Initiation of DNA interstrand cross-link repair in mammalian cells

Environmental and Molecular Mutagenesis

Volumn 51, Issue 6, 2010, Pages 604-624

  Hlavin, Erica M ^a   Smeaton, Michael B ^a   Miller, Paul S ^a  

^a JOHNS HOPKINS BLOOMBERG SCHOOL OF PUBLIC HEALTH   (United States)

Author keywords

Cross link structure; Cross link unhooking; Global genome repair; Replication coupled repair; Transcription coupled repair

Indexed keywords

4' HYDROXYMETHYL 4,5',8 TRIMETHYLPSORALEN; BRCA1 PROTEIN; BRCA2 PROTEIN; CHLORMETHINE; CISPLATIN; CYCLOPROPANE; ENDONUCLEASE; EXCISION REPAIR CROSS COMPLEMENTING PROTEIN 1; FANCONI ANEMIA GROUP A PROTEIN; FANCONI ANEMIA GROUP D2 PROTEIN; HISTONE H2AX; MITOMYCIN C; MUS81 MMS4 PROTEIN; PSORALEN; UNCLASSIFIED DRUG; WERNER SYNDROME PROTEIN; XERODERMA PIGMENTOSUM GROUP D PROTEIN; XPF PROTEIN EXCISION REPAIR CROSS COMPLEMENTING PROTEIN 1; CROSS LINKING REAGENT; MITOMYCIN;

CANCER CELL; CELL CYCLE G1 PHASE; CELL CYCLE PHASE; CELL CYCLE S PHASE; CYTOTOXICITY; DNA CROSS LINKING; DNA REPAIR; EXCISION REPAIR; FANCONI ANEMIA; HOMOLOGOUS RECOMBINATION; HUMAN; MAMMAL CELL; NONHUMAN; REVIEW; ANIMAL; DRUG EFFECT; GENETIC TRANSCRIPTION; START CODON;

MAMMALIA;

ANIMALS; CISPLATIN; CODON, INITIATOR; CROSS-LINKING REAGENTS; DNA REPAIR; HUMANS; MITOMYCIN; TRANSCRIPTION, GENETIC;

EID: 77951889437     PISSN: 08936692     EISSN: 10982280     Source Type: Journal    
DOI: 10.1002/em.20559     Document Type: Review

References (130)

