Advances in understanding the complex mechanisms of DNA inter strand cross-link repair

Cold Spring Harbor Perspectives in Medicine

Volumn 3, Issue 10, 2013, Pages

  Clauson, Cheryl ^a   Schärer, Orlando D ^b   Niedernhofer, Laura ^a,c  

^a UNIVERSITY OF PITTSBURGH   (United States)

^b STONY BROOK UNIVERSITY   (United States)

^c SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CROSS LINKING REAGENT; DNA; DNA BINDING PROTEIN; FANCONI ANEMIA PROTEIN;

BIOLOGICAL MODEL; DNA DAMAGE; DNA REPAIR; DNA REPLICATION; GENETIC RECOMBINATION; GENETICS; HOMOLOGOUS RECOMBINATION; HUMAN; METABOLISM; PHYSIOLOGY; REVIEW; SIGNAL TRANSDUCTION;

CROSS-LINKING REAGENTS; DNA; DNA DAMAGE; DNA REPAIR; DNA REPLICATION; DNA-BINDING PROTEINS; FANCONI ANEMIA COMPLEMENTATION GROUP PROTEINS; HOMOLOGOUS RECOMBINATION; HUMANS; MODELS, GENETIC; RECOMBINATION, GENETIC; SIGNAL TRANSDUCTION;

EID: 84885024085     PISSN: None     EISSN: 21571422     Source Type: Journal    
DOI: 10.1101/cshperspect.a012732     Document Type: Article

References (160)

1. Abraham J, Lemmers B, Hande MP, Moynahan ME, Chah-wan C, Ciccia A, Essers J, Hanada K, Chahwan R, Khaw AK, et al. 2003. Eme1 is involved in DNA damage processing and maintenance of genomic stability in mammalian cells. EMBO J 22: 6137-6147.
2. Albertella MR, Green CM, Lehmann AR, O'Connor MJ. 2005. A role for polymerase h in the cellular tolerance to cisplatin-induced damage. Cancer Res 65: 9799-9806.
3. Al-Minawi AZ, Lee Y-F, Håkansson D, Johansson F, Lundin C, Saleh-Gohari N, Schultz N, Jenssen D, Bryant HE, Meuth M, et al. 2009. The ERCC1/XPF endonuclease is required for completion of homologous recombination at DNA replication forks stalled by inter-strand cross links. Nucleic Acids Res 37: 6400-6413.
4. Andersen SL, Bergstralh DT, Kohl KP, LaRocque JR, Moore CB, Sekelsky J. 2009. Drosophila MUS312 and the verte-brateortholog BTBD12 interact with DNA structure-specific endonucleases in DNA repair and recombination. Mol Cell 35: 128-135.
5. Andreassen PR, D'Andrea AD, Taniguchi T. 2004. ATR couples FANCD2 monoubiquitination to the DNA-damage response. Genes Dev 18: 1958-1963.
6. Auerbach AD. 2009. Fanconi anemia and its diagnosis. Mu-tat Res 668: 4-10.
7. Ben-Yehoyada M, Wang LC, Kozekov ID, Rizzo CJ, Gottes-man ME, Gautier J. 2009. Checkpoint signaling from a single DNA inter strand crosslink. Mol Cell 35: 704-715.
8. Berardini M, Mackay W, Loechler EL. 1997. Evidence for a recombination-independent pathway for the repair of DNA inter strand cross-links based on a site-specific study with nitrogen mustard. Biochemistry 36: 3506-3513.
9. Berardini M, Foster PL, Loechler EL. 1999. DNA polymerase II (polB) is involved in a new DNA repair pathway for DNA inter strand cross-links in Escherichia coli. J Bacteriol 181: 2878-2882.
10. 0 to the cross-linked base and removes a 22- to 28-nucleotide-long damage-free strand. Mol Cell Biol 17: 6822-6830.
11. Bhagwat N, Olsen AL, Wang AT, Hanada K, Stuckert P, Ka-naar R, D'Andrea A, Niedernhofer LJ, McHugh PJ. 2009. XPF-ERCC1 participates in the Fanconi anemia pathway of cross-link repair. Mol Cell Biol 29: 6427-6437.
12. Bogliolo M, Schuster B, Stoepker C, Derkunt B, Su Y, Raams A, Trujillo JP, Minguillon J, Ramirez MJ, Pujol R, et al. 2013. Mutations in ERCC4, encoding the DNA-repair endonuclease XPF, cause Fanconi anemia. Am J Human Genet 92: 800-806.
13. Bunting SF, Callen E, Kozak ML, Kim JM, Wong N, Lopez-Contreras AJ, Ludwig T, Baer R, Faryabi RB, Malhowski A, et al. 2012. BRCA1 functions independentlyof homologous recombination in DNA inter strand crosslink repair. Mol Cell 46: 125-135.
14. Cattell E, Sengerová B, McHugh PJ. 2010. The SNM1/Pso2 family of ICL repair nucleases: From yeast to man. Environ Mol Mutagen 51: 635-645.
15. Chen X-B, Melchionna R, Denis C-M, Gaillard P-HL, Bla-sina A, Van de Weyer I, Boddy MN, Russell P, Vialard J, McGowan CH.2001.Human Mus81-associated endonu-clease cleaves Holliday junctions in vitro. Mol Cell 8: 1117-1127.
