Pol32 is required for Polζ-dependent translesion synthesis and prevents double-strand breaks at the replication fork

Mutation Research - Fundamental and Molecular Mechanisms of Mutagenesis

Volumn 625, Issue 1-2, 2007, Pages 164-176

  Hanna, Michelle ^a   Ball, Lindsay G ^a   Tong, Amy H ^b   Boone, Charles ^b   Xiao, Wei ^a  

^a UNIVERSITY OF SASKATCHEWAN   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

Author keywords

Checkpoint; Double strand break; Recombination repair; Replication; Translesion synthesis

Indexed keywords

DNA POLYMERASE; DNA POLYMERASE DELTA SUBUNIT 3; DOUBLE STRANDED DNA; POL32 PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CELL CYCLE; CELL GROWTH; CELL SURVIVAL; DNA REPAIR; DNA REPLICATION; GENETIC ANALYSIS; GENOMIC INSTABILITY; HOMOLOGOUS RECOMBINATION; NONHUMAN; PRIORITY JOURNAL;

DNA BREAKS, DOUBLE-STRANDED; DNA HELICASES; DNA REPAIR; DNA REPLICATION; DNA, FUNGAL; DNA-DIRECTED DNA POLYMERASE; GENES, FUNGAL; MODELS, BIOLOGICAL; MUTAGENESIS; MUTATION; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; ULTRAVIOLET RAYS;

EID: 35549010590     PISSN: 00275107     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mrfmmm.2007.06.008     Document Type: Article

References (69)