1. Ahmad A, Robinson AR, Duensing A, van Drunen E, Beverloo HB, Weisberg DB, Hasty P, Hoeijmakers JH, Niedernhofer LJ. 2008. ERCC1-XPF endonuclease facilitates DNA double-strand break repair. Mol Cell Biol 28:5082-5092.
2. Ahn B, Kang D, Kim H, Wei Q. 2004. Repair of mitomycin C cross-linked DNA in mammalian cells measured by a host cell reactivation assay. Mol Cells 18:249-255.
3. Akkari YM, Bateman RL, Reifsteck CA, Olson SB, Grompe M. 2000. DNA replication is required to elicit cellular responses to psoralen-induced DNA interstrand cross-links. Mol Cell Biol 20:8283-8289.
4. Al-Minawi AZ, Saleh-Gohari N, Helleday T. 2008. The ERCC1/XPF endonuclease is required for efficient single-strand annealing and gene conversion in mammalian cells. Nucleic Acids Res 36:1-9.
5. Al-Minawi AZ, Lee YF, Hakansson D, Johansson F, Lundin C, Saleh-Gohari N, Schultz N, Jenssen D, Bryant HE, Meuth M, Hinz JM, Helleday T. 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.
6. Andersson BS, Sadeghi T, Siciliano MJ, Legerski R, Murray D. 1996. Nucleotide excision repair genes as determinants of cellular sensitivity to cyclophosphamide analogs. Cancer Chemother Pharmacol 38:406-416.
7. Andersen SL, Bergstralh DT, Kohl KP, LaRocque JR, Moore CB, Sekelsky J. 2009. Drosophila MUS312 and the vertebrate ortholog BTBD12 interact with DNA structure-specific endonucleases in DNA repair and recombination. Mol Cell 35:128-135.
8. Andreassen PR, Ren K. 2009. Fanconi anemia proteins, DNA interstrand crosslink repair pathways and cancer therapy. Curr Cancer Drug Targets 9:101-117.
9. Atanassov B, Gospodinov A, Stoimenov I, Mladenov E, Russev G, Tsaneva I, Anachkova B. 2005. Repair of DNA interstrand crosslinks may take place at the nuclear matrix. J Cell Biochem 96:126-136.
10. Bachs O, Lanini L, Serratosa J, Coll MJ, Bastos R, Aligue R, Rius E, Carafoli E. 1990. Calmodulin-binding proteins in the nuclei of quiescent and proliferatively activated rat liver cells. J Biol Chem 265:18595-18600.
11. Balajee AS, May A, Dianov GL, Friedberg EC, Bohr VA. 1997. Reduced RNA polymerase II transcription in intact and permeabilized Cockayne syndrome group B cells. Proc Natl Acad Sci USA 94:4306-4311.
12. Ben-Yehoyada M, Wang LC, Kozekov ID, Rizzo CJ, Gottesman ME, Gautier J. 2009. Checkpoint signaling from a single DNA interstrand crosslink. Mol Cell 35:704-715.
13. Berardini M, Mackay W, Loechler EL. 1997. Evidence for a recombination-independent pathway for the repair of DNA interstrand cross-links based on a site-specific study with nitrogen mustard. Biochemistry 36:3506-3513.
14. Berardini M, Foster PL, 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.
15. Bergstralh DT, Sekelsky J. 2008. Interstrand crosslink repair: Can XPF-ERCC1 be let off the hook? Trends Genet 24:70-76.
16. Bessho T. 2003. Induction of DNA replication-mediated double strand breaks by psoralen DNA interstrand cross-links. J Biol Chem 278:5250-5254.
17. Bessho T, Mu D, Sancar A. 1997a. 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.
18. Bessho T, Sancar A, Thompson LH, Thelen MP. 1997b. Reconstitution of human excision nuclease with recombinant XPF-ERCC1 complex. J Biol Chem 272:3833-3837.
19. Bhagwat N, Olsen AL, Wang AT, Hanada K, Stuckert P, Kanaar R, D'Andrea A, Niedernhofer LJ, McHugh PJ. 2009. XPF-ERCC1 participates in the Fanconi anemia pathway of crosslink repair. Mol Cell Biol 29:6427-6437.
20. Bohr VA, Smith CA, Okumoto DS, Hanawalt PC. 1985. DNA repair in an active gene: Removal of pyrimidine dimers from the DHFR gene of CHO cells is much more efficient than in the genome overall. Cell 40:359-369.
21. Boulton SJ. 2006. Cellular functions of the BRCA tumour-suppressor proteins. Biochem Soc Trans 34 (Part 5):633-645.
