DNA interstrand crosslink repair in mammalian cells: Step by step

Critical Reviews in Biochemistry and Molecular Biology

Volumn 45, Issue 1, 2010, Pages 23-49

  Muniandy, Parameswary A ^a   Liu, Jia ^a   Majumdar, Alokes ^a   Liu, Su Ting ^a   Seidman, Michael M ^a  

^a NATIONAL INSTITUTE ON AGING   (United States)

Author keywords

Chemotherapy; Cisplatin; Lesion bypass; Psoralen; Replication arrest; Unhooking

Indexed keywords

CHLORMETHINE; CISPLATIN; MITOMYCIN C; NATURAL PRODUCT; PSORALEN;

CELL CYCLE; CELL CYCLE G1 PHASE; DNA CROSS LINKING; DNA REPAIR; DNA SYNTHESIS; DRUG STRUCTURE; ESCHERICHIA COLI; EXCISION REPAIR; MAMMAL CELL; MISMATCH REPAIR; PRIORITY JOURNAL; REVIEW;

ANIMALS; CELL CYCLE; CROSS-LINKING REAGENTS; DNA; DNA DAMAGE; DNA REPAIR; FANCONI ANEMIA; HUMANS; RECOMBINATION, GENETIC;

MAMMALIA;

EID: 77249167871     PISSN: 10409238     EISSN: 15497798     Source Type: Journal    
DOI: 10.3109/10409230903501819     Document Type: Review

References (277)

1. Adair GM, Rolig RL, Moore-Faver D, Zabelshansky M, Wilson JH and Nairn RS. 2000. Role of ERCC1 in removal of long non-homologous tails during targeted homologous recombination. EMBO J 19:5552-5561.
2. Ahmad A, Robinson AR, Duensing A, van DE, Beverloo HB, Weisberg DB, Hasty P, Hoeijmakers JH and Niedernhofer LJ. 2008. ERCC1-XPF endonuclease facilitates DNA double-strand break repair. Mol Cell Biol 28:5082-5092.
3. Akagi J, Masutani C, Kataoka Y, Kan T, Ohashi E, Mori T, Ohmori H and Hanaoka F. 2009. Interaction with DNA polymerase eta is required for nuclear accumulation of REV1 and suppression of spontaneous mutations in human cells. DNA Repair (Amst) 8:585-599.
4. Akkari YM, Bateman RL, Reifsteck CA, Olson SB and Grompe M. 2000. DNA replication is required to elicit cellular responses to psoralen-induced DNA interstrand cross-links. Mol Cell Biol 20:8283-8289.
5. Allan JM, Engelward BP, Dreslin AJ, Wyatt MD, Tomasz M and Samson LD. 1998. Mammalian 3-methyladenine DNA glycosylase protects against the toxicity and clastogenicity of certain chemo-therapeutic DNA cross-linking agents. Cancer Res 58:3965-3973.
6. Andersen SL, Bergstralh DT, Kohl KP, LaRocque JR, Moore CB and Sekelsky J. 2009. Drosophila MUS312 and the vertebrate ortholog BTBD12 interact with DNA structure-specifc endonucleases in DNA repair and recombination. Mol Cell 35:128-135.
7. Andreassen PR and Ren K. 2009. Fanconi anemia proteins, DNA interstrand crosslink repair pathways, and cancer therapy. Curr Cancer Drug Targets 9:101-117.
8. Angelov T, Guainazzi A and Scharer OD. 2009. Generation of DNA interstrand cross-links by post-synthetic reductive amination. Org Lett 11:661-664.
9. Averbeck D, Papadopoulo D and Moustacchi E. 1988. Repair of 4 5′ 8-trimethylpsoralen plus light-induced DNA damage in normal and Fanconi's anemia cell lines. Cancer Res 48:2015-2020.
10. Bae JB, Mukhopadhyay SS, Liu L, Zhang N, Tan J, Akhter S, Liu X, Shen X, Li L and Legerski RJ. 2008. Snm1B/Apollo mediates replication fork collapse and S Phase checkpoint activation in response to DNA interstrand cross-links. Oncogene 27:5045-5056.
11. Baik MH, Friesner RA and Lippard SJ. 2002. Teoretical study on the stability of N-glycosyl bonds: why does N7-platination not promote depurination? J Am Chem Soc 124:4495-4503.
12. Balcome S, Park S, Quirk Dorr DR, Hafner L, Phillips L and Tretyakova N. 2004. Adenine-containing DNA-DNA cross-links of antitumor nitrogen mustards. Chem Res Toxicol 17:950-962.
13. Barber LJ, Ward TA, Hartley JA and 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.
14. Baure J, Izadi A, Suarez V, Giedzinski E, Cleaver JE, Fike JR and Limoli CL. 2009. Histone H2AX phosphorylation in response to changes in chromatin structure induced by altered osmolarity. Mutagenesis 24:161-167.
15. Behe MJ. 1995. An overabundance of long oligopurine tracts occurs in the genome of simple and complex eukaryotes. Nucleic Acids Res 23:689-695.
16. Beljanski V, Marzilli LG and Doetsch PW. 2004. DNA damage-processing pathways involved in the eukaryotic cellular response to anticancer DNA cross-linking drugs. Mol Pharmacol 65:1496-1506.
17. Ben-Yehoyada M, Wang LC, Kozekov ID, Rizzo CJ, Gottesman ME and Gautier J. 2009. Checkpoint signaling from a single DNA inter-strand crosslink. Mol Cell 35:704-715.
18. Berardini M, Mackay W and Loechler EL. 1997. Evidence for a recombination-independent pathway for the repair of DNA inter-strand cross-links based on a site-specifc study with nitrogen mustard. Biochemistry 36:3506-3513.
19. Berardini M, Foster PL and Loechler EL. 1999. DNA polymerase II (polB) is involved in a new DNA repair pathway for DNA interstrand cross-links in Escherichia coli. J Bacteriol 181:2878-2882.
20. Bergstralh DT and Sekelsky J. 2008. Interstrand crosslink repair: can XPF-ERCC1 be let of the hook? Trends Genet 24:70-76.
21. Bessho T. 2003. Induction of DNA replication-mediated double strand breaks by psoralen DNA interstrand cross-links. J Biol Chem 278:5250-5254.
22. Bessho T, Mu D and Sancar A. 1997. Initiation of DNA interstrand cross-link repair in humans: the nucleotide excision repair system makes dual incisions 5′ to the cross-linked base and removes a 22-to 28-nucleotide-long damage-free strand. Mol Cell Biol 17:6822-6830.
23. Bhagwat N, Olsen AL, Wang AT, Hanada K, Stuckert P, Kanaar R, D'Andrea A, Niedernhofer LJ and McHugh PJ. 2009. XPF-ERCC1 participates in the Fanconi anemia pathway of crosslink repair. Mol Cell Biol 29:6427-6437.
24. Bolderson E, Scorah J, Helleday T, Smythe C and Meuth M. 2004. ATM is required for the cellular response to thymidine induced replication fork stress. Hum Mol Genet 13:2937-2945.
25. Boyer V, Moustacchi E and Sage E. 1988. Sequence specifcity in pho-toreaction of various psoralen derivatives with DNA: role in biological activity. Biochemistry 27:3011-3018.
26. Bredberg A and Soderhall S. 1985. Normal rate of DNA breakage in xeroderma pigmentosum complementation group E cells treated with 8-methoxypsoralen plus near-ultraviolet radiation. Biochim Biophys Acta 824:268-271.
27. Broyde S, Wang L, Rechkoblit O, Geacintov NE and Patel DJ. 2008. Lesion processing: high-fdelity versus lesion-bypass DNA polymerases. Trends Biochem Sci 33:209-219.
28. Budzowska M and Kanaar R. 2009. Mechanisms of dealing with DNA damage-induced replication problems. Cell Biochem Biophys 53:17-31.
29. Cai Y, Patel DJ, Geacintov NE and Broyde S. 2009. Diferential nucle-otide excision repair susceptibility of bulky DNA adducts in diferent sequence contexts: hierarchies of recognition signals. J Mol Biol 385:30-44.
30. Camenisch U, Trautlein D, Clement FC, Fei J, Leitenstorfer A, Ferrando-May E and Naegeli H. 2009. Two-stage dynamic DNA quality check by xeroderma pigmentosum group C protein. EMBO J 28:2387-2399.