1. Weinert T.A., and Hartwell L.H. The RAD9 gene controls the cell cycle response to DNA damage in Saccharomyces cerevisiae. Science 241 (1988) 317-322
2. Zhou B.B., and Elledge S.J. The DNA damage response: putting checkpoints in perspective. Nature 408 (2000) 433-439
3. Barbour L., and Xiao W. Regulation of alternative replication bypass pathways at stalled replication forks and its effects on genome stability: a yeast model. Mutat. Res. 532 (2003) 137-155
4. Cotta-Ramusino C., Fachinetti D., Lucca C., Doksani Y., Lopes M., Sogo J., and Foiani M. Exo1 processes stalled replication forks and counteracts fork reversal in checkpoint-defective cells. Mol. Cell 17 (2005) 153-159
5. Liberi G., Maffioletti G., Lucca C., Chiolo I., Baryshnikova A., Cotta-Ramusino C., Lopes M., Pellicioli A., Haber J.E., and Foiani M. Rad51-dependent DNA structures accumulate at damaged replication forks in sgs1 mutants defective in the yeast ortholog of BLM RecQ helicase. Genes Dev. 19 (2005) 339-350
6. Ira G., Malkova A., Liberi G., Foiani M., and Haber J.E. Srs2 and Sgs1-Top3 suppress crossovers during double-strand break repair in yeast. Cell 115 (2003) 401-411
7. Prakash L. Characterization of postreplication repair in Saccharomyces cerevisiae and effects of rad6, rad18, rev3 and rad52 mutations. Mol. Gen. Genet. 184 (1981) 471-478
8. di Caprio L., and Cox B.S. DNA synthesis in UV-irradiated yeast. Mutat. Res. 82 (1981) 69-85
9. Jentsch S., McGrath J.P., and Varshavsky A. The yeast DNA repair gene RAD6 encodes a ubiquitin-conjugating enzyme. Nature 329 (1987) 131-134
10. Bailly V., Lamb J., Sung P., Prakash S., and Prakash L. Specific complex formation between yeast RAD6 and RAD18 proteins: a potential mechanism for targeting RAD6 ubiquitin-conjugating activity to DNA damage sites. Genes Dev. 8 (1994) 811-820
11. Hoege C., Pfander B., Moldovan G.L., Pyrowolakis G., and Jentsch S. RAD6-dependent DNA repair is linked to modification of PCNA by ubiquitin and SUMO. Nature 419 (2002) 135-141
12. Xiao W., Chow B.L., Broomfield S., and Hanna M. The Saccharomyces cerevisiae RAD6 group is composed of an error-prone and two error-free postreplication repair pathways. Genetics 155 (2000) 1633-1641
13. Nelson J.R., Lawrence C.W., and Hinkle D.C. Thymine-thymine dimer bypass by yeast DNA polymerase ζ. Science 272 (1996) 1646-1649
14. Nelson J.R., Lawrence C.W., and Hinkle D.C. Deoxycytidyl transferase activity of yeast REV1 protein. Nature 382 (1996) 729-731
15. Johnson R.E., Henderson S.T., Petes T.D., Prakash S., Bankmann M., and Prakash L. Saccharomyces cerevisiae RAD5-encoded DNA repair protein contains DNA helicase and zinc-binding sequence motifs and affects the stability of simple repetitive sequences in the genome. Mol. Cell Biol. 12 (1992) 3807-3818
16. Broomfield S., Chow B.L., and Xiao W. MMS2, encoding a ubiquitin-conjugating-enzyme-like protein, is a member of the yeast error-free postreplication repair pathway. Proc. Natl. Acad. Sci. U.S.A. 95 (1998) 5678-5683
17. Brusky J., Zhu Y., and Xiao W. UBC13, a DNA-damage-inducible gene, is a member of the error-free postreplication repair pathway in Saccharomyces cerevisiae. Curr. Genet. 37 (2000) 168-174
18. Hofmann R.M., and Pickart C.M. Noncanonical MMS2-encoded ubiquitin-conjugating enzyme functions in assembly of novel polyubiquitin chains for DNA repair. Cell 96 (1999) 645-653
19. Broomfield S., Hryciw T., and Xiao W. DNA postreplication repair and mutagenesis in Saccharomyces cerevisiae. Mutat. Res. 486 (2001) 167-184
20. Ulrich H.D., and Jentsch S. Two RING finger proteins mediate cooperation between ubiquitin-conjugating enzymes in DNA repair. EMBO J. 19 (2000) 3388-3397
21. Stelter P., and Ulrich H.D. Control of spontaneous and damage-induced mutagenesis by SUMO and ubiquitin conjugation. Nature 425 (2003) 188-191
22. Pfander B., Moldovan G.L., Sacher M., Hoege C., and Jentsch S. SUMO-modified PCNA recruits Srs2 to prevent recombination during S phase. Nature 436 (2005) 428-433
23. Papouli E., Chen S., Davies A.A., Huttner D., Krejci L., Sung P., and Ulrich H.D. Crosstalk between SUMO and ubiquitin on PCNA is mediated by recruitment of the helicase Srs2p. Mol. Cell 19 (2005) 123-133
24. Pastushok L., and Xiao W. DNA postreplication repair modulated by ubiquitination and sumoylation. Adv. Protein Chem. 69 (2004) 279-306
25. Giot L., Chanet R., Simon M., Facca C., and Faye G. Involvement of the yeast DNA polymerase δ in DNA repair in vivo. Genetics 146 (1997) 1239-1251
