Mutagenic Repair of DNA Interstrand Crosslinks

Overview

Journal Environ Mol Mutagen

Specialties Environmental Health
Molecular Biology

Date 2010 Mar 9

PMID 20209624

Citations 20

Authors

Xi Shen

Lei Li

Affiliations

Soon will be listed here.

Abstract

Formation of DNA interstrand crosslinks (ICLs) in chromosomal DNA imposes acute obstruction of all essential DNA functions. For over 70 years bifunctional alkylators, also known as DNA crosslinkers, have been an important class of cancer chemotherapeutic regimens. The mechanisms of ICL repair remains largely elusive. Here, we review a eukaryotic mutagenic ICL repair pathway discovered by work from several laboratories. This repair pathway, alternatively termed recombination-independent ICL repair, involves the incision activities of the nucleotide excision repair (NER) mechanism and lesion bypass polymerase(s). Repair of the ICL is initiated by dual incisions flanking the ICL on one strand of the double helix; the resulting gap is filled in by lesion bypass polymerases. The remaining lesion is subsequently removed by a second round of NER reaction. The mutagenic repair of ICL likely interacts with other cellular mechanisms such as the Fanconi anemia pathway and recombinational repair of ICLs. These aspects will also be discussed.

Citing Articles

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Head and Neck Cancer Susceptibility and Metabolism in Fanconi Anemia.

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Formation and repair of unavoidable, endogenous interstrand cross-links in cellular DNA.

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APOBEC3 enzymes mediate efficacy of cisplatin and are epistatic with base excision repair and mismatch repair in platinum response.

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Nucleotide Excision Repair, XPA-1, and the Translesion Synthesis Complex, POLZ-1 and REV-1, Are Critical for Interstrand Cross-Link Repair in Germ Cells.

Oh S, Bae W, Alfhili M, Lee M Biochemistry. 2020; 59(38):3554-3561.

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References

Esposito G, Godindagger I, Klein U, Yaspo M, Cumano A, Rajewsky K . Disruption of the Rev3l-encoded catalytic subunit of polymerase zeta in mice results in early embryonic lethality. Curr Biol. 2000; 10(19):1221-4. DOI: 10.1016/s0960-9822(00)00726-0. View

Smogorzewska A, Matsuoka S, Vinciguerra P, McDonald 3rd E, Hurov K, Luo J . Identification of the FANCI protein, a monoubiquitinated FANCD2 paralog required for DNA repair. Cell. 2007; 129(2):289-301. PMC: 2175179. DOI: 10.1016/j.cell.2007.03.009. View

Minko I, Harbut M, Kozekov I, Kozekova A, Jakobs P, Olson S . Role for DNA polymerase kappa in the processing of N2-N2-guanine interstrand cross-links. J Biol Chem. 2008; 283(25):17075-82. PMC: 2427349. DOI: 10.1074/jbc.M801238200. View

Tang M, Shen X, Frank E, ODonnell M, Woodgate R, Goodman M . UmuD'(2)C is an error-prone DNA polymerase, Escherichia coli pol V. Proc Natl Acad Sci U S A. 1999; 96(16):8919-24. PMC: 17708. DOI: 10.1073/pnas.96.16.8919. View

Zhao J, Jain A, Iyer R, Modrich P, Vasquez K . Mismatch repair and nucleotide excision repair proteins cooperate in the recognition of DNA interstrand crosslinks. Nucleic Acids Res. 2009; 37(13):4420-9. PMC: 2715249. DOI: 10.1093/nar/gkp399. View

Pham P, Bertram J, ODonnell M, Woodgate R, Goodman M . A model for SOS-lesion-targeted mutations in Escherichia coli. Nature. 2001; 409(6818):366-70. DOI: 10.1038/35053116. View

Kannouche P, Wing J, Lehmann A . Interaction of human DNA polymerase eta with monoubiquitinated PCNA: a possible mechanism for the polymerase switch in response to DNA damage. Mol Cell. 2004; 14(4):491-500. DOI: 10.1016/s1097-2765(04)00259-x. View

Muniandy P, Thapa D, Thazhathveetil A, Liu S, Seidman M . Repair of laser-localized DNA interstrand cross-links in G1 phase mammalian cells. J Biol Chem. 2009; 284(41):27908-27917. PMC: 2788842. DOI: 10.1074/jbc.M109.029025. View

Sladek F, Munn M, RUPP W, HOWARD-FLANDERS P . In vitro repair of psoralen-DNA cross-links by RecA, UvrABC, and the 5'-exonuclease of DNA polymerase I. J Biol Chem. 1989; 264(12):6755-65. View

10.

Plosky B, Woodgate R . Switching from high-fidelity replicases to low-fidelity lesion-bypass polymerases. Curr Opin Genet Dev. 2004; 14(2):113-9. DOI: 10.1016/j.gde.2004.02.002. View

11.

Stelter P, Ulrich H . Control of spontaneous and damage-induced mutagenesis by SUMO and ubiquitin conjugation. Nature. 2003; 425(6954):188-91. DOI: 10.1038/nature01965. View

12.

Shen X, Jun S, ONeal L, Sonoda E, Bemark M, Sale J . 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; 281(20):13869-72. DOI: 10.1074/jbc.C600071200. View

13.

Glode A, Jarkowski A . Bendamustine: a new treatment option for chronic lymphocytic leukemia. Pharmacotherapy. 2009; 29(11):1375-84. DOI: 10.1592/phco.29.11.1375. View

14.

Sarkar S, Davies A, Ulrich H, McHugh P . DNA interstrand crosslink repair during G1 involves nucleotide excision repair and DNA polymerase zeta. EMBO J. 2006; 25(6):1285-94. PMC: 1422152. DOI: 10.1038/sj.emboj.7600993. View

15.

Hishiki A, Shimizu T, Hanafusa T, Ohmori H, Sato M, Hashimoto H . Initial crystallographic study of human PCNA in complex with a peptide containing the noncanonical PIP-box sequence of human DNA polymerase iota. Acta Crystallogr Sect F Struct Biol Cryst Commun. 2008; 64(Pt 10):954-6. PMC: 2564886. DOI: 10.1107/S1744309108028522. View

16.

Knipscheer P, Raschle M, Smogorzewska A, Enoiu M, Ho T, Scharer O . The Fanconi anemia pathway promotes replication-dependent DNA interstrand cross-link repair. Science. 2009; 326(5960):1698-701. PMC: 2909596. DOI: 10.1126/science.1182372. View

17.

Vasquez K, Christensen J, Li L, Finch R, Glazer P . Human XPA and RPA DNA repair proteins participate in specific recognition of triplex-induced helical distortions. Proc Natl Acad Sci U S A. 2002; 99(9):5848-53. PMC: 122865. DOI: 10.1073/pnas.082193799. View

18.

Cheng S, Sancar A, Hearst J . RecA-dependent incision of psoralen-crosslinked DNA by (A)BC excinuclease. Nucleic Acids Res. 1991; 19(3):657-63. PMC: 333662. DOI: 10.1093/nar/19.3.657. View

19.

Lin W, Wu X, Wang Z . A full-length cDNA of hREV3 is predicted to encode DNA polymerase zeta for damage-induced mutagenesis in humans. Mutat Res. 1999; 433(2):89-98. DOI: 10.1016/s0921-8777(98)00065-2. View

20.

McHugh P, Gill R, Waters R, Hartley J . Excision repair of nitrogen mustard-DNA adducts in Saccharomyces cerevisiae. Nucleic Acids Res. 1999; 27(16):3259-66. PMC: 148558. DOI: 10.1093/nar/27.16.3259. View