Coordination of Structure-Specific Nucleases by Human SLX4/BTBD12 Is Required for DNA Repair

Molecular Cell

Volumn 35, Issue 1, 2009, Pages 116-127

  Muñoz, Ivan M ^a   Hain, Karolina ^a   Déclais, Anne Cécile ^a   Gardiner, Mary ^a   Toh, Geraldine W ^a   Sanchez Pulido, Luis ^b   Heuckmann, Johannes M ^a   Toth, Rachel ^a   Macartney, Thomas ^a   Eppink, Berina ^c   Kanaar, Roland ^c   Ponting, Chris P ^b   Lilley, David M J ^a   Rouse, John ^a  

^a UNIVERSITY OF DUNDEE   (United Kingdom)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c ERASMUS MEDICAL CENTER   (Netherlands)

Author keywords

DNA

Indexed keywords

BTBD12 PROTEIN; EXCISION REPAIR CROSS COMPLEMENTING PROTEIN 1; NUCLEASE; PROTEIN; PROTEIN DERIVATIVE; SLX1 PROTEIN; SLX4 PROTEIN; TOXIN; UNCLASSIFIED DRUG;

ARTICLE; CROSS LINKING; DNA REPAIR; DNA STRUCTURE; EMBRYO; ENZYME ACTIVITY; HOLLIDAY JUNCTION; HOMOLOGOUS RECOMBINATION; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN PROTEIN INTERACTION;

BLOTTING, WESTERN; CELL LINE; CELL LINE, TUMOR; DNA BREAKS, DOUBLE-STRANDED; DNA REPAIR; DNA-BINDING PROTEINS; ENDONUCLEASES; GREEN FLUORESCENT PROTEINS; HUMANS; IMMUNOPRECIPITATION; PROTEIN BINDING; RECOMBINASES; RNA, SMALL INTERFERING; TRANSFECTION; TWO-HYBRID SYSTEM TECHNIQUES;

SACCHAROMYCETALES;

EID: 67649641641     PISSN: 10972765     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molcel.2009.06.020     Document Type: Article

References (41)

