Recruitment and Positioning Determine the Specific Role of the XPF-ERCC1 Endonuclease in Interstrand Crosslink Repair

Overview

Journal EMBO J

Specialties Biotechnology
Molecular Biology

Date 2017 Mar 16

PMID 28292785

Citations 30

Authors

Daisy Klein Douwel

Wouter S Hoogenboom

Rick Acm Boonen

Puck Knipscheer

Affiliations

Soon will be listed here.

Abstract

XPF-ERCC1 is a structure-specific endonuclease pivotal for several DNA repair pathways and, when mutated, can cause multiple diseases. Although the disease-specific mutations are thought to affect different DNA repair pathways, the molecular basis for this is unknown. Here we examine the function of XPF-ERCC1 in DNA interstrand crosslink (ICL) repair. We used egg extracts to measure both ICL and nucleotide excision repair, and we identified mutations that are specifically defective in ICL repair. One of these separation-of-function mutations resides in the helicase-like domain of XPF and disrupts binding to SLX4 and recruitment to the ICL A small deletion in the same domain supports recruitment of XPF to the ICL, but inhibited the unhooking incisions most likely by disrupting a second, transient interaction with SLX4. Finally, mutation of residues in the nuclease domain did not affect localization of XPF-ERCC1 to the ICL but did prevent incisions on the ICL substrate. Our data support a model in which the ICL repair-specific function of XPF-ERCC1 is dependent on recruitment, positioning and substrate recognition.

Citing Articles

Repair of genomic interstrand crosslinks.

Bellani M, Shaik A, Majumdar I, Ling C, Seidman M DNA Repair (Amst). 2024; 141:103739.

PMID: 39106540 PMC: 11423799. DOI: 10.1016/j.dnarep.2024.103739.

Replication-Independent ICL Repair: From Chemotherapy to Cell Homeostasis.

Ahmed A, Kato N, Gautier J J Mol Biol. 2024; 436(13):168618.

PMID: 38763228 PMC: 11227339. DOI: 10.1016/j.jmb.2024.168618.

Persistent TFIIH binding to non-excised DNA damage causes cell and developmental failure.

Muniesa-Vargas A, Davo-Martinez C, Ribeiro-Silva C, van der Woude M, Thijssen K, Haspels B Nat Commun. 2024; 15(1):3490.

PMID: 38664429 PMC: 11045817. DOI: 10.1038/s41467-024-47935-9.

Association between ERCC1 Gene Polymorphism (rs11615) and Colorectal Cancer Susceptibility: A Meta-Analysis of Medical Image Fusion and Safety Applications.

Liu M, Qiu Z, Yang Q Comput Math Methods Med. 2022; 2022:9988513.

PMID: 36277013 PMC: 9586779. DOI: 10.1155/2022/9988513.

Association of ERCC1 rs11615 Polymorphism with the Risk of Cervical Cancer Especially in Chinese Populations: A Meta-Analysis.

Zhang Y, Teng Y, Zhu Y, Wu Y, Wen Y, Liu X J Oncol. 2022; 2022:1790993.

PMID: 36245993 PMC: 9568358. DOI: 10.1155/2022/1790993.

References

Spivak G . Nucleotide excision repair in humans. DNA Repair (Amst). 2015; 36:13-18. PMC: 4688078. DOI: 10.1016/j.dnarep.2015.09.003. View

Yildiz O, Majumder S, Kramer B, Sekelsky J . Drosophila MUS312 interacts with the nucleotide excision repair endonuclease MEI-9 to generate meiotic crossovers. Mol Cell. 2002; 10(6):1503-9. PMC: 3206640. DOI: 10.1016/s1097-2765(02)00782-7. View

Mamrak N, Shimamura A, Howlett N . Recent discoveries in the molecular pathogenesis of the inherited bone marrow failure syndrome Fanconi anemia. Blood Rev. 2016; 31(3):93-99. PMC: 5391297. DOI: 10.1016/j.blre.2016.10.002. View

Li L, Peterson C, Lu X, Legerski R . Mutations in XPA that prevent association with ERCC1 are defective in nucleotide excision repair. Mol Cell Biol. 1995; 15(4):1993-8. PMC: 230426. DOI: 10.1128/MCB.15.4.1993. View

