New features on Pso2 protein family in DNA interstrand cross-link repair and in the maintenance of genomic integrity in Saccharomyces cerevisiae

Fungal Genetics and Biology

Volumn 60, Issue , 2013, Pages 122-132

  Munari, Fernanda Mosena ^a   Guecheva, Temenouga Nikolova ^a   Bonatto, Diego ^a   Henriques, João AntÔnio Pêgas ^a,b  

^a FEDERAL UNIVERSITY OF RIO GRANDE DO SUL   (Brazil)

^b UNIVERSITY OF CAXIAS DO SUL   (Brazil)

Author keywords

8 Methoxypsoralen; Bifunctional chemotherapeutic drugs; DNA interstrand crosslink repair; Double strand breaks; PSO2 SNM1; Saccharomyces cerevisiae

Indexed keywords

CHLORMETHINE; CISPLATIN; FANCONI ANEMIA PROTEIN; METALLO BETA LACTAMASE; METHOXSALEN; MITOMYCIN; MRE11 RAD50 XRS2 PROTEIN; NUCLEIC ACID BINDING PROTEIN; PROTEIN PSO2; PSORALEN; UNCLASSIFIED DRUG;

ARTICLE; DNA CROSS LINKING; DNA END JOINING REPAIR; DNA REPAIR; DOUBLE STRANDED DNA BREAK; ENZYME ACTIVITY; FANCONI ANEMIA; FUNGAL GENOME; GENE MUTATION; HUMAN; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; SACCHAROMYCES CEREVISIAE;

MAMMALIA; SACCHAROMYCES CEREVISIAE;

8-METHOXYPSORALEN; BIFUNCTIONAL CHEMOTHERAPEUTIC DRUGS; DNA INTERSTRAND CROSSLINK REPAIR; DOUBLE STRAND BREAKS; PSO2/SNM1; SACCHAROMYCES CEREVISIAE;

DNA BREAKS, DOUBLE-STRANDED; DNA END-JOINING REPAIR; DNA REPAIR; DNA, FUNGAL; DNA-BINDING PROTEINS; ENDODEOXYRIBONUCLEASES; FANCONI ANEMIA; GENOMIC INSTABILITY; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 84887613990     PISSN: 10871845     EISSN: 10960937     Source Type: Journal    
DOI: 10.1016/j.fgb.2013.09.003     Document Type: Article

References (133)