22. Busch DB, van Vuuren H, de Wit J, Collins A, Zdzienicka MZ, Mitchell DL, Brookman KW, Stefanini M, Riboni R, Thompson LH, Albert RB, van Gool AJ, Hoeijmakers J. 1997. Phenotypic heterogeneity in nucleotide excision repair mutants of rodent complementation groups 1 and 4. Mutat Res 383:91-106.
23. Caldecott K, Jeggo P. 1991. Cross-sensitivity of gamma-ray-sensitive hamster mutants to cross-linking agents. Mutat Res 255:111-121.
24. Carreau M, Alon N, Bosnoyan-Collins L, Joenje H, Buchwald M. 1999. Drug sensitivity spectra in Fanconi anemia lymphoblastoid cell lines of defined complementation groups. Mutat Res 435:103-109.
25. Caulfield JL, Wishnok JS, Tannenbaum SR. 2003. Nitric oxide-induced interstrand cross-links in DNA. Chem Res Toxicol 16:571-574.
26. Cheng WH, Kusumoto R, Opresko PL, Sui X, Huang S, Nicolette ML, Paull TT, Campisi J, Seidman M, Bohr VA. 2006. Collaboration of Werner syndrome protein and BRCA1 in cellular responses to DNA interstrand cross-links. Nucleic Acids Res 34:2751-2760.
27. Ciccia A, Constantinou A, West SC. 2003. Identification and characterization of the human mus81-eme1 endonuclease. J Biol Chem 278:25172-25178.
28. Ciccia A, McDonald N, West SC. 2008. Structural and functional relationships of the XPF/MUS81 family of proteins. Annu Rev Biochem 77:259-287.
29. Cipak L, Watanabe N, Bessho T. 2006. The role of BRCA2 in replication-coupled DNA interstrand cross-link repair in vitro. Nat Struct Mol Biol 13:729-733.
30. Citterio E, Van Den Boom V, Schnitzler G, Kanaar R, Bonte E, Kingston RE, Hoeijmakers JH, Vermeulen W. 2000. ATP-dependent chromatin remodeling by the Cockayne syndrome B DNA repair-transcription-coupling factor. Mol Cell Biol 20:7643-7653.
31. Cleaver JE. 1980. DNA damage, repair systems and human hypersensitive diseases. J Environ Pathol Toxicol 3(4 Spec No):53-68.
32. Cole RS. 1973. Repair of DNA containing interstrand crosslinks in Escherichia coli: Sequential excision and recombination. Proc Natl Acad Sci USA 70:1064-1068.
33. Cole RS, Sinden RR. 1975. Repair of cross-linked DNA in Escherichia coli. Basic Life Sci 5B:487-495.
34. Damia G, Imperatori L, Stefanini M, D'Incalci M. 1996. Sensitivity of CHO mutant cell lines with specific defects in nucleotide excision repair to different anti-cancer agents. Int J Cancer 66:779-783.
35. De Silva IU, McHugh PJ, Clingen PH, Hartley JA. 2000. Defining the roles of nucleotide excision repair and recombination in the repair of DNA interstrand cross-links in mammalian cells. Mol Cell Biol 20:7980-7990.
36. De Silva IU, McHugh PJ, Clingen PH, Hartley JA. 2002. Defects in interstrand cross-link uncoupling do not account for the extreme sensitivity of ERCC1 and XPF cells to cisplatin. Nucleic Acids Res 30:3848-3856.
37. Dendouga N, Gao H, Moechars D, Janicot M, Vialard J, 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.
38. Dronkert ML, Kanaar R. 2001. Repair of DNA interstrand cross-links. Mutat Res 486:217-247.
39. Episkopou H, Kyrtopoulos SA, Sfikakis PP, Fousteri M, Dimopoulos MA, Mullenders LH, Souliotis VL. 2009. Association between transcriptional activity, local chromatin structure, and the efficiencies of both subpathways of nucleotide excision repair of melphalan adducts. Cancer Res 69:4424-4433.
40. Evans E, Moggs JG, Hwang JR, Egly JM, Wood RD. 1997. Mechanism of open complex and dual incision formation by human nucleotide excision repair factors. Embo J 16:6559-6573.
41. 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, Gaillard PH. 2009. Human SLX4 is a Holliday junction resolvase subunit that binds multiple DNA repair/recombination endonucleases. Cell 138:78-89.
42. Fisher LA, Bessho M, Bessho T. 2008. Processing of a psoralen DNA interstrand cross-link by XPF-ERCC1 complex in vitro. J Biol Chem 283:1275-1281.
43. Fousteri M, Mullenders LH. 2008. Transcription-coupled nucleotide excision repair in mammalian cells: Molecular mechanisms and biological effects. Cell Res 18:73-84.
