A prototypical Fanconi anemia pathway in lower eukaryotes?

Cell Cycle

Volumn 11, Issue 20, 2012, Pages 3739-3744

  McHugh, Peter J ^a   Ward, Thomas A ^a   Chovanec, Miroslav ^b  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b CANCER RESEARCH INSTITUTE   (Slovakia)

Author keywords

DNA interstrand cross link repair; Fanconi anemia; S phase; Saccharomyces cerevisiae

Indexed keywords

EID: 84868034865     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.21727     Document Type: Article

References (57)

1. Lehoczký P, McHugh PJ, Chovanec M. DNA interstrand cross-link repair in Saccharomyces cere-visiae. FEMS Microbiol Rev 2007;31:109-33; PMID:17096663; http://dx.doi.org/10.1111/j.1574-6976.2006.00046.x. (Pubitemid 46227141)
2. Cole RS. Repair of DNA containing interstrand crosslinks in Escherichia coli: sequential excision and recombination. Proc Natl Acad Sci USA 1973;70:1064-8; PMID:4577788; http://dx.doi.org/10.1073/pnas.70.4.1064.
3. Dronkert MLG, Kanaar R. Repair of DNA inter-strand cross-links. Mutat Res 2001;486:217-47; PMID:11516927; http://dx.doi.org/10.1016/S0921-8777 (01) 00092-1.
4. Brendel M, Bonatto D, Strauss M, Revers LF, Pungartnik C, Saffi J, et al. Role of PSO genes in repair of DNA damage of Saccharomyces cerevisiae. Mutat Res 2003;544:179-93; PMID:14644320; http://dx.doi.org/10.1016/j.mrrev. 2003.06.018. (Pubitemid 37487660)
5. Henriques JAP, Brozmanová 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;39:185-96; PMID:9253198; http://dx.doi.org/10.1016/S1011-1344 (97) 00020-1. (Pubitemid 27356830)
6. 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; PMID:3282695; http://dx.doi.org/10.1007/BF00365754.
7. Henriques JA, Moustacchi E. Isolation and characterization of pso mutants sensitive to photo-addition of psoralen derivatives in Saccharomyces cerevisiae. Genetics 1980;95:273-88; PMID:7009316. (Pubitemid 11235201)
8. Ruhland A, Kircher M, Wilborn F, Brendel M. A yeast mutant specifically sensitive to bifunctional alkyla-tion. Mutat Res 1981;91:457-62; PMID:7027037; http://dx.doi.org/10.1016/0165-7992 (81) 90052-X. (Pubitemid 11095464)
9. Ruhland A, Haase E, Siede W, Brendel M. Isolation of yeast mutants sensitive to the bifunctional alkyl-ating agent nitrogen mustard. Mol Gen Genet 1981;181:346-51; PMID:7017347; http://dx.doi.org/10.1007/BF00425609. (Pubitemid 11073640)
10. McHugh PJ, Sones WR, Hartley JA. Repair of intermediate structures produced at DNA interstrand cross-links in Saccharomyces cerevisiae. Mol Cell Biol 2000;20:3425-33; PMID:10779332; http://dx.doi.org/10.1128/MCB.20.10.3425- 3433.2000. (Pubitemid 30243888)
11. De Silva IU, McHugh PJ, Clingen PH, Hartley JA. Defining the roles of nucleotide excision repair and recombination in the repair of DNA inter-strand cross-links in mammalian cells. Mol Cell Biol 2000;20:7980-90; PMID:11027268; http://dx.doi.org/10.1128/MCB.20.21.7980-7990.2000.
12. Wang AT, Sengerová B, Cattell E, Inagawa T, Hartley JM, Kiakos K, et al. Human SNM1A and XPF-ERCC1 collaborate to initiate DNA inter-strand cross-link repair. Genes Dev 2011;25:1859-70; PMID:21896658; http://dx.doi.org/10.1101/g a d.1569 9 211.
13. Callebaut I, Moshous D, Mornon JP, de Villartay JP. Metallo-β- lactamase fold within nucleic acids processing enzymes: the β-CASP family. Nucleic Acids Res 2002;30:3592-601; PMID:12177301; http://dx.doi.org/10.1093/ nar/gk f470. (Pubitemid 34919215)