31. Chen Z, Xu XS, Yang J and Wang G. 2003. Defning the function of XPC protein in psoralen and cisplatin-mediated DNA repair and mutagenesis. Carcinogenesis 24:1111-1121.
32. Cheng S, Sancar A and Hearst JE. 1991. RecA-dependent incision of psoralen-crosslinked DNA by (A)BC excinuclease. Nucleic Acids Res 19:657-663.
33. Chin JY and Glazer PM. 2009. Repair of DNA lesions associated with triplex-forming oligonucleotides. Mol Carcinog 48:389-399.
34. Chin JY, Schleifman EB and Glazer PM. 2007. Repair and recombination induced by triple helix DNA. Front Biosci 12:4288-4297.
35. Chiou CC and Yang JL. 1995. Mutagenicity and specifc mutation spectrum induced by 8-methoxypsoralen plus a low dose of UVA in the hprt gene in diploid human fbroblasts. Carcinogenesis 16:1357-1362.
36. Christensen LA, Wang H, Van Houten B and Vasquez KM. 2008. Efcient processing of TFO-directed psoralen DNA inter-strand crosslinks by the UvrABC nuclease. Nucleic Acids Res 36:7136-7145.
37. Cimino GD, Gamper H, Isaacs ST and Hearst JE. 1985. Psoralens as photoactive probes of nucleic acid structure and function: organic chemistry, photochemistry, and biochemistry. Annu Rev Biochem 54:1151-1193.
38. Cipak L, Watanabe N and Bessho T. 2006. The role of BRCA2 in replication-coupled DNA interstrand cross-link repair in vitro. Nat Struct Mol Biol 13:729-733.
39. Clingen PH, Arlett CF, Hartley JA and Parris CN. 2007. Chemosensitivity of primary human fbroblasts with defective unhooking of DNA interstrand cross-links. Exp Cell Res 313:753-760.
40. Clingen PH, Wu JY, Miller J, Mistry N, Chin F, Wynne P, Prise KM and Hartley JA. 2008. Histone H2AX phosphorylation as a molecular pharmacological marker for DNA interstrand crosslink cancer chemotherapy. Biochem Pharmacol 76:19-27.
41. Cohen SM, Brylawski BP, Cordeiro-Stone M and Kaufman DG. 2002. Mapping of an origin of DNA replication near the transcriptional promoter of the human HPRT gene. J Cell Biochem 85:346-356.
42. Cole RS. 1973. Repair of DNA containing interstrand crosslinks in Escherichia coli: sequential excision and recombination. Proc Natl Acad Sci USA 70:1064-1068.
43. Cole RS, Levitan D and Sinden RR. 1976. Removal of psoralen inter-strand cross-links from DNA of Escherichia coli: mechanism and genetic control. J Mol Biol 103:39-59.
44. Collins AR. 1993. Mutant rodent cell lines sensitive to ultraviolet light, ionizing radiation and cross-linking agents: a comprehensive survey of genetic and biochemical characteristics. Mutat Res 293:99-118.
45. Collins AR. 2004. Te comet assay for DNA damage and repair: principles, applications, and limitations. Mol Biotechnol 26:249-261.
46. Collis SJ, Ciccia A, Deans AJ, Horejsi Z, Martin JS, Maslen SL, Skehel JM, Elledge SJ, West SC and Boulton SJ. 2008. FANCM and FAAP24 function in ATR-mediated checkpoint signaling independently of the Fanconi anemia core complex. Mol Cell 32:313-324.
47. Couve S, Mace-Aime G, Rosselli F and Saparbaev MK. 2009. Te human oxidative DNA glycosylase NEIL1 excises psoralen-induced interstrand DNA cross-links in a three-stranded DNA structure. J Biol Chem 284:11963-11970.
48. Couve-Privat S, Mace G, Rosselli F and Saparbaev MK. 2007. Psoralen-induced DNA adducts are substrates for the base excision repair pathway in human cells. Nucleic Acids Res 35:5672-5682.
49. Damia G, Imperatori L, Stefanini M and D'Incalci M. 1996. Sensitivity of CHO mutant cell lines with specifc defects in nucleotide excision repair to diferent anti-cancer agents. Int J Cancer 66:779-783.
50. da Silva MW, Wilds CJ, Noronha AM, Colvin OM, Miller PS and Gamcsik MP. 2004. Accommodation of mispair aligned N3T-ethyl-N3T DNA interstrand cross link. Biochemistry 43:12549-12554.
51. Demuth I, Digweed M and Concannon P. 2004. Human SNM1B is required for normal cellular response to both DNA interstrand crosslink-inducing agents and ionizing radiation. Oncogene 23:8611-8618.
52. Dendouga N, Gao H, Moechars D, Janicot M, Vialard J and McGowan CH. 2005. Disruption of murine Mus81 increases genomic instability and DNA damage sensitivity but does not promote tumorigenesis. Mol Cell Biol 25:7569-7579.
53. De Silva IU, McHugh PJ, Clingen PH and Hartley JA. 2000. Defning 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.
54. De Silva IU, McHugh PJ, Clingen PH and 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.
55. de Winter JP and Joenje H. 2009. Te genetic and molecular basis of Fanconi anemia. Mutat Res 668:11-19.
56. Dooley PA, Tsarouhtsis D, Korbel GA, Nechev LV, Shearer J, Zegar IS, Harris CM, Stone MP and Harris TM. 2001. Structural studies of an oligodeoxynucleotide containing a trimethylene interstrand cross-link in a 5′-(CpG) motif: model of a malondialdehyde cross-link. J Am Chem Soc 123:1730-1739.
57. Dooley PA, Zhang M, Korbel GA, Nechev LV, Harris CM, Stone MP and Harris TM. 2003. NMR determination of the conformation of a trimethylene interstrand cross-link in an oligodeoxynucleotide duplex containing a 5′-d(GpC) motif. J Am Chem Soc 125:62-72.
58. Dronkert ML and Kanaar R. 2001. Repair of DNA interstrand crosslinks. Mutat Res 486:217-247.
59. Dronkert ML, de Wit J, Boeve M, Vasconcelos ML, van Steeg H, Tan TL, Hoeijmakers JH and Kanaar R. 2000. Disruption of mouse SNM1 causes increased sensitivity to the DNA interstrand cross-linking agent mitomycin C. Mol Cell Biol 20:4553-4561.
60. Eichman BF, Mooers BH, Alberti M, Hearst JE and Ho PS. 2001. Te crystal structures of psoralen cross-linked DNAs: drug-dependent formation of Holliday junctions. J Mol Biol 308:15-26.
61. Fan Y-H and Gold B. 1999. Sequence-specifcity for DNA interstrand cross-linking by α ?-alkanediol dimethylsulfonate esters: evidence for DNA distortion by the initial monofunctional lesion. J Am Chem Soc 121:11942-11946.
62. Faruqi AF, Seidman MM, Segal DJ, Carroll D and Glazer PM. 1996. Recombination induced by triple-helix-targeted DNA damage in mammalian cells. Mol Cell Biol 16:6820-6828.
63. Fekairi S, Scaglione S, Chahwan C, Taylor ER, Tissier A, Coulon S, Dong MQ, Ruse C, Yates JR, III, Russell P, Fuchs RP, McGowan CH and Gaillard PH. 2009. Human SLX4 is a Holliday junction resolvase subunit that binds multiple DNA repair/recombination endonucleases. Cell 138:78-89.
64. Felsenfeld G, Davies DR and Rich A. 1957. Formation of a three stranded polynucleotide molecule. J Am Chem Soc 79:2023-2024.
65. Fisher LA, Bessho M and Bessho T. 2008. Processing of a psoralen DNA interstrand cross-link by XPF-ERCC1 complex in vitro. J Biol Chem 283:1275-1281.
66. Fitch ME, Nakajima S, Yasui A and Ford JM. 2003. In vivo recruitment of XPC to UV-induced cyclobutane pyrimidine dimers by the DDB2 gene product. J Biol Chem 278:46906-46910.
67. Fiumicino S, Martinelli S, Colussi C, Aquilina G, Leonetti C, Crescenzi M and Bignami M. 2000. Sensitivity to DNA cross-linking chemotherapeutic agents in mismatch repair-defective cells in vitro and in xenografts. Int J Cancer 85:590-596.