26. Torres-Ramos C.A., Prakash S., and Prakash L. Requirement of yeast DNA polymerase δ in post-replicational repair of UV-damaged DNA. J. Biol. Chem. 272 (1997) 25445-25448
27. Boulet A., Simon M., Faye G., Bauer G.A., and Burgers P.M. Structure and function of the Saccharomyces cerevisiae CDC2 gene encoding the large subunit of DNA polymerase III. EMBO J. 8 (1989) 1849-1854
28. Sugimoto K., Sakamoto Y., Takahashi O., and Matsumoto K. HYS2, an essential gene required for DNA replication in Saccharomyces cerevisiae. Nucleic Acids Res. 23 (1995) 3493-3500
29. Gerik K.J., Li X., Pautz A., and Burgers P.M. Characterization of the two small subunits of Saccharomyces cerevisiae DNA polymerase δ. J. Biol. Chem. 273 (1998) 19747-19755
30. Huang M.E., Le Douarin B., Henry C., and Galibert F. The Saccharomyces cerevisiae protein YJR043C (Pol32) interacts with the catalytic subunit of DNA polymerase α and is required for cell cycle progression in G2/M. Mol. Gen. Genet. 260 (1999) 541-550
31. Huang M.E., Cadieu E., Souciet J.L., and Galibert F. Disruption of six novel yeast genes reveals three genes essential for vegetative growth and one required for growth at low temperature. Yeast 13 (1997) 1181-1194
32. Sherman F., Fink G., and Hicks J. Methods in Yeast Genetics (1983), Cold Spring Harbor Laboratory, Cold Spring Harbor, New York
33. Ito H., Fukuda Y., Murata K., and Kimura A. Transformation of intact yeast cells treated with alkali cations. J. Bacteriol. 153 (1983) 163-168
34. Rothstein R.J. One-step gene disruption in yeast. Methods Enzymol. 101 (1983) 202-211
35. Saxe D., Datta A., and Jinks-Robertson S. Stimulation of mitotic recombination events by high levels of RNA polymerase II transcription in yeast. Mol. Cell Biol. 20 (2000) 5404-5414
36. Roche H., Gietz R.D., and Kunz B.A. Specificity of the yeast rev3Δ antimutator and REV3 dependency of the mutator resulting from a defect (rad1Δ) in nucleotide excision repair. Genetics 137 (1994) 637-646
37. McDonald J.P., Levine A.S., and Woodgate R. The Saccharomyces cerevisiae RAD30 gene, a homologue of Escherichia coli dinB and umuC, is DNA damage inducible and functions in a novel error-free postreplication repair mechanism. Genetics 147 (1997) 1557-1568
38. Xiao W., Chow B.L., Fontanie T., Ma L., Bacchetti S., Hryciw T., and Broomfield S. Genetic interactions between error-prone and error-free postreplication repair pathways in Saccharomyces cerevisiae. Mutat. Res. 435 (1999) 1-11
39. Berben G., Dumont J., Gilliquet V., Bolle P.A., and Hilger F. The YDp plasmids: a uniform set of vectors bearing versatile gene disruption cassettes for Saccharomyces cerevisiae. Yeast 7 (1991) 475-477
40. Alani E., Cao L., and Kleckner N. A method for gene disruption that allows repeated use of URA3 selection in the construction of multiply disrupted yeast strains. Genetics 116 (1987) 541-545
41. Tishkoff D.X., Filosi N., Gaida G.M., and Kolodner R.D. A novel mutation avoidance mechanism dependent on S. cerevisiae RAD27 is distinct from DNA mismatch repair. Cell 88 (1997) 253-263
42. Swanson R.L., Morey N.J., Doetsch P.W., and Jinks-Robertson S. Overlapping specificities of base excision repair, nucleotide excision repair, recombination, and translesion synthesis pathways for DNA base damage in Saccharomyces cerevisiae. Mol. Cell Biol. 19 (1999) 2929-2935
43. Williamson M.S., Game J.C., and Fogel S. Meiotic gene conversion mutants in Saccharomyces cerevisiae. I. Isolation and characterization of pms1-1 and pms1-2. Genetics 110 (1985) 609-646
44. Tong A.H., Evangelista M., Parsons A.B., Xu H., Bader G.D., Page N., Robinson M., Raghibizadeh S., Hogue C.W., Bussey H., Andrews B., Tyers M., and Boone C. Systematic genetic analysis with ordered arrays of yeast deletion mutants. Science 294 (2001) 2364-2368
45. Tong A.H.Y., and Boone C. Synthetic genetic array analysis in Saccharomyces cerevisiae. In: Xiao W. (Ed). Yeast Protocols. second ed. (2006), Humana Press Inc., Totowa, NJ, USA 171-191
46. Torres-Ramos C.A., Yoder B.L., Burgers P.M., Prakash S., and Prakash L. Requirement of proliferating cell nuclear antigen in RAD6-dependent postreplicational DNA repair. Proc. Natl. Acad. Sci. U.S.A. 93 (1996) 9676-9681
47. Huang M.E., de Calignon A., Nicolas A., and Galibert F. POL32, a subunit of the Saccharomyces cerevisiae DNA polymerase δ, defines a link between DNA replication and the mutagenic bypass repair pathway. Curr. Genet. 38 (2000) 178-187
48. Johnson R.E., Prakash S., and Prakash L. Efficient bypass of a thymine-thymine dimer by yeast DNA polymerase, Polη. Science 283 (1999) 1001-1004