14. Aravind L, Walker DR, Koonin E V. Conserved domains in DNA repair proteins and evolution of repair systems. Nucleic Acids Res 1999;27:1223-42; PMID:9973609; http://dx.doi.org/10.1093/nar/27.5.1223. (Pubitemid 29206430)
15. Dominski Z. Nucleases of the metallo-beta-lac-tamase family and their role in DNA and RNA metabolism. Crit Rev Biochem Mol Biol 2007;42:67-93; PMID:17453916; http://dx.doi.org/10.1080/10409230701279118. (Pubitemid 46598189)
16. Cattell E, Sengerová B, McHugh PJ. The SNM1/Pso2 family of ICL repair nucleases: from yeast to man. Environ Mol Mutagen 2010;51:635-45; PMID:20175117.
17. Li X, Hejna J, Moses RE. The yeast Snm1 protein is a DNA 5'-exonuclease. DNA Repair (Amst) 2005;4:163-70; PMID:15590324; http://dx.doi.org/10.1016/j. dnarep. 2004.08.012. (Pubitemid 39601404)
18. Tiefenbach T, Junop M. Pso2 (SNM1) is a DNA structure-specific endonuclease. Nucleic Acids Res 2012;40:2131-9; PMID:22102580; http://dx.doi.org/10.1093/nar/gkr1059.
19. Li X, Moses RE. The β-lactamase motif in Snm1 is required for repair of DNA double-strand breaks caused by interstrand crosslinks in S. cerevisiae. DNA Repair (Amst) 2003;2:121-9; PMID:12509272; http://dx.doi.org/10.1016/S1568- 7864 (02) 00192-1. (Pubitemid 35435443)
20. Bonatto D, Revers LF, Brendel M, Henriques JA. The eukaryotic Pso2/Snm1/Artemis proteins and their function as genomic and cellular caretakers. Braz J Med Biol Res 2005;38:321-34; PMID:15761611; http://dx.doi.org/10.1590/S0100-879X2005000300002. (Pubitemid 40485171)
21. Dronkert MLG, de Wit J, Boeve M, Vasconcelos ML, van Steeg H, Tan TLR, et al. Disruption of mouse SNM1 causes increased sensitivity to the DNA inter-strand cross-linking agent mitomycin C. Mol Cell Biol 2000;20:4553-61; PMID:10848582; http://dx.doi.org/10.1128/MCB.20.13.4553-4561.2000. (Pubitemid 30396103)
22. Ma Y, Pannicke U, Schwarz K, Lieber MR. Hairpin opening and overhang processing by an Artemis/DNA-dependent protein kinase complex in nonho-mologous end joining and V (D) J recombination. Cell 2002;108:781-94; PMID:11955432; http://dx.doi.org/10.1016/S0092-8674 (02) 00671-2. (Pubitemid 34327530)
23. Riballo E, Kühne M, Rief N, Doherty A, Smith GC, Recio MJ, et al. A pathway of double-strand break rejoining dependent upon ATM, Artemis, and proteins locating to γ-H2AX foci. Mol Cell 2004;16:715-24; PMID:15574327; http://dx.doi.org/10.1016/j.molcel.2004.10.029. (Pubitemid 39586530)
24. Ishiai M, Kimura M, Namikoshi K, Yamazoe M, Yamamoto K, Arakawa H, et al. DNA cross-link repair protein SNM1A interacts with PIAS1 in nuclear focus formation. Mol Cell Biol 2004;24:10733-41; PMID:15572677; http://dx.doi.org/10. 1128/MCB.24.24.10733-10741.2004. (Pubitemid 39603130)
25. 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;23:8611-8; PMID:15467758; http://dx.doi.org/10.1038/ sj.onc.1207895. (Pubitemid 39576468)
26. Bae JB, Mukhopadhyay SS, Liu L, Zhang N, Tan J, Akhter S, et al. Snm1B/Apollo mediates replication fork collapse and S Phase checkpoint activation in response to DNA interstrand cross-links. Oncogene 2008;27:5045-56; PMID:18469862; http://dx.doi.org/10.1038/onc.2008.139.
27. Mason JM, Sekiguchi JM. Snm1B/Apollo functions in the Fanconi anemia pathway in response to DNA interstrand crosslinks. Hum Mol Genet 2011;20:2549-59; PMID:21478198; http://dx.doi.org/10.1093/hmg/ddr153.
