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PMID: 20730555 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Review

Using synthetic DNA interstrand crosslinks to elucidate repair pathways and identify new therapeutic targets for cancer chemotherapy.

Cellular and molecular life sciences : CMLS ·Vol. 67 ·No. 21 ·2010-11-00 ·Pages 3683-97

Guainazzi A, Schärer OD

Abstract

Many cancer chemotherapeutic agents form DNA interstrand crosslinks (ICLs), extremely cytotoxic lesions that form covalent bonds between two opposing DNA strands, blocking DNA replication and transcription. However, cellular responses triggered by ICLs can cause resistance in tumor cells, limiting the efficacy of such treatment. Here we discuss recent advances in our understanding of the mechanisms of ICL repair that cause this resistance. The recent development of strategies for the synthesis of site-specific ICLs greatly contributed to these insights. Key features of repair are similar for all ICLs, but there is increasing evidence that the specifics of lesion recognition and synthesis past ICLs by DNA polymerases are dependent upon the structure of ICLs. These new insights provide a basis for the improvement of antitumor therapy by targeting DNA repair pathways that lead to resistance to treatment with crosslinking agents.

MeSH Terms
Animals Antineoplastic Agents/chemistry,pharmacology DNA Repair/drug effects Humans Intercalating Agents/chemistry,pharmacology Neoplasms/drug therapy,genetics
Chemicals
Antineoplastic Agents Intercalating Agents
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Guainazzi Angelo
Department of Pharmacological Sciences, Stony Brook University, Stony Brook, NY 11794-3400, USA.
Schärer Orlando D
References (142)
142 references, click to expand
  1. ERCC1 is required for FANCD2 focus formation.
    Mol Genet Metab. 2008 Sep-Oct;95(1-2):66-73 PMID: 18672388
  2. Psoralen and ultraviolet a light therapy for psoriasis.
    N Engl J Med. 2007 Aug 16;357(7):682-90 PMID: 17699818
  3. Binding of nuclear proteins associated with mammalian DNA repair to the mitomycin C-DNA interstrand crosslink.
    Environ Mol Mutagen. 1998;31(1):70-81 PMID: 9464318
  4. How the fanconi anemia pathway guards the genome.
    Annu Rev Genet. 2009;43:223-49 PMID: 19686080
  5. Synthesis and characterization of DNA containing an N1-2'-deoxyinosine-ethyl-N3-thymidine interstrand cross-link: a structural mimic of the cross-link formed by 1,3-bis-(2-chloroethyl)-1-nitrosourea.
    Chem Res Toxicol. 2008 Mar;21(3):686-95 PMID: 18257558
  6. Interstrand psoralen cross-links do not introduce appreciable bends in DNA.
    Biochemistry. 1984 Dec 18;23(26):6299-303 PMID: 6529552
  7. DNA polymerase II (polB) is involved in a new DNA repair pathway for DNA interstrand cross-links in Escherichia coli.
    J Bacteriol. 1999 May;181(9):2878-82 PMID: 10217781
  8. Versatile protection from mutagenic DNA lesions conferred by bipartite recognition in nucleotide excision repair.
    Mutat Res. 2008 Mar-Apr;658(3):271-86 PMID: 18321768
  9. Crystal structure of a double-stranded DNA containing a cisplatin interstrand cross-link at 1.63 A resolution: hydration at the platinated site.
    Nucleic Acids Res. 1999 Apr 15;27(8):1837-46 PMID: 10101191
  10. Novel enzymatic function of DNA polymerase nu in translesion DNA synthesis past major groove DNA-peptide and DNA-DNA cross-links.
    Chem Res Toxicol. 2010 Mar 15;23(3):689-95 PMID: 20102227
  11. DNA polymerases and human disease.
    Nat Rev Genet. 2008 Aug;9(8):594-604 PMID: 18626473
  12. Two-step error-prone bypass of the (+)- and (-)-trans-anti-BPDE-N2-dG adducts by human DNA polymerases eta and kappa.