68. Furuta T, Ueda T, Aune G, Sarasin A, Kraemer KH and Pommier Y. 2002. Transcription-coupled nucleotide excision repair as a determinant of cisplatin sensitivity of human cells. Cancer Res 62:4899-4902.
69. Fuxreiter M, Luo N, Jedlovszky P, Simon I and Osman R. 2002. Role of base fipping in specifc recognition of damaged DNA by repair enzymes. J Mol Biol 323:823-834.
70. Gargiulo D, Kumar GS, Musser SS and Tomasz M. 1995. Structural and function modifcation of DNA by mitomycin C. Mechanism of the DNA sequence specifcity of mitomycins. Nucleic Acids Symp Ser 34:169-170.
71. Gari K, Decaillet C, Delannoy M, Wu L and Constantinou A. 2008a. Remodeling of DNA replication structures by the branch point translocase FANCM. Proc Natl Acad Sci USA 105:16107-16112.
72. Gari K, Decaillet C, Stasiak AZ, Stasiak A and Constantinou A. 2008b. Te Fanconi anemia protein FANCM can promote branch migration of Holliday junctions and replication forks. Mol Cell 29:141-148.
73. Geacintov NE, Broyde S, Buterin T, Naegeli H, Wu M, Yan S and Patel DJ. 2002. Termodynamic and structural factors in the removal of bulky DNA adducts by the nucleotide excision repair machinery. Biopolymers 65:202-210.
74. Giovannangeli C, Tuong NT and Helene C. 1992. Oligodeoxynucleotide- directed photo-induced cross-linking of HIV proviral DNA via triple-helix formation. Nucleic Acids Res 20:4275-4281.
75. Grillari J, Katinger H and Voglauer R. 2007. Contributions of DNA interstrand cross-links to aging of cells and organisms. Nucleic Acids Res 35:7566-7576.
76. Grossmann KF, Ward AM, Matkovic ME, Folias AE and Moses RE. 2001. S. cerevisiae has three pathways for DNA interstrand crosslink repair. Mutat Res 487:73-83.
77. Guo C, Fischhaber PL, Luk-Paszyc MJ, Masuda Y, Zhou J, Kamiya K, Kisker C and Friedberg EC. 2003. Mouse Rev1 protein interacts with multiple DNA polymerases involved in translesion DNA synthesis. EMBO J 22:6621-6630.
78. Gupta R, Sharma S, Sommers JA, Kenny MK, Cantor SB and Brosh Jr RM. 2007. FANCJ (BACH1) helicase forms DNA damage inducible foci with replication protein A and interacts physically and functionally with the single-stranded DNA-binding protein. Blood 110:2390-2398.
79. Hanada K, Budzowska M, Modesti M, Maas A, Wyman C, Essers J and Kanaar R. 2006. Te structure-specifc endonuclease Mus81-Eme1 promotes conversion of interstrand DNA crosslinks into double-strands breaks. EMBO J 25:4921-4932.
80. Hanada K, Budzowska M, Davies SL, van DE, Onizawa H, Beverloo HB, Maas A, Essers J, Hickson ID and Kanaar R. 2007. Te structure-specifc endonuclease Mus81 contributes to replication restart by generating double-strand DNA breaks. Nat Struct Mol Biol 14:1096-1104.
81. Haran TE and Crothers DM. 1988. Phased psoralen cross-links do not bend the DNA double helix. Biochemistry 27:6967-6971.
82. Harris P V, Mazina OM, Leonhardt EA, Case RB, Boyd JB and Burtis KC. 1996. Molecular cloning of Drosophila mus308, a gene involved in DNA cross-link repair with homology to prokaryotic DNA polymerase I genes. Mol Cell Biol 16:5764-5771.
83. Havre PA, Gunther EJ, Gasparro FP and Glazer PM. 1993. Targeted mutagenesis of DNA using triple helix-forming oligonucleotides linked to psoralen. Proc Natl Acad Sci USA 90:7879-7883.
84. Hazrati A, Ramis-Castelltort M, Sarkar S, Barber LJ, Schofeld CJ, Hartley JA and McHugh PJ. 2008. Human SNM1A suppresses the DNA repair defects of yeast pso2 mutants. DNA Repair (Amst) 7:230-238.
85. Hejna J, Philip S, Ott J, Faulkner C and Moses R. 2007. Te hSNM1 protein is a DNA 5′-exonuclease. Nucleic Acids Res 35:6115-6123.
86. Hejna J, Holtorf M, Hines J, Mathewson L, Hemphill A, Al-Dhalimy M, Olson SB and Moses RE. 2008. Tip60 is required for DNA inter-strand cross-link repair in the Fanconi anemia pathway. J Biol Chem 283:9844-9851.
87. Hemphill AW, Bruun D, Trun L, Akkari Y, Torimaru Y, Hejna K, Jakobs PM, Hejna J, Jones S, Olson SB and Moses RE. 2008. Mammalian SNM1 is required for genome stability. Mol Genet Metab 94:38-45.
88. Hinz JM, Nham PB, Salazar EP and Tompson LH. 2006. Te Fanconi anemia pathway limits the severity of mutagenesis. DNA Repair (Amst) 5:875-884.
89. Hoy CA, Tompson LH, Mooney CL and Salazar EP. 1985a. Defective DNA cross-link removal in Chinese hamster cell mutants hypersensitive to bifunctional alkylating agents. Cancer Res 45:1737-1743.
90. Hoy CA, Tompson LH, Salazar EP and Stewart SA. 1985b. Diferent genetic alterations underlie dual hypersensitivity of CHO mutant UV-1 to DNA methylating and cross-linking agents. Somat Cell Mol Genet 11:523-532.
91. Huang H, Zhu L, Reid BR, Drobny GP and Hopkins PB. 1995. Solution structure of a cisplatin-induced DNA interstrand cross-link. Science 270:1842-1845.
92. Hwang GS, Kim JK and Choi BS. 1996. Te solution structure of a pso-ralen cross-linked DNA duplex by NMR and relaxation matrix refnement. Biochem Biophys Res Commun 219:191-197.
93. Isaacs RJ and Spielmann HP. 2004. A model for initial DNA lesion recognition by NER and MMR based on local conformational fex-ibility. DNA Repair (Amst) 3:455-464.
94. Islas AL, Baker FJ and Hanawalt PC. 1994. Transcription-coupled repair of psoralen cross-links but not monoadducts in Chinese hamster ovary cells. Biochemistry 33:10794-10799.
95. Jamieson ER and Lippard SJ. 1999. Structure, recognition, and processing of cisplatin-DNA adducts. Chem Rev 99:2467-2498.
96. Janicijevic A, Sugasawa K, Shimizu Y, Hanaoka F, Wijgers N, Djurica M, Hoeijmakers JH and Wyman C. 2003. DNA bending by the human damage recognition complex XPC-HR23B. DNA Repair (Amst) 2:325-336.
97. Johnson RE, Washington MT, Haracska L, Prakash S and Prakash L. 2000. Eukaryotic polymerases iota and zeta act sequentially to bypass DNA lesions. Nature 406:1015-1019.
98. Johnston BH, Johnson MA, Moore CB and Hearst JE. 1977. Psoralen-DNA photoreaction: controlled production of mono-and diadducts with nanosecond ultraviolet laser pulses. Science 197:906-908.
99. Kanne D, Rapoport H and Hearst JE. 1984. 8-Methoxypsoralen-nucleic acid photoreaction. Efect of methyl substitution on pyrone vs. furan photoaddition. J Med Chem 27:531-534.
100. Kannouche PL and Lehmann AR. 2004. Ubiquitination of PCNA and the polymerase switch in human cells. Cell Cycle 3:1011-1013.
101. Kannouche P, Fernandez de Henestrosa AR, Coull B, Vidal AE, Gray C, Zicha D, Woodgate R and Lehmann AR. 2003. Localization of DNA polymerases eta and iota to the replication machinery is tightly co-ordinated in human cells. EMBO J 22:1223-1233.
102. Kaye J, Smith CA and Hanawalt PC. 1980. DNA repair in human cells containing photoadducts of 8-methoxypsoralen or angelicin. Cancer Res 40:696-702.
103. Koehler DR and Hanawalt PC. 1996. Recruitment of damaged DNA to the nuclear matrix in hamster cells following ultraviolet irradiation. Nucleic Acids Res 24:2877-2884.