1. Akhter S., Richie C.T., Deng J.M., et al. Deficiency in SNM1 abolishes an early mitotic checkpoint induced by spindle stress. Mol. Cell. Biol. 2004, 24:10448-10455.
2. Akhter S., Lam Y.C., Chang S., et al. The telomeric protein SNM1B/Apollo is required for normal cell proliferation and embryonic development. Aging Cell 2010, 9:1047-1056.
3. Auerbach A.D. Fanconi anemia and its diagnosis. Mutat. Res. 2009, 668:4-10.
4. Ausubel F., Brent R., Kingston R.E., Moore D.D., Seidman J.G., Smith J.A., Struhl K. Short Protocols in Molecular Biology 1995, John Wiley & Sons Inc., New York. third ed.
5. Bae J.-B., Mukhopadhyay S.S., Liu L., et al. Snm1B/Apollo mediates replication fork collapse and S phase checkpoint activation in response to DNA interstrand cross-links. Oncogene 2008, 27:5045-5056.
6. Barber L.J., Ward T.A., Hartley J.A., et al. 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. 2005, 25:2297-2309.
7. Bauer G.B., Povirk L.F. Specificity and kinetics of interstrand and intrastrand bifunctional alkylation by nitrogen mustards at a G-G-C sequence. Nucleic Acids Res. 1997, 25:1211-1218.
8. Bonatto D., Brendel M., Henriques J.A.P. A new group of plant-specific ATP-dependent DNA ligases identified by protein phylogeny, hydrophobic cluster analysis and 3-dimensional modelling. Funct. Plant Biol. 2005, 32:161-174.
9. Bonatto D., Brendel M., Henriques J.A.P. The eukaryotic Pso2p/Snm1p family revisited: in silico analyses of Pso2p A, B and Plasmodium groups. Comput. Biol. Chem. 2005, 29:420-433.
10. Bonatto D., Brendel M., Henriques J.A.P. In silico identification and analysis of new Artemis/Artemis-like sequences from fungal and metazoan species. Prot. J. 2005, 24:399-411.
11. Bonatto D., Revers L.F., Brendel M., et al. The eukaryotic Pso2/Snm1/Artemis proteins and their function as genomic and cellular caretakers. Braz. J. Medic. Biol. Res. 2005, 38:321-334.
12. Boulton S.J., Jackson S.P. Identification of a Saccharomyces cerevisiae Ku80 homologue: roles in DNA double strand break rejoining and in telomeric maintenance. Nucleic Acids Res. 1996, 24:4639-4648.
13. Brendel M., Henriques J.A.P. The pso mutants of Saccharomyces cerevisiae comprise two groups: one deficient in DNA repair and another with altered mutagen metabolism. Mutat. Res. 2001, 489:79-96.
14. Brendel M., Bonatto D., Strauss M., et al. Role of PSO genes in repair of DNA damage of Saccharomyces cerevisiae. Mutat. Res. 2003, 544:179-193.
15. Brendel M., Marisco G., Ganda I., et al. DNA repair mutant pso2 of Saccharomyces cerevisiae is sensitive to intracellular acetaldehyde accumulated by disulfiram-mediated inhibition of acetaldehyde dehydrogenase. Gen. Mol. Res. 2010, 9:48-57.
16. Callebaut I., Moshous D., Mornon J.-P., et al. Metallo-beta-lactamase fold within nucleic acids processing enzymes: the beta-CASP family. Nucleic Acids Res. 2002, 30:3592-3601.
17. Cannavo E., Cejka P., Kowalczykowski C. Relationship of DNA degradation by Saccharomyces cerevisiae Exonuclease 1 and its stimulation by RPA and Mre11-Rad50-Xrs2 to DNA end resection. Proc. Natl. Acad. Sci. USA 2013, E1661-E1668.
18. Cassier C., Chanet R., Henriques J.A.P., et al. The effects of three PSO genes on induced mutagenesis: a novel class of mutationally defective yeast. Genetics 1980, 96:841-857.
19. Cassier-Chauvat C., Moustacchi E. Allelism between pso1-1 and rev3-1 mutants and between pso2-1 and snm1 mutants in Saccharomyces cerevisiae. Curr. Genet. 1988, 13:37-40.
20. Cattell E., Sengerová B., McHugh P.J. The SNM1/Pso2 family of ICL repair nucleases: from yeast to man. Environ. Mol. Mutagen. 2010, 51:635-645.
21. Cole R.S. Repair of DNA containing interstrand crosslinks. Proc. Natl. Acad. Sci. USA 1973, 70:1064-1068.
22. Corneo B., Wendland R.L., Deriano L., et al. Rag mutations reveal robust alternative end joining. Nature 2007, 449:483-486.