44. Fousteri M, Vermeulen W, van Zeeland AA, Mullenders LH. 2006. Cockayne syndrome A, B proteins differentially regulate recruitment of chromatin remodeling and repair factors to stalled RNA polymerase II in vivo. Mol Cell 23:471-482.
45. Friedberg EC, Ehmann UK, Williams JI. 1979. Human diseases associated with defective DNA repair. Adv Radiat Biol 8:86-174.
46. Fujiwara Y. 1982. Defective repair of mitomycin C crosslinks in Fanconi's anemia and loss in confluent normal human and xeroderma pigmentosum cells. Biochim Biophys Acta 699:217-225.
47. Futscher BW, Pieper RO, Dalton WS, Erickson LC. 1992. Gene-specific DNA interstrand cross-links produced by nitrogen mustard in the human tumor cell line Colo320HSR. Cell Growth Differ 3:217-223.
48. Grillari J, Katinger H, Voglauer R. 2007. Contributions of DNA interstrand cross-links to aging of cells and organisms. Nucleic Acids Res 35:7566-7576.
49. Groisman R, Polanowska J, Kuraoka I, Sawada J, Saijo M, Drapkin R, Kisselev AF, Tanaka K, Nakatani Y. 2003. The ubiquitin ligase activity in the DDB2 and CSA complexes is differentially regulated by the COP9 signalosome in response to DNA damage. Cell 113:357-367.
50. Groisman R, Kuraoka I, Chevallier O, Gaye N, Magnaldo T, Tanaka K, Kisselev AF, Harel-Bellan A, Nakatani Y. 2006. CSA-dependent degradation of CSB by the ubiquitin-proteasome pathway establishes a link between complementation factors of the Cockayne syndrome. Genes Dev 20:1429-1434.
51. Hanada K, Budzowska M, Modesti M, Maas A, Wyman C, Essers J, Kanaar R. 2006. The structure-specific endonuclease Mus81-Eme1 promotes conversion of interstrand DNA crosslinks into double-strands breaks. Embo J 25:4921-4932.
52. Hoy CA, Thompson LH, Mooney CL, Salazar EP. 1985. Defective DNA cross-link removal in Chinese hamster cell mutants hypersensitive to bifunctional alkylating agents. Cancer Res 45:1737-1743.
53. Huang JC, Sancar A. 1994. Determination of minimum substrate size for human excinuclease. J Biol Chem 269:19034-19040.
54. Islas AL, Vos JM, Hanawalt PC. 1991. Differential introduction and repair of psoralen photoadducts to DNA in specific human genes. Cancer Res 51:2867-2873.
55. Islas AL, Baker FJ, Hanawalt PC. 1994. Transcription-coupled repair of psoralen cross-links but not monoadducts in Chinese hamster ovary cells. Biochemistry 33:10794-10799.
56. Jones JC, Zhen WP, Reed E, Parker RJ, Sancar A, Bohr VA. 1991. Gene-specific formation and repair of cisplatin intrastrand adducts and interstrand cross-links in Chinese hamster ovary cells. J Biol Chem 266:7101-7107.
57. Kennedy RD, D'Andrea AD. 2005. The Fanconi Anemia/BRCA pathway: New faces in the crowd. Genes Dev 19:2925-2940.
58. Kozekov ID, Nechev LV, Moseley MS, Harris CM, Rizzo CJ, Stone MP, Harris TM. 2003. DNA interchain cross-links formed by acrolein and crotonaldehyde. J Am Chem Soc 125:50-61.
59. Kumaresan KR, 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.
60. Kumaresan KR, Hang B, Lambert MW. 1995. Human endonucleolytic incision of DNA 3′ and 5′ to a site-directed psoralen monoadduct and interstrand cross-link. J Biol Chem 270:30709-30716.
61. Kumaresan KR, Hwang M, Thelen MP, 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.
62. Kumaresan KR, Sridharan DM, McMahon LW, Lambert MW. 2007. Deficiency in incisions produced by XPF at the site of a DNA interstrand cross-link in Fanconi anemia cells. Biochemistry 46:14359-14368.
63. Kumari A, Minko IG, Harbut MB, Finkel SE, Goodman MF, Lloyd RS. 2008. Replication bypass of interstrand cross-link intermediates by Escherichia coli DNA polymerase IV. J Biol Chem 283:27433-27437.
64. Kuraoka I, Kobertz WR, Ariza RR, Biggerstaff M, Essigmann JM, Wood RD. 2000. Repair of an interstrand DNA cross-link initiated by ERCC1-XPF repair/recombination nuclease. J Biol Chem 275:26632-26636.