104. Kropachev K, Kolbanovskii M, Cai Y, Rodriguez F, Kolbanovskii A, Liu Y, Zhang L, Amin S, Patel D, Broyde S and Geacintov NE. 2009. Te sequence dependence of human nucleotide excision repair efciencies of benzo[a]pyrene-derived DNA lesions: insights into the structural factors that favor dual incisions. J Mol Biol 386:1193-1203.
105. Kumaresan KR and Lambert MW. 2000. Fanconi anemia, complementation group A, cells are defective in ability to produce incisions at sites of psoralen interstrand cross-links. Carcinogenesis 21:741-751.
106. Kumaresan KR, Ramaswamy M and Yeung AT. 1992. Structure of the DNA interstrand cross-link of 4 5′ 8-trimethylpsoralen. Biochemistry 31:6774-6783.
107. Kumaresan KR, Hang B and Lambert MW. 1995. Human endonucleo-lytic incision of DNA 3′ and 5′ to a site-directed psoralen monoad-duct and interstrand cross-link. J Biol Chem 270:30709-30716.
108. Kumaresan KR, Hwang M, Telen MP and Lambert MW. 2002. Contribution of XPF functional domains to the 5′ and 3′ incisions produced at the site of a psoralen interstrand cross-link. Biochemistry 41:890-896.
109. Kumaresan KR, Sridharan DM, McMahon LW and Lambert MW. 2007. Defciency in incisions produced by XPF at the site of a DNA interstrand cross-link in Fanconi anemia cells. Biochemistry 46:14359-14368.
110. Kumari A, Minko IG, Harbut MB, Finkel SE, Goodman MF and Lloyd RS. 2008. Replication bypass of interstrand cross-link intermediates by Escherichia coli DNA polymerase IV. J Biol Chem 283:27433-27437.
111. Kuraoka I, Kobertz WR, Ariza RR, Biggerstaf M, Essigmann JM and Wood RD. 2000. Repair of an interstrand DNA crosslink initiated by ERCC1-XPF repair/recombination nuclease. J Biol Chem 275:26632-26636.
112. Lage C, Padula M, de Alencar TA, da Fonseka Goncalves SR, da Silva Vidal C, Cabral-Neto J, Leitao AC. 2003. New insights on how nucleotide excision repair could remove DNA adducts induced by chemotherapeutic agents and psoralens plus UV-A (PUVA) in Escherichia coli cells. Mutat Res 544:143-157.
113. Lai C, Cao H, Hearst JE, Corash L, Luo H and Wang Y. 2008. Quantitative analysis of DNA interstrand cross-links and monoadducts formed in human cells induced by psoralens and UVA irradiation. Anal Chem 80:8790-8798.
114. Lan L, Nakajima S, Oohata Y, Takao M, Okano S, Masutani M, Wilson SH and Yasui A. 2004. In situ analysis of repair processes for oxidative DNA damage in mammalian cells. Proc Natl Acad Sci USA 101:13738-13743.
115. Lange SS, Reddy MC and Vasquez KM. 2009. Human HMGB1 directly facilitates interactions between nucleotide excision repair proteins on triplex-directed psoralen interstrand crosslinks. DNA Repair (Amst) 8:865-872.
116. Lao Y and Hecht SS. 2005. Synthesis and properties of an acetalde-hyde-derived oligonucleotide interstrand cross-link. Chem Res Toxicol 18:711-721.
117. Laquerbe A, Guillouf C, Moustacchi E and Papadopoulo D. 1995. Te mutagenic processing of psoralen photolesions leaves a highly specifc signature at an endogenous human locus. J Mol Biol 254:38-49.
118. Lawley PD and Phillips DH. 1996. DNA adducts from chemotherapeu-tic agents. Mutat Res 355:13-40.
119. Lawrence CW, Gibbs PE, Murante RS, Wang XD, Li Z, McManus TP, McGregor WG, Nelson JR, Hinkle DC and Maher VM. 2000. Roles of DNA polymerase zeta and Rev1 protein in eukaryotic muta-genesis and translesion replication. Cold Spring Harb Symp Quant Biol 65:61-69.
120. Lee YJ, Park SJ, Ciccone SL, Kim CR and Lee SH. 2006. An in vivo analysis of MMC-induced DNA damage and its repair. Carcinogenesis 27:446-453.
121. Lehmann AR. 2006. Translesion synthesis in mammalian cells. Exp Cell Res 312:2673-2676.
122. Lehmann AR, Niimi A, Ogi T, Brown S, Sabbioneda S, Wing JF, Kannouche PL and Green CM. 2007. Translesion synthesis: Y-family polymerases and the polymerase switch. DNA Repair (Amst) 6:891-899.
123. Lehoczky P, McHugh PJ and Chovanec M. 2007. DNA interstrand cross-link repair in Saccharomyces cerevisiae. FEMS Microbiol Rev 31:109-133.
124. Li J, Wang QE, Zhu Q, El-Mahdy MA, Wani G, Praetorius-Ibba M and Wani AA. 2006. DNA damage binding protein component DDB1 participates in nucleotide excision repair through DDB2 DNA-binding and cullin 4A ubiquitin ligase activity. Cancer Res 66:8590-8597.
125. Li L, Peterson CA, Lu X, Wei P and Legerski RJ. 1999. Interstrand cross-links induce DNA synthesis in damaged and undamaged plasmids in mammalian cell extracts. Mol Cell Biol 19:5619-5630.
126. Li L, Peterson CA, Zhang X and Legerski RJ. 2000. Requirement for PCNA and RPA in interstrand crosslink-induced DNA synthesis. Nucleic Acids Res 28:1424-1427.
127. Li X, Hejna J and Moses RE. 2005. Te yeast Snm1 protein is a DNA 5′-exonuclease. DNA Repair (Amst) 4:163-170.
128. Liu N, Lamerdin JE, Tebbs RS, Schild D, Tucker JD, Shen MR, Brookman KW, Siciliano MJ, Walter CA, Fan W, Narayana LS, Zhou ZQ, Adamson AW, Sorensen KJ, Chen DJ, Jones NJ and Tompson LH. 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.
129. Liu X, Lao Y, Yang IY, Hecht SS and Moriya M. 2006. Replication-coupled repair of crotonaldehyde/acetaldehyde-induced guanine-guanine interstrand cross-links and their mutagenic-ity. Biochemistry 45:12898-12905.
130. Loeber RL, Michaelson-Richie ED, Codreanu SG, Liebler DC, Campbell CR and Tretyakova NY. 2009. Proteomic analysis of DNA-protein cross-linking by antitumor nitrogen mustards. Chem Res Toxicol 22:1151-1162.
131. Ma Y, Pannicke U, Schwarz K and Lieber MR. 2002. Hairpin opening and overhang processing by an Artemis/DNA-dependent protein kinase complex in nonhomologous end joining and V(D)J recombination. Cell 108:781-794.
132. Maillard O, Camenisch U, Clement FC, Blagoev KB and Naegeli H. 2007a. DNA repair triggered by sensors of helical dynamics. Trends Biochem Sci 32:494-499.
133. Maillard O, Solyom S and Naegeli H. 2007b. An aromatic sensor with aversion to damaged strands confers versatility to DNA repair. PLoS Biol 5:e79.
134. Maillard O, Camenisch U, Blagoev KB and Naegeli H. 2008. Versatile protection from mutagenic DNA lesions conferred by bipartite recognition in nucleotide excision repair. Mutat Res 658:271-286.
135. Majumdar A, Khorlin A, Dyatkina N, Lin FL, Powell J, Liu J, Fei Z, Khripine Y, Watanabe KA, George J, Glazer PM and Seidman MM. 1998. Targeted gene knockout mediated by triple helix forming oligonucleotides. Nat Genet 20:212-214.
136. Majumdar A, Puri N, Cuenoud B, Natt F, Martin P, Khorlin A, Dyatkina N, George AJ, Miller PS and Seidman MM. 2003. Cell cycle modulation of gene targeting by a triple helix-forming oli-gonucleotide. J Biol Chem 278:11072-11077.
137. Majumdar A, Muniandy PA, Liu J, Liu JL, Liu ST, Cuenoud B and Seidman MM. 2008. Targeted gene knock in and sequence modulation mediated by a psoralen-linked triplex-forming oligonucle-otide. J Biol Chem 283:11244-11252.
