Components of a Fanconi-Like Pathway Control Pso2-Independent DNA Interstrand Crosslink Repair in Yeast

PLoS Genetics

Volumn 8, Issue 8, 2012, Pages

  Ward, Thomas A ^a   Dudášová, Zuzana ^b   Sarkar, Sovan ^a   Bhide, Mangesh R ^c   Vlasáková, Danuša ^b   Chovanec, Miroslav ^b   McHugh, Peter J ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b CANCER RESEARCH INSTITUTE   (Slovakia)

^c UNIVERSITY OF VETERINARY MEDICINE   (Slovakia)

Author keywords

[No Author keywords available]

Indexed keywords

DOUBLE STRANDED DNA; EXODEOXYRIBONUCLEASE I; EXONUCLEASE; FANCONI ANEMIA PROTEIN; FUNGAL PROTEIN; INTERMEDIN; MICROORGANISM PROTEIN; MITOCHONDRIAL DNA; MITOCHONDRIAL GENOME MAINTENANCE FACTOR101; PROTEIN MSH2; PROTEIN MSH6; PROTEIN MUTS APHA; PROTEIN PSO2; RAD51 PROTEIN; UNCLASSIFIED DRUG;

3' UNTRANSLATED REGION; 5' UNTRANSLATED REGION; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL FRACTIONATION; CHROMATIN; CHROMOSOME REARRANGEMENT; CONTROLLED STUDY; DNA CROSS LINKING; DNA DAMAGE; DNA REPAIR; HOMOLOGOUS RECOMBINATION; LIQUID CHROMATOGRAPHY; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; NONHUMAN; PROTEIN CLEAVAGE; PROTEIN DETERMINATION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; YEAST;

CHROMOSOMAL PROTEINS, NON-HISTONE; DEAD-BOX RNA HELICASES; DNA BREAKS, DOUBLE-STRANDED; DNA REPAIR; DNA-BINDING PROTEINS; ENDODEOXYRIBONUCLEASES; EXODEOXYRIBONUCLEASES; FANCONI ANEMIA; HUMANS; MITOCHONDRIAL PROTEINS; MODELS, BIOLOGICAL; MUTS HOMOLOG 2 PROTEIN; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SIGNAL TRANSDUCTION;

SACCHAROMYCETALES;

EID: 84866156212     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1002884     Document Type: Article

References (87)

