Crystal structures of the structure-selective nuclease Mus81-Eme1 bound to flap DNA substrates

EMBO Journal

Volumn 33, Issue 9, 2014, Pages 1061-1072

  Gwon, Gwang Hyeon ^a   Jo, Aera ^a   Baek, Kyuwon ^a   Jin, Kyeong Sik ^a   Fu, Yaoyao ^a   Lee, Jong Bong ^a   Kim, Youngchang ^b   Cho, Yunje ^a  

^a Pohang University of Science and Technology (POSTECH)   (South Korea)

^b ARGONNE NATIONAL LABORATORY   (United States)

Author keywords

crystal structure; flap DNA; homologous recombination; interstrand cross link repair; Mus81

Indexed keywords

DNA; DOUBLE STRANDED DNA; NUCLEASE;

ARTICLE; CRYSTAL STRUCTURE; DNA BINDING; DNA CONFORMATION; ENZYME ACTIVE SITE; ENZYME SUBSTRATE; HYDROPHOBICITY; PRIORITY JOURNAL; PROTEIN DNA INTERACTION;

5' FLANKING REGION; CRYSTALLOGRAPHY, X-RAY; DNA; DNA BREAKS, SINGLE-STRANDED; DNA-BINDING PROTEINS; ENDODEOXYRIBONUCLEASES; ENDONUCLEASES; HUMANS; MODELS, MOLECULAR; NUCLEIC ACID CONFORMATION; PROTEIN BINDING; PROTEIN STRUCTURE, QUATERNARY; STRUCTURE-ACTIVITY RELATIONSHIP; SUBSTRATE SPECIFICITY;

EID: 84899814719     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1002/embj.201487820     Document Type: Article

References (51)

