction resolvase. Cell 107: 537-548.
5. Caspari, T. and Carr, A.M. 1999. DNA structure checkpoint pathways in Schizosaccharomyces pombe. Biochemie 81: 173-181.
6. Caspari, T., Dahlen, M., Kanter-Smoler, G., Lindsay, H.D., Hoffmann, K., Papadimitriou, K., Sunnerhagen, P., and Carr, A.M. 2000. Characterization of Schizosaccharomyces pombe Hus1: A PCNA-related protein that associates with Rad1 and Rad9. Mol. Cell. Biol. 74: 1254-1262.
7. Datta, A., Scheits, J.L., Amin, N.S., Lau, P.J., Myung, K., and Kolodner, R.D. 2000. Checkpoint-dependent activation of mutagenic repair in Saccharomyces cerevisiae po13-01 mutants. Mol. Cell 6: 593-603.
8. Desany, B.A., Alcasabas, A.A., Bachant, J.B., and Elledge, S.J. 1998. Recovery from DNA replicational stress is the essential function of the S-phase checkpoint pathway. Genes & Dev. 12: 2956-2970.
9. Edwards, P.J., Bentley, N.J., and Carr, A.M. 1999. A Rad3-Rad26 complex responds to DNA damage independently of other checkpoint proteins. Nat. Cell Biol. 1: 393-398.
10. Elledge, S.J. 1996. Cell cycle checkpoints: Preventing an identity crisis. Science 274: 1664-1672.
11. Fischhaber, P.L., Gerlach, V.L., Feaver, W.J., Hatahet, Z., Wallace, S.S., and Friedberg, E.C. 2002. Human DNA polymerase kappa bypasses and extends beyond thymine glycols during translesion synthesis in vitro, preferentially incorporating correct nucleotides. J. Biol. Chem. 277: 37604-37611.
12. Friedberg, E.C., Walker, G.C., and Siede, W. 1995. DNA repair and mutagenesis. ASM Press, Washington D.C.
13. Friedberg, E.C., Feaver, W.J., and Gerlach, V.L. 2000. The many faces of DNA polymerases: strategies for mutagenesis and for mutational avoidance. Proc. Natl Acad. Sci. 97: 5681-5683.
14. Friedberg, E.C., Wagner, R., and Radman, M. 2002. Specialized DNA polymerases, cellular survival, and the genesis of mutations. Science 296: 1627-1630.
15. Goodman, M.F. 2002. Error-prone repair DNA polymerases in prokaryotes and eukaryotes. Annu. Rev. Biochem. 71: 17-50.
16. Griffiths, D.J.F., Barbet, N.C., McCready, S., Lehmann, A.R., and Carr, A.M. 1995. Fission yeast rad17: A homologue of budding yeast RAD24 that shares regions of sequence similarity with DNA polymerase accessory proteins. EMBO J. 14: 5812-5823.
17. Griffiths, D., Uchiyama, M., Nurse, P., and Wang, T.S.F. 2000. A novel allele of the chromatin-bound fission yeast checkpoint protein Rad17 separates the DNA structure checkpoints. J. Cell Sci. 113: 1075-1088.
18. Gutz, H., Heslot, H., Leupold, U., and Loprieno, N. 1974. Schizosaccharomyces pombe. In Handbook of genetics 1 (ed. R.C. King), pp. 395-446. Plenum Press, New York, NY.
19. Haracska, L., Unk, I., Johnson, R.E., Phillips, B.B., Hurwitz, J., Prakash, L., and Prakash, S. 2002. Stimulation of DNA synthesis activity of human DNA polymerase κ by PCNA. Mol. Cell. Biol. 22: 784-791.
20. Hartwell, L.H. and Kastan, M.B. 1994. Cell cycle control and cancer. Science 266: 1821-1828.
21. Johnson, R.E., Prakash, S., and Prakash, L. 1999. Efficient bypass of a thymine-thymine dimer by yeast DNA polymerase, Polη. Science 283: 1001-1004.