138. Malinge JM, Perez C and Leng M. 1994. Base sequence-independent distorsions induced by interstrand cross-links in cis-diamminedichloroplatinum (II)-modifed DNA. Nucleic Acids Res 22:3834-3839.
139. Malinge JM, Giraud-Panis MJ and Leng M. 1999. Interstrand crosslinks of cisplatin induce striking distortions in DNA. J Inorg Biochem 77:23-29.
140. Malkova A, Ivanov EL and Haber JE. 1996. Double-strand break repair in the absence of RAD51 in yeast: a possible role for break-induced DNA replication. Proc Natl Acad Sci USA 93:7131-7136.
141. Manor H, Rao BS and Martin RG. 1988. Abundance and degree of dispersion of genomic d(GA)n.d(TC)n sequences. J Mol Evol 27:96-101.
142. Maor-Shoshani A, Meira LB, Yang X and Samson LD. 2008. 3-Methyladenine DNA glycosylase is important for cellular resistance to psoralen interstrand cross-links. DNA Repair (Amst) 7:1399-1406.
143. Marini F, Kim N, Schufert A and Wood RD. 2003. POLN, a nuclear PolA family DNA polymerase homologous to the DNA cross-link sensitivity protein Mus308. J Biol Chem 278:32014-32019.
144. Marti TM, Hefner E, Feeney L, Natale V and Cleaver JE. 2006. H2AX phosphorylation within the G1 phase after UV irradiation depends on nucleotide excision repair and not DNA double-strand breaks. Proc Natl Acad Sci USA 103:9891-9896.
145. Masuda Y, Ohmae M, Masuda K and Kamiya K. 2003. Structure and enzymatic properties of a stable complex of the human REV1 and REV7 proteins. J Biol Chem 278:12356-12360.
146. Matsumoto A, Vos JM and Hanawalt PC. 1989. Repair analysis of mito-mycin C-induced DNA crosslinking in ribosomal RNA genes in lymphoblastoid cells from Fanconi's anemia patients. Mutat Res 217:185-192.
147. McCabe KM, Hemphill A, Akkari Y, Jakobs PM, Pauw D, Olson SB, Moses RE and Grompe M. 2008. ERCC1 is required for FANCD2 focus formation. Mol Genet Metab 95:66-73.
148. McCabe KM, Olson SB and Moses RE. 2009. DNA interstrand crosslink repair in mammalian cells. J Cell Physiol 220:569-573.
149. McHugh PJ and Sarkar S. 2006. DNA interstrand cross-link repair in the cell cycle: a critical role for polymerase zeta in G(1) phase. Cell Cycle 5:1044-1047.
150. McHugh PJ, Sones WR and Hartley JA. 2000. Repair of intermediate structures produced at DNA interstrand cross-links in Saccharomyces cerevisiae. Mol Cell Biol 20:3425-3433.
151. McHugh PJ, Spanswick VJ and Hartley JA. 2001. Repair of DNA inter-strand crosslinks: molecular mechanisms and clinical relevance. Lancet Oncol 2:483-490.
152. McKay BC, Becerril C and Ljungman M. 2001. P53 plays a protective role against UV-and cisplatin-induced apoptosis in transcription-coupled repair profcient fbroblasts. Oncogene 20:6805-6808.
153. McMahon LW, Sangerman J, Goodman SR, Kumaresan K and Lambert MW. 2001. Human alpha spectrin II and the FANCA, FANCC, and FANCG proteins bind to DNA containing psoralen interstrand cross-links. Biochemistry 40:7025-7034.
154. McMahon LW, Zhang P, Sridharan DM, Leferts JA and Lambert MW. 2009. Knockdown of alphaII spectrin in normal human cells by siRNA leads to chromosomal instability and decreased DNA interstrand cross-link repair. Biochem Biophys Res Commun 381:288-293.
155. Meniel V, Magana-Schwencke N and Averbeck D. 1995a. Preferential repair in Saccharomyces cerevisiae rad mutants after induction of interstrand cross-links by 8-methoxypsoralen plus UVA. Mutagenesis 10:543-548.
156. Meniel V, Magana-Schwencke N and Averbeck D. 1995b. Preferential repair in yeast after induction of interstrand cross-links by 8-methoxypsoralen plus UVA. Mutat Res 329:121-130.
157. Miao F, Bouziane M, Dammann R, Masutani C, Hanaoka F, Pfeifer G and O'Connor TR. 2000. 3-methyladenine-DNA glycosylase (MPG protein) interacts with human RAD23 proteins. J Biol Chem 275:28433-28438.
158. Millard JT, Raucher S and Hopkins PB. 1990. Mechlorethamine crosslinks deoxyguanosine residues at 5′GNC residues in duplex DNA fragments. J Am Chem Soc 112:2549-2560.
159. Millington GW and Levell NJ. 2007. Vitiligo: the historical curse of depigmentation. Int J Dermatol 46:990-995.
160. Min JH and Pavletich NP. 2007. Recognition of DNA damage by the Rad4 nucleotide excision repair protein. Nature 449:570-575.
161. Minko IG, Harbut MB, Kozekov ID, Kozekova A, Jakobs PM, Olson SB, Moses RE, Harris TM, Rizzo CJ and Lloyd RS. 2008. Role for DNA polymerase kappa in the processing of N2-N2-guanine inter-strand cross-links. J Biol Chem 283:17075-17082.
162. Mirchandani KD and D'Andrea AD. 2006. Te Fanconi anemia/ BRCA pathway: a coordinator of cross-link repair. Exp Cell Res 312:2647-2653.
163. Mirchandani KD, McCafrey RM and D'Andrea AD. 2008. Te Fanconi anemia core complex is required for efcient point mutagenesis and Rev1 foci assembly. DNA Repair (Amst) 7:902-911.
164. Misra RR and Vos JM. 1993. Defective replication of psoralen adducts detected at the gene-specifc level in xeroderma pigmentosum variant cells. Mol Cell Biol 13:1002-1012.
165. Mitchell JR, Hoeijmakers JH and Niedernhofer LJ. 2003. Divide and conquer: nucleotide excision repair battles cancer and ageing. Curr Opin Cell Biol 15:232-240.
166. Mogi S, Butcher CE and Oh DH. 2008. DNA polymerase eta reduces the gamma-H2AX response to psoralen interstrand crosslinks in human cells. Exp Cell Res 314:887-895.
167. Mogi S and Oh DH. 2006. gamma-H2AX formation in response to interstrand crosslinks requires XPF in human cells. DNA Repair (Amst) 5:731-740.
168. Moldovan GL and D'Andrea AD. 2009. How the Fanconi anemia pathway guards the genome. Annu Rev Genet 43:223-249.
169. Mu D, Bessho T, Nechev LV, Chen DJ, Harris TM, Hearst JE and Sancar A. 2000. DNA interstrand cross-links induce futile repair synthesis in mammalian cell extracts. Mol Cell Biol 20:2446-2454.
170. Muniandy PA, Tapa D, Tazhathveetil AK, Liu ST and Seidman MM. 2009. Repair of laser localized DNA interstrand crosslinks in G1 phase mammalian cells. J Biol Chem 284:27908-27917.
171. Munoz IM, Hain K, Declais AC, Gardiner M, Toh GW, Sanchez-Pulido L, Heuckmann JM, Toth R, Macartney T, Eppink B, Kanaar R, Ponting CP, Lilley DM and Rouse J. 2009. Coordination of structure-specifc nucleases by human SLX4/BTBD12 is required for DNA repair. Mol Cell 35:116-127.
172. Murray D and Meyn RE. 1986. Cell cycle-dependent cytotoxic-ity of alkylating agents: determination of nitrogen mustard-induced DNA cross-links and their repair in Chinese hamster ovary cells synchronized by centrifugal elutriation. Cancer Res 46:2324-2329.
173. Nakanishi K, Taniguchi T, Ranganathan V, New HV, Moreau LA, Stotsky M, Mathew CG, Kastan MB, Weaver DT and D'Andrea AD. 2002. Interaction of FANCD2 and NBS1 in the DNA damage response. Nat Cell Biol 4:913-920.
174. Nick McElhinny SA, Pavlov YI and Kunkel TA. 2006. Evidence for extrinsic exonucleolytic proofreading. Cell Cycle 5:958-962.