1. McHugh PJ, Spanswick VJ, Hartley JA, (2001) Repair of DNA interstrand crosslinks: molecular mechanisms and clinical relevance. Lancet Oncol 2: 483-490.
2. Dronkert ML, Kanaar R, (2001) Repair of DNA interstrand cross-links. Mutat Res 486: 217-247.
3. Lehoczky P, McHugh PJ, Chovanec M, (2007) DNA interstrand cross-link repair in Saccharomyces cerevisiae. FEMS Microbiol Rev 31: 109-133.
4. Ruhland A, Brendel M, (1979) Mutagenesis by cytostatic alkylating agents in yeast strains of differing repair capacities. Genetics 92: 83-97.
5. Miller RD, Prakash L, Prakash S, (1982) Genetic control of excision of Saccharomyces cerevisiae interstrand DNA cross-links induced by psoralen plus near-UV light. Mol Cell Biol 2: 939-948.
6. McHugh PJ, Sones WR, Hartley JA, (2000) Repair of intermediate structures produced at DNA interstrand cross-links in Saccharomyces cerevisiae. Mol Cell Biol 20: 3425-3433.
7. Jachymczyk WJ, von Borstel RC, Mowat MR, Hastings PJ, (1981) Repair of interstrand cross-links in DNA of Saccharomyces cerevisiae requires two systems for DNA repair: the RAD3 system and the RAD51 system. Mol Gen Genet 182: 196-205.
8. Zheng H, Wang X, Warren AJ, Legerski RJ, Nairn RS, et al. (2003) Nucleotide excision repair- and polymerase eta-mediated error-prone removal of mitomycin C interstrand cross-links. Mol Cell Biol 23: 754-761.
9. Niedernhofer LJ, Odijk H, Budzowska M, van Drunen E, Maas A, et al. (2004) The structure-specific endonuclease Ercc1-Xpf is required to resolve DNA interstrand cross-link-induced double-strand breaks. Mol Cell Biol 24: 5776-5787.
10. Sarkar S, Davies AA, Ulrich HD, McHugh PJ, (2006) DNA interstrand crosslink repair during G1 involves nucleotide excision repair and DNA polymerase zeta. Embo J 25: 1285-1294.
11. Raschle M, Knipscheer P, Enoiu M, Angelov T, Sun J, et al. (2008) Mechanism of replication-coupled DNA interstrand crosslink repair. Cell 134: 969-980.
12. Niedzwiedz W, Mosedale G, Johnson M, Ong CY, Pace P, et al. (2004) The Fanconi anaemia gene FANCC promotes homologous recombination and error-prone DNA repair. Mol Cell 15: 607-620.
13. Knipscheer P, Raschle M, Smogorzewska A, Enoiu M, Ho TV, et al. (2009) The Fanconi anemia pathway promotes replication-dependent DNA interstrand cross-link repair. Science 326: 1698-1701.
14. Long DT, Raschle M, Joukov V, Walter JC, (2011) Mechanism of RAD51-dependent DNA interstrand cross-link repair. Science 333: 84-87.
15. Joenje H, Patel KJ, (2001) The emerging genetic and molecular basis of Fanconi anaemia. Nat Rev Genet 2: 446-457.
16. Meetei AR, Medhurst AL, Ling C, Xue Y, Singh TR, et al. (2005) A human ortholog of archaeal DNA repair protein Hef is defective in Fanconi anemia complementation group M. Nat Genet 37: 958-963.
17. Mosedale G, Niedzwiedz W, Alpi A, Perrina F, Pereira-Leal JB, et al. (2005) The vertebrate Hef ortholog is a component of the Fanconi anemia tumor-suppressor pathway. Nat Struct Mol Biol 12: 763-771.
18. Entian KD, Schuster T, Hegemann JH, Becher D, Feldmann H, et al. (1999) Functional analysis of 150 deletion mutants in Saccharomyces cerevisiae by a systematic approach. Mol Gen Genet 262: 683-702.
19. Scheller J, Schurer A, Rudolph C, Hettwer S, Kramer W, (2000) MPH1, a yeast gene encoding a DEAH protein, plays a role in protection of the genome from spontaneous and chemically induced damage. Genetics 155: 1069-1081.
20. Schurer KA, Rudolph C, Ulrich HD, Kramer W, (2004) Yeast MPH1 gene functions in an error-free DNA damage bypass pathway that requires genes from Homologous recombination, but not from postreplicative repair. Genetics 166: 1673-1686.
21. Sun W, Nandi S, Osman F, Ahn JS, Jakovleska J, et al. (2008) The FANCM ortholog Fml1 promotes recombination at stalled replication forks and limits crossing over during DNA double-strand break repair. Mol Cell 32: 118-128.
22. Banerjee S, Smith S, Oum JH, Liaw HJ, Hwang JY, et al. (2008) Mph1p promotes gross chromosomal rearrangement through partial inhibition of homologous recombination. J Cell Biol 181: 1083-1093.