16. Chen Y-w, Cleaver JE, Hanaoka F, Chang C-f, Chou K-m. 2006. A novel role of DNA polymerase h in modulating cellular sensitivity to chemotherapeutic agents. Mol Can cer Res 4: 257-265.
17. Cherry JM, Hong EL, Amundsen C, Balakrishnan R, Binkley G, Chan ET, Christie KR, Costanzo MC, Dwight SS, Engel SR, et al. 2011. Saccharomyces Genome Database: The genomics resource of budding yeast. Nucleic Acids Res 40: D169-D179.
18. Ciccia A, Ling C, Coulthard R, Yan Z, Xue Y, Meetei AR, Laghmani EH, Joenje H, McDonald N, de Winter JP, et al. 2007. Identification of FAAP24, a Fanconi anemia core complex protein that interacts with FANCM. Mol Cell 25: 331-343.
19. Cimino GD, Gamper HB, Isaacs ST, Hearst JE. 1985. Psora-lens as photoactive probes of nucleic acid structure and function: Organic chemistry, photochemistry, and biochemistry. Annu Rev Biochem 54: 1151-1193.
20. Cohn MA, Kowal P, Yang K, Haas W, Huang TT, Gygi SP, D'Andrea AD. 2007. A UAF1-containing multisubunit protein complex regulates the Fanconi anemia pathway. Mol Cell 28: 786-797.
21. Collis SJ, Barber LJ, Ward JD, Martin JS, Boulton SJ. 2006. C. elegans FANCD2 responds to replication stress and functions in inter strand cross-link repair. DNA Repair (Amst) 5: 1398-1406.
22. Crossan GP, van der Weyden L, Rosado IV, Langevin F, Gail-lard P-HL, McIntyre RE, Gallagher F, Kettunen MI, Lewis DY, Brindle K, et al. 2011. Disruption of mouse Slx4, a regulator of structure-specific nucleases, phenocopies Fanconi anemia. Nat Genet 43: 147-152.
23. Cui B, Johnson SP, Bullock N, Ali-Osman F, Bigner DD, Friedman HS. 2009. Bifunctional DNA alkylator 1,3-bis(2-chloroethyl)-1-nitrosourea activates the ATR-Chk1 pathway independently of the mismatch repair pathway. Mol Pharmacol 75: 1356-1363.
24. Deans AJ, West SC. 2009. FANCM connects the genome instability disorders Bloom's syndrome and Fanconi anemia. Mol Cell 36: 943-953.
25. Deans AJ, West SC. 2011. DNA inter strand crosslink repair and cancer. Nat Rev Cancer 11: 467-480.
26. dos Santos LS, Van Houten B. 2010. DNA repair database (https://dnapittcrew.upmc.com). University of Pittsburgh, Pittsburgh, PA.
27. Duquette ML, Zhu Q, Taylor ER, Tsay AJ, Shi LZ, Berns MW, McGowan CH. 2012. CtIP is required to initiate replication-dependent inter strand crosslink repair. PLoS Genet 8: e1003050.
28. Dutta S, Chowdhury G, Gates KS. 2007. Inter strand cross links generated byabasic sites in duplex DNA. JAm Chem Soc 129: 1852-1853.
29. Enoiu M, Jiricny J, Schärer OD. 2012. Repair of cisplatin-induced DNA inter strand cross links by a replication-independent pathway involving transcription-coupled repair and translesion synthesis. Nucleic Acids Res 40: 8953-8964.
30. Fekairi S, Scaglione S, Chahwan C, Taylor ER, Tissier A, Coulon S, Dong MQ, Ruse C, Yates JR 3rd, Russell P, et al. 2009. Human SLX4 is a Holliday junction resolvase subunit that binds multiple DNA repair/recombination endonucleases. Cell 138: 78-89.
31. 3 of deoxycytidine on opposite strands of duplex DNA. Cancer Res 59: 4363-4368.
32. Gan GN, Wittschieben JP, Wittschieben BO, Wood RD. 2008. DNA polymerase z (pol z) in higher eukaryotes. Cell Res 18: 174-183.
33. Garaycoechea JI, Crossan GP, Langevin F, Daly M, Arends MJ, Patel KJ. 2012. Genotoxic consequences of endogenous aldehydes on mouse haematopoietic stem cell function. Nature 489: 571-575.
34. Gari K, Décaillet C, Delannoy M, Wu L, Constantinou A. 2008a. Remodeling of DNA replication structures by the branch point translocase FANCM. Proc Natl Acad Sci 105: 16107-16112.
35. Gari K, Décaillet C, Stasiak AZ, Stasiak A, Constantinou A. 2008b. The Fanconi anemia protein FANCM can promote branch migration of Holliday junctions and replication forks. Mol Cell 29: 141-148.
36. Grossmann KF, Ward AM, Matkovic ME, Folias AE, Moses RE. 2001. S cerevisiae has three pathways for DNA inter-strand crosslink repair. Mutat Res 487: 73-83.