28. Hazrati A, Ramis-Castelltort M, Sarkar S, Barber LJ, Schofield CJ, Hartley JA, et al. Human SNM1A suppresses the DNA repair defects of yeast pso2 mutants. DNA Repair (Amst) 2008;7:230-8; PMID:18006388; http://dx.doi.org/10. 1016/j. dnarep. 2007.09.013.
29. Su X, Huang J. The Fanconi anemia pathway and DNA interstrand cross-link repair. Protein Cell 2011;2:704-11; PMID:21948210; http://dx.doi.org/10.1007/ s13238-011-1098-y.
30. Deans AJ, West SC. DNA interstrand crosslink repair and cancer. Nat Rev Cancer 2011;11:467-80; PMID:21701511; http://dx.doi.org/10.1038/nrc3088.
31. Joenje H, Patel KJ. The emerging genetic and molecular basis of Fanconi anaemia. Nat Rev Genet 2001;2:446-57; PMID:11389461; http://dx.doi.org/10.1038/ 35076590. (Pubitemid 33673411)
32. Sengerová B, Wang AT, McHugh PJ. Orchestrating the nucleases involved in DNA interstrand crosslink (ICL) repair. Cell Cycle 2011;10:3999-4008; PMID:22101340; http://dx.doi.org/10.4161/cc.10.23.18385.
33. Palle K, Vaziri C. Rad18 E3 ubiquitin ligase activity mediates Fanconi anemia pathway activation and cell survival following DNA Topoisomerase 1 inhibition. Cell Cycle 2011;10:1625-38; PMID:21478670; http://dx.doi.org/10. 4161/cc.10.10.15617.
34. Wang W. Emergence of a DNA-damage response network consisting of Fanconi anaemia and BRCA proteins. Nat Rev Genet 2007;8:735-48; PMID:17768402; http://dx.doi.org/10.1038/n r g 2159. (Pubitemid 47429206)
35. Matsushita N, Kitao H, Ishiai M, Nagashima N, Hirano S, Okawa K, et al. A FancD2-monoubiquitin fusion reveals hidden functions of Fanconi anemia core complex in DNA repair. Mol Cell 2005;19:841-7; PMID:16168378; http://dx.doi.org/10.1016/j. molcel.2005.08.018. (Pubitemid 41316677)
36. Niedernhofer LJ. The Fanconi anemia signalosome anchor. Mol Cell 2007;25:487-90; PMID:17317622; http://dx.doi.org/10.1016/j.molcel.2007.02.002. (Pubitemid 46274451)
37. Ciccia A, McDonald N, West SC. Structural and functional relationships of the XPF/MUS81 family of proteins. Annu Rev Biochem 2008;77:259-87; PMID:18518821; http://dx.doi.org/10.1146/annurev. biochem.77.070306.102408.
38. Ciccia A, Ling C, Coulthard R, Yan Z, Xue Y, Meetei AR, et al. Identification of FAAP24, a Fanconi anemia core complex protein that interacts with FANCM. Mol Cell 2007;25:331-43; PMID:17289582; http://dx.doi.org/10.1016/j. molcel.2007.01.003. (Pubitemid 46206138)
39. Deans AJ, West SC. FANCM connects the genome instability disorders Bloom's Syndrome and Fanconi Anemia. Mol Cell 2009;36:943-53; http://dx.doi.org/10.1016/j.molcel.2009.12.006.
40. Gari K, Décaillet C, Delannoy M, Wu L, Constantinou A. Remodeling of DNA replication structures by the branch point translocase FANCM. Proc Natl Acad Sci USA 2008;105:16107-12; PMID:18843105; http://dx.doi.org/10.1073/pnas. 0804777105.
41. Cybulski KE, Howlett NG. FANCP/SLX4: a Swiss army knife of DNA interstrand crosslink repair. Cell Cycle 2011;10:1757-63; PMID:21527828; http://dx.doi.org/10.4161/cc.10.11.15818.
42. Kim Y, Lach FP, Desetty R, Hanenberg H, Auerbach AD, Smogorzewska A. Mutations of the SLX4 gene in Fanconi anemia. Nat Genet 2011;43:142-6; PMID:21240275; http://dx.doi.org/10.1038/ng.750.
43. Yamamoto KN, Kobayashi S, Tsuda M, Kurumizaka H, Takata M, Kono K, et al. Involvement of SLX4 in interstrand cross-link repair is regulated by the Fanconi anemia pathway. Proc Natl Acad Sci USA 2011;108:6492-6; PMID:21464321; http://dx.doi.org/10.1073/pnas.1018487108.