23. Prakash R, Satory D, Dray E, Papusha A, Scheller J, et al. (2009) Yeast Mph1 helicase dissociates Rad51-made D-loops: implications for crossover control in mitotic recombination. Genes Dev 23: 67-79.
24. Prakash R, Krejci L, Van Komen S, Anke Schurer K, Kramer W, et al. (2005) Saccharomyces cerevisiae MPH1 gene, required for homologous recombination-mediated mutation avoidance, encodes a 3′ to 5′ DNA helicase. J Biol Chem 280: 7854-7860.
25. Gari K, Decaillet C, Stasiak AZ, Stasiak A, Constantinou A, (2008) The Fanconi anemia protein FANCM can promote branch migration of Holliday junctions and replication forks. Mol Cell 29: 141-148.
26. Xue Y, Li Y, Guo R, Ling C, Wang W, (2008) FANCM of the Fanconi anemia core complex is required for both monoubiquitination and DNA repair. Hum Mol Genet.
27. Rosado IV, Niedzwiedz W, Alpi AF, Patel KJ, (2009) The Walker B motif in avian FANCM is required to limit sister chromatid exchanges but is dispensable for DNA crosslink repair. Nucleic Acids Res 37: 4360-4370.
28. Schwab RA, Blackford AN, Niedzwiedz W, (2010) ATR activation and replication fork restart are defective in FANCM-deficient cells. Embo J 29: 806-818.
29. Collis SJ, Ciccia A, Deans AJ, Horejsi Z, Martin JS, et al. (2008) FANCM and FAAP24 function in ATR-mediated checkpoint signaling independently of the Fanconi anemia core complex. Mol Cell 32: 313-324.
30. Luke-Glaser S, Luke B, Grossi S, Constantinou A, (2010) FANCM regulates DNA chain elongation and is stabilized by S-phase checkpoint signalling. Embo J 29: 795-805.
31. Henriques JA, Moustacchi E, (1980) Isolation and characterization of pso mutants sensitive to photo-addition of psoralen derivatives in Saccharomyces cerevisiae. Genetics 95: 273-288.
32. Ruhland A, Haase E, Siede W, Brendel M, (1981) Isolation of yeast mutants sensitive to the bifunctional alkylating agent nitrogen mustard. Mol Gen Genet 181: 346-351.
33. Ruhland A, Kircher M, Wilborn F, Brendel M, (1981) A yeast mutant specifically sensitive to bifunctional alkylation. Mutat Res 91: 457-462.
34. Grossmann KF, Ward AM, Moses RE, (2000) Saccharomyces cerevisiae lacking Snm1, Rev3 or Rad51 have a normal S-phase but arrest permanently in G2 after cisplatin treatment. Mutat Res 461: 1-13.
35. Magana-Schwencke N, Henriques JA, Chanet R, Moustacchi E, (1982) The fate of 8-methoxypsoralen photoinduced crosslinks in nuclear and mitochondrial yeast DNA: comparison of wild-type and repair-deficient strains. Proc Natl Acad Sci U S A 79: 1722-1726.
36. Wilborn F, Brendel M, (1989) Formation and stability of interstrand cross-links induced by cis- and trans-diamminedichloroplatinum (II) in the DNA of Saccharomyces cerevisiae strains differing in repair capacity. Curr Genet 16: 331-338.
37. Li X, Moses RE, (2003) The beta-lactamase motif in Snm1 is required for repair of DNA double-strand breaks caused by interstrand crosslinks in S. cerevisiae. DNA Repair (Amst) 2: 121-129.
38. Barber LJ, Ward TA, Hartley JA, McHugh PJ, (2005) DNA interstrand cross-link repair in the Saccharomyces cerevisiae cell cycle: overlapping roles for PSO2 (SNM1) with MutS factors and EXO1 during S phase. Mol Cell Biol 25: 2297-2309.
39. De Silva IU, McHugh PJ, Clingen PH, Hartley JA, (2000) Defining the roles of nucleotide excision repair and recombination in the repair of DNA interstrand cross-links in mammalian cells. Mol Cell Biol 20: 7980-7990.
40. Akkari YM, Bateman RL, Reifsteck CA, Olson SB, Grompe M, (2000) DNA replication is required To elicit cellular responses to psoralen-induced DNA interstrand cross-links. Mol Cell Biol 20: 8283-8289.
41. Bessho T, (2003) Induction of DNA replication-mediated double strand breaks by psoralen DNA interstrand cross-links. J Biol Chem 278: 5250-5254.
42. Hanada K, Budzowska M, Modesti M, Maas A, Wyman C, et al. (2006) The structure-specific endonuclease Mus81-Eme1 promotes conversion of interstrand DNA crosslinks into double-strands breaks. Embo J 25: 4921-4932.