23. Cruz, L.A., 2012. Estudo da interação entre remodeladores de cromatina e vias de reparação de DNA em resposta ao dano induzido por agentes antineoplásicos e ditelureto de difenila em Saccharomyces cerevisiae. PhD Thesis, UFRGS, Porto Alegre, RS, Brazil.
24. da Silva K.V.C.L., Henriques J.A.P., Jungmann D.M. Interaction between the pso2-1 mutation that confers sensitivity to psoralen photoaddition and the rad mutations that control the sensitivity to radiation in yeast after 254 nm UV-light treatment. Photochem. Photobiol. 1980, 31:557-563.
25. Daee D.L., Myung K. Fanconi-like crosslink repair in yeast. Genome Integrity 2012, 3:7.
26. Daee D.L., Ferrari E., Longerich S., et al. Rad5-dependent DNA repair functions of the Saccharomyces cerevisiae FANCM protein homolog Mph1. J. Biol. Chem. 2012, 287:26563-26575.
27. D'Amours D., Jackson S.P. The yeast Xrs2 complex functions in S phase checkpoint regulation. Genes Dev. 2001, 15:2238-2249.
28. D'Amours D., Jackson S.P. The MRE11 complex: at the crossroads of DNA repair and checkpoint signalling. Nat. Rev. Mol. Cell Biol. 2002, 3:317-327.
29. Decottignies A. Microhomology-mediated end joining in fission yeast is repressed by pku70 and relies on genes involved in homologous recombination. Genetics 2007, 176:1403-1415.
30. Degrandi T.H., De Oliveira I.M., d' Almeida G.S. Evaluation of the cytotoxicity, genotoxicity and mutagenicity of diphenyl ditelluride in several biological models. Mutagenesis 2010, 25:257-269.
31. Demuth I., Digweed M., Concannon P. Human SNM1B is required for normal cellular response to both DNA interstrand crosslink-inducing agents and ionizing radiation. Oncogene 2004, 23:8611-8618.
32. Dominski Z. Nucleases of the metallo-β-lactamase family and their role in DNA and RNA metabolism. Crit. Rev. Biochem. Mol. Biol. 2007, 42:67-93.
33. Dronkert M.L.G., Kanaar R. Repair of DNA interstrand cross-links. Mutat. Res. 2001, 486:217-247.
34. Dronkert M.L.G., De Wit J., Boeve M., et al. Disruption of mouse SNM1 causes increased sensitivity to the DNA interstrand cross-linking agent mitomycin C. Mol. Cell. Biol. 2000, 20:4553-4561.
35. Dudás A., Vlasáková D., Dudásová Z., et al. Further characterization of the role of Pso2 in the repair of DNA interstrand cross-link-associated double-strand breaks in Saccharomyces cerevisiae. Neoplasma 2007, 54:189-194.
36. Engman L., Kandra T., Gallegos A., et al. Water-soluble organotellurium compounds inhibit thioredoxin reductase and the growth of human cancer cells. Anticancer Drug Des. 2000, 15:323-330.
37. Grey M., Düsterhöft A., Henriques J.A.P., et al. Allelism of PSO4 and PRP19 links pre-mRNA processing with recombination and error-prone DNA-repair in Saccharomyces cerevisiae. Nucleic Acids Res. 1996, 24:4009-4014.
38. Grossmann K.F., Ward A.M., Matkovic M.E., et al. S. cerevisiae has three pathways for DNA interstrand crosslink repair. Mut. Res. 2001, 487:73-83.
39. Guainazzi A., Schärer O.D. Using synthetic DNA interstrand crosslinks to elucidate repair pathways and identify new therapeutic targets for cancer chemotherapy. Cell. Mol. Life Sci. 2010, 67:3683-3697.
40. Guirouilh-Barbat J., Huck S., Bertrand P., et al. Impact of the KU80 pathway on NHEJ-induced genome rearrangements in mammalian cells. Mol. Cell 2004, 14:611-623.
41. Guirouilh-Barbat J., Rass E., Plo I., et al. Defects in XRCC4 and KU80 differentially affect the joining of distal nonhomologous ends. Proc. Natl. Acad. Sci. USA 2007, 104:20902-20907.
42. Haber J.E. Alternative endings. Proc. Natl. Acad. Sci. USA 2008, 105:405-406.
43. Hart G.T., Lee I., Marcotte E.R. A high-accuracy consensus map of yeast protein complexes reveals modular nature of gene essentiality. BMC Bioinform. 2007, 8:236.