22. Johnson, R.E., Washington, M.T., Prakash, S., and Prakash, L. 2000. Fidelity of human DNA polymerase eta. J. Biol. Chem. 275: 7447-7450.
23. Kai, M., Tanaka, H., and Wang, T.S.F. 2001. Fission yeast Rad17 binds to chromatin in response to replication arrest or DNA damage. Mol. Cell. Biol. 21: 3289-3301.
24. Kondo, T., Wakayama, T., Naiki, T., Matsumoto, K., and Sugimoto, K. 2001. Recruitment of Mec1 and Ddc1 checkpoint proteins to double-strand breaks through distinct mechanisms. Science 294: 867-870.
25. Lea, D.E. and Coulson, C.A. 1949. The distribution of the numbers of mutants in bacterial populations. J. Genet. 49: 264-285.
26. Lengauer, C., Kinzler, K.W., and Vogelstein, B. 1998. Genetic instabilities in human cancers. Nature 396: 643-649.
27. Lindsay, H.D., Griffiths, D.J.F., Edwards, R., Murray, J.M., Christensen, P.U., Walworth, N., and Carr, A.M. 1998. S-phase-specific activation of Cds1 kinase defines a subpathway of the checkpoint response in S. pombe. Genes & Dev. 12: 382-395.
28. Liu, V.F., Bhaumik, D., and Wang, T.S.F. 1999. Mutator phenotype induced by aberrant replication. Mol. Cell. Biol. 19: 1126-1135.
29. Lopes, M., Cotta-Ramusino, C., Pellicioli, A., Liberi, G., Plevani, P., Muzi-Falconi, M., Newlon, C.S., and Foiani, M. 2001. The DNA replication checkpoint response stabilizes stalled replication forks. Nature 412: 557-561.
30. Maniatis, T., Fritsch, E.F., and Sambrook, J. 1982. Molecular cloning: A laboratory manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, New York, NY.
31. Masutani, C., Araki, M., Yamada, A., Kusumoto, T., Nogimori, T., Maekawa, T., Iwai, S., and Hanaoka, F. 1999. Xeroderma pigmentosum variant (XP-V) correcting protein from HeLa cells has a thymine dimer bypass DNA polymerase activity. EMBO J. 18: 3491-3501.
32. Matsuda, T., Bebenek, K., Masutani, C., Rogozin, I.B., Hanaoka, F., and Kunkel, T.A. 2001. Error rate and specificity of human and murine DNA polymerase eta. J. Mol. Biol. 312: 335-346.
33. Melo, J. and Toczyski, D. 2002. A unified view of the DNA-damage checkpoint. Curr. Opin. Cell. Biol. 14: 237-245.
34. Melo, J.A., Cohen, J., and Toczyski, D.P. 2001. Two checkpoint complexes are independently recruited to sites of DNA damage in vivo. Genes & Dev. 15: 2809-2821.
35. Michelson, R. and Weinert, T. 1999. Sensor-less checkpoint activation? Na. Cell Biol. 1: 177-178.
36. Moreno, S., Klar, A., and Nurse, P. 1991. Molecular genetic analysis of fission yeast Schizosaccharomyces pombe. Methods Enzymol. 194: 795-823.
37. Nelson, J.R., Lawrence, C.W., and Hinkle, C.D. 1996. Thymine-thymine dimer bypass by yeast DNA polymerase zeta. Science 272: 1646-1649.
38. O'Connell, M.J., Walworth, N.C., and Carr, A.M. 2000. The G2-phase DNA damage checkpoint. Trends Cell Biol. 10: 296-303.
39. Ohashi, E., Bebenek, K., Matsuda, T., Feaver, W.J., Gerlach, V.L., Friedberg, E.C., Ohmori, H., and Kunkel, T.A. 2000a. Fidelity and processivity of DNA synthesis by DNA polymerase κ, the product of the human DINB1 gene. J. Biol. Chem. 275: 39678-39684.
40. Ohashi, E., Ogi, T., Kusumoto, R., Iwai, S., Masutani, C., Hanaoka, F., and Ohmori, H. 2000b. Error-prone bypass of certain DNA lesions by the human DNA polymerase κ. Genes & Dev. 14: 1589-1594.