    Mutat Res. 2002 Dec 29;510(1-2):23-35 PMID: 12459440
  13. A human ortholog of archaeal DNA repair protein Hef is defective in Fanconi anemia complementation group M.
    Nat Genet. 2005 Sep;37(9):958-63 PMID: 16116422
  14. The Fanconi anemia pathway promotes replication-dependent DNA interstrand cross-link repair.
    Science. 2009 Dec 18;326(5960):1698-701 PMID: 19965384
  15. A histone-fold complex and FANCM form a conserved DNA-remodeling complex to maintain genome stability.
    Mol Cell. 2010 Mar 26;37(6):865-78 PMID: 20347428
  16. Oxygen independent DNA interstrand cross-link formation by a nucleotide radical.
    J Am Chem Soc. 2006 Jan 18;128(2):485-91 PMID: 16402835
  17. Repair of DNA containing interstrand crosslinks in Escherichia coli: sequential excision and recombination.
    Proc Natl Acad Sci U S A. 1973 Apr;70(4):1064-8 PMID: 4577788
  18. Recruitment of fanconi anemia and breast cancer proteins to DNA damage sites is differentially governed by replication.
    Mol Cell. 2009 Sep 11;35(5):716-23 PMID: 19748364
  19. A modified thymine for the synthesis of site-specific thymine-guanine DNA interstrand crosslinks.
    Nucleic Acids Res. 2006;34(16):4458-66 PMID: 16945959
  20. Role of homologous recombination in DNA interstrand crosslink repair.
    Environ Mol Mutagen. 2010 Jul;51(6):582-603 PMID: 20658649
  21. 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. 2004 Jan;24(1):123-34 PMID: 14673148
  22. Thermal and thermodynamic properties of duplex DNA containing site-specific interstrand cross-link of antitumor cisplatin or its clinically ineffective trans isomer.
    J Biol Chem. 2001 Mar 30;276(13):9655-61 PMID: 11104778
  23. Nitrogen mustard therapy; use of methyl-bis (beta-chloroethyl) amine hydrochloride and tris (beta-chloroethyl) amine hydrochloride for Hodgkin's disease, lymphosarcoma, leukemia and certain allied and miscellaneous disorders.
    J Am Med Assoc. 1946 Sep 21;132:126-32 PMID: 20997191
  24. The Biological Actions and Therapeutic Applications of the B-Chloroethyl Amines and Sulfides.
    Science. 1946 Apr 5;103(2675):409-36 PMID: 17751251
  25. What a difference a decade makes: insights into translesion DNA synthesis.
    Proc Natl Acad Sci U S A. 2007 Oct 2;104(40):15591-8 PMID: 17898175
  26. Checkpoint signaling from a single DNA interstrand crosslink.
    Mol Cell. 2009 Sep 11;35(5):704-15 PMID: 19748363
  27. Mammalian BTBD12/SLX4 assembles a Holliday junction resolvase and is required for DNA repair.
    Cell. 2009 Jul 10;138(1):63-77 PMID: 19596235
  28. Generation of DNA interstrand cross-links by post-synthetic reductive amination.
    Org Lett. 2009 Feb 5;11(3):661-4 PMID: 19132933
  29. Solution structures of psoralen monoadducted and cross-linked DNA oligomers by NMR spectroscopy and restrained molecular dynamics.
    Biochemistry. 1995 Oct 10;34(40):12937-53 PMID: 7548052
  30. Repair of intermediate structures produced at DNA interstrand cross-links in Saccharomyces cerevisiae.
    Mol Cell Biol. 2000 May;20(10):3425-33 PMID: 10779332
  31. Chemosensitization to cisplatin by inhibitors of the Fanconi anemia/BRCA pathway.
    Mol Cancer Ther. 2006 Apr;5(4):952-61 PMID: 16648566
  32. FANCM and FAAP24 function in ATR-mediated checkpoint signaling independently of the Fanconi anemia core complex.
    Mol Cell. 2008 Nov 7;32(3):313-24 PMID: 18995830
  33. Preferential binding of human full-length XPA and the minimal DNA binding domain (XPA-MF122) with the mitomycin C-DNA interstrand cross-link.