37. Guainazzi A, Schärer OD. 2010. Using synthetic DNA inter-strand cross links to elucidate repair pathways and identify new therapeutic targets for cancer chemotherapy. Cell Mol Life Sci 67: 3683-3697.
38. Guainazzi A, Campbell AJ, Angelov T, Simmerling C, Schärer OD. 2010. Synthesis and molecular modeling of a nitrogen mustard DNA inter strand crosslink. Eur J Chem 16: 12100-12103.
39. Guan L, Greenberg MM. 2009. DNA inter strand cross-link formation by the 1,4-dioxobutane a basic lesion. J Am Chem Soc 131: 15225-15231.
40. Hanada K, Budzowska M, Modesti M, Maas A, Wyman C, Essers J, Kanaar R. 2006. The structure-specific endonu-clease Mus81-Eme1 promotes conversion of inter strand DNA cross links into double-strands breaks. EMBO J 25: 4921-4932.
41. Hanada K, Budzowska M, Davies SL, van Drunen E, Oni-zawa H, Beverloo HB, Maas A, Essers J, Hickson ID, Kanaar R. 2007. The structure-specific endonuclease Mus81 contributes to replication restart by generating double-strand DNA breaks. Nat Struct Mol Biol 14: 1096-1104.
42. Hanlon Newell AE, Hemphill A, Akkari YM, Hejna J, Moses RE, Olson SB. 2008. Loss of homologous recombination or non-homologous end-joining leads to radial formation following DNA inter strand crosslink damage. Cyto-genet Genome Res 121: 174-180.
43. Harris TW, Antoshechkin I, Bieri T, Blasiar D, Chan J, Chen WJ, De La Cruz N, Davis P, Duesbury M, Fang R, et al. 2010. WormBase: A comprehensive resource for nema- tode research. Nucleic Acids Res 38: D463-D467.
44. 0-deoxyguanosines. J Organ Chem 65: 2959-2964.
45. Hazrati A, Ramis-Castelltort M, Sarkar S, Barber LJ, Scho-field CJ, Hartley JA, McHugh PJ. 2008. Human SNM1A suppresses the DNA repair defects of yeast pso2 mutants. DNA Rep 7: 230-238.
46. Hentschel S, Alzeer J, Angelov T, Schärer OD, Luedtke NW. 2012. Synthesis of DNA inter strand cross-links using a photocaged nucleobase. Angew Chem Int Ed Engl 51: 3466-3469.
47. Hlavin EM, Smeaton MB, Noronha AM, Wilds CJ, Miller PS. 2010. Cross-link structure affects replication-independent DNA inter strand cross-link repair in mammalian cells. Biochemistry 49: 3977-3988.
48. Ho TV, Schärer OD. 2010. Translesion DNA synthesis poly-merases in DNA inter strand crosslink repair. Environ Mol Mutagen 51: 552-566.
49. Ho TV, Guainazzi A, Derkunt SB, Enoiu M, Schärer OD. 2011. Structure-dependent bypass of DNA inter strand cross links by translesion synthesis polymerases. Nucleic Acids Res 39: 7455-7464.
50. Huang M, D'Andrea AD. 2010. A new nuclease member of the FAN club. Nat Struct Mol Biol 17: 926-928.
51. Huang H, Kozekov ID, Kozekova A, Wang H, Lloyd RS, Rizzo CJ, Stone MP. 2010a. DNA cross-link induced by trans-4-hydroxynonenal. Environ Mol Mutagen 51: 625- 634.
52. Huang M, Kim JM, Shiotani B, Yang K, Zou L, D'Andrea AD. 2010b. The FANCM/FAAP24 complex is required for the DNA inter strand crosslink-induced checkpoint response. Mol Cell 39: 259-268.
53. Jachymczyk WJ, von Borstel RC, Mowat MR, Hastings PJ. 1981. Repairof inter strand cross-links in DNA of Saccha-romyces cerevisiae requires two systems for DNA repair: the RAD3 system and the RAD51 system. Mol Gen Genet 182: 196-205.
54. Jamieson ER, Lippard SJ. 1999. Structure, recognition, and processing of cisplatin-DNA adducts. Chem Rev 99: 2467-2498.
55. 0-CAp sequences in duplex DNA. J Am Chem Soc 135: 1015-1025.
56. Johnson LAA, Malayappan B, Tretyakova N, Campbell C, MacMillan ML, Wagner JE, Jacobson PA. 2012b. Formation of cyclophosphamide specific DNA adducts in he-matological diseases. Pediatr Blood Cancer 58: 708-714.
57. Kashiyama K, Nakazawa Y, Pilz DT, Guo C, Shimada M, Sasaki K, Fawcett H, Wing JF, Lewin SO, Carr L, et al. 2013. Malfunction of nuclease ERCC1-XPF results in diverse clinical manifestations and causes Cockayne syndrome, xeroderma pigmentosum, and Fanconi anemia. Am J Hum Genet 92: 807-819.
58. Kim JM, Parmar K, Huang M, Weinstock DM, Ruit CA, Kutok JL, D'Andrea AD. 2009. Inactivation of murine Usp1 results in genomic instability and a Fanconi anemia phenotype. Dev Cell 16: 314-320.