1. Ahmad A., Robinson A.R., Duensing A., van Drunen E., Beverloo H.B., Weisberg D.B., Hasty P., Hoeijmakers J.H.J., and Niedernhofer L.J. ERCC1-XPF endonuclease facilitates DNA double-strand break repair. Mol. Cell. Biol. 28 (2008) 5082-5092
2. Al-Minawi A.Z., Saleh-Gohari N., and Helleday T. The ERCC1/XPF endonuclease is required for efficient single-strand annealing and gene conversion in mammalian cells. Nucleic Acids Res. 36 (2008) 1-9
3. Andersen S.L., Bergstralh D.T., Kohl K.P., LaRocque J.R., Moore C.B., and Sekelsky J. Drosophila MUS312 and the vertebrate ortholog BTBD12 interact with DNA structure-specific endonucleases in DNA repair and recombination. Mol. Cell 35 (2009) 128-135 this issue
4. Aravind L., and Koonin E.V. Prokaryotic homologs of the eukaryotic DNA-end-binding protein Ku, novel domains in the Ku protein and prediction of a prokaryotic double-strand break repair system. Genome Res. 11 (2001) 1365-1374
5. Bachrati C.Z., and Hickson I.D. RecQ helicases: guardian angels of the DNA replication fork. Chromosoma 117 (2008) 219-233
6. Bardwell A.J., Bardwell L., Tomkinson A.E., and Friedberg E.C. Specific cleavage of model recombination and repair intermediates by the yeast Rad1-Rad10 DNA endonuclease. Science 265 (1994) 2082-2085
7. Bergstralh D.T., and Sekelsky J. Interstrand crosslink repair: can XPF-ERCC1 be let off the hook?. Trends Genet. 24 (2008) 70-76
8. Bohr V.A. Rising from the RecQ-age: the role of human RecQ helicases in genome maintenance. Trends Biochem. Sci. 33 (2008) 609-620
9. Ciccia A., McDonald N., and West S.C. Structural and functional relationships of the XPF/MUS81 family of proteins. Annu. Rev. Biochem. 77 (2008) 259-287
10. Costa R.M.A., Chigancas V., Galhardo R.D., Carvalho H., and Menck C.F.M. The eukaryotic nucleotide excision repair pathway. Biochimie 85 (2003) 1083-1099
11. Coulon S., Gaillard P.H., Chahwan C., McDonald W.H., Yates III J.R., and Russell P. Slx1-Slx4 are subunits of a structure-specific endonuclease that maintains ribosomal DNA in fission yeast. Mol. Biol. Cell 15 (2004) 71-80
12. Coulon S., Noguchi E., Noguchi C., Du L.L., Nakamura T.M., and Russell P. Rad22Rad52-dependent repair of ribosomal DNA repeats cleaved by Slx1-Slx4 endonuclease. Mol. Biol. Cell 17 (2006) 2081-2090
13. Davies A.A., Friedberg E.C., Tomkinson A.E., Wood R.D., and West S.C. Role of the Rad1 and Rad10 proteins in nucleotide excision-repair and recombination. J. Biol. Chem. 270 (1995) 24638-24641
14. de Laat W.L., Jaspers N.G.J., and Hoeijmakers J.H.J. Molecular mechanism of nucleotide excision repair. Genes Dev. 13 (1999) 768-785
15. Dendouga N., Gao H., Moechars D., Janicot M., Vialard J., and McGowan C.H. Disruption of murine Mus81 increases genomic instability and DNA damage sensitivity but does not promote tumorigenesis. Mol. Cell. Biol. 25 (2005) 7569-7579
16. Fishman-Lobell J., and Haber J.E. Removal of nonhomologous DNA ends in double-strand break recombination: the role of the yeast ultraviolet repair gene RAD1. Science 258 (1992) 480-484
17. Flott S., Alabert C., Toh G.W., Toth R., Sugawara N., Campbell D.G., Haber J.E., Pasero P., and Rouse J. Phosphorylation of Slx4 by mec1 and tel1 regulates the single-strand annealing mode of DNA repair in budding yeast. Mol. Cell. Biol. 27 (2007) 6433-6445
18. Fricke W.M., and Brill S.J. Slx1-Slx4 is a second structure-specific endonuclease functionally redundant with Sgs1-Top3. Genes Dev. 17 (2003) 1768-1778
19. Hanada K., Budzowska M., Modesti M., Maas A., Wyman C., Essers J., and Kanaar R. The structure-specific endonuclease Mus81-Eme1 promotes conversion of interstrand DNA crosslinks into double-strands breaks. EMBO J. 25 (2006) 4921-4932
20. Hanada K., Budzowska M., Davies S.L., van Drunen E., Onizawa H., Beverloo H.B., Maas A., Essers J., Hickson I.D., and Kanaar R. The structure-specific endonuclease Mus81 contributes to replication restart by generating double-strand DNA breaks. Nat. Struct. Mol. Biol. 14 (2007) 1096-1104
21. Ip S.C.Y., Rass U., Blanco M.G., Flynn H.R., Skehel J.M., and West S.C. Identification of Holliday junction resolvases from humans and yeast. Nature 456 (2008) 357-361