1. Abraham J, Lemmers B, Hande MP, Moynahan ME, Chahwan C, Ciccia A, Essers J, Hanada K, Chahwan R, Khaw AK, (2003) Eme1 is involved in DNA damage processing and maintenance of genomic stability in mammalian cells. EMBO J 22: 6137-6147
2. Adams PD, Afonine PV, Bunkóczi G, Chen VB, Davis IW, Echols N, Headd JJ, Hung LW, Kapral GJ, Grosse-Kunstleve RW, McCoy AJ, Moriarty NW, Oeffner R, Read RJ, Richardson DC, Richardson JS, Terwilliger TC, Zwart PH, (2010) PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr D 66: 213-221
3. Bastin-Shanower SA, Fricke WM, Mullen JR, Brill SJ, (2003) The mechanism of Mus81-Mms4 cleavage site selection distinguishes it from the homologous endonuclease Rad1-Rad10. Mol Cell Biol 23: 3487-3496
4. Boddy MN, Gaillard PH, McDonald WH, Shanahan P, Yates JR 3rd, Russell P, (2001) Mus81-Eme1 are essential components of a Holliday junction resolvase. Cell 107: 537-548
5. Castor D, Nair N, Déclais AC, Lachaud C, Toth R, Macartney TJ, Lilley DM, Arthur JS, Rouse J, (2013) Cooperative Control of Holliday junction resolution and DNA repair by the SLX1 and MUS81-EME1 Nucleases. Mol Cell 52: 221-233
6. Cejka P, Plank JL, Bachrati CZ, Hickson ID, Kowalczykowski SC, (2010) Rmi stimulates decatenation of double Holliday junctions during dissolution by Sgs1-Top3. Nat Struct Mol Biol 17: 1377-1382
7. Chang JH, Kim JJ, Choi JM, Lee JH, Cho Y, (2008) Crystal structure of the Mus81-Eme1 complex. Genes Dev 22: 1093-1106
8. Chen XB, Melchionna R, Denis CM, Gaillard PH, Blasina A, Van WI, Boddy MN, Russell P, Vialard J, McGowan CH, (2001) Human Mus81-associated endonuclease cleaves Holliday junctions in vitro. Mol Cell 8: 1117-1127
9. Ciccia A, McDonald N, West SC, (2008) Structural and functional relationships of the XPF/MUS81 family of proteins. Annu Rev Biochem 77: 259-287
10. Constantinou A, Chen XB, McGowan CH, West SC, (2002) Holliday junction resolution in human cells: two junction endonucleases with distinct substrate specificities. EMBO J 21: 5577-5585
11. Coulthard R, Deans AJ, Swuec P, Bowles M, Costa A, West SC, McDonald NQ, (2013) Architecture and DNA recognition elements of the Fanconi anemia FANCM-FAAP24 complex. Structure 21: 1648-1658
12. Deans AJ, West SC, (2011) DNA interstrand crosslink repair and cancer. Nat Rev Cancer 11: 467-480
13. 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
14. Doe CL, Ahn JS, Dixon J, Whitby MC, (2002) Mus81-Eme1 and Rqh1 involvement in processing stalled and collapsed replication forks. J Biol Chem 277: 32753-32759
15. Ehmsen KT, Heyer WD, (2008) Saccharomyces cerevisiae Mus81-Mms4 is a catalytic, DNA structure-selective endonuclease. Nucleic Acids Res 36: 2182-2195
16. Ehmsen KT, Heyer WD, (2009) A junction branch point adjacent to a DNA backbone nick directs substrate cleavage by Saccharomyces cerevisiae Mus81-Mms4. Nucleic Acids Res 37: 2026-2036
17. Emsley P, Cowtan K, (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr D 60: 2126-2132
18. Fekairi S, Scaglione S, Chahwan C, Taylor ER, Tissier A, Coulon S, Dong MQ, Ruse C, Yates JR 3rd, Russell P, (2009) Human SLX4 is a Holliday junction resolvase subunit that binds multiple DNA repair/recombination endonucleases. Cell 138: 78-89
19. Freudenthal BD, Beard WA, Shock DD, Wilson SH, (2013) Observing a DNA polymerase choose right from wrong. Cell 154: 157-168
20. Fricke WM, Bastin-shanower SA, Brill SJ, (2005) Substrate specificity of the Saccharomyces cerevisiae Mus81-Mms4 endonuclease. DNA Repair (Amst) 4: 243-251
21. Gaillard PH, Noguchi E, Shanahan P, Russell P, (2003) The endogenous Mus81-Eme1 complex resolves Holliday junctions by a nick and counternick mechanism. Mol Cell 12: 747-759
22. Garner E, Kim Y, Lach FP, Kottemann MC, Smogorzewska A, (2013) Human GEN1 and the SLX4-Associated Nucleases MUS81 and SLX1 are essential for the resolution of replication-induced Holliday junctions. Cell Rep 5: 1-9
23. Gaskell LJ, Osman F, Gilbert RJ, Whitby MC, (2007) Mus81 cleavage of Holliday junctions: a failsafe for processing meiotic recombination intermediates? EMBO J 26: 1891-1901
24. Górecka KM, Komorowska W, Nowotny M, (2013) Crystal structure of RuvC resolvase in complex with Holliday junction substrate. Nucleic Acids Res 41: 9945-9955
25. Grasby JA, Finger LD, Tsutakawa SE, Atack JM, Tainer JA, (2012) Unpairing and gating: sequence-independent substrate recognition by FEN superfamily nucleases. Trends Biochem Sci 37: 74-84