44. Hazrati A., Ramis-Castelltort M., Sarkar S., et al. Human SNM1A suppresses the DNA repair defects of yeast pso2 mutants. DNA Repair 2008, 7:230-238.
45. Hejna J., Philip S., Ott J., et al. The hSNM1 protein is a DNA 5'-exonuclease. Nucleic Acids Res. 2007, 35:6115-6123.
46. Hemphill A.W., Bruun D., Thrun L., et al. Mammalian SNM1 is required for genome stability. Mol. Gen. Metab. 2008, 94:38-45.
47. Henriques J.A.P., Brendel M. The role of PSO and SNM genes in DNA repair of the yeast Saccharomyces cerevisiae. Curr. Genet. 1990, 18:387-393.
48. Henriques J.A.P., Moustacchi E. Isolation and characterization of pso mutants sensitive to photo-addition of psoralen derivatives in Saccharomyces cerevisiae. Genetics 1980, 95:273-288.
49. Henriques J.A.P., Moustacchi E. Interactions between mutations for sensitivity to psoralen photoaddition (pso) and to radiation (rad) in Saccharomyces cerevisiae. J. Bacteriol. 1981, 148:248-256.
50. Henriques J.A.P., Brozmanova J., Brendel M. Role of PSO genes in the repair of photoinduced interstrand cross-links and photooxidative damage in the DNA of the yeast Saccharomyces cerevisiae. J. Photochem. Photobiol., B 1997, 39:185-196.
51. Hinz J.M. Role of homologous recombination in DNA interstrand crosslink repair. Environ. Mol. Mutagen. 2010, 51:582-603.
52. Ho H.-C., Burgess S.M. Pch2 acts through Xrs2 and Tel1/ATM to modulate interhomolog bias and checkpoint function during meiosis. PLoS Genet. 2011, 7:e1002351.
53. Ho T.V., Schärer O.D. Translesion DNA synthesis polymerase in DNA interstrand crosslink repair. Environ. Mol. Mutagen. 2010, 51:552-566.
54. Ho Y., Gruhler A., Heilbut A., et al. Systematic identification of protein complexes in Saccharomyces cerevisiae by mass spectrometry. Nature 2002, 415:180-183.
55. Ho T.V., Guainazzi A., Derkunt, et al. Structure-dependent bypass of DNA interstrand crosslinks by translesion synthesis polymerases. Nucleic Acids Res. 2011, 39:7455-7464.
56. Hoch N.C., Santos R.S., Rosa R.M., et al. Allelism of Saccharomyces cerevisiae gene PSO10, involved in error-prone repair of psoralen-induced DNA damage, with SUMO ligase-encoding MMS21. Curr. Genet. 2008, 53:361-371.
57. Huefner N.D., Mizuno Y., Weil C.F., et al. Breadth by depth: expanding our understanding of the repair of transposon-induced DNA double strand breaks via deep-sequencing. DNA Repair 2011, 10:1023-1033.
58. Ishiai M., Kimura M., Namikoshi K., et al. DNA cross-link repair protein SNM1A interacts with PIAS1 in nuclear focus formation. Mol. Cell. Biol. 2004, 24:10733-10741.
59. Jeggo P., O'Neill P. The Greek Goddess, Artemis, reveals the secrets of her cleavage. DNA Repair 2002, 1:771-777.
60. Jenny A., Minvielle-Sebastia L., Preker P.J., et al. Sequence similarity between the 73-kilodalton protein of mammalian CPSF and a subunit of yeast polyadenylation factor I. Science 1996, 274:1514-1517.
61. Kabotyanski E.B., Gomelsky L., Han J., et al. Double-strand break repair in Ku86- and XRCC4-deficient cells. Nucleic Acids Res. 1998, 26:5333-5342.
62. Kimura S., Saotome A., Uchiyama Y., et al. The expression of the rice (Oryza sativa L.) homologue of Snm1 is induced by DNA damages. Biochem. Biophys. Res. Commun. 2005, 329:668-672.
63. Kondo T., Matsumoto K., Sugimoto K. Role of complex containing Rad17, Mec3, and Ddc1 in the yeast DNA damage checkpoint pathway. Mol. Cell. Biol. 1999, 19:1136-1143.
64. Krogh B.O., Symington L.S. Recombination proteins in yeast. Annu. Rev. Genet. 2004, 38:233-271.
65. Lam A.F., Krogh B.O., Symington L.S. Unique and overlapping functions of the Exo1, Mre11 and Pso2 nucleases in DNA repair. DNA Repair 2008, 7:655-662.
66. Lee K., Lee S.E. Saccharomyces cerevisiae Sae2- and Tel1-dependent single-strand DNA formation at DNA break promotes microhomology-mediated end joining. Genetics 2007, 176:2003-2014.