22. Ivanov E.L., and Haber J.E. Rad1 and Rad10, but not other excision-repair genes, are required for double-strand break-induced recombination in Saccharomyces cerevisiae. Mol. Cell. Biol. 15 (1995) 2245-2251
23. Jowsey P.A., Doherty A.J., and Rouse J. hPTIP facilitates ATM-mediated activation of p53 and promotes cellular resistance to ionising radiation. J. Biol. Chem. 279 (2004) 55562-55569
24. Kaliraman V., and Brill S.J. Role of SGS1 and SLX4 in maintaining rDNA structure in Saccharomyces cerevisiae. Curr. Genet. 41 (2002) 389-400
25. Li F.Y., Dong J.C., Pan X.W., Oum J.H., Boeke J.D., and Lee S.E. Microarray-based genetic screen defines SAW1, a gene required for Rad1/Rad10-dependent processing of recombination intermediates. Mol. Cell 30 (2008) 325-335
26. Lyndaker A.M., Goldfarb T., and Alani E. Mutants defective in Rad1-Rad10-Slx4 exhibit a unique pattern of viability during mating-type switching in Saccharomyces cerevisiae. Genetics 179 (2008) 1807-1821
27. Matsuoka S., Ballif B.A., Smogorzewska A., McDonald E.R., Hurov K.E., Luo J., Bakalarski C.E., Zhao Z.M., Solimini N., Lerenthal Y., et al. ATM and ATR substrate analysis reveals extensive protein networks responsive to DNA damage. Science 316 (2007) 1160-1166
28. Maxam A.M., and Gilbert W. Sequencing end-labeled DNA with base-specific chemical cleavages. Methods Enzymol. 65 (1980) 499-560
29. McPherson J.P., Lemmers B., Chahwan R., Pamidi A., Migon E., Matysiak-Zablocki E., Moynahan M.E., Essers J., Hanada K., Poonepalli A., et al. Involvement of mammalian Mus81 in genome integrity and tumor suppression. Science 304 (2004) 1822-1826
30. Mullen J.R., Kaliraman V., Ibrahim S.S., and Brill S.J. Requirement for three novel protein complexes in the absence of the Sgs1 DNA helicase in Saccharomyces cerevisiae. Genetics 157 (2001) 103-118
31. Niedernhofer L.J., Odijk H., Budzowska M., van Drunen E., Maas A., Theil A.F., de Wit J., Jaspers N.G.J., Beverloo H.B., Hoeijmakers J.H.J., and Kanaar R. The structure-specific endonuclease Ercc1-Xpf is required to resolve DNA interstrand cross-link-induced double-strand breaks. Mol. Cell. Biol. 24 (2004) 5776-5787
32. Niedernhofer L.J., Garinis G.A., Raams A., Lalai A.S., Robinson A.R., Appeldoorn E., Odijk H., Oostendorp R., Ahmad A., Van Leeuwen W., et al. A new progeroid syndrome reveals that genotoxic stress suppresses the somatotroph axis. Nature 444 (2006) 1038-1043
33. Osman F., and Whitby M.C. Exploring the roles of Mus81-Eme1/Mms4 at perturbed replication forks. DNA Repair (Amst.) 6 (2007) 1004-1017
34. Paques F., and Haber J.E. Multiple pathways of recombination induced by double-strand breaks in Saccharomyces cerevisiae. Microbiol. Mol. Biol. Rev. 63 (1999) 349-404
35. Perez-Torrado R., Yamada D., and Defossez P.A. Born to bind: the BTB protein-protein interaction domain. Bioessays 28 (2006) 1194-1202
36. Puget N., Knowlton M., and Scully R. Molecular analysis of sister chromatid recombination in mammalian cells. DNA Repair (Amst.) 4 (2005) 149-161
37. Rodriguez K., Wang Z.G., Friedberg E.C., and Tomkinson A.E. Identification of functional domains within the RAD1 center dot RAD10 repair and recombination endonuclease of Saccharomyces cerevisiae. J. Biol. Chem. 271 (1996) 20551-20558
38. Rouse J. Control of genome stability by Slx protein complexes. Biochem. Soc. Trans. 37 (2009) 495-510
39. Tripsianes K., Folkers G., Ab E., Das D., Odijk H., Jaspers N.G.J., Hoeijmakers J.H.J., Kaptein R., and Boelens R. The structure of the human ERCC1/XPF interaction domains reveals a complementary role for the two proteins in nucleotide excision repair. Structure 13 (2005) 1849-1858
40. Tsodikov O.V., Enzlin J.H., Scharer O.D., and Ellenberger T. Crystal structure and DNA binding functions of ERCC1, a subunit of the DNA structure-specific endonuclease XPF-ERCC1. Proc. Natl. Acad. Sci. USA 102 (2005) 11236-11241
41. Yildiz O., Majumder S., Kramer B., and Sekelsky J.J. Drosophila MUS312 interacts with the nucleotide excision repair endonuclease MEI-9 to generate meiotic crossovers. Mol. Cell 10 (2002) 1503-1509