    Biochemistry. 2001 Jun 19;40(24):7158-64 PMID: 11401562
  34. Interaction of the Fanconi anemia proteins and BRCA1 in a common pathway.
    Mol Cell. 2001 Feb;7(2):249-62 PMID: 11239454
  35. Drug-induced DNA damage and tumor chemosensitivity.
    J Clin Oncol. 1990 Dec;8(12):2062-84 PMID: 2230898
  36. Targeting the DNA repair defect in BRCA mutant cells as a therapeutic strategy.
    Nature. 2005 Apr 14;434(7035):917-21 PMID: 15829967
  37. A history of cancer chemotherapy.
    Cancer Res. 2008 Nov 1;68(21):8643-53 PMID: 18974103
  38. DNA interstrand cross-links induce futile repair synthesis in mammalian cell extracts.
    Mol Cell Biol. 2000 Apr;20(7):2446-54 PMID: 10713168
  39. 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. 1990 Mar 20;29(11):2861-75 PMID: 2346750
  40. Repair of DNA interstrand crosslinks: molecular mechanisms and clinical relevance.
    Lancet Oncol. 2001 Aug;2(8):483-90 PMID: 11905724
  41. Inhibition of poly(ADP-ribose) polymerase in tumors from BRCA mutation carriers.
    N Engl J Med. 2009 Jul 9;361(2):123-34 PMID: 19553641
  42. Synthesis and characterization of DNA duplexes containing an N(4)C-ethyl-N(4)C interstrand cross-link.
    J Am Chem Soc. 2001 Apr 18;123(15):3405-11 PMID: 11472110
  43. Drosophila MUS312 and the vertebrate ortholog BTBD12 interact with DNA structure-specific endonucleases in DNA repair and recombination.
    Mol Cell. 2009 Jul 10;35(1):128-35 PMID: 19595722
  44. Synthesis and molecular modeling of a nitrogen mustard DNA interstrand crosslink.
    Chemistry. 2010 Oct 25;16(40):12100-3 PMID: 20842675
  45. Reaction of DNA with chemically or enzymatically activated mitomycin C: isolation and structure of the major covalent adduct.
    Proc Natl Acad Sci U S A. 1986 Sep;83(18):6702-6 PMID: 3018744
  46. Fanconi anemia (cross)linked to DNA repair.
    Cell. 2005 Dec 29;123(7):1191-8 PMID: 16377561
  47. The chloroethylnitrosoureas: sensitivity and resistance to cancer chemotherapy at the molecular level.
    Cancer Invest. 1997;15(6):588-98 PMID: 9412665
  48. Interstrand DNA cross-links induced by alpha,beta-unsaturated aldehydes derived from lipid peroxidation and environmental sources.
    Acc Chem Res. 2008 Jul;41(7):793-804 PMID: 18500830
  49. DNA polymerase zeta (pol zeta) in higher eukaryotes.
    Cell Res. 2008 Jan;18(1):174-83 PMID: 18157155
  50. Emergence of a DNA-damage response network consisting of Fanconi anaemia and BRCA proteins.
    Nat Rev Genet. 2007 Oct;8(10):735-48 PMID: 17768402
  51. "Reversible" DNA.
    Proc Natl Acad Sci U S A. 1961 Jul 15;47:950-5 PMID: 13704192
  52. Targeting Fanconi anemia/BRCA2 pathway defects in cancer: the significance of preclinical pharmacogenomic models.
    Clin Cancer Res. 2007 Jan 1;13(1):4-10 PMID: 17200332
  53. Alkylation of guanosine by phosphoramide mustard, chloromethine hydrochloride and chlorambucil.
    Acta Pharmacol Toxicol (Copenh). 1984 Mar;54(3):214-20 PMID: 6720319
  54. DNA Cross-Linking Agents as Antitumor Drugs.
    Chem Rev. 1998 Dec 17;98(8):2723-2796 PMID: 11848977
  55. XPF-ERCC1 participates in the Fanconi anemia pathway of cross-link repair.
    Mol Cell Biol. 2009 Dec;29(24):6427-37 PMID: 19805513
  56. Defining the roles of nucleotide excision repair and recombination in the repair of DNA interstrand cross-links in mammalian cells.
