Homologous recombination rescues ssDNA gaps generated by nucleotide excision repair and reduced translesion DNA synthesis in yeast G2 cells

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 31, 2013, Pages

  Ma, Wenjian ^a   Westmoreland, James W ^a   Resnick, Michael A ^a  

^a NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA DIRECTED DNA POLYMERASE ETA; PYRIMIDINE DIMER; RAD51 PROTEIN; RAD52 PROTEIN; SINGLE STRANDED DNA; THALLIUM;

ARTICLE; CELL CYCLE G2 PHASE; CELL SURVIVAL; CHROMOSOMAL INSTABILITY; CONTROLLED STUDY; DNA SYNTHESIS; EXCISION REPAIR; FUNGAL GENOME; HAPLOIDY; HOMOLOGOUS RECOMBINATION; IONIZING RADIATION; NONHUMAN; PRIORITY JOURNAL; RECOMBINATION REPAIR; SACCHAROMYCES CEREVISIAE; SISTER CHROMATID; ULTRAVIOLET IRRADIATION; ULTRAVIOLET RADIATION;

DNA BREAKS, SINGLE-STRANDED; DNA REPAIR; DNA, FUNGAL; DNA, SINGLE-STRANDED; G2 PHASE; HUMANS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; ULTRAVIOLET RAYS;

EID: 84881086190     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1301676110     Document Type: Article

References (55)