49. Roush A.A., Suarez M., Friedberg E.C., Radman M., and Siede W. Deletion of the Saccharomyces cerevisiae gene RAD30 encoding an Escherichia coli DinB homolog confers UV radiation sensitivity and altered mutability. Mol. Gen. Genet. 257 (1998) 686-692
50. Lemontt J.F. Pathways of ultraviolet mutability in Saccharomyces cerevisiae. II. The effect of rev genes on recombination. Mutat. Res. 13 (1971) 319-326
51. Lemontt J.F. Mutants of yeast defective in mutation by ultraviolet light. Genetics 68 (1971) 21-33
52. Lawrence C.W. Cellular functions of DNA polymerase ζ and Rev1 protein. Adv. Protein Chem. 69 (2004) 167-203
53. Minesinger B.K., and Jinks-Robertson S. Roles of RAD6 epistasis group members in spontaneous polζ-dependent translesion synthesis in Saccharomyces cerevisiae. Genetics 169 (2005) 1939-1955
54. Lawrence C.W., and Christensen R.B. Metabolic suppressors of trimethoprim and ultraviolet light sensitivities of Saccharomyces cerevisiae rad6 mutants. J. Bacteriol. 139 (1979) 866-876
55. Aboussekhra A., Chanet R., Zgaga Z., Cassier-Chauvat C., Heude M., and Fabre F. RADH, a gene of Saccharomyces cerevisiae encoding a putative DNA helicase involved in DNA repair. Characteristics of radH mutants and sequence of the gene. Nucleic Acids Res. 17 (1989) 7211-7219
56. Tong A.H., Lesage G., Bader G.D., Ding H., Xu H., Xin X., Young J., Berriz G.F., Brost R.L., Chang M., Chen Y., Cheng X., Chua G., Friesen H., Goldberg D.S., Haynes J., Humphries C., He G., Hussein S., Ke L., Krogan N., Li Z., Levinson J.N., Lu H., Menard P., Munyana C., Parsons A.B., Ryan O., Tonikian R., Roberts T., Sdicu A.M., Shapiro J., Sheikh B., Suter B., Wong S.L., Zhang L.V., Zhu H., Burd C.G., Munro S., Sander C., Rine J., Greenblatt J., Peter M., Bretscher A., Bell G., Roth F.P., Brown G.W., Andrews B., Bussey H., and Boone C. Global mapping of the yeast genetic interaction network. Science 303 (2004) 808-813
57. Kim R.A., and Wang J.C. Identification of the yeast TOP3 gene product as a single strand-specific DNA topoisomerase. J. Biol. Chem. 267 (1992) 17178-17185
58. Gangloff S., McDonald J.P., Bendixen C., Arthur L., and Rothstein R. The yeast type I topoisomerase Top3 interacts with Sgs1, a DNA helicase homolog: a potential eukaryotic reverse gyrase. Mol. Cell Biol. 14 (1994) 8391-8398
59. Mohaghegh P., and Hickson I.D. DNA helicase deficiencies associated with cancer predisposition and premature ageing disorders. Hum. Mol. Genet. 10 (2001) 741-746
60. Burgers P.M., and Gerik K.J. Structure and processivity of two forms of Saccharomyces cerevisiae DNA polymerase δ. J. Biol. Chem. 273 (1998) 19756-19762
61. Gibbs P.E., McDonald J., Woodgate R., and Lawrence C.W. The relative roles in vivo of Saccharomyces cerevisiae Poλη, Pol ζ, Rev1 protein and Pol32 in the bypass and mutation induction of an abasic site, T-T (6-4) photoadduct and T-T cis-syn cyclobutane dimer. Genetics 169 (2005) 575-582
62. Johansson E., Garg P., and Burgers P.M. The Pol32 subunit of DNA polymerase δ contains separable domains for processive replication and proliferating cell nuclear antigen (PCNA) binding. J. Biol. Chem. 279 (2004) 1907-1915
63. Huang M.E., Rio A.G., Galibert M.D., and Galibert F. Pol32, a subunit of Saccharomyces cerevisiae DNA polymerase δ, suppresses genomic deletions and is involved in the mutagenic bypass pathway. Genetics 160 (2002) 1409-1422
64. D'Amours D., and Jackson S.P. The Mre11 complex: at the crossroads of DNA repair and checkpoint signalling. Nat. Rev. Mol. Cell Biol. 3 (2002) 317-327
65. Katou Y., Kanoh Y., Bando M., Noguchi H., Tanaka H., Ashikari T., Sugimoto K., and Shirahige K. S-phase checkpoint proteins Tof1 and Mrc1 form a stable replication-pausing complex. Nature 424 (2003) 1078-1083
66. Cobb J.A., Bjergbaek L., Shimada K., Frei C., and Gasser S.M. DNA polymerase stabilization at stalled replication forks requires Mec1 and the RecQ helicase Sgs1. EMBO J. 22 (2003) 4325-4336
67. Krejci L., Van Komen S., Li Y., Villemain J., Reddy M.S., Klein H., Ellenberger T., and Sung P. DNA helicase Srs2 disrupts the Rad51 presynaptic filament. Nature 423 (2003) 305-309
68. Veaute X., Jeusset J., Soustelle C., Kowalczykowski S.C., Le Cam E., and Fabre F. The Srs2 helicase prevents recombination by disrupting Rad51 nucleoprotein filaments. Nature 423 (2003) 309-312
69. Naiki T., Wakayama T., Nakada D., Matsumoto K., and Sugimoto K. Association of Rad9 with double-strand breaks through a Mec1-dependent mechanism. Mol. Cell Biol. 24 (2004) 3277-3285