175. Niedernhofer LJ, Essers J, Weeda G, Beverloo B, de Wit J, Muijtjens M, Odijk H, Hoeijmakers JH and Kanaar R. 2001. Te structure-specifc endonuclease Ercc1-Xpf is required for targeted gene replacement in embryonic stem cells. EMBO J 20:6540-6549.
176. Niedernhofer LJ, Odijk H, Budzowska M, van Drunen E, Maas A, Teil AF, de Wit J, Jaspers NG, Beverloo HB, Hoeijmakers JH and Kanaar R. 2004. The structure-specifc endonuclease Ercc1-Xpf is required to resolve DNA interstrand cross-link-induced double-strand breaks. Mol Cell Biol 24:5776-5787.
177. Niedernhofer LJ, Lalai AS and Hoeijmakers JH. 2005. Fanconi anemia (cross)linked to DNA repair. Cell 123:1191-1198.
178. Niedzwiedz W, Mosedale G, Johnson M, Ong CY, Pace P and Patel KJ. 2004. Te Fanconi anaemia gene FANCC promotes homologous recombination and error-prone DNA repair. Mol Cell 15:607-620.
179. Nojima K, Hochegger H, Saberi A, Fukushima T, Kikuchi K, Yoshimura M, Orelli BJ, Bishop DK, Hirano S, Ohzeki M, Ishiai M, Yamamoto K, Takata M, Arakawa H, Buerstedde JM, Yamazoe M, Kawamoto T, Araki K, Takahashi JA, Hashimoto N, Takeda S and Sonoda E. 2005. Multiple repair pathways mediate tolerance to chemotherapeutic cross-linking agents in vertebrate cells. Cancer Res 65:11704-11711.
180. Noll DM, Noronha AM, Wilds CJ and Miller PS. 2004. Preparation of interstrand cross-linked DNA oligonucleotide duplexes. Front Biosci 9:421-437.
181. Noll DM, Webba da SM, Noronha AM, Wilds CJ, Colvin OM, Gamcsik MP and Miller PS. 2005. Structure, fexibility, and repair of two diferent orientations of the same alkyl interstrand DNA cross-link. Biochemistry 44:6764-6775.
182. Noll DM, Mason TM and Miller PS. 2006. Formation and repair of interstrand cross-links in DNA. Chem Rev 106:277-301.
183. Norman D, Live D, Sastry M, Lipman R, Hingerty BE, Tomasz M, Broyde S and Patel DJ. 1990. NMR and computational characterization of mitomycin cross-linked to adjacent deoxyguanosines in the minor groove of the d(T-A-C-G-T-A).d(T-A-C-G-T-A) duplex. Biochemistry 29:2861-2875.
184. Noronha AM, Noll DM, Wilds CJ and Miller PS. 2002. N(4)C-ethyl-N(4)C cross-linked DNA: synthesis and characterization of duplexes with interstrand cross-links of diferent orientations. Biochemistry 41:760-771.
185. Ojwang JO, Grueneberg DA and Loechler EL. 1989. Synthesis of a duplex oligonucleotide containing a nitrogen mustard inter-strand DNA-DNA cross-link. Cancer Res 49:6529-6537.
186. Oshige M, Aoyagi N, Harris PV, Burtis KC and Sakaguchi K. 1999. A new DNA polymerase species from Drosophila melanogaster: a probable mus308 gene product. Mutat Res 433:183-192.
187. Osman F and Whitby MC. 2007. Exploring the roles of Mus81-Eme1/ Mms4 at perturbed replication forks. DNA Repair (Amst) 6:1004-1017.
188. Palom Y, Belcourt MF, Musser SM, Sartorelli AC, Rockwell S and Tomasz M. 2000. Structure of adduct X, the last unknown of the six major DNA adducts of mitomycin C formed in EMT6 mouse mammary tumor cells. Chem Res Toxicol 13:479-488.
189. Papadopoulo D, Averbeck D and Moustacchi E. 1987. The fate of 8-methoxypsoralen-photoinduced DNA interstrand crosslinks in Fanconi's anemia cells of defned genetic complementation groups. Mutat Res 184:271-280.
190. Papadopoulo D, Guillouf C, Porfrio B and Moustacchi E. 1990a. Decreased mutagenicity in Fanconi's anemia lymphoblasts following treatment with photoactivated psoralens. Prog Clin Biol Res 340A:241-248.
191. Papadopoulo D, Porfrio B and Moustacchi E. 1990b. Mutagenic response of Fanconi's anemia cells from a defned complementation group after treatment with photoactivated bifunctional psoralens. Cancer Res 50:3289-3294.
192. Patel KJ and Joenje H. 2007. Fanconi anemia and DNA replication repair. DNA Repair (Amst) 6:885-890.
193. Patrick SM, Tillison K and Horn JM. 2008. Recognition of cisplatin-DNA interstrand cross-links by replication protein A. Biochemistry 47:10188-10196.
194. Payne A and Chu G. 1994. Xeroderma pigmentosum group E binding factor recognizes a broad spectrum of DNA damage. Mutat Res 310:89-102.
195. Peng M, Litman R, Xie J, Sharma S, Brosh Jr RM, and Cantor SB. 2007. The FANCJ/MutLalpha interaction is required for correction of the cross-link response in FA-J cells. EMBO J 26:3238-3249.
196. Perez C, Leng M and Malinge JM. 1997. Rearrangement of interstrand cross-links into intrastrand cross-links in cis-diamminedichloroplatinum(II)- modifed DNA. Nucleic Acids Res 25:896-903.
197. Pichierri P, Averbeck D and Rosselli F. 2002. DNA cross-link-dependent RAD50/MRE11/NBS1 subnuclear assembly requires the Fanconi anemia C protein. Hum Mol Genet 11:2531-2546.
198. Poklar N, Pilch DS, Lippard SJ, Redding EA, Dunham SU and Breslauer KJ. 1996. Infuence of cisplatin intrastrand crosslinking on the conformation, thermal stability, and energetics of a 20-mer DNA duplex. Proc Natl Acad Sci USA 93:7606-7611.
199. Poll EH, Arwert F, Kortbeek HT and Eriksson AW. 1984. Fanconi anaemia cells are not uniformly defcient in unhooking of DNA inter-strand crosslinks, induced by mitomycin C or 8-methoxypsoralen plus UVA. Hum Genet 68:228-234.
200. Pritsos CA and Sartorelli AC. 1986. Generation of reactive oxygen radicals through bioactivation of mitomycin antibiotics. Cancer Res 46:3528-3532.
201. Puri N, Majumdar A, Cuenoud B, Natt F, Martin P, Boyd A, Miller PS and Seidman MM. 2001. Targeted gene knockout by 2′-O-aminoethyl modifed triplex forming oligonucleotides. J Biol Chem 276:28991-28998.
202. Puri N, Majumdar A, Cuenoud B, Natt F, Martin P, Boyd A, Miller PS and Seidman MM. 2002. Minimum number of 2′-O-(2-aminoethyl) residues required for gene knockout activity by triple helix forming oligonucleotides. Biochemistry 41:7716-7724.
203. Puri N, Majumdar A, Cuenoud B, Miller PS and Seidman MM. 2004. Importance of clustered 2′-O-(2-aminoethyl) residues for the gene targeting activity of triple helix-forming oligonucleotides. Biochemistry 43:1343-1351.
204. Raha M, Wang G, Seidman MM and Glazer PM. 1996. Mutagenesis by third-strand-directed psoralen adducts in repair-def-cient human cells: high frequency and altered spectrum in a xeroderma pigmentosum variant. Proc Natl Acad Sci USA 93:2941-2946.
205. Rajski SR and Williams RM. 1998. DNA cross-linking agents as antitumor drugs. Chem Rev 98:2723-2796.
206. Raschle M, Knipsheer P, Enoiu M, Angelov T, Sun J, Grifth JD, Ellenberger TE, Scharer OD and Walter JC. 2008. Mechanism of replication-coupled DNA interstrand crosslink repair. Cell 134:969-980.
207. Reardon JT, Nichols AF, Keeney S, Smith CA, Taylor JS, Linn S and Sancar A. 1993. Comparative analysis of binding of human damaged DNA-binding protein (XPE) and Escherichia coli damage recognition protein (UvrA) to the major ultraviolet pho-toproducts: T[c s]T, T[t s]T, T[6-4]T, and T[Dewar]T. J Biol Chem 268:21301-21308.