67. Lees-Miller S. Repair of DNA double strand breaks by non-homologous end joining. Biochimie 2003, 85:1161-1173.
68. Lehoczký P., McHugh P.J., Chovanec M. DNA interstrand cross-link repair in Saccharomyces cerevisiae. FEMS Microbiol. Rev. 2007, 31:109-133.
69. Lenain C., Bauwens S., Amiard S., et al. The Apollo 5' exonuclease functions together with TRF2 to protect telomeres from DNA repair. Curr. Biol. 2006, 16:1303-1310.
70. Li X., Moses R.E. The beta-lactamase motif in Snm1 is required for repair of DNA double-strand breaks caused by interstrand crosslinks in S. cerevisiae. DNA Repair 2003, 2:121-129.
71. Li X., Hejna J., Moses R.E. The yeast Snm1 protein is a DNA 5'-exonuclease. DNA Repair 2005, 4:163-170.
72. Liu L., Akhter S., Bae J.B. SNM1B/Apollo interacts with astrin and is required for the prophase cell cycle checkpoint. Cell Cycle 2009, 8:628-638.
73. Ma Y., Pannicke U., Schwarz K., et al. Hairpin opening and overhang processing by an Artemis/DNA-dependent protein kinase complex in nonhomologous end joining and V(D)J recombination. Cell 2002, 108:781-794.
74. Ma J., Kim E.M., Haber J.E., et al. Yeast Mre11 and Rad1 proteins define a Ku-independent mechanism to repair double-strand breaks lacking overlapping end sequences. Mol. Cell. Biol. 2003, 23:8820-8828.
75. Ma Y., Pannicke U., Lu H., et al. The DNA-dependent protein kinase catalytic subunit phosphorylation sites in human Artemis. J. Biol. Chem. 2005, 280:33839-338346.
76. Magaña-Schwencke N., Henriques J.A.P., Chanet R., et al. 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. USA 1982, 79:1722-1726.
77. Mason J.M., Sekiguchi J.M. Snm1B/Apollo functions in the Fanconi anemia pathway in response to DNA interstrand crosslinks. Hum. Mol. Genet. 2011, 20:2549-2559.
78. Matsuzaki K., Shinohara A., Shinohara M. Forkhead-associated domain of yeast Xrs2, a homolog of human Nbs1, promotes nonhomologous end joining through interaction with a ligase IV partner protein, Lif1. Genetics 2008, 179:213-225.
79. McHugh P.J., Sones W.R., Hartley J.A. Repair of intermediate structures produced at DNA interstrand cross-links in Saccharomyces cerevisiae. Mol. Cell. Biol. 2000, 20:3425-3433.
80. McHugh P.J., Spanswick V.J., Hartley J.A. Repair of DNA interstrand crosslinks: molecular mechanisms and clinical relevance. Lancet Oncol. 2001, 2:483-490.
81. McHugh P.J., Ward T.A., Chovanec M. A prototypical Fanconi anemia pathway in lower eukaryotes?. Cell Cycle 2012, 11:3739-3744.
82. McVey M. Insights from worms, flies, frogs, and slime molds. Environ. Mol. Mutagen. 2010, 51:646-658.
83. McVey M., Lee S.E. MMEJ repair of double-strand breaks (director's cut): deleted sequences and alternative endings. Trends Genet. 2008, 24:529-538.
84. Meetei A.R., Medhurst A.L., Ling, et al. A human ortholog of archaeal DNA repair protein Hef is defective in Fanconi anemia complementation group M. Nat. Genet. 2005, 37:958-963.
85. Mimitou E.P., Symington L.S. Ku prevents Exo1 and Sgs1-dependent resection of DNA ends in the absence of a functional MRX complex or Sae2. EMBO J. 2010, 29:3358-3369.
86. Molinier J., Stamm M.E., Hohn B. SNM-dependent recombinational repair of oxidatively induced DNA damage in Arabidopsis thaliana. EMBO Rep. 2004, 5:994-999.
87. Moshous D., Callebaut I., De Chasseval R., et al. Artemis, a novel DNA double-strand break repair/V(D)J recombination protein, is mutated in human severe combined immune deficiency. Cell 2001, 105:177-186.
88. Muniandy P., Liu J., Majumdar A., et al. DNA interstrand cross-link repair in mammalian cells. Step by step. Crit. Rev. Biochem. Mol. Biol. 2010, 45:23-49.
89. Niedernhofer L.J., Daniels J.S., Rouzer, et al. Malondialdehyde, a product of lipid peroxidation, is mutagenic in human cells. J. Biol. Chem. 2003, 278:31426-31433.