59. Kim Y, Lach FP, Desetty R, Hanenberg H, Auerbach AD, Smogorzewska A. 2011. Mutations of the SLX4 gene in Fanconi anemia. Nat Genet 43: 142-146.
60. Kim H, Yang K, Dejsuphong D, D'Andrea AD. 2012. Regulation of Rev1 by the Fanconi anemia core complex. Nat Struct Mol Biol 19: 164-170.
61. Kim Y, Spitz GS, Veturi U, Lach FP, Auerbach AD, Smogor-zewska A. 2013. Regulation of multiple DNA repair pathways by the Fanconi anemia protein SLX4. Blood 121: 54-63.
62. 0-CG. J Am Chem Soc 114: 4021-4027.
63. Kitao H, Yamamoto K, Matsushita N, Ohzeki M, Ishiai M, Takata M. 2006. Functional interplay between BRCA2/ FancD1 and FancC in DNA repair. J Biol Chem 281: 21312-21320.
64. 2-deoxyguanosine inter strand cross links by human DNA polymerases h and i. Chem Res Toxicol 25: 755-762.
65. Knipscheer P, Räschle M, Smogorzewska A, Enoiu M, Ho TV, Schärer OD, Elledge SJ, Walter JC. 2009. The Fanconi anemia pathway promotes replication-dependent DNA inter strand cross-link repair. Science 326: 1698-1701.
66. Kratz K, Schöpf B, Kaden S, Sendoel A, Eberhard R, Lade-mann C, Cannavó E, Sartori AA, Hengartner MO, Jiricny J. 2010. Deficiency of FANCD2-associated nuclease KIAA1018/FAN1 sensitizes cells to inter strand crosslink-ing agents. Cell 142: 77-88.
67. Kumari A, Minko IG, Harbut MB, Finkel SE, Goodman MF, Lloyd RS. 2008. Replication bypass of inter strand crosslink intermediates by Escherichia coli DNA polymerase IV. J Biol Chem 283: 27433-27437.
68. Larimer FW, Perry JR, Hardigree AA. 1989. The REV1 gene of Saccharomyces cerevisiae: Isolation, sequence, and functional analysis. J Bacteriol 171: 230-237.
69. Lee KY, Chung KY, Koo HS. 2010. The involvement of FANCM, FANCI, and checkpoint proteins in the inter-strand DNA crosslink repair pathway is conserved in C. elegans. DNA Rep 9: 374-382.
70. Lestini R, Duan Z, Allers T. 2010. The archaeal Xpf/Mus81/ FANCM homolog Hef and the Holliday junction resol-vase Hjc define alternative pathways that are essential for cell viability in Haloferax volcanii. DNA Rep 9: 994-1002.
71. Leung JWC, Wang Y, Fong KW, Huen MSY, Li L, Chen J. 2012. Fanconi anemia (FA) binding protein FAAP20 stabilizes FA complementation group A (FANCA) and participates in inter strand cross-link repair. Proc Natl Acad Sci 109: 4491-4496.
72. Léveillé F, Ferrer M, Medhurst AL, Laghmani EH, Rooimans MA, Bier P, Steltenpool J, Titus TA, Postlethwait JH, Hoatlin ME, et al. 2006. The nuclear accumulation of the Fanconi anemia protein FANCE dependsonFANCC. DNA Rep 5: 556-565.
73. Liu N, Lamerdin JE, Tebbs RS, Schild D, Tucker JD, Shen MR, Brookman KW, Siciliano MJ, Walter CA, Fan W, et al. 1998. XRCC2 and XRCC3, new human Rad51-family members, promote chromosome stability and protect against DNA cross-links and other damages. Mol Cell 1: 783-793.
74. Liu T, Ghosal G, Yuan J, Chen J, Huang J. 2010. FAN1 acts with FANCI-FANCD2 to promote DNA inter strand cross-link repair. Science 329: 693-696.
75. Long DT, Räschle M, Joukov V, Walter JC. 2011. Mechanism of RAD51-dependent DNA inter strand cross-link repair. Science 333: 84-87.
76. MacKay C, Déclais A-C, Lundin C, Agostinho A, Deans AJ, MacArtney TJ, Hofmann K, Gartner A, West SC, Helleday T, et al. 2010. Identification of KIAA1018/FAN1, a DNA repair nuclease recruited to DNA damage by mono-ubiquitinated FANCD2. Cell 142: 65-76.
77. Magana-Schwencke N, Henriques JA, Chanet R, Moustac-chi E. 1982. The fate of 8-methoxypsoralen photoin-duced cross links in nuclear and mitochondrial yeast DNA: comparison of wild-type and repair-deficient strains. Proc Natl Acad Sci 79: 1722-1726.
78. Majumdar A, Muniandy PA, Liu J, Liu JL, Liu ST, Cuenoud B, Seidman MM. 2008. Targeted gene knock in and sequence modulation mediated by a psoralen-linked triplex-forming oligonucleotide. J Biol Chem 283: 11244- 11252.
79. Mason JM, Sekiguchi JM. 2011. Snm1B/Apollo functions in the Fanconi anemia pathway in response to DNA inter strand cross links. Hum Mol Genet 20: 2549-2559.