    Mol Cell Biol. 2000 Nov;20(21):7980-90 PMID: 11027268
  57. Defective DNA cross-link removal in Chinese hamster cell mutants hypersensitive to bifunctional alkylating agents.
    Cancer Res. 1985 Apr;45(4):1737-43 PMID: 3919945
  58. Achieving broad substrate specificity in damage recognition by binding accessible nondamaged DNA.
    Mol Cell. 2007 Oct 26;28(2):184-6 PMID: 17964258
  59. A novel cell-free screen identifies a potent inhibitor of the Fanconi anemia pathway.
    Int J Cancer. 2009 Feb 15;124(4):783-92 PMID: 19048618
  60. 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. 2001 Feb 28;123(8):1730-9 PMID: 11456774
  61. The structure-specific endonuclease Mus81-Eme1 promotes conversion of interstrand DNA crosslinks into double-strands breaks.
    EMBO J. 2006 Oct 18;25(20):4921-32 PMID: 17036055
  62. Targeted gene knock in and sequence modulation mediated by a psoralen-linked triplex-forming oligonucleotide.
    J Biol Chem. 2008 Apr 25;283(17):11244-52 PMID: 18303025
  63. Disruption of murine Mus81 increases genomic instability and DNA damage sensitivity but does not promote tumorigenesis.
    Mol Cell Biol. 2005 Sep;25(17):7569-79 PMID: 16107704
  64. Mispair-aligned N3T-alkyl-N3T interstrand cross-linked DNA: synthesis and characterization of duplexes with interstrand cross-links of variable lengths.
    J Am Chem Soc. 2004 Aug 4;126(30):9257-65 PMID: 15281815
  65. Nucleotide excision repair- and polymerase eta-mediated error-prone removal of mitomycin C interstrand cross-links.
    Mol Cell Biol. 2003 Jan;23(2):754-61 PMID: 12509472
  66. Effect of cross-link structure on DNA interstrand cross-link repair synthesis.
    Chem Res Toxicol. 2009 Jul;22(7):1285-97 PMID: 19580249
  67. Formation and repair of interstrand cross-links in DNA.
    Chem Rev. 2006 Feb;106(2):277-301 PMID: 16464006
  68. Photoaffinity labeling reveals nuclear proteins that uniquely recognize cisplatin-DNA interstrand cross-links.
    Biochemistry. 2009 Jun 9;48(22):4916-25 PMID: 19364127
  69. Disruption of mouse RAD54 reduces ionizing radiation resistance and homologous recombination.
    Cell. 1997 Apr 18;89(2):195-204 PMID: 9108475
  70. Involvement of nucleotide excision repair in a recombination-independent and error-prone pathway of DNA interstrand cross-link repair.
    Mol Cell Biol. 2001 Feb;21(3):713-20 PMID: 11154259
  71. Human SLX4 is a Holliday junction resolvase subunit that binds multiple DNA repair/recombination endonucleases.
    Cell. 2009 Jul 10;138(1):78-89 PMID: 19596236
  72. Specific killing of BRCA2-deficient tumours with inhibitors of poly(ADP-ribose) polymerase.
    Nature. 2005 Apr 14;434(7035):913-7 PMID: 15829966
  73. Removal of psoralen interstrand cross-links from DNA of Escherichia coli: mechanism and genetic control.
    J Mol Biol. 1976 May 5;103(1):39-59 PMID: 785009
  74. A novel ubiquitin ligase is deficient in Fanconi anemia.
    Nat Genet. 2003 Oct;35(2):165-70 PMID: 12973351
  75. DNA interstrand crosslink repair during G1 involves nucleotide excision repair and DNA polymerase zeta.
    EMBO J. 2006 Mar 22;25(6):1285-94 PMID: 16482220
  76. 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. 2006 May 19;281(20):13869-72 PMID: 16571727
  77. The role of DNA repair in nitrogen mustard drug resistance.
    Anticancer Drugs. 2002 Mar;13(3):211-20 PMID: 11984064
  78. Psoralen conjugates for visualization of genomic interstrand cross-links localized by laser photoactivation.
    Bioconjug Chem. 2007 Mar-Apr;18(2):431-7 PMID: 17373769
  79. The structure-specific endonuclease Ercc1-Xpf is required to resolve DNA interstrand cross-link-induced double-strand breaks.