1. Kuper J, Kisker C (2012) Damage recognition in nucleotide excision DNA repair. Curr Opin Struct Biol 22(1):88-93.
2. Nouspikel T (2009) DNA repair in mammalian cells: Nucleotide excision repair: Variations on versatility. Cell Mol Life Sci 66(6):994-1009.
3. Hanawalt PC (2002) Subpathways of nucleotide excision repair and their regulation. Oncogene 21(58):8949-8956.
4. Mocquet V, et al. (2008) Sequential recruitment of the repair factors during NER: The role of XPG in initiating the resynthesis step. EMBO J 27(1):155-167.
5. Muniandy PA, Liu J, Majumdar A, Liu ST, Seidman MM (2010) DNA interstrand crosslink repair in mammalian cells: Step by step. Crit Rev Biochem Mol Biol 45(1): 23-49.
6. Moriel-Carretero M, Aguilera A (2010) Replication fork breakage and re-start: New insights into Rad3/XPD-associated deficiencies. Cell Cycle 9(15):2958-2962.
7. Eppink B, et al. (2011) The response of mammalian cells to UV-light reveals Rad54-dependent and independent pathways of homologous recombination. DNA Repair (Amst) 10(11):1095-1105.
8. Ma W, et al. (2009) The transition of closely opposed lesions to double-strand breaks during long-patch base excision repair is prevented by the coordinated action of DNA polymerase delta and Rad27/Fen1. Mol Cell Biol 29(5):1212-1221.
9. Ma W, Westmoreland JW, Gordenin DA, Resnick MA (2011) Alkylation base damage is converted into repairable double-strand breaks and complex intermediates in G2 cells lacking AP endonuclease. PLoS Genet 7(4):e1002059.
10. Malyarchuk S, Castore R, Harrison L (2008) DNA repair of clustered lesions in mammalian cells: Involvement of non-homologous end-joining. Nucleic Acids Res 36(15):4872-4882.
11. Staresincic L, et al. (2009) Coordination of dual incision and repair synthesis in human nucleotide excision repair. EMBO J 28(8):1111-1120.
12. Luijsterburg MS, et al. (2010) Stochastic and reversible assembly of a multiprotein DNA repair complex ensures accurate target site recognition and efficient repair. J Cell Biol 189(3):445-463.
13. Sertic S, Pizzi S, Lazzaro F, Plevani P, Muzi-Falconi M (2012) NER and DDR: Classical music with new instruments. Cell Cycle 11(4):668-674.
14. Giannattasio M, et al. (2010) Exo1 competes with repair synthesis, converts NER intermediates to long ssDNA gaps, and promotes checkpoint activation. Mol Cell 40(1):50-62.
15. Yang W, Woodgate R (2007) What a difference a decade makes: Insights into translesion DNA synthesis. Proc Natl Acad Sci USA 104(40):15591-15598.
16. Prakash S, Johnson RE, Prakash L (2005) Eukaryotic translesion synthesis DNA polymerases: Specificity of structure and function. Annu Rev Biochem 74:317-353.
17. Beljanski V, Marzilli LG, Doetsch PW (2004) DNA damage-processing pathways involved in the eukaryotic cellular response to anticancer DNA cross-linking drugs. Mol Pharmacol 65(6):1496-1506.
18. Westmoreland J, et al. (2009) RAD50 is required for efficient initiation of resection and recombinational repair at random, gamma-induced double-strand break ends. PLoS Genet 5(9):e1000656.
19. Douki T, Cadet J (1992) Far-UV photochemistry and photosensitization of 2′-deoxycytidylyl-(3′-5′)-thymidine: Isolation and characterization of the main photoproducts. J Photochem Photobiol B 15(3):199-213.
20. Tornaletti S, Pfeifer GP (1994) Slow repair of pyrimidine dimers at p53 mutation hotspots in skin cancer. Science 263(5152):1436-1438.
21. McCulloch SD, et al. (2004) Preferential cis-syn thymine dimer bypass by DNA polymerase eta occurs with biased fidelity. Nature 428(6978):97-100.
22. Livneh Z, Ziv O, Shachar S (2010) Multiple two-polymerase mechanisms in mammalian translesion DNA synthesis. Cell Cycle 9(4):729-735.
23. Ma W, Resnick MA, Gordenin DA (2008) Apn1 and Apn2 endonucleases prevent accumulation of repair-associated DNA breaks in budding yeast as revealed by direct chromosomal analysis. Nucleic Acids Res 36(6):1836-1846.
24. McDonald JP, Levine AS, Woodgate R (1997) 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(4): 1557-1568.
25. Resnick MA, Setlow JK (1972) Repair of pyrimidine dimer damage induced in yeast by ultraviolet light. J Bacteriol 109(3):979-986.
26. Chaudhry MA, Weinfeld M (1995) Induction of double-strand breaks by S1 nuclease, mung bean nuclease and nuclease P1 in DNA containing abasic sites and nicks. Nucleic Acids Res 23(19):3805-3809.
27. Geigl EM, Eckardt-Schupp F (1991) Repair of gamma ray-induced S1 nuclease hypersensitive sites in yeast depends on homologous mitotic recombination and a RAD18-dependent function. Curr Genet 20(1-2):33-37.
28. Westmoreland JW, Resnick MA (2013) Coincident resection at both ends of random, γ-induced double-strand breaks requires MRX (MRN), Sae2 (Ctp1), and Mre11-nuclease. PLoS Genet 9(3):e1003420.