80. McCabe KM, Hemphill A, Akkari Y, Jakobs PM, Pauw D, Olson SB, Moses RE, Grompe M. 2008. ERCC1 is required for FANCD2 focus formation. Mol Genet Metab 95: 66-73.
81. McHugh PJ, Sarkar S. 2006. DNA inter strand cross-link repair in the cell cycle: A critical role for polymerase z in G1 phase. Cell Cycle 5: 1044-1047.
82. McHugh PJ, Sones WR, Hartley JA. 2000. Repair of intermediate structures produced at DNA inter strand cross links in Saccharomyces cerevisiae. Mol Cell Biol 20: 3425-3433.
83. McQuilton P, StPierre SE, Thurmond J, Consortium TF. 2012. FlyBase 101-the basics of navigating FlyBase. Nucleic Acids Res 40: D706-D714.
84. Meier B, Barber LJ, Liu Y, Shtessel L, Boulton SJ, Gartner A, Ahmed S.2009. The MRT-1 nuclease isrequired for DNA crosslink repair and telomerase activity in vivo in Caeno-rhabditis elegans. EMBO J 28: 3549-3563.
85. 0-GNC sequences in duplex DNA fragments. J Am Chem Soc 112: 2459-2460.
86. 2-guanine inter strand cross-links. J Biol Chem 283: 17075-17082.
87. Minko IG, Yamanaka K, Kozekov ID, Kozekova A, Indiani C, O'Donnell ME, Jiang Q, Goodman MF, Rizzo CJ, Lloyd RS. 2008b. Replication bypass of the acrolein-mediated deoxyguanine DNA-peptide cross-links by DNA poly-merases of the DinB family. Chem Res Toxicol 21: 1983-1990.
88. Misra RR, Vos JM. 1993. Defective replication of psoralen adducts detected at the gene-specific level in xeroderma pigmentosum variant cells. Mol Cell Biol 13: 1002-1012.
89. Mogi S, Butcher CE, Oh DH. 2008. DNA polymerase h reduces the g-H2AX response to psoralen inter strand cross links in human cells. Exp Cell Res 314: 887-895.
90. Moldovan G-L, Madhavan MV, Mirchandani KD, McCaffrey RM, Vinciguerra P, D'Andrea AD. 2010. DNA poly-merase POLN participates in cross-link repair and homologous recombination. Mol Cell Biol 30: 1088-1096.
91. Mu D, Bessho T, Nechev LV, Chen DJ, Harris TM, Hearst JE, Sancar A. 2000. DNA inter strand cross-links induce futile repair synthesis in mammalian cell extracts. Mol Cell Biol 20: 2446-2454.
92. Muniandy PA, Thapa D, Thazhathveetil AK, Liu S-t, Seidman MM. 2009. Repair of laser-localized DNA inter-strand cross-links in G1 phase mammalian cells. J Biol Chem 284: 27908-27917.
93. Muñoz IM, Hain K, Déclais A-C, Gardiner M, Toh GW, Sanchez-Pulido L, Heuckmann JM, Toth R, Macartney T, Eppink B, et al. 2009. Coordination of structure-specific nucleases by human SLX4/BTBD12 is required for DNA repair. Mol Cell 35: 116-127.
94. Niedernhofer LJ. 2007. The Fanconi anemia signalosome anchor. Mol Cell 25: 487-490.
95. Niedernhofer LJ, Odijk H, Budzowska M, van Drunen E, Maas A, Theil AF, de Wit J, Jaspers NGJ, Beverloo HB, Hoeijmakers JHJ, et al. 2004. The structure-specific en-donuclease Ercc1-Xpf is required to resolve DNA inter-strand cross-link-induced double-strand breaks. Mol Cell Biol 24: 5776-5787.
96. Niedzwiedz W, Mosedale G, Johnson M, Ong CY, Pace P, Patel KJ. 2004. The Fanconi anaemia gene FANCC promotes homologous recombination and error-prone DNA repair. Mol Cell 15: 607-620.
97. Nijman SMB, Huang TT, Dirac AMG, Brummelkamp TR, Kerkhoven RM, D'Andrea AD, Bernards R. 2005. The deubiquitinating enzyme USP1 regulates the Fanconi anemia pathway. Mol Cell 17: 331-339.
98. Nishimura K, Ishiai M, Horikawa K, Fukagawa T, Takata M, Takisawa H, KanemakiMasato T. 2012. Mcm8 andMcm9 form a complex that functions in homologous recombination repair induced by DNA inter strand cross links. Mol Cell 47: 511-522.
99. Nojima K, Hochegger H, Saberi A, Fukushima T, Kikuchi K, Yoshimura M, Orelli BJ, Bishop DK, Hirano S, Ohzeki M, et al. 2005. Multiple repair pathways mediate tolerance to chemotherapeutic cross-linking agents invertebrate cells. Cancer Res 65: 11704-11711.
100. Oestergaard VH, Langevin F, Kuiken HJ, Pace P, Niedzwiedz W, Simpson LJ, Ohzeki M, Takata M, Sale JE, Patel KJ. 2007. Deubiquitination of FANCD2 is required for DNA crosslink repair. Mol Cell 28: 798-809.