90. Niewolik D., Pannicke U., Lu H., et al. DNA-PKcs dependence of Artemis endonucleolytic activity, differences between hairpins and 5' or 3' overhangs. J. Biol. Chem. 2006, 281:33900-33909.
91. Noll D.M., Mason T.M., Miller P.S. Formation and repair of interstrand cross-links in DNA. Chem. Rev. 2006, 106:277-301.
92. Nussenzweig A., Nussenzweig M.C. A backup DNA repair pathway moves to the forefront. Cell 2007, 131:2006-2008.
93. Paesi-Toresan S.O., Pich C.T., Grey, et al. Gene PSO5 of Saccharomyces cerevisiae, involved in repair of oxidative damage, is allelic to RAD16. Curr. Genet. 1995, 27:493-495.
94. Pannicke U., Ma Y., Hopfner K.-P., et al. Functional and biochemical dissection of the structure-specific nuclease ARTEMIS. EMBO J. 2004, 23:1987-1997.
95. Pungartnik C., Brendel M., Henriques J.A.P. Mutant allele pso7-1, that sensitizes Saccharomyces cerevisiae to photoactivated psoralen, is allelic with COX11, encoding a protein indispensable for a functional cytochrome c oxidase. Curr. Genet. 1999, 36:124-129.
96. Pungartnik C., Picada J., Brendel M., et al. Further phenotypic characterization of pso mutants of Saccharomyces cerevisiae with respect to DNA repair and response to oxidative stress. Genet. Mol. Res. 2002, 1:79-89.
97. Räschle M., Knipscheer P., Enoiu M., et al. Mechanism of replication-coupled DNA interstrand crosslink repair. Cell 2008, 134:969-980.
98. Riballo E., Kühne M., Rief N., et al. A pathway of double-strand break rejoining dependent upon ATM, Artemis, and proteins locating to γ-H2AX foci. Mol. Cell 2004, 16:715-724.
99. Rolla H., Grey M., Schmidt C.L., et al. Mutant pso8-1 of Saccharomyces cerevisiae, sensitive to photoactivated psoralens, UV radiation, and chemical mutagens, contains a rad6 missense mutant allele. Curr. Genet. 2002, 41:217-223.
100. Rooney S., Alt F.W., Lombard D., et al. Defective DNA repair and increased genomic instability in Artemis-deficient murine cells. J. Exp. Med. 2003, 197:553-565.
101. Rooney S., Sekiguchi J., Whitlow S., et al. Artemis and p53 cooperate to suppress oncogenic N-myc amplification in progenitor B cells. Proc. Natl. Acad. Sci. USA 2004, 101:2410-2415.
102. Ruhland A., Haase E., Siede W., et al. Isolation of yeast mutants sensitive to the bifunctional alkylating agent nitrogen mustard. Mol. Gen. Genet. 1981, 181:346-351.
103. Ruhland A., Kircher M., Wilborn F., et al. A yeast mutant specifically sensitive to bifunctional alkylation. Mutat. Res. 1981, 91:457-462.
104. Rupnik A., Lowndes N.F., Grenon M. MRN and the race to the break. Chromosoma 2010, 119:115-135.
105. Saffi J., Feldmann H., Winnacker E.L., et al. Interaction of the yeast Pso5/Rad16 and Sgs1 proteins: influences on DNA repair and aging. Mutat. Res. 2001, 486:195-206.
106. Sarkar S., Davies A.A., Ulrich H.D., et al. DNA interstrand crosslink repair during G1 involves nucleotide excision repair and DNA polymerase zeta. EMBO J. 2006, 25:1285-1294.
107. Schärer O.D. DNA interstrand crosslinks: natural and drug-induced DNA adducts that induce unique cellular responses. ChemBioChem 2005, 6:27-32.
108. Schmidt C.L., Grey M., Schmidt M., et al. Allelism of Saccharomyces cerevisiae genes PSO6, involved in survival after 3-CPs+UVA induced damage, and ERG3, encoding the enzyme sterol C-5 desaturase. Yeast 1999, 15:1503-1510.
109. Shen X., Li L. Mutagenic repair of DNA interstrand crosslinks. Environ. Mol. Mutagen. 2010, 51:493-499.
110. Shim E.Y., Chung W.-H., Nicolette M.L., et al. Saccharomyces cerevisiae Mre11/Rad50/Xrs2 and Ku proteins regulate association of Exo1 and Dna2 with DNA breaks. EMBO J. 2010, 29:3370-3380.
111. Singh T.R., Saro D., Ali A.M., et al. MHF1-MHF2, a histone-fold-containing protein complex, participates in the Fanconi Anemia pathway via FANCM. Mol. Cell 2011, 37:879-886.