208. Richards S, Liu ST, Majumdar A, Liu JL, Nairn RS, Bernier M, Maher V and Seidman MM. 2005. Triplex targeted genomic crosslinks enter separable deletion and base substitution pathways. Nucleic Acids Res 33:5382-5393.
209. Rink SM and Hopkins PB. 1995. A mechlorethamine-induced DNA interstrand cross-link bends duplex DNA. Biochemistry 34:1439-1445.
210. Rink SM, Lipman R, Alley SC, Hopkins PB and Tomasz M. 1996. Bending of DNA by the mitomycin C-induced, GpG intrastrand cross-link. Chem Res Toxicol 9:382-389.
211. Rogakou EP, Boon C, Redon C and Bonner WM. 1999. Megabase chro-matin domains involved in DNA double-strand breaks in vivo. J Cell Biol 146:905-916.
212. Roques C, Coulombe Y, Delannoy M, Vignard J, Grossi S, Brodeur I, Rodrigue A, Gautier J, Stasiak AZ, Stasiak A, Constantinou A and Masson JY. 2009. MRE11-RAD50-NBS1 is a critical regulator of FANCD2 stability and function during DNA double-strand break repair. EMBO J 28:2400-2413.
213. Rosenberg B. 1977. Noble metal complexes in cancer chemotherapy. Adv Exp Med Biol 91:129-150.
214. Rosenberg B, VanCamp L and Krigas T. 1965. Inhibition of cell division in E. coli by electrolysis products from a platinum electrode. Nature 205:698-699.
215. Rothfuss A and Grompe M. 2004. Repair kinetics of genomic inter-strand DNA cross-links: evidence for DNA double-strand break-dependent activation of the Fanconi anemia/BRCA pathway. Mol Cell Biol 24:123-134.
216. Saenz-Méndez P, Guedes RC, dos Santos D and Eriksson LA. 2007. Teoretical study of sequence selectivity and preferred binding mode of psoralen with DNA. Research Letters in Physical Chemistry vol.2007, Article ID 60623, 5 pages, 2007. doi:10.1155/2007/60623.
217. Safran WA, Ahmed S, Bellevue S, Pereira G, Patrick T, Sanchez W, Tomas S, Alberti M and Hearst JE. 2004. DNA repair defects channel interstrand DNA cross-links into alternate recombinational and error-prone repair pathways. J Biol Chem 279:36462-36469.
218. Sage E, Drobetsky EA and Moustacchi E. 1993. 8-Methoxypsoralen induced mutations are highly targeted at crosslinkable sites of photoaddition on the non-transcribed strand of a mammalian chromosomal gene. EMBO J 12:397-402.
219. Sargent RG, Rolig RL, Kilburn AE, Adair GM, Wilson JH and Nairn RS. 1997. Recombination-dependent deletion formation in mammalian cells defcient in the nucleotide excision repair gene ERCC1. Proc Natl Acad Sci USA 94:13122-13127.
220. Sarkar S, Davies AA, Ulrich HD and McHugh PJ. 2006. DNA interstrand crosslink repair during G1 involves nucleotide excision repair and DNA polymerase zeta. EMBO J 25:1285-1294.
221. Sartorelli AC, Hodnick WF, Belcourt MF, Tomasz M, Hafty B, Fischer JJ and Rockwell S. 1994. Mitomycin C: a prototype bioreductive agent. Oncol Res 6:501-508.
222. Sasaki MS, Takata M, Sonoda E, Tachibana A and Takeda S. 2004. Recombination repair pathway in the maintenance of chromosomal integrity against DNA interstrand crosslinks. Cytogenet Genome Res 104:28-34.
223. Schroth GP and Ho PS. 1995. Occurrence of potential cruciform and H-DNA forming sequences in genomic DNA. Nucleic Acids Res 23:1977-1983.
224. Scrima A, Konickova R, Czyzewski BK, Kawasaki Y, Jefrey PD, Groisman R, Nakatani Y, Iwai S, Pavletich NP and Toma NH. 2008. Structural basis of UV DNA-damage recognition by the DDB1-DDB2 complex. Cell 135:1213-1223.
225. Seidman MM and Glazer PM. 2003. The potential for gene repair via triple helix formation. J Clin Invest 112:487-494.
226. Seidman MM, Puri N, Majumdar A, Cuenoud B, Miller PS and Alam R. 2005. The development of bioactive triple helix-forming oligonu-cleotides. Ann NY Acad Sci 1058:119-127.
227. Seki M and Wood RD. 2008. DNA polymerase theta (POLQ) can extend from mismatches and from bases opposite a (6-4) photoproduct. DNA Repair (Amst) 7:119-127.
228. Seki M, Marini F and Wood RD. 2003. POLQ (Pol theta), a DNA polymerase and DNA-dependent ATPase in human cells. Nucleic Acids Res 31:6117-6126.
229. Shachar S, Ziv O, Avkin S, Adar S, Wittschieben J, Reissner T, Chaney S, Friedberg EC, Wang Z, Carell T, Geacintov N and Livneh Z. 2009. Two-polymerase mechanisms dictate error-free and error-prone translesion DNA synthesis in mammals. EMBO J 28:383-393.
230. Shahid KA, Majumdar A, Alam R, Liu ST, Kuan JY, Sui X, Cuenoud B, Glazer PM, Miller PS and Seidman MM. 2006. Targeted cross-linking of the human beta-globin gene in living cells mediated by a triple helix forming oligonucleotide. Biochemistry 45:1970-1978.
231. Shen X, Jun S, O'Neal LE, Sonoda E, Bemark M, Sale JE and Li L. 2006. REV3 and REV1 play major roles in recombination-independent repair of DNA interstrand cross-links mediated by monoubiq-uitinated proliferating cell nuclear antigen (PCNA). J Biol Chem 281:13869-13872.
232. Sinden RR and Hagerman PJ. 1984. Interstrand psoralen cross-links do not introduce appreciable bends in DNA. Biochemistry 23:6299-6303.
233. Sladek FM, Melian A and Howard-Flanders P. 1989a. Incision by UvrABC excinuclease is a step in the path to mutagenesis by psoralen crosslinks in Escherichia coli. Proc Natl Acad Sci USA 86:3982-3986.
234. Sladek FM, Munn MM, Rupp WD and Howard-Flanders P. 1989b. In vitro repair of psoralen-DNA cross-links by RecA, UvrABC, and the 5′-exonuclease of DNA polymerase I. J Biol Chem 264:6755-6765.
235. Smeaton MB, Hlavin EM, McGregor MT, Noronha AM, Wilds CJ and Miller PS. 2008. Distortion-dependent unhooking of inter-strand cross-links in mammalian cell extracts. Biochemistry 47:9920-9930.
236. Smeaton MB, Hlavin EM, Noronha AM, Murphy SP, Wilds CJ and Miller PS. 2009. Efect of cross-link structure on DNA interstrand cross-link repair synthesis. Chem Res Toxicol 22:1285-1297.
237. Spielmann HP, Dwyer TJ, Hearst JE and Wemmer DE. 1995a. Solution structures of psoralen monoadducted and cross-linked DNA oli-gomers by NMR spectroscopy and restrained molecular dynamics. Biochemistry 34:12937-12953.
238. Spielmann HP, Dwyer TJ, Sastry SS, Hearst JE and Wemmer DE. 1995b. DNA structural reorganization upon conversion of a psoralen furan-side monoadduct to an interstrand cross-link: implications for DNA repair. Proc Natl Acad Sci USA 92:2345-2349.
239. Stern RS. 2007. Psoralen and ultraviolet a light therapy for psoriasis. N Engl J Med 357:682-690.
240. Sugasawa K and Hanaoka F. 2007. Sensing of DNA damage by XPC/Rad4: one protein for many lesions. Nat Struct Mol Biol 14:887-888.
241. Sugasawa K, Shimizu Y, Iwai S and Hanaoka F. 2002. A molecular mechanism for DNA damage recognition by the xeroderma pigmentosum group C protein complex. DNA Repair (Amst) 1:95-107.