65. Laine JP, Egly JM. 2006a. Initiation of DNA repair mediated by a stalled RNA polymerase IIO. EMBO J 25:387-397.
66. Laine JP, Egly JM. 2006b. When transcription and repair meet: A complex system. Trends Genet 22:430-436.
67. Larminat F, Bohr VA. 1994. Role of the human ERCC-1 gene in gene-specific repair of cisplatin-induced DNA damage. Nucleic Acids Res 22:3005-3010.
68. Larminat F, Zhen W, Bohr VA. 1993. Gene-specific DNA repair of interstrand cross-links induced by chemotherapeutic agents can be preferential. J Biol Chem 268:2649-2654.
69. Legerski R. Mechanisms of S phase repair of interstrand crosslinks. Environ Mol Mutag (in press).
70. Li L, Peterson CA, Lu X, Wei P, Legerski RJ. 1999. Interstrand cross-links induce DNA synthesis in damaged and undamaged plasmids in mammalian cell extracts. Mol Cell Biol 19:5619-5630.
71. Li L, Peterson CA, Zhang X, Legerski RJ. 2000. Requirement for PCNA and RPA in interstrand crosslink-induced DNA synthesis. Nucleic Acids Res 28:1424-1427.
72. Lu X, Zhang N, Vasquez K, Barton M, Legerski R. 2005. Repair of psoralen interstrand cross-links in Xenopus laevis egg extracts is highly mutagenic. Biochem Biophys Res Commun 336:69-75.
73. Marti TM, Hefner E, Feeney L, Natale V, 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.
74. Mason TM, Smeaton MB, Cheung JC, Hanakahi LA, Miller PS. 2008. End modification of a linear DNA duplex enhances NER-mediated excision of an internal Pt(II)-lesion. Bioconjug Chem 19:1064-1070.
75. McHugh PJ, Sarkar S. 2006. DNA interstrand cross-link repair in the cell cycle: A critical role for polymerase zeta in G1 phase. Cell Cycle 5:1044-1047.
76. McHugh PJ, Sones WR, Hartley JA. 2000. Repair of intermediate structures produced at DNA interstrand cross-links in Saccharomyces cerevisiae. Mol Cell Biol 20:3425-3433.
77. McHugh PJ, Spanswick VJ, Hartley JA. 2001. Repair of DNA interstrand crosslinks: Molecular mechanisms and clinical relevance. Lancet Oncol 2:483-490.
78. McMahon LW, Sangerman J, Goodman SR, Kumaresan K, Lambert MW. 2001. Human alpha spectrin II, the FANCA, FANCC, and FANCG proteins bind to DNA containing psoralen interstrand cross-links. Biochemistry 40:7025-7034.
79. McPherson JP, Lemmers B, Chahwan R, Pamidi A, Migon E, Matysiak-Zablocki E, Moynahan ME, Essers J, Hanada K, Poonepalli A, Sanchez-Sweatman O, Khokha R, Kanaar R, Jasin M, Hande MP, Hakem R. 2004. Involvement of mammalian Mus81 in genome integrity and tumor suppression. Science 304:1822-1826.
80. Mellon I, Bohr VA, Smith CA, Hanawalt PC. 1986. Preferential DNA repair of an active gene in human cells. Proc Natl Acad Sci USA 83:8878-8882.
81. Mellon I, Spivak G, Hanawalt PC. 1987. Selective removal of transcription-blocking DNA damage from the transcribed strand of the mammalian DHFR gene. Cell 51:241-249.
82. Mitchell JR, Hoeijmakers JH, Niedernhofer LJ. 2003. Divide and conquer: Nucleotide excision repair battles cancer and ageing. Curr Opin Cell Biol 15:232-240.
83. Mu D, Bessho T, Nechev LV, Chen DJ, Harris TM, Hearst JE, Sancar A. 2000. DNA interstrand cross-links induce futile repair synthesis in mammalian cell extracts. Mol Cell Biol 20:2446-2454.
84. Muniandy PA, Thapa D, Thazhathveetil AK, Liu ST, Seidman MM. 2009. Repair of laser localized DNA interstrand crosslinks in G1 phase mammalian cells. J Biol Chem 284:27908-27917.
85. Muñoz IM, Hain K, Déclais AC, Gardiner M, Toh GW, Sanchez-Pulido L, Heuckmann JM, Toth R, Macartney T, Eppink B, Kanaar R, Ponting CP, Lilley DM, Rouse J. 2009. Coordination of structure-specific nucleases by human SLX4/BTBD12 is required for DNA repair. Mol Cell 35:116-127.
86. Mustra DJ, Warren AJ, Hamilton JW. 2001. Preferential binding of human full-length XPA, the minimal DNA binding domain (XPA-MF122) with the mitomycin C-DNA interstrand cross-link. Biochemistry 40:7158-7164.