43. Wang AT, Sengerova B, Cattell E, Inagawa T, Hartley JM, et al. (2011) Human SNM1A and XPF-ERCC1 collaborate to initiate DNA interstrand cross-link repair. Genes Dev 25: 1859-1870.
44. Zhang N, Lu X, Zhang X, Peterson CA, Legerski RJ, (2002) hMutSbeta is required for the recognition and uncoupling of psoralen interstrand cross-links in vitro. Mol Cell Biol 22: 2388-2397.
45. Wu Q, Christensen LA, Legerski RJ, Vasquez KM, (2005) Mismatch repair participates in error-free processing of DNA interstrand crosslinks in human cells. EMBO Rep 6: 551-557.
46. Lan L, Hayashi T, Rabeya RM, Nakajima S, Kanno S, et al. (2004) Functional and physical interactions between ERCC1 and MSH2 complexes for resistance to cis-diamminedichloroplatinum(II) in mammalian cells. DNA Repair (Amst) 3: 135-143.
47. Ho Y, Gruhler A, Heilbut A, Bader GD, Moore L, et al. (2002) Systematic identification of protein complexes in Saccharomyces cerevisiae by mass spectrometry. Nature 415: 180-183.
48. Chen XJ, Guan MX, Clark-Walker GD, (1993) MGM101, a nuclear gene involved in maintenance of the mitochondrial genome in Saccharomyces cerevisiae. Nucleic Acids Res 21: 3473-3477.
49. Meeusen S, Tieu Q, Wong E, Weiss E, Schieltz D, et al. (1999) Mgm101p is a novel component of the mitochondrial nucleoid that binds DNA and is required for the repair of oxidatively damaged mitochondrial DNA. J Cell Biol 145: 291-304.
50. Meeusen S, Nunnari J, (2003) Evidence for a two membrane-spanning autonomous mitochondrial DNA replisome. J Cell Biol 163: 503-510.
51. Mbantenkhu M, Wang X, Nardozzi JD, Wilkens S, Hoffman E, et al. (2011) Mgm101 is a Rad52-related protein required for mitochondrial DNA recombination. J Biol Chem.
52. Zuo X, Xue D, Li N, Clark-Walker GD, (2007) A functional core of the mitochondrial genome maintenance protein Mgm101p in Saccharomyces cerevisiae determined with a temperature-conditional allele. FEMS Yeast Res 7: 131-140.
53. Drummond JT, Genschel J, Wolf E, Modrich P, (1997) DHFR/MSH3 amplification in methotrexate-resistant cells alters the hMutSalpha/hMutSbeta ratio and reduces the efficiency of base-base mismatch repair. Proc Natl Acad Sci U S A 94: 10144-10149.
54. Contamine V, Picard M, (2000) Maintenance and integrity of the mitochondrial genome: a plethora of nuclear genes in the budding yeast. Microbiol Mol Biol Rev 64: 281-315.
55. Reenan RA, Kolodner RD, (1992) Isolation and characterization of two Saccharomyces cerevisiae genes encoding homologs of the bacterial HexA and MutS mismatch repair proteins. Genetics 132: 963-973.
56. Chen C, Kolodner RD, (1999) Gross chromosomal rearrangements in Saccharomyces cerevisiae replication and recombination defective mutants. Nat Genet 23: 81-85.
57. Kolodner RD, Putnam CD, Myung K, (2002) Maintenance of genome stability in Saccharomyces cerevisiae. Science 297: 552-557.
58. Myung K, Datta A, Chen C, Kolodner RD, (2001) SGS1, the Saccharomyces cerevisiae homologue of BLM and WRN, suppresses genome instability and homeologous recombination. Nat Genet 27: 113-116.
59. Smith S, Hwang JY, Banerjee S, Majeed A, Gupta A, et al. (2004) Mutator genes for suppression of gross chromosomal rearrangements identified by a genome-wide screening in Saccharomyces cerevisiae. Proc Natl Acad Sci U S A 101: 9039-9044.
60. Tishkoff DX, Boerger AL, Bertrand P, Filosi N, Gaida GM, et al. (1997) Identification and characterization of Saccharomyces cerevisiae EXO1, a gene encoding an exonuclease that interacts with MSH2. Proc Natl Acad Sci U S A 94: 7487-7492.
61. Tran PT, Erdeniz N, Dudley S, Liskay RM, (2002) Characterization of nuclease-dependent functions of Exo1p in Saccharomyces cerevisiae. DNA Repair (Amst) 1: 895-912.
62. Symington LS, Gautier J, (2010) Double-Strand Break End Resection and Repair Pathway Choice. Annu Rev Genet.
63. White MF, (2009) Structure, function and evolution of the XPD family of iron-sulfur-containing 5′→3′ DNA helicases. Biochem Soc Trans 37: 547-551.
64. Stoepker C, Hain K, Schuster B, Hilhorst-Hofstee Y, Rooimans MA, et al. (2011) SLX4, a coordinator of structure-specific endonucleases, is mutated in a new Fanconi anemia subtype. Nat Genet 43: 138-141.