41. 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., et al. 2001. The Y-family of DNA polymerases. Mol. Cell 8: 7-8.
42. Opperman, T., Murli, S., Smith, B.T., and Walker, G.C. 1999. A model for a umuDC-dependent prokaryotic DNA damage checkpoint. Proc. Natl. Acad. Sci. 96: 9218-9223.
43. Paques, F. and Haber, J.E. 1999. Multiple pathways of recombination induced by double-strand breaks in Saccharomyces cerevisiae. Microbiol. Mol. Biol. Rev. 63: 349-404.
44. Paulovich, A.G., Armour, C.D., and Hartwell, L.H. 1998. The Saccharomyces cerevisiae RAD9, RAD17, RAD24 and MEC3 genes are required for tolerating irreparable, ultraviolet-induced DNA damage. Genetics 150: 75-93.
45. Rhind, N. and Russell, P. 1998. Mitotic DNA damage and replication checkpoints in yeast. Curr. Opin. Cell Biol. 10: 749-758.
46. -. 2000. Chk1 and Cds1: Linchpins of the DNA damage and replication checkpoint pathways. J. Cell Sci. 113: 3889-3896.
47. Sogo, J.M., Lopes, M., and Foiani, M. 2002. Fork reversal and ssDNA accumulation at stalled replication forks owing to checkpoint defects. Science 297: 599-602.
48. Sutton, M.D., Smith, B.T., Godoy, V.G., and Walker, G.C. 2000. The SOS response: Recent insights into umuDC-dependent mutagenesis and DNA damage tolerance. Annu. Rev. Genet. 34: 479-497.
49. Tanaka, K., Yonekawa, Y., Kawasaki, Y., Kai, M., Furuya, K., Iwasaki, M., Murakami, H., Yanagida, M., and Okayama, H. 2000. Fission yeast Eso1p is required for establishing sister chromatid cohesion during S phase. Mol. Cell. Biol. 20: 3459-3469.
50. Tanaka, K., Boddy, M.N., Chen, X.B., McGowan, C.H., and Russell, P. 2001. Threonine-11, phosphorylated by Rad3 and ATM in vitro, is required for activation of fission yeast checkpoint kinase Cds1. Mol. Cell. Biol. 21: 3398-3404.
51. Tercero, J.A. and Diffley, J.F. 2001. Regulation of DNA replication fork progression through damaged DNA by the Mec1/Rad53 checkpoint. Nature 412: 553-557.
52. Venclovas, C. and Thelen, M.P. 2000. Structure-based predictions of Rad1, Rad9, Hus1 and Rad17 participation in sliding clamp and clamp-loading complexes. Nucleic Acids Res. 28: 2481-2493.
53. Wagner, J., Gruz, P., Kim, S.R., Yamada, M., Matsui, K., Fuchs, R.P., and Nohmi, T. 1999. The dinB gene encodes a novel E. coli DNA polymerase, DNA pol IV, involved in mutagenesis. Mol. Cell 4: 281-286.
54. Wang, Z. 2001. Translesion synthesis by the UmuC family of DNA polymerases. Mutat. Res. 486: 59-70.
55. Washington, M.T., Johnson, R.E., Prakash, L., and Prakash, S. 2001. Accuracy of lesion bypass by yeast and human DNA polymerase eta. Proc. Natl. Acad. Sci. 98: 8355-8360.
56. -. 2002. Human DINBI-encoded DNA polymerase κ is a promiscuous extender of mispaired primer termini. Proc. Natl. Acad. Sci. 99: 1910-1914.
57. Woodgate, R. 1999. A plethora of lesion-replicating DNA polymerases. Genes & Dev. 13:2191-2195.
58. Zhou, B.B. and Elledge, S.J. 2000. The DNA damage response: Putting checkpoints in perspective. Nature 408: 433-439.
59. Zou, L., Cortez, D., and Elledge, S.J. 2002. Regulation of ATR substrate selection by Rad17-dependent loading of Rad9 complexes onto chromatin. Genes & Dev. 16: 198-208.