87. Mustra DJ, Warren AJ, Wilcox DE, Hamilton JW. 2007. Preferential binding of human XPA to the mitomycin C-DNA interstrand crosslink and modulation by arsenic and cadmium. Chem Biol Interact 168:159-168.
88. Nairn RS. Multiple roles of ERCC1-XPF in mammalian interstrand crosslink repair. Environ Mol Mutag (in press).
89. Niedernhofer LJ, Essers J, Weeda G, Beverloo B, de Wit J, Muijtjens M, Odijk H, Hoeijmakers JH, Kanaar R. 2001. The structure-specific endonuclease Ercc1-Xpf is required for targeted gene replacement in embryonic stem cells. EMBO J 20:6540-6549.
90. Niedernhofer LJ, Odijk H, Budzowska M, van Drunen E, Maas A, Theil AF, de Wit J, Jaspers NG, Beverloo HB, Hoeijmakers JH, Kanaar R. 2004. The structure-specific endonuclease Ercc1-Xpf is required to resolve DNA interstrand cross-link-induced double-strand breaks. Mol Cell Biol 24:5776-5787.
91. Niedernhofer LJ, Lalai AS, Hoeijmakers JH. 2005. Fanconi anemia (cross)linked to DNA repair. Cell 123:1191-1198.
92. Noll DM, Noronha AM, Wilds CJ, Miller PS. 2004. Preparation of interstrand cross-linked DNA oligonucleotide duplexes. Front Biosci 9:421-437.
93. Noll DM, Webba da Silva M, Noronha AM, Wilds CJ, Colvin OM, Gamcsik MP, Miller PS. 2005. Structure, flexibility, and repair of two different orientations of the same alkyl interstrand DNA cross-link. Biochemistry 44:6764-6775.
94. Noll DM, Mason TM, Miller PS. 2006. Formation and repair of interstrand cross-links in DNA. Chem Rev 106:277-301.
95. Nouspikel TP, Hyka-Nouspikel N, Hanawalt PC. 2006. Transcription domain-associated repair in human cells. Mol Cell Biol 26:8722-8730.
96. Osman F, Whitby MC. 2007. Exploring the roles of Mus81-Eme1/Mms4 at perturbed replication forks. DNA Repair (Amst) 6:1004-1017.
97. Rajski SR, Williams RM. 1998. DNA cross-linking agents as antitumor drugs. Chem Rev 98:2723-2796.
98. Raschle M, Knipscheer P, Enoiu M, Angelov T, Sun J, Griffith JD, Ellenberger TE, Scharer OD, Walter JC. 2008. Mechanism of replication-coupled DNA interstrand crosslink repair. Cell 134:969-980.
99. Reddy MC, Christensen J, Vasquez KM. 2005. Interplay between human high mobility group protein 1 and replication protein A on psoralen-cross-linked DNA. Biochemistry 44:4188-4195.
100. Rothfuss A, Grompe M. 2004. Repair kinetics of genomic interstrand DNA cross-links: Evidence for DNA double-strand break-dependent activation of the Fanconi anemia/BRCA pathway. Mol Cell Biol 24:123-134.
101. Sage E, Drobetsky EA, 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.
102. Sarkar S, Davies AA, Ulrich HD, McHugh PJ. 2006. DNA interstrand crosslink repair during G1 involves nucleotide excision repair and DNA polymerase zeta. EMBO J 25:1285-1294.
103. Scicchitano DA, Olesnicky EC, Dimitri A. 2004. Transcription and DNA adducts: What happens when the message gets cut off? DNA Repair (Amst) 3:1537-1548.
104. Sczepanski JT, Jacobs AC, Greenberg MM. 2008. Self-promoted DNA interstrand cross-link formation by an abasic site. J Am Chem Soc 130:9646-9647.
105. Selby CP, Sancar A. 1997a. Cockayne syndrome group B protein enhances elongation by RNA polymerase II. Proc Natl Acad Sci USA 94:11205-11209.
106. Selby CP, Sancar A. 1997b. Human transcription-repair coupling factor CSB/ERCC6 is a DNA-stimulated ATPase but is not a helicase and does not disrupt the ternary transcription complex of stalled RNA polymerase II. J Biol Chem 272:1885-1890.
107. Shen X, Jun S, O'Neal LE, Sonoda E, Bemark M, Sale JE, Li L. 2006. REV3 and REV1 play major roles in recombination-independent repair of DNA interstrand cross-links mediated by monoubiquitinated proliferating cell nuclear antigen (PCNA). J Biol Chem 281:13869-13872.
108. Sijbers AM, de Laat WL, Ariza RR, Biggerstaff M, Wei YF, Moggs JG, Carter KC, Shell BK, Evans E, de Jong MC, Rademakers S, de Rooij J, Jaspers NG, Hoeijmakers JH, Wood RD. 1996. Xeroderma pigmentosum group F caused by a defect in a structure-specific DNA repair endonuclease. Cell 86:811-822.