242. Sugasawa K, Okuda Y, Saijo M, Nishi R, Matsuda N, Chu G, Mori T, Iwai S, Tanaka K, Tanaka K and Hanaoka F. 2005. UV-induced ubiquitylation of XPC protein mediated by UV-DDB-ubiquitin ligase complex. Cell 121:387-400.
243. Sun W, Nandi S, Osman F, Ahn JS, Jakovleska J, Lorenz A and Whitby MC. 2008. Te FANCM ortholog Fml1 promotes recombination at stalled replication forks and limits crossing over during DNA double-strand break repair. Mol Cell 32:118-128.
244. Takata K, Shimizu T, Iwai S and Wood RD. 2006. Human DNA polymer-ase N (POLN) is a low fdelity enzyme capable of error-free bypass of 5S-thymine glycol. J Biol Chem 281:23445-23455.
245. Taniguchi T, Garcia-Higuera I, Andreassen PR, Gregory RC, Grompe M and D'Andrea AD. 2002. S-phase-specifc interaction of the Fanconi anemia protein, FANCD2, with BRCA1 and RAD51. Blood 100:2414-2420.
246. Tazhathveetil AK, Liu ST, Indig FE and Seidman MM. 2007. Psoralen conjugates for visualization of genomic interstrand cross-links localized by laser photoactivation. Bioconjug Chem 18:431-437.
247. Toma BS, Wakasugi M, Christensen J, Reddy MC and Vasquez KM. 2005. Human XPC-hHR23B interacts with XPA-RPA in the recognition of triplex-directed psoralen DNA interstrand crosslinks. Nucleic Acids Res 33:2993-3001.
248. Tomas CB, Kohn KW and Bonner WM. 1978. Characterization of DNA-protein cross-links formed by treatment of L1210 cells and nuclei with bis(2-chloroethyl)methylamine (nitrogen mustard). Biochemistry 17:3954-3958.
249. Tompson LH and Hinz JM. 2009. Cellular and molecular consequences of defective Fanconi anemia proteins in replication-coupled DNA repair: Mechanistic insights. Mutat Res 668:54-72.
250. Tompson LH and Schild D. 2002. Recombinational DNA repair and human disease. Mutat Res 509:49-78.
251. Tompson LH, Hinz JM, Yamada NA and Jones NJ. 2005. How Fanconi anemia proteins promote the four Rs: replication, recombination, repair, and recovery. Environ Mol Mutagen 45:128-142.
252. Van HB, Gamper H, Holbrook SR, Hearst JE and Sancar A. 1986. Action mechanism of ABC excision nuclease on a DNA substrate containing a psoralen crosslink at a defned position. Proc Natl Acad Sci USA 83:8077-8081.
253. Vidal LS, Santos LB, Lage C and Leitao AC. 2006. Enhanced sensitivity of Escherichia coli uvrB mutants to mitomycin C points to a UV-C distinct repair for DNA adducts. Chem Res Toxicol 19:1351-1356.
254. Vogel EW, Barbin A, Nivard MJ, Stack H F, Waters MD and Lohman PH. 1998. Heritable and cancer risks of exposures to anticancer drugs: inter-species comparisons of covalent deoxyribonucleic acid-binding agents. Mutat Res 400:509-540.
255. Vos JM and Hanawalt PC. 1987. Processing of psoralen adducts in an active human gene: repair and replication of DNA containing monoadducts and interstrand cross-links. Cell 50:789-799.
256. Wang G, Levy DD, Seidman MM and Glazer PM. 1995. Targeted muta-genesis in mammalian cells mediated by intracellular triple helix formation. Mol Cell Biol 15:1759-1768.
257. Wang QE, Zhu Q, Wani G, Chen J and Wani AA. 2004. UV radiation-induced XPC translocation within chromatin is mediated by damaged-DNA binding protein, DDB2. Carcinogenesis 25:1033-1043.
258. Wang X, Peterson CA, Zheng H, Nairn RS, Legerski RJ and Li L. 2001. Involvement of nucleotide excision repair in a recombination-independent and error-prone pathway of DNA interstrand crosslink repair. Mol Cell Biol 21:713-720.
259. Webba da SM, Noronha AM, Noll DM, Miller PS, Colvin OM and Gamcsik M P. 2002. Solution structure of a DNA duplex containing mispair-aligned N4C-ethyl-N4C interstrand cross-linked cytosines. Biochemistry 41:15181-15188.
260. Weidner MF, Sigurdsson ST and Hopkins PB. 1990. Sequence preferences of DNA interstrand cross-linking agents: dG-to-dG cross-linking at 5′-CG by structurally simplifed analogues of mitomycin C. Biochemistry 29:9225-9233.
261. Wu HI, Brown JA, Dorie MJ, Lazzeroni L and Brown JM. 2004. Genome-wide identifcation of genes conferring resistance to the antican-cer agents cisplatin, oxaliplatin, and mitomycin C. Cancer Res 64:3940-3948.
262. Wu JH, Wilson JB, Wolfreys AM, Scott A and Jones NJ. 2009. Optimization of the comet assay for the sensitive detection of PUVA-induced DNA interstrand cross-links. Mutagenesis 24:173-181.
263. Wu Q, Christensen LA, Legerski RJ and Vasquez KM. 2005. Mismatch repair participates in error-free processing of DNA interstrand crosslinks in human cells. EMBO Rep 6:551-557.
264. Wu Y and Brosh Jr RM. 2009. FANCJ helicase operates in the Fanconi Anemia DNA repair pathway and the response to replicational stress. Curr Mol Med 9:470-482.
265. Yang SC, Lin JG, Chiou CC, Chen LY and Yang JL. 1994. Mutation spe-cifcity of 8-methoxypsoralen plus two doses of UVA irradiation in the hprt gene in diploid human fbroblasts. Carcinogenesis 15:201-207.
266. Yang W. 2008. Structure and mechanism for DNA lesion recognition. Cell Res 18:184-197.
267. Yang W and Woodgate R. 2007. What a diference a decade makes: insights into translesion DNA synthesis. Proc Natl Acad Sci USA 104:15591-15598.
268. Youds JL, Barber LJ, Ward JD, Collis SJ, O'Neil NJ, Boulton SJ and Rose AM. 2008. DOG-1 is the Caenorhabditis elegans BRIP1/ FANCJ homologue and functions in interstrand cross-link repair. Mol Cell Biol 28:1470-1479.
269. Youds JL, Barber LJ and Boulton SJ. 2009. C. elegans: A model of Fanconi anemia and ICL repair. Mutat Res 668:103-116.
270. Zamble DB, Mu D, Reardon JT, Sancar A and Lippard SJ. 1996. Repair of cisplatin-DNA adducts by the mammalian excision nuclease. Biochemistry 35:10004-10013. (Pubitemid 26269915)
271. Zhang N, Lu X, Zhang X, Peterson CA and Legerski RJ. 2002. hMutSbeta is required for the recognition and uncoupling of psoralen inter-strand cross-links in vitro. Mol Cell Biol 22:2388-2397.
272. Zhang N, Lu X and Legerski RJ. 2003. Partial reconstitution of human interstrand cross-link repair in vitro: characterization of the roles of RPA and PCNA. Biochem Biophys Res Commun 309:71-78.
273. Zhang N, Kaur R, Lu X, Shen X, Li L and Legerski RJ. 2005. Te Pso4 mRNA splicing and DNA repair complex interacts with WRN for processing of DNA interstrand cross-links. J Biol Chem 280:40559-40567.
274. Zhang N, Liu X, Li L and Legerski R. 2007. Double-strand breaks induce homologous recombinational repair of interstrand cross-links via cooperation of MSH2, ERCC1-XPF, REV3, and the Fanconi anemia pathway. DNA Repair (Amst) 6:1670-1678.
275. Zheng H, Wang X, Warren AJ, Legerski RJ, Nairn RS, Hamilton JW and Li L. 2003. Nucleotide excision repair-and polymerase eta-mediated error-prone removal of mitomycin C interstrand crosslinks. Mol Cell Biol 23:754-761.
276. Zhu G and Lippard SJ. 2009. Photoafnity labeling reveals nuclear proteins that uniquely recognize cisplatin-DNA interstrand crosslinks. Biochemistry 48:4916-4925.
277. Zietlow L, Smith LA, Bessho M and Bessho T. 2009. Evidence for the involvement of human DNA polymerase N in the repair of DNA interstrand cross-links. Biochemistry 48:11817-11824.