    Mol Cell Biol. 2004 Jul;24(13):5776-87 PMID: 15199134
  80. DNA repair pathways as targets for cancer therapy.
    Nat Rev Cancer. 2008 Mar;8(3):193-204 PMID: 18256616
  81. 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. 2003 Jan 8;125(1):62-72 PMID: 12515507
  82. Inter-strand crosslinking of DNA by nitrogen mustard.
    J Mol Biol. 1966 Aug;19(2):266-88 PMID: 4961329
  83. XRCC2 and XRCC3, new human Rad51-family members, promote chromosome stability and protect against DNA cross-links and other damages.
    Mol Cell. 1998 May;1(6):783-93 PMID: 9660962
  84. The solution structure of a psoralen cross-linked DNA duplex by NMR and relaxation matrix refinement.
    Biochem Biophys Res Commun. 1996 Feb 6;219(1):191-7 PMID: 8619806
  85. Alkylation of guanosine and deoxyguanosine by phosphoramide mustard.
    Cancer Res. 1980 Nov;40(11):4183-6 PMID: 7471059
  86. Bending of DNA by the mitomycin C-induced, GpG intrastrand cross-link.
    Chem Res Toxicol. 1996 Mar;9(2):382-9 PMID: 8839039
  87. Malondialdehyde, a product of lipid peroxidation, is mutagenic in human cells.
    J Biol Chem. 2003 Aug 15;278(33):31426-33 PMID: 12775726
  88. INHIBITION OF CELL DIVISION IN ESCHERICHIA COLI BY ELECTROLYSIS PRODUCTS FROM A PLATINUM ELECTRODE.
    Nature. 1965 Feb 13;205:698-9 PMID: 14287410
  89. Multiple repair pathways mediate tolerance to chemotherapeutic cross-linking agents in vertebrate cells.
    Cancer Res. 2005 Dec 15;65(24):11704-11 PMID: 16357182
  90. Efficient DNA interstrand cross-link formation from a nucleotide radical.
    J Am Chem Soc. 2005 Mar 23;127(11):3692-3 PMID: 15771492
  91. Evidence for a recombination-independent pathway for the repair of DNA interstrand cross-links based on a site-specific study with nitrogen mustard.
    Biochemistry. 1997 Mar 25;36(12):3506-13 PMID: 9132000
  92. Stabilities of 7-alkylguanosines and 7-deoxyguanosines formed by phosphoramide mustard and nitrogen mustard.
    Chem Biol Interact. 1986 Jan;57(1):85-96 PMID: 3948286
  93. Reactions of formaldehyde plus acetaldehyde with deoxyguanosine and DNA: formation of cyclic deoxyguanosine adducts and formaldehyde cross-links.
    Chem Res Toxicol. 2003 Feb;16(2):145-52 PMID: 12588185
  94. The resurgence of platinum-based cancer chemotherapy.
    Nat Rev Cancer. 2007 Aug;7(8):573-84 PMID: 17625587
  95. Initiation of DNA interstrand cross-link repair in mammalian cells.
    Environ Mol Mutagen. 2010 Jul;51(6):604-24 PMID: 20658650
  96. Recognition of DNA damage by the Rad4 nucleotide excision repair protein.
    Nature. 2007 Oct 4;449(7162):570-5 PMID: 17882165
  97. Coordination of structure-specific nucleases by human SLX4/BTBD12 is required for DNA repair.
    Mol Cell. 2009 Jul 10;35(1):116-27 PMID: 19595721
  98. Solution structure of a nitrous acid induced DNA interstrand cross-link.
    Nucleic Acids Res. 2004 May 20;32(9):2785-94 PMID: 15155847
  99. Regulated chromosomal DNA replication in the absence of a nucleus.
    Mol Cell. 1998 Mar;1(4):519-29 PMID: 9660936
  100. Structure, Recognition, and Processing of Cisplatin-DNA Adducts.
    Chem Rev. 1999 Sep 8;99(9):2467-98 PMID: 11749487
  101. Isolation and structure of a covalent cross-link adduct between mitomycin C and DNA.
    Science. 1987 Mar 6;235(4793):1204-8 PMID: 3103215
  102. Identification of FAAP24, a Fanconi anemia core complex protein that interacts with FANCM.
    Mol Cell. 2007 Feb 9;25(3):331-43 PMID: 17289582
  103. Synthesis of a duplex oligonucleotide containing a nitrogen mustard interstrand DNA-DNA cross-link.
    Cancer Res. 1989 Dec 1;49(23):6529-37 PMID: 2819709
  104. Measurement of DNA interstrand crosslinking in individual cells using the Single Cell Gel Electrophoresis (Comet) assay.