109. Smeaton MB, Miller PS, Ketner G, Hanakahi LA. 2007. Small-scale extracts for the study of nucleotide excision repair and non-homologous end joining. Nucleic Acids Res 35:e152.
110. Smeaton MB, Hlavin EM, McGregor Mason T, Noronha AM, Wilds CJ, Miller PS. 2008. Distortion-dependent unhooking of interstrand cross-links in mammalian cell extracts. Biochemistry 47:9920-9930.
111. Smeaton MB, Hlavin EM, Noronha AM, Murphy SP, Wilds CJ, Miller PS. 2009. Effect of cross-link structure on DNA interstrand cross-link repair synthesis. Chem Res Toxicol 22:1285-1297.
112. Sridharan D, Brown M, Lambert WC, McMahon LW, Lambert MW. 2003. Nonerythroid alphaII spectrin is required for recruitment of FANCA and XPF to nuclear foci induced by DNA interstrand cross-links. J Cell Sci 116 (Part 5):823-835.
113. Staresincic L, Fagbemi AF, Enzlin JH, Gourdin AM, Wijgers N, Dunand-Sauthier I, Giglia-Mari G, Clarkson SG, Vermeulen W, Scharer OD. 2009. Coordination of dual incision and repair synthesis in human nucleotide excision repair. EMBO J 28:1111-1120.
114. Stone MP, Cho YJ, Huang H, Kim HY, Kozekov ID, Kozekova A, Wang H, Minko IG, Lloyd RS, Harris TM, Rizzo CJ. 2008. Interstrand DNA cross-links induced by alpha,beta-unsaturated aldehydes derived from lipid peroxidation and environmental sources. Acc Chem Res 41:793-804.
115. Summerfield FW, Tappel AL. 1984. Detection and measurement by high-performance liquid chromatography of malondialdehyde crosslinks in DNA. Anal Biochem 143:265-271.
116. 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.
117. Swenson MC, Paranawithana SR, Miller PS, Kielkopf CL. 2007. Structure of a DNA repair substrate containing an alkyl interstrand cross-link at 1.65 Å resolution. Biochemistry 46:4545-4553.
118. Thoma BS, Wakasugi M, Christensen J, Reddy MC, 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.
119. Thompson LH, Hinz JM. 2009. Cellular and molecular consequences of defective Fanconi anemia proteins in replication-coupled DNA repair: Mechanistic insights. Mutat Res 668:54-72.
120. Vos JM, 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.
121. 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 interstrand cross-link repair. Mol Cell Biol 21:713-720.
122. Wood RD. Mammalian nucleotide excision repair proteins and interstrand crosslink repair. Environ Mol Mutag (in press).
123. Wu Q, Christensen LA, Legerski RJ, Vasquez KM. 2005. Mismatch repair participates in error-free processing of DNA interstrand crosslinks in human cells. EMBO Rep 6:551-557.
124. Zhang N, Zhang X, Peterson C, Li L, Legerski R. 2000. Differential processing of UV mimetic and interstrand crosslink damage by XPF cell extracts. Nucleic Acids Res 28:4800-4804.
125. Zhang N, Lu X, Zhang X, Peterson CA, Legerski RJ. 2002. hMutSbeta is required for the recognition and uncoupling of psoralen interstrand cross-links in vitro. Mol Cell Biol 22:2388-2397.
126. Zhang N, Kaur R, Lu X, Shen X, Li L, Legerski RJ. 2005. The Pso4 mRNA splicing and DNA repair complex interacts with WRN for processing of DNA interstrand cross-links. J Biol Chem 280:40559-40567.
127. Zhang N, Liu X, Li L, 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.
128. Zhao J, Jain A, Iyer RR, Modrich PL, Vasquez KM. 2009. Mismatch repair and nucleotide excision repair proteins cooperate in the recognition of DNA interstrand crosslinks. Nucleic Acids Res 37:4420-4429.
129. Zheng H, Wang X, Warren AJ, Legerski RJ, Nairn RS, Hamilton JW, Li L. 2003. Nucleotide excision repair- and polymerase eta-mediated error-prone removal of mitomycin C interstrand cross-links. Mol Cell Biol 23:754-761.
130. Zheng H,Wang X, Legerski RJ, Glazer PM, Li L. 2006. Repair of DNA interstrand cross-links: Interactions between homology-dependent and homology-independent pathways. DNA Repair (Amst) 5:566-574.