Fekairi S, Scaglione S, Chahwan C, Taylor E, Tissier A, Coulon S . Human SLX4 is a Holliday junction resolvase subunit that binds multiple DNA repair/recombination endonucleases. Cell. 2009; 138(1):78-89. PMC: 2861413. DOI: 10.1016/j.cell.2009.06.029. View

Gaillard P, Martini E, Kaufman P, Stillman B, MOUSTACCHI E, Almouzni G . Chromatin assembly coupled to DNA repair: a new role for chromatin assembly factor I. Cell. 1996; 86(6):887-96. DOI: 10.1016/s0092-8674(00)80164-6. View

Su Y, Orelli B, Madireddy A, Niedernhofer L, Scharer O . Multiple DNA binding domains mediate the function of the ERCC1-XPF protein in nucleotide excision repair. J Biol Chem. 2012; 287(26):21846-55. PMC: 3381147. DOI: 10.1074/jbc.M111.337899. View

Ahmad A, Enzlin J, Bhagwat N, Wijgers N, Raams A, Appledoorn E . Mislocalization of XPF-ERCC1 nuclease contributes to reduced DNA repair in XP-F patients. PLoS Genet. 2010; 6(3):e1000871. PMC: 2832669. DOI: 10.1371/journal.pgen.1000871. View

Walter J, Sun L, Newport J . Regulated chromosomal DNA replication in the absence of a nucleus. Mol Cell. 1998; 1(4):519-29. DOI: 10.1016/s1097-2765(00)80052-0. View

10.

Bergstralh D, Sekelsky J . Interstrand crosslink repair: can XPF-ERCC1 be let off the hook?. Trends Genet. 2008; 24(2):70-6. DOI: 10.1016/j.tig.2007.11.003. View

11.

Huang J, Svoboda D, Reardon J, Sancar A . Human nucleotide excision nuclease removes thymine dimers from DNA by incising the 22nd phosphodiester bond 5' and the 6th phosphodiester bond 3' to the photodimer. Proc Natl Acad Sci U S A. 1992; 89(8):3664-8. PMC: 48929. DOI: 10.1073/pnas.89.8.3664. View

12.

Osorio A, Bogliolo M, Fernandez V, Barroso A, de la Hoya M, Caldes T . Evaluation of rare variants in the new fanconi anemia gene ERCC4 (FANCQ) as familial breast/ovarian cancer susceptibility alleles. Hum Mutat. 2013; 34(12):1615-8. DOI: 10.1002/humu.22438. View

13.

Hodskinson M, Silhan J, Crossan G, Garaycoechea J, Mukherjee S, Johnson C . Mouse SLX4 is a tumor suppressor that stimulates the activity of the nuclease XPF-ERCC1 in DNA crosslink repair. Mol Cell. 2014; 54(3):472-84. PMC: 4017094. DOI: 10.1016/j.molcel.2014.03.014. View

14.

Bogliolo M, Schuster B, Stoepker C, Derkunt B, Su Y, Raams A . Mutations in ERCC4, encoding the DNA-repair endonuclease XPF, cause Fanconi anemia. Am J Hum Genet. 2013; 92(5):800-6. PMC: 3644630. DOI: 10.1016/j.ajhg.2013.04.002. View

15.

McNeil E, Melton D . DNA repair endonuclease ERCC1-XPF as a novel therapeutic target to overcome chemoresistance in cancer therapy. Nucleic Acids Res. 2012; 40(20):9990-10004. PMC: 3488251. DOI: 10.1093/nar/gks818. View

16.

Tutter A, Walter J . Chromosomal DNA replication in a soluble cell-free system derived from Xenopus eggs. Methods Mol Biol. 2006; 322:121-37. DOI: 10.1007/978-1-59745-000-3_9. View

17.

Kirschner K, Melton D . Multiple roles of the ERCC1-XPF endonuclease in DNA repair and resistance to anticancer drugs. Anticancer Res. 2010; 30(9):3223-32. View

18.

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

19.

Friedberg E . Nucleotide excision repair of DNA: The very early history. DNA Repair (Amst). 2011; 10(7):668-72. DOI: 10.1016/j.dnarep.2011.04.018. View

20.

Newman M, Murray-Rust J, Lally J, Rudolf J, Fadden A, Knowles P . Structure of an XPF endonuclease with and without DNA suggests a model for substrate recognition. EMBO J. 2005; 24(5):895-905. PMC: 554130. DOI: 10.1038/sj.emboj.7600581. View