    Methods Mol Biol. 2010;613:267-82 PMID: 19997890
  105. Repair of laser-localized DNA interstrand cross-links in G1 phase mammalian cells.
    J Biol Chem. 2009 Oct 9;284(41):27908-27917 PMID: 19684342
  106. Interstrand crosslink repair: can XPF-ERCC1 be let off the hook?
    Trends Genet. 2008 Feb;24(2):70-6 PMID: 18192062
  107. DNA interstrand crosslink repair in mammalian cells: step by step.
    Crit Rev Biochem Mol Biol. 2010 Feb;45(1):23-49 PMID: 20039786
  108. Mitomycin C in the treatment of gastrointestinal tumours: recent data and perspectives.
    Onkologie. 2008 May;31(5):271-81 PMID: 18497518
  109. Role for DNA polymerase kappa in the processing of N2-N2-guanine interstrand cross-links.
    J Biol Chem. 2008 Jun 20;283(25):17075-82 PMID: 18434313
  110. Eukaryotic translesion synthesis DNA polymerases: specificity of structure and function.
    Annu Rev Biochem. 2005;74:317-53 PMID: 15952890
  111. Targeted disruption of FANCC and FANCG in human cancer provides a preclinical model for specific therapeutic options.
    Gastroenterology. 2006 Jun;130(7):2145-54 PMID: 16762635
  112. Platinum compounds: a new class of potent antitumour agents.
    Nature. 1969 Apr 26;222(5191):385-6 PMID: 5782119
  113. Transcription-coupled DNA repair: two decades of progress and surprises.
    Nat Rev Mol Cell Biol. 2008 Dec;9(12):958-70 PMID: 19023283
  114. The XPA-binding domain of ERCC1 is required for nucleotide excision repair but not other DNA repair pathways.
    J Biol Chem. 2010 Feb 5;285(6):3705-3712 PMID: 19940136
  115. Solution structure of a cisplatin-induced DNA interstrand cross-link.
    Science. 1995 Dec 15;270(5243):1842-5 PMID: 8525382
  116. Molecular mechanisms of mammalian global genome nucleotide excision repair.
    Chem Rev. 2006 Feb;106(2):253-76 PMID: 16464005
  117. Rev1 is essential for DNA damage tolerance and non-templated immunoglobulin gene mutation in a vertebrate cell line.
    EMBO J. 2003 Apr 1;22(7):1654-64 PMID: 12660171
  118. Structural and functional relationships of the XPF/MUS81 family of proteins.
    Annu Rev Biochem. 2008;77:259-87 PMID: 18518821
  119. The Fanconi anaemia gene FANCC promotes homologous recombination and error-prone DNA repair.
    Mol Cell. 2004 Aug 27;15(4):607-20 PMID: 15327776
  120. DNA replication is required To elicit cellular responses to psoralen-induced DNA interstrand cross-links.
    Mol Cell Biol. 2000 Nov;20(21):8283-9 PMID: 11027296
  121. 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. 1997 Dec;17(12):6822-30 PMID: 9372913
  122. The structure-specific endonuclease Mus81 contributes to replication restart by generating double-strand DNA breaks.
    Nat Struct Mol Biol. 2007 Nov;14(11):1096-104 PMID: 17934473
  123. Direct demonstration in synthetic oligonucleotides that N,N'-bis(2-chloroethyl)-nitrosourea cross links N1 of deoxyguanosine to N3 of deoxycytidine on opposite strands of duplex DNA.