44. Muñoz IM, Hain K, Déclais AC, Gardiner M, Toh GW, Sanchez-Pulido L, et al. Coordination of structure-specific nucleases by human SLX4/BTBD12 is required for DNA repair. Mol Cell 2009;35:116-27; PMID:19595721; http://dx.doi.org/10.1016/j.mol-cel.2009.06.020.
45. Collis SJ, Barber LJ, Ward JD, Martin JS, Boulton SJ. C. elegans FANCD2 responds to replication stress and functions in interstrand cross-link repair. DNA Repair (Amst) 2006;5:1398-406; PMID:16914393; http://dx.doi.org/10.1016/j. dnarep. 2006.06.010. (Pubitemid 44573937)
46. Petalcorin MI, Sandall J, Wigley DB, Boulton SJ. CeBRC-2 stimulates D-loop formation by RAD-51 and promotes DNA single-strand annealing. J Mol Biol 2006;361:231-42; PMID:16843491; http://dx.doi.org/10.1016/j.jmb.2006.06.020. (Pubitemid 44092785)
47. Youds JL, Barber LJ, Ward JD, Collis SJ, O'Neil NJ, Boulton SJ, et al. DOG-1 is the Caenorhabditis elegans BRIP1/FANCJ homologue and functions in interstrand cross-link repair. Mol Cell Biol 2008;28:1470-9; PMID:18086896; http://dx.doi. or g/10.11 2 8/M C B.016 41-0 7.
48. Marek LR, Bale AE. Drosophila homologs of FANCD2 and FANCL function in DNA repair. DNA Repair (Amst) 2006;5:1317-26; PMID:16860002; http://dx.doi.org/10.1016/j.dnarep. 2006.05.044. (Pubitemid 44573930)
49. Lo T, Pellegrini L, Venkitaraman AR, Blundell TL. Sequence fingerprints in BRCA2 and RAD51: implications for DNA repair and cancer. DNA Repair (Amst) 2003;2:1015-28; PMID:12967658; http://dx.doi.org/10.1016/S1568-7864 (03) 00097-1. (Pubitemid 37088163)
50. Meetei AR, Medhurst AL, Ling C, Xue Y, Singh TR, Bier P, et al. A human ortholog of archaeal DNA repair protein Hef is defective in Fanconi anemia complementation group M. Nat Genet 2005;37:958-63; PMID:16116422; http://dx.doi.org/10.1038/ng1626. (Pubitemid 43086152)
51. Sun W, Nandi S, Osman F, Ahn JS, Jakovleska J, Lorenz A, 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;32:118-28; PMID:18851838; http://dx.doi.org/10.1016/j.molcel.2008.08.024.
52. Patel KJ, Joenje H. Fanconi anemia and DNA replication repair. DNA Repair (Amst) 2007;6:885-90; PMID:17481966; http://dx.doi.org/10.1016/j. dnarep. 2007.02.002. (Pubitemid 46880469)
53. McVey M. Strategies for DNA interstrand crosslink repair: insights from worms, flies, frogs, and slime molds. Environ Mol Mutagen 2010;51:646-58; PMID:20143343.
54. Daee DL, Ferrari E, Longerich S, Zheng XF, Xue X, Branzei D, et al. Rad5-dependent DNA repair functions of the Saccharomyces cerevisiae FANCM homolog Mph1. J Biol Chem 2012;287:26563-75; PMID:22696213; http://dx.doi.org/ 10.1074/jbc. M112.369918.
55. Ward T, Dudášová Z, Sarkar S, Bhide M, Vlasáková D, Chovanec M, et al. Components of a Fanconi-like pathway control Pso2-independent DNA interstrand crosslink repair in yeast. PLoS Genet 2012;8:e1002884; PMID:22912599; http://dx.doi.org/10.1371/journal.pgen. 1002884.
56. Yang H, Zhang T, Tao Y, Wu L, Li HT, Zhou JQ, et al. Saccharomyces cerevisiae MHF complex structurally resembles the histones (H3-H4) 2 hetero-tetramer and functions as a heterotetramer. Structure 2012;20:364-70; PMID:22325783; http://dx.doi.org/10.1016/j.str.2011.12.012.
57. Barber LJ, Ward TA, Hartley JA, McHugh PJ. DNA interstrand cross-link repair in the Saccharomyces cere-visiae cell cycle: overlapping roles for PSO2 (SNM1) with MutS factors and EXO1 during S phase. Mol Cell Biol 2005;25:2297-309; PMID:15743825; http://dx.doi.org/10.1128/MCB.25.6.2297-2309. 2005. (Pubitemid 40354626)