101. Ojwang JO, Grueneberg DA, Loechler EL. 1989. Synthesis of a duplex oligonucleotide containing a nitrogen mustard inter strand DNA-DNA cross-link. Cancer Res 49: 6529- 6537.
102. Olive PL, Wlodek D, Banath JP. 1991. DNA double-strand breaks measured in individual cells subjected to gel elec-trophoresis. Cancer Res 51: 4671-4676.
103. Orelli B, McClendon TB, Tsodikov OV, Ellenberger T, Nie-dernhofer LJ, Schärer OD. 2010. The XPA-binding domain of ERCC1 is required for nucleotide excision repair but not other DNA repair pathways. J Biol Chem 285: 3705-3712.
104. Paz MM, Ladwa S, Champeil E, Liu Y, Rockwell S, Boamah EK, Bargonetti J, Callahan J, Roach J, Tomasz M. 2008. Mapping DNA adducts of mitomycin C and decarba-moyl mitomycin C in cell lines using liquid chromatog-raphy/electrospray tandem mass spectrometry. Chem Res Toxicol 21: 2370-2378.
105. Peng M, Litman R, Xie J, Sharma S, Brosh RM, Cantor SB. 2007. The FANCJ/MutLa interaction is required for correction of the cross-link response in FA-J cells. EMBO J 26: 3238-3249.
106. Penkner A, Portik-Dobos Z, Tang L, Schnabel R, Novatch-kova M, Jantsch V, Loidl J. 2007. Aconserved function for a Caenorhabditis elegans Com1/Sae2/CtIP protein ho-molog in meiotic recombination. EMBO J 26: 5071- 5082.
107. Phillips DH. 1996. DNA adducts in human tissues: Bio-markers of exposure to carcinogens in tobacco smoke. Environ Health Perspect 104 453-458.
108. Raha M, Wang G, Seidman MM, Glazer PM. 1996. Muta-genesis by third-strand-directed psoralen adducts in repair-deficient human cells: High frequency and altered spectrum in a xeroderma pigmentosum variant. Proc Natl Acad Sci 93: 2941-2946.
109. Räschle M, Knipscheer P, Enoiu M, Angelov T, Sun J, Griffith JD, Ellenberger TE, Schärer OD, Walter JC. 2008. Mechanism of replication-coupled DNA inter strand crosslink repair. Cell 134: 969-980.
110. Rink SM, Hopkins PB. 1995. A mechlorethamine-induced DNA inter strand cross-link bends duplex DNA. Biochemistry 34: 1439-1445.
111. 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.
112. Salewsky B, Schmiester M, Schindler D, Digweed M, De-muth I. 2012. The nuclease hSNM1B/Apollo is linked to the Fanconi anemia pathway via its interaction with FANCP/SLX4. Hum Mol Genet 21: 4948-4956.
113. Sarkar S, Davies AA, Ulrich HD, McHugh PJ. 2006. DNA inter strand crosslink repair during G1 involves nucleotide excision repair and DNA polymerase z. EMBO J 25: 1285-1294.
114. Sartori AA, Lukas C, Coates J, Mistrik M, Fu S, Bartek J, Baer R, Lukas J, Jackson SP. 2007. Human CtIP promotes DNA end resection. Nature 450: 509-514.
115. Sato K, Ishiai M, Toda K, Furukoshi S, Osakabe A, Tachi-wana H, Takizawa Y, Kagawa W, Kitao H, Dohmae N, et al. 2012. Histone chaperone activity of Fanconi anemia proteins, FANCD2 and FANCI, is required for DNA crosslink repair. EMBO J 31: 3524-3536.
116. Sengerová B, Allerston CK, Abu M, Lee SY, Hartley J, Kiakos K, Schofield CJ, Hartley JA, Gileadi O, McHugh PJ. 2012. Characterization of the human SNM1A and SNM1B/ Apollo DNA repair exonucleases. J Biol Chem 287: 26254-26267.
117. Shapiro R, Dubelman S, Feinberg AM, Crain PF, McCloskey JA. 1977. Isolation and identification of cross-linked nu-cleosides from nitrous acid treated deoxyribonucleic acid. J Am Chem Soc 99: 302-303.
118. Sharma S, Helchowski CM, Canman CE. 2013. The roles of DNA polymerase z and the Y family DNA polymerases in promoting or preventing genome instability. Mutat Res 743-744: 97-110.
119. Shen X, Jun S, O'Neal LE, Sonoda E, Bemark M, Sale JE, LiL. 2006. REV3 and REV1 play major roles in recombination-independent repair of DNA inter strand cross-links mediated by monoubiquitinated proliferating cell nuclear antigen (PCNA). J Biol Chem 281: 13869-13872.
120. Shen X, Do H, Li Y, Chung W-H, Tomasz M, de Winter JP, Xia B, Elledge SJ, Wang W, Li L. 2009a. Recruitment of Fanconi anemia and breast cancer proteins to DNA damage sites is differentially governed by replication. Mol Cell 35: 716-723.
121. Shen X, Do H, Li Y, Chung WH, Tomasz M, de Winter JP, Xia B, Elledge SJ, Wang W, Li L. 2009b. Recruitment of Fanconi anemia and breast cancer proteins to DNA damage sites is differentially governed by replication. Mol Cell 35: 716-723.