    Cancer Res. 1999 Sep 1;59(17):4363-8 PMID: 10485484
  124. Distortion-dependent unhooking of interstrand cross-links in mammalian cell extracts.
    Biochemistry. 2008 Sep 16;47(37):9920-30 PMID: 18702509
  125. A mechlorethamine-induced DNA interstrand cross-link bends duplex DNA.
    Biochemistry. 1995 Jan 31;34(4):1439-45 PMID: 7827092
  126. MHF1-MHF2, a histone-fold-containing protein complex, participates in the Fanconi anemia pathway via FANCM.
    Mol Cell. 2010 Mar 26;37(6):879-86 PMID: 20347429
  127. Methods for the large-scale synthesis of psoralen furan-side monoadducts and diadducts.
    Proc Natl Acad Sci U S A. 1992 May 15;89(10):4514-8 PMID: 1584785
  128. Platinum resistance: the role of DNA repair pathways.
    Clin Cancer Res. 2008 Mar 1;14(5):1291-5 PMID: 18316546
  129. Isolation and identification of cross-linked nucleosides from nitrous acid treated deoxyribonucleic acid.
    J Am Chem Soc. 1977 Jan 5;99(1):302-3 PMID: 830687
  130. Psoralens as photoactive probes of nucleic acid structure and function: organic chemistry, photochemistry, and biochemistry.
    Annu Rev Biochem. 1985;54:1151-93 PMID: 2411210
  131. DNA repair and cancer stem-like cells--potential partners in glioma drug resistance?
    Cancer Treat Rev. 2008 Oct;34(6):558-67 PMID: 18501520
  132. Repair of cisplatin--DNA adducts by the mammalian excision nuclease.
    Biochemistry. 1996 Aug 6;35(31):10004-13 PMID: 8756462
  133. Construction of a human shuttle vector containing a single nitrogen mustard interstrand, DNA-DNA cross-link at a unique plasmid location.
    Cancer Res. 1991 May 1;51(9):2268-72 PMID: 2015591
  134. Mechanism of replication-coupled DNA interstrand crosslink repair.
    Cell. 2008 Sep 19;134(6):969-80 PMID: 18805090
  135. The reaction of mono- and di-functional alkylating agents with nucleic acids.
    Biochem J. 1961 Sep;80(3):496-503 PMID: 16748923
  136. Mismatch repair and nucleotide excision repair proteins cooperate in the recognition of DNA interstrand crosslinks.
    Nucleic Acids Res. 2009 Jul;37(13):4420-9 PMID: 19468048
  137. DNA interstrand crosslinks: natural and drug-induced DNA adducts that induce unique cellular responses.
    Chembiochem. 2005 Jan;6(1):27-32 PMID: 15637664
  138. The structure of the catalytic subunit FANCL of the Fanconi anemia core complex.
    Nat Struct Mol Biol. 2010 Mar;17(3):294-8 PMID: 20154706
  139. Beyond DNA cross-linking: history and prospects of DNA-targeted cancer treatment--fifteenth Bruce F. Cain Memorial Award Lecture.
    Cancer Res. 1996 Dec 15;56(24):5533-46 PMID: 8971150
  140. Structural determinants of human FANCF protein that function in the assembly of a DNA damage signaling complex.
    J Biol Chem. 2007 Jan 19;282(3):2047-55 PMID: 17082180
  141. Identification of the FANCI protein, a monoubiquitinated FANCD2 paralog required for DNA repair.
    Cell. 2007 Apr 20;129(2):289-301 PMID: 17412408
  142. Nitric oxide-induced interstrand cross-links in DNA.
    Chem Res Toxicol. 2003 May;16(5):571-4 PMID: 12755585
Article Info
Journal
Cellular and molecular life sciences : CMLS
Abbr.
Cell Mol Life Sci
ISSN
1420-9071
DOI
10.1007/s00018-010-0492-6
Published
2010-11-00
Epub
2010-00-21
Pages
3683-97
Language
English
Region
Switzerland
NLM ID
9705402
PMCID
PMC3732395
Subset
IM
Grants
NIGMS NIH HHS · R01 GM080454 · United States
NIEHS NIH HHS · ES004068 · United States
NCI NIH HHS · P01 CA092584 · United States
NCI NIH HHS · R01 CA165911 · United States
NCI NIH HHS · CA092584 · United States
NIEHS NIH HHS · P01 ES004068 · United States
NIGMS NIH HHS · GM080454 · United States
External Links
PubMed source DOI: 10.1007/s00018-010-0492-6 PMC Full Text View journal details
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