112. Soulas-Sprauel P., Guyader G.L., Rivera-Munoz P., et al. Role for DNA repair factor XRCC4 in immunoglobulin class switch recombination. J. Exp. Med. 2007, 204:1717-1727.
113. Strauss M., Grey M., Henriques J.A.P., et al. RNR4 mutant alleles pso3-1 and rnr4δ block induced mutation in Saccharomyces cerevisiae. Curr. Genet. 2007, 51:221-231.
114. Sun W., Nandi S., Osman F., et al. The FANCM ortholog Fml1 promotes recombination at stalled replication forks and limits crossing over during DNA double-strand break repair. Mol. Cell 2008, 32:118-128.
115. Symington L.S. Role of RAD52 epistasis group genes in homologous recombination and double-strand break repair. Microbiol. Mol. Biol. Rev. 2002, 66:630-670.
116. Symington L.S., Gautier J. Double-strand break end resection and repair pathway choice. Annu. Rev. Genet. 2011, 45:247-271.
117. Takaku H. A candidate prostate cancer susceptibility gene encodes tRNA 3' processing endoribonuclease. Nucleic Acids Res. 2003, 31:2272-2278.
118. Tiefenbach T., Junop M. Pso2 (SNM1) is a DNA structure-specific endonuclease. Nucleic Acids Res. 2012, 40:2131-2139.
119. Touzot F., Callebaut I., Soulier J., et al. Function of Apollo (SNM1B) at telomere highlighted by a splice variant identified in a patient with Hoyeraal-Hreidarsson syndrome. Proc. Natl. Acad. Sci. USA 2010, 107:10097-10102.
120. Truong L.N., Li Y., Shi L.Z., et al. Microhomology-mediated end joining and homologous recombination share the initial end resection step to repair DNA double-strand breaks in mammalian cells. Proc. Natl. Acad. Sci. USA 2013, 110:7720-7725.
121. Ungar L., Harari Y., Toren A., et al. Tor complex 1 controls telomere length by affecting the level of Ku. Curr. Biol. 2011, 21:2115-2120.
122. Van Overbeek M., De Lange T. Apollo, an Artemis-related nuclease, interacts with TRF2 and protects human telomeres in S phase. Curr. Biol. 2006, 16:1295-1302.
123. Verkaik N.S., Esveldt-van Lange R.E.E., Van Heemst D. Different types of V(D)J recombination and end-joining defects in DNA double-strand break repair mutant mammalian cells. Eur. J. Immunol. 2002, 32:701-709.
124. Wang W. Emergence of a DNA-damage response network consisting of Fanconi anaemia and BRCA proteins. Nat. Rev. Genet. 2007, 8:735-748.
125. Wang A.T., Sengerová B., Cattell E., et al. Human SNM1A and XPF - ERCC1 collaborate to initiate DNA interstrand cross-link repair. Genes Dev. 2011, 25:1859-1870.
126. Ward T.A., Dudášová Z., Sarkar S., et al. Components of a Fanconi-like pathway control Pso2-independent DNA interstrand crosslink repair in yeast. PLoS Genet. 2012, 8:e1002884.
127. Waterworth W.M., Masnavi G., Bhardwaj R.M., et al. A plant DNA ligase is an important determinant of seed longevity. Plant J. 2010, 63:848-860.
128. Wilborn F., Brendel M. Formation and stability of interstrand cross-links induced by cis-diamminedichloroplatinum and trans-diamminedichloroplatinum (II) in the DNA of Saccharomyces cerevisiae strains differing in repair capacity. Curr. Genet. 1989, 16:331-338.
129. Wood R.D. Mammalian nucleotide excision repair proteins and interstrand crosslink repair. Environ. Mol. Mutagen. 2010, 51:520-526.
130. Wu W., Wang M., Singh S.K., et al. Repair of radiation induced DNA double strand breaks by backup NHEJ is enhanced in G2. DNA Repair 2008, 7:329-338.
131. Yan Y., Akhter S., Zhang X., et al. The multifunctional SNM1 gene family: not just nucleases. Future Oncol. 2010, 6:1015-1029.
132. Yan Y., Zhang X., Legerski R.J. Artemis interacts with the Cul4A-DDB1(DDB2) ubiquitin E3 ligase and regulates degradation of the CDK inhibitor p27. Cell Cycle 2011, 10:4098-4109.
133. Zhang X., Paull T.T. The Mre11/Rad50/Xrs2 complex and non-homologous end-joining of incompatible ends in S. cerevisiae. DNA Repair 2005, 4:1281-1294.