122. Sinden RR, Cole RS. 1978a. Repair of cross-linked DNA and survival of Escherichia coli treated with psoralen and light: Effects of mutations influencing genetic recombination and DNA metabolism. J Bacteriol 136: 538-547.
123. Sinden RR, Cole RS. 1978b. Topography and kinetics of genetic recombination in Escherichia coli treated with psoralen and light. Proc Natl Acad Sci 75: 2373-2377.
124. Smeaton MB, Hlavin EM, McGregor Mason T, Noronha AM, Wilds CJ, Miller PS. 2008. Distortion-dependent unhooking of inter strand cross-links in mammalian cell extracts. Biochemistry 47: 9920-9930.
125. Smogorzewska A, Matsuoka S, Vinciguerra P, McDonald ER 3rd, Hurov KE, Luo J, Ballif BA, Gygi SP, Hofmann K, D'Andrea AD, et al. 2007. Identification of the FANCI protein, a monoubiquitinated FANCD2 paralog required for DNA repair. Cell 129: 289-301.
126. Smogorzewska A, Desetty R, Saito TT, Schlabach M, Lach FP, Sowa ME, Clark AB, Kunkel TA, Harper JW, Colaiá-covo MP, et al. 2010. A genetic screen identifies FAN1, a Fanconi anemia-associated nuclease necessary for DNA inter strand crosslink repair. Mol Cell 39: 36-47.
127. Somyajit K, Subramanya S, Nagaraju G. 2012. Distinct roles of FANCO/RAD51C protein in DNA damage signaling and repair. J Biol Chem 287: 3366-3380.
128. Sonoda E, Okada T, Zhao GY, Tateishi S, Araki K, Yamaizumi M, Yagi T, Verkaik NS, van Gent DC, Takata M, et al. 2003. Multiple roles of Rev3, the catalytic subunit of pol z in maintaining genome stability in vertebrates. EMBO J 22: 3188-3197.
129. Spanswick VJ, Hartley JM, Hartley JA. 2010. Measurement of DNA inter strand crosslinking in individual cells using the single cell gel electrophoresis (comet) assay. Methods Mol Biol 613: 267-282.
130. Stoepker C, Hain K, Schuster B, Hilhorst-Hofstee Y, Rooimans MA, Steltenpool J, Oostra AB, Eirich K, Korthof ET, Nieuwint AW, et al. 2011. SLX4, a coordinator of structure-specific endonucleases, is mutated in a new Fanconi anemia subtype. Nat Genet 43: 138-141.
131. Stone MP, Cho Y-J, Huang H, Kim H-Y, Kozekov ID, Koze-kova A, Wang H, Minko IG, Lloyd RS, Harris TM, et al. 2008. Inter strand DNA cross-links induced by a,b-un-saturated aldehydes derived from lipid peroxidation and environmental sources. Acc Chem Res 41: 793-804.
132. Sugahara R, Mon H, Lee JM, Kusakabe T. 2012. Monoubi-quitination-dependent chromatin loading of FancD2 in silkworms, a species lacking the FA core complex. Gene 501: 180-187.
133. Svendsen JM, Smogorzewska A, Sowa ME, O'Connell BC, Gygi SP, Elledge SJ, Harper JW. 2009. Mammalian BTBD12/SLX4 assembles a Holliday junction resolvase and is required for DNA repair. Cell 138: 63-77.
134. Thazhathveetil AK, Liu ST, Indig FE, Seidman MM. 2007. Psoralen conjugates for visualization of genomic inter-strand cross-links localized by laser photoactivation. Bio-conj Chem 18: 431-437.
135. Tiefenbach T, Junop M. 2012. Pso2 (SNM1) is a DNA structure-specific endonuclease. Nucleic Acids Res 40: 2131- 2139.
136. Tomasz M. 1995. Mitomycin C: Small, fast and deadly (but very selective). Chem Biol 2: 575-579.
137. Trujillo JP, Mina LB, Pujol R, Bogliolo M, Andrieux J, Holder M, Schuster B, Schindler D, Surrallés J. 2012. On the role of FAN1 in Fanconi anemia. Blood 120: 86-89.
138. Vare D, Groth P, Carlsson R, Johansson F, Erixon K, Jenssen D. 2012. DNA inter strand cross links induce a potent replication block followed by formation and repairofdouble strand breaks in intact mammalian cells. DNA Rep 11: 976-985.
139. Vaz F, Hanenberg H, Schuster B, Barker K, Wiek C, Erven V, Neveling K, Endt D, Kesterton I, Autore F, et al. 2010. Mutation of the RAD51C gene in a Fanconi anemialike disorder. Nat Genet 42: 406-409.
140. Volker M, Moné MJ, Karmakar P, van Hoffen A, Schul W, Vermeulen W, Hoeijmakers JHJ, van Driel R, van Zeeland AA, Mullenders LHF. 2001. Sequential assembly of the nucleotide excision repair factors in vivo. Mol Cell 8: 213-224.
141. Wang X, Peterson CA, Zheng H, Nairn RS, Legerski RJ, Li L. 2001. Involvement of nucleotide excision repair in a recombination-independent and error-prone pathway of DNA inter strand cross-link repair. Mol Cell Biol 21: 713-720.