65. Crossan GP, van der Weyden L, Rosado IV, Langevin F, Gaillard PH, et al. (2011) Disruption of mouse Slx4, a regulator of structure-specific nucleases, phenocopies Fanconi anemia. Nat Genet 43: 147-152.
66. Kim Y, Lach FP, Desetty R, Hanenberg H, Auerbach AD, et al. (2011) Mutations of the SLX4 gene in Fanconi anemia. Nat Genet 43: 142-146.
67. Zuo XM, Clark-Walker GD, Chen XJ, (2002) The mitochondrial nucleoid protein, Mgm101p, of Saccharomyces cerevisiae is involved in the maintenance of rho(+) and ori/rep-devoid petite genomes but is not required for hypersuppressive rho(-) mtDNA. Genetics 160: 1389-1400.
68. De Silva IU, McHugh PJ, Clingen PH, Hartley JA, (2002) Defects in interstrand cross-link uncoupling do not account for the extreme sensitivity of ERCC1 and XPF cells to cisplatin. Nucleic Acids Res 30: 3848-3856.
69. Li X, Hejna J, Moses RE, (2005) The yeast Snm1 protein is a DNA 5′-exonuclease. DNA Repair (Amst) 4: 163-170.
70. Hazrati A, Ramis-Castelltort M, Sarkar S, Barber LJ, Schofield CJ, et al. (2007) Human SNM1A rescues the DNA repair defects of yeast pso2 mutants. DNA Repair (Amst) in press.
71. Peng M, Litman R, Xie J, Sharma S, Brosh RM Jr, et al. (2007) The FANCJ/MutLalpha interaction is required for correction of the cross-link response in FA-J cells. Embo J 26: 3238-3249.
72. Williams SA, Wilson JB, Clark AP, Mitson-Salazar A, Tomashevski A, et al. (2011) Functional and physical interaction between the mismatch repair and FA-BRCA pathways. Hum Mol Genet.
73. Huang M, Kennedy R, Ali AM, Moreau LA, Meetei AR, et al. (2011) Human MutS and FANCM complexes function as redundant DNA damage sensors in the Fanconi Anemia pathway. DNA Repair (Amst).
74. Hemphill AW, Bruun D, Thrun L, Akkari Y, Torimaru Y, et al. (2008) Mammalian SNM1 is required for genome stability. Mol Genet Metab 94: 38-45.
75. Yang K, Moldovan GL, D'Andrea AD, (2010) RAD18-dependent recruitment of SNM1A to DNA repair complexes by a ubiquitin-binding zinc finger. J Biol Chem 285: 19085-19091.
76. Marsit CJ, Liu M, Nelson HH, Posner M, Suzuki M, et al. (2004) Inactivation of the Fanconi anemia/BRCA pathway in lung and oral cancers: implications for treatment and survival. Oncogene 23: 1000-1004.
77. Wreesmann VB, Estilo C, Eisele DW, Singh B, Wang SJ, (2007) Downregulation of Fanconi anemia genes in sporadic head and neck squamous cell carcinoma. ORL J Otorhinolaryngol Relat Spec 69: 218-225.
78. Taniguchi T, Tischkowitz M, Ameziane N, Hodgson SV, Mathew CG, et al. (2003) Disruption of the Fanconi anemia-BRCA pathway in cisplatin-sensitive ovarian tumors. Nat Med 9: 568-574.
79. Jiricny J, (1998) Eukaryotic mismatch repair: an update. Mutat Res 409: 107-121.
80. Wach A, Brachat A, Pohlmann R, Philippsen P, (1994) New heterologous modules for classical or PCR-based gene disruptions in Saccharomyces cerevisiae. Yeast 10: 1793-1808.
81. Longtine MS, McKenzie A 3rd, Demarini DJ, Shah NG, Wach A, et al. (1998) Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 14: 953-961.
82. Goldstein AL, McCusker JH, (1999) Three new dominant drug resistance cassettes for gene disruption in Saccharomyces cerevisiae. Yeast 15: 1541-1553.
83. Tong AH, Evangelista M, Parsons AB, Xu H, Bader GD, et al. (2001) Systematic genetic analysis with ordered arrays of yeast deletion mutants. Science 294: 2364-2368.
84. Suckau D, Resemann A, Schuerenberg M, Hufnagel P, Franzen J, et al. (2003) A novel MALDI LIFT-TOF/TOF mass spectrometer for proteomics. Anal Bioanal Chem 376: 952-965.
85. Zinser E, Daum G, (1995) Isolation and biochemical characterization of organelles from the yeast, Saccharomyces cerevisiae. Yeast 11: 493-536.
86. Liang C, Stillman B, (1997) Persistent initiation of DNA replication and chromatin-bound MCM proteins during the cell cycle in cdc6 mutants. Genes Dev 11: 3375-3386.
87. McHugh PJ, Gill RD, Waters R, Hartley JA, (1999) Excision repair of nitrogen mustard-DNA adducts in Saccharomyces cerevisiae. Nucleic Acids Res 27: 3259-3266.