29. Bardwell AJ, Bardwell L, Tomkinson AE, Friedberg EC (1994) Specific cleavage of model recombination and repair intermediates by the yeast Rad1-Rad10 DNA endonuclease. Science 265(5181):2082-2085.
30. Guzder SN, Sommers CH, Prakash L, Prakash S (2006) Complex formation with damage recognition protein Rad14 is essential for Saccharomyces cerevisiae Rad1-Rad10 nuclease to perform its function in nucleotide excision repair in vivo. Mol Cell Biol 26(3):1135-1141.
31. Habraken Y, Sung P, Prakash L, Prakash S (1993) Yeast excision repair gene RAD2 encodes a single-stranded DNA endonuclease. Nature 366(6453):365-368.
32. Reynolds RJ (1987) Induction and repair of closely opposed pyrimidine dimers in Saccharomyces cerevisiae. Mutat Res 184(3):197-207.
33. St Charles J, et al. (2012) High-resolution genome-wide analysis of irradiated (UV and γ-rays) diploid yeast cells reveals a high frequency of genomic loss of heterozygosity (LOH) events. Genetics 190(4):1267-1284.
34. Haber JE (2008) Evolution of models of homologous recombination. Recombination and Meiosis, Genome Dynamics and Stability, ed Egel R, Lankenau D-H (Springer, Berlin), pp 1-64.
35. Wittschieben JP, Reshmi SC, Gollin SM, Wood RD (2006) Loss of DNA polymerase zeta causes chromosomal instability in mammalian cells. Cancer Res 66(1):134-142.
36. Sonoda E, et al. (2003) Multiple roles of Rev3, the catalytic subunit of polzeta in maintaining genome stability in vertebrates. EMBO J 22(12):3188-3197.
37. Sharma S, et al. (2012) REV1 and polymerase ξ facilitate homologous recombination repair. Nucleic Acids Res 40(2):682-691.
38. Yang Y, Sterling J, Storici F, Resnick MA, Gordenin DA (2008) Hypermutability of damaged single-strand DNA formed at double-strand breaks and uncapped telomeres in yeast Saccharomyces cerevisiae. PLoS Genet 4(11):e1000264.
39. Van Houten B, Eisen JA, Hanawalt PC (2002) A cut above: Discovery of an alternative excision repair pathway in bacteria. Proc Natl Acad Sci USA 99(5): 2581-2583.
40. Ogi T, et al. (2010) Three DNA polymerases, recruited by different mechanisms, carry out NER repair synthesis in human cells. Mol Cell 37(5):714-727.
41. Ogi T, Lehmann AR (2006) The Y-family DNA polymerase kappa (pol kappa) functions in mammalian nucleotide-excision repair. Nat Cell Biol 8(6):640-642.
42. Hanawalt PC, Cooper PK, Ganesan AK, Smith CA (1979) DNA repair in bacteria and mammalian cells. Annu Rev Biochem 48:783-836.
43. Grossman L, Braun A, Feldberg R, Mahler I (1975) Enzymatic repair of DNA. Annu Rev Biochem 44:19-43.
44. Masker W, Hanawalt P, Shizuya H (1973) Role of DNA polymerase II in repair replication in Escherichia coli. Nat New Biol 244(138):242-243.
45. Tourrière H, Pasero P (2007) Maintenance of fork integrity at damaged DNA and natural pause sites. DNA Repair (Amst) 6(7):900-913.
46. Ward JD, Barber LJ, Petalcorin MI, Yanowitz J, Boulton SJ (2007) Replication blocking lesions present a unique substrate for homologous recombination. EMBO J 26(14): 3384-3396.
47. Adar S, Izhar L, Hendel A, Geacintov N, Livneh Z (2009) Repair of gaps opposite lesions by homologous recombination in mammalian cells. Nucleic Acids Res 37(17):5737-5748.
48. Kaykov A, Arcangioli B (2004) A programmed strand-specific and modified nick in S. pombe constitutes a novel type of chromosomal imprint. Curr Biol 14(21):1924-1928.
49. Lee GS, Neiditch MB, Salus SS, Roth DB (2004) RAG proteins shepherd double-strand breaks to a specific pathway, suppressing error-prone repair, but RAG nicking initiates homologous recombination. Cell 117(2):171-184.
50. Metzger MJ, McConnell-Smith A, Stoddard BL, Miller AD (2011) Single-strand nicks induce homologous recombination with less toxicity than double-strand breaks using an AAV vector template. Nucleic Acids Res 39(3):926-935.
51. van Nierop GP, de Vries AA, Holkers M, Vrijsen KR, Gonçalves MA (2009) Stimulation of homology-directed gene targeting at an endogenous human locus by a nicking endonuclease. Nucleic Acids Res 37(17):5725-5736.
52. Tran PT, Erdeniz N, Symington LS, Liskay RM (2004) EXO1-A multi-tasking eukaryotic nuclease. DNA Repair (Amst) 3(12):1549-1559.
53. Karras GI, Jentsch S (2010) The RAD6 DNA damage tolerance pathway operates uncoupled from the replication fork and is functional beyond S phase. Cell 141(2):255-267.
54. Covo S, Westmoreland JW, Gordenin DA, Resnick MA (2010) Cohesin Is limiting for the suppression of DNA damage-induced recombination between homologous chromosomes. PLoS Genet 6(7):e1001006.
55. Wach A (1996) PCR-synthesis of marker cassettes with long flanking homology regions for gene disruptions in S. cerevisiae. Yeast 12(3):259-265.