142. Wang X, Kennedy RD, Ray K, Stuckert P, Ellenberger T, D'Andrea AD. 2007. Chklmediated phosphorylation of FANCE is required for the Fanconi anemia/BRCA pathway. Mol Cell Biol 27: 3098-3108.
143. Wang AT, Sengerová B, Cattell E, Inagawa T, Hartley JM, Kiakos K, Burgess-Brown NA, Swift LP, Enzlin JH, Scho-field CJ, et al. 2011. Human SNM1A and XPF-ERCC1 collaborate to initiate DNA inter strand cross-link repair. Genes Dev 25: 1859-1870.
144. Wang Y, Leung Justin W, Jiang Y, Lowery Megan G, Do H, Vasquez Karen M, Chen J, Wang W, Li L. 2013. FANCM and FAAP24 maintain genome stability via cooperative as well as unique functions. Mol Cell 49: 997-1009.
145. Williams Hannah L, Gottesman Max E, Gautier J. 2012. Replication-independent repair of DNA inter strand cross links. Mol Cell 47: 140-147.
146. Wu HI, Brown JA, Dorie MJ, Lazzeroni L, Brown JM. 2004. Genome-wide identification of genes conferring resistance to the anticancer agents cisplatin, oxaliplatin, and mitomycin C. Cancer Res 64: 3940-3948.
147. Wu JH, Wilson JB, Wolfreys AM, Scott A, Jones NJ. 2009. Optimization of the comet assay for the sensitive detection of PUVA-induced DNA inter strand cross-links. Mu-tagenesis 24: 173-181.
148. Xue Y, Li Y, Guo R, Ling C, Wang W. 2008. FANCM of the Fanconi anemia core complex is required for both mono-ubiquitination and DNA repair. Hum Mol Genet 17: 1641-1652.
149. Yamamoto KN, Kobayashi S, Tsuda M, Kurumizaka H, Ta-kata M, Kono K, Jiricny J, Takeda S, Hirota K. 2011. Involvement of SLX4 in inter strand cross-link repair is regulated by the Fanconi anemia pathway. Proc Natl Acad Sci 108: 6492-6496.
150. Yamanaka K, Minko IG, Takata K-I, Kolbanovskiy A, Kozekov ID, Wood RD, Rizzo CJ, Lloyd RS. 2010. Novel enzymatic function of DNA polymerasenin trans-lesion DNA synthesis past major groove DNA-peptide and DNA-DNA cross-links. Chem Res Toxicol 23: 689-695.
151. Yan Y, Akhter S, Zhang X, Legerski R. 2010a. The multifunctional SNM1 gene family: Not just nucleases. Future Oncol 6: 1015-1029.
152. Yan Z, Delannoy M, Ling C, Daee D, Osman F, Muniandy PA, Shen X, Oostra AB, Du H, Steltenpool J, et al. 2010b. A histone-fold complex and FANCM form a conserved DNA-remodeling complex to maintain genome stability. Mol Cell 37: 865-878.
153. Yan Z, Guo R, Paramasivam M, Shen W, Ling C, Fox D 3rd, Wang Y, Oostra AB, Kuehl J, Lee DY, et al. 2012. A ubiq-uitin-binding protein, FAAP20, links RNF8-mediated ubiquitination to the Fanconi anemia DNA repair network. Mol Cell 47: 61-75.
154. Youds JL, Barber LJ, Ward JD, Collis SJ, O'Neil NJ, Boulton SJ, Rose AM. 2008. DOG-1 is the Caenorhabditis elegans BRIP1/FANCJ homologue and functions in inter strand cross-link repair. Mol Cell Biol 28: 1470-1479.
155. Zamble DB, Mu D, Reardon JT, Sancar A, Lippard SJ. 1996. Repair of cisplatin-DNA adducts by the mammalian excision nuclease. Biochemistry 35: 10004-10013.
156. Zhao J, Jain A, Iyer RR, Modrich PL, Vasquez KM. 2009. Mismatch repair and nucleotide excision repair proteins cooperate in the recognition of DNA inter strand cross links. Nucleic Acids Res 37: 4420-4429.
157. Zheng H, Wang X, Warren AJ, Legerski RJ, Nairn RS, Hamilton JW, Li L. 2003. Nucleotide excision repair- and polymerase h-mediated error-prone removal of mito-mycin C inter strand cross-links. Mol Cell Biol 23: 754-761.
158. Zhou W, Otto EA, Cluckey A, Airik R, Hurd TW, Chaki M, Diaz K, Lach FP, Bennett GR, Gee HY, et al. 2012. FAN1 mutations cause karyomegalic interstitial nephritis, linking chronic kidney failure to defective DNA damage repair. Nat Genet 44: 910-915.
159. Zietlow L, Smith LA, Bessho M, Bessho T.2009. Evidence for the involvement of human DNA polymerase N in the repair of DNA inter strand cross-links. Biochemistry 48: 11817-11824.
160. Zou L, Elledge SJ. 2003. Sensing DNA damage through ATRIP recognition of RPA-ssDNA complexes. Science 300: 1542-1548.