26. Hadden JM, Déclais AC, Carr SB, Lilley DM, Phillips SE, (2007) The structural basis of holliday junction resolution by T7 endonuclease 1. Nature 449: 621-624
27. Hanada K, Budzowska M, Davies SL, Drunen E, Onizawa H, Beverloo HB, Maas A, Essers J, Hickson ID, Kanaar R, (2007) The structure-selective endonuclease Mus81 contributes to replication restart by generating double-strand DNA breaks. Nat Struct Mol Biol 14: 1096-1104
28. 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
29. Hiyama T, Katsura M, Yoshihara T, Ishida M, Kinomura A, Tonda T, Asahara T, Miyagawa K, (2006) Haploinsufficiency of the Mus81-Eme1 endonuclease activates the intra-S-phase and G2/M checkpoints and promotes rereplication in human cells. Nucleic Acids Res 34: 880-892
30. Hollingsworth NM, Brill SJ, (2004) The Mus81 solution to resolution: generating meiotic crossovers without Holliday junctions. Genes Dev 18: 117-125
31. Interthal H, Heyer WD, (2000) MUS81 encodes a novel helix-hairpin-helix protein involved in the response to UV- and methylation-induced DNA damage in Saccharomyces cerevisiae. Mol Gen Genet 263: 812-827
32. Ip SC, Rass U, Blanco MG, Flynn HR, Skehel JM, West SC, (2008) Identification of Holliday junction resolvases from humans and yeast. Nature 456: 357-361
33. McCoy AJ, Grosse-Kunstleve RW, Adams PD, Winn MD, Storoni LC, Read RJ, (2007) Phaser crystallographic software. J Appl Cryst 40: 658-674
34. 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-selective nucleases by human SLX4/BTBD12 is required for DNA repair. Mol Cell 35: 116-127
35. Naim V, Wilhelm T, Debatisse M, Rosselli F, (2013) ERCC1 and MUS81-EME1 promote sister chromatid separation by processing late replication intermediates at common fragile sites during mitosis. Nat Cell Biol 8: 1008-1015
36. Newman M, Murray-Rust J, Lally J, Rudolf J, Fadden A, Knowles PP, White MF, McDonald NQ, (2005) Structure of an XPF endonuclease with and without DNA suggests a model for substrate recognition. EMBO J 24: 895-905
37. Nishino T, Komori K, Ishino Y, Morikawa K, (2005) Structural and functional analyses of an archaeal XPF/Rad1/Mus81 nuclease: asymmetric DNA binding and cleavage mechanisms. Structure 13: 1183-1192
38. Orans J, McSweeney EA, Iyer RR, Hast MA, Hellinga HW, Modrich P, Beese LS, (2011) Structures of human exonuclease 1 DNA complexes suggest a unified mechanism for nuclease family. Cell 145: 212-223
39. Otwinowski Z, Minor W, (1997) Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol 276: 307-326
40. Roberts JA, White MF, (2005) DNA end-directed and processive nuclease activities of the archaeal XPF enzyme. Nucleic Acids Res 33: 6662-6670
41. Schwartz EK, Heyer WD, (2011) Processing of joint molecule intermediates by structure-selective endonucleases during homologous recombination in eukaryotes. Chromosoma 120: 109-127
42. 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
43. Tsodikov OV, Enzlin JH, Scharer OD, Ellenberger T, (2005) Crystal structure and DNA binding functions of ERCC1, a subunit of the DNA structure-specific endonuclease XPF-ERCC1. Proc Natl Acad Sci 102: 11236-11241
44. Tsutakawa SE, Classen S, Chapados BR, Arvai AS, Finger LD, Guenther G, Tomlinson CG, Thompson P, Sarker AH, Shen B, Cooper PK, Grasby JA, Tainer JA, (2011) Human flap endonuclease structures, DNA double-base flipping, and a unified understanding of the FEN1 superfamily. Cell 145: 198-211
45. Wechsler T, Newman S, West SC, (2011) Aberrant chromosome morphology in human cells defective for Holliday junction resolution. Nature 471: 642-646
46. Whitby MC, Osman F, Dixon J, (2003) Cleavage of model replication forks by fission yeast Mus81-Eme1 and budding yeast Mus81-Mms4. J Biol Chem 278: 6928-6935
47. Wu L, Hickson ID, (2003) The Bloom's syndrome helicase suppresses crossing over during homologous recombination. Nature 426: 870-874
48. Wyatt HD, Sarbajna S, Matos J, West SC, (2013) Coordinated Actions of SLX1-SLX4 and MUS81-EME1 for Holliday junction resolution in Human Cells. Mol Cell 52: 1-14
49. Yang W, (2008) An equivalent metal ion in one- and two-metal-ion catalysis. Nat Struct Mol Biol 15: 1228-1231
50. 2+-ion catalysis and substrate specificity. Mol Cell 22: 5-13
51. Ying S, Minocherhomji S, Chan KL, Palmai-Pallag T, Chu WK, Wass T, Mankouri HW, Liu Y, Hickson ID, (2013) MUS81 promotes common fragile site expression. Nat Cell Biol 15: 1001-1007