Crystal structure of the Mus81-Eme1 complex

Genes and Development

Volumn 22, Issue 8, 2008, Pages 1093-1106

  Jeong, Ho Chang ^a   Jeong, Joo Kim ^a   Jung, Min Choi ^a   Jung, Hoon Lee ^a   Cho, Yunje ^a  

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

Author keywords

Crystal structure; Mus81 Eme1; Nicked Holliday junction; Structure specific endonuclease; Substrate preference

Indexed keywords

DNA; ENDONUCLEASE; MUS81 EME1 COMPLEX; UNCLASSIFIED DRUG;

ARTICLE; CRYSTAL STRUCTURE; HOLLIDAY JUNCTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN MOTIF;

BINDING SITES; CRYSTALLOGRAPHY, X-RAY; DNA; DNA, CRUCIFORM; DNA-BINDING PROTEINS; ENDODEOXYRIBONUCLEASES; ENDONUCLEASES; HUMANS; MODELS, BIOLOGICAL; MODELS, MOLECULAR; MUTATION; PROTEIN STRUCTURE, TERTIARY;

ARCHAEA; EUKARYOTA;

EID: 42149183549     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.1618708     Document Type: Article

References (47)

1. Abraham, J., Lemmers, B., Hande, M.P., Moynahan, M.E., Chahwan, C., Ciccia, A., Essers, J., Hanada, K., Chahwan, R., Khaw, A.K., et al. 2003. Eme1 is involved in DNA damage processing and maintenance of genomic stability in mammalian cells. EMBO J. 22: 6137-6147.
2. Bastin-Shanower, S.A., Fricke, W.M., Mullen, J.R., and Brill, S.J. 2003. The mechanism of Mus81-Mms4 cleavage site selection distinguishes it from the homologous endonuclease Rad1-Rad10. Mol. Cell. Biol. 23: 3487-3496.
3. Blais, V., Gao, H., Elwell, C.A., Boddy, M.N., Gaillard, P.H., Russel, P., and McGowan, C.H. 2004. RNA interference inhibition of Mus81 reduces mitotic recombination in human cells. Mol. Biol. Cell 15: 552-562.
4. Boddy, M.N., Lopez-Girona, A., Shanahan, P., Interthal, H., Heyer, W.D., and Russell, P. 2000. Damage tolerance protein Mus81 associates with the FHA1 domain of checkpoint kinase Cds1. Mol. Cell. Biol. 20: 8758-8766.
5. Boddy, M.N., Gaillard, P.-H.L., McDonald, W.H., Shanahan, P., Yates III, J.R., and Russell, P. 2001. Mus81-Eme1 are essential components of a Holliday junction resolvase. Cell 107: 537-548.
6. Brünger, A.T., Adams, P.D., Clore, G.M., DeLano, W.L., Gros, P., Grosse-Kunstleve, R.W., Jiang, J.S., Kuszewski, J., Nilges, M., Pannu, N.S., et al. 1998. Crystallography and NMR system: A new software suite for macromolecular structure determination. Acta Crstallogr. D Biol. Crystallogr. 54: 905-921.
7. Chen, X.B., Melchionna, R., Denis, C.M., Gaillard, P.H., Blasina, A., Van de Weyer, I., Boddy, M.N., Russell, P., Vialard, J., and McGowan, C.H. 2001. Human Mus81-associated endonuclease cleaves Holliday junctions in vitro. Mol. Cell 8: 1117-1127.
8. Ciccia, A., Constantinou, A., and West, S.C. 2003. Identification and characterization of the human mus81-eme1 endonuclease. J. Biol. Chem. 278: 25172-25178.
9. Constantinou, A., Chen, X.-B., McGowan, C.H., and West, S.C. 2002. Holliday junction resolution in human cells: Two junction endonucleases with distinct substrate specificities. EMBO J. 21: 5577-5585.
10. Cox, M.M., Goodman, M.F., Kreuzer, K.N., Sherratt, D.J., Sandler, S.J., and Marians, K.J. 2000. The importance of repairing stalled replication forks. Nature 404: 37-41.
11. De Laat, W.L., Appeldoorn, E., Jaspers, N.G.J., and Hoeijmakers, J.H.J. 1998. DNA structural elements required for ERCC1-XPF endonuclease activity. J. Biol. Chem. 273: 7835-7842.
12. de los Santos, T., Loidl, J., Larkin, B., and Hollingsworth, N.M. 2001. A role for MMS4 in the processing of recombination intermediates during meiosis in Saccharomyces cerevisiae. Genetics 159: 1511-1525.
13. Doe, C.L., Ahn, J.S., Dixon, J., and Whitby, M.C. 2002. Mus81-Eme1 and Rqh1 involvement in processing stalled and collapsed replication forks. J. Biol. Chem. 277: 32753-32759.
14. Emsley, P. and Cowtan, K. 2004. Coot: Model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60: 2126-2132.
15. Fricke, W.M., Bastin-shanower, S.A., and Brill, S.J. 2005. Substrate specificity of the Saccharomyces cerevisiae Mus81-Mms4 endonuclease. DNA Repair (Amst.) 4: 243-251.
16. Fu, Y. and Xiao, W. 2003. Functional domains required for the Saccharomyces cerevisiae Mus81-Mms4 endonuclease complex formation and nuclear localization. DNA Repair (Amst.) 2: 1435-1447.
17. Gaillard, P.H., Noguchi, E., Shanahan, P., and Russell, P. 2003. The endogenous Mus81-Eme1 complex resolves Holliday junctions by a nick and counternick mechanism. Mol. Cell 12: 747-759.
18. Gao, H., Chen, X.B., and McGowan, C.H. 2003. Mus81 endonuclease localizes to nucleoli and to regions of DNA damage in human S-phase cells. Mol. Biol. Cell 14: 4826-4834.
19. Gaskell, L.J., Osman, F., Gilbert, R.J.C., and Whitby, M.C. 2007. Mus81 cleavage of Holliday junctions: A failsafe for processing meiotic recombination intermediates? EMBO J. 26: 1891-1901.
20. Hartung, F., Suer, S., Bergmann, T., and Puchta, H. 2006. The role of AtMUS81 in DNA repair and its genetic interaction with the helicase AtRecQ4A. Nucleic Acids Res. 34: 4438-4448.
21. Heyer, W.D., Ehmsen, K.T., and Solinger, J.A. 2003. Holliday junctions in the eukaryotic nucleus: Resolution in sight? Trends Biochem. Sci. 28: 548-557.
22. Hiyama, T., Katsura, M., Yoshihara, T., Ishida, M., Kinomura, A., Tonda, T., Asahara, T., and 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.
23. Holliday, R.A. 1964. A mechanism for gene conversion in fungi. Genet. Res. 5: 282-304.
24. Hollingsworth, N.M. and Brill, S.J. 2004. The Mus81 solution to resolution: Generating meiotic crossovers without Holliday junctions. Genes & Dev. 18: 117-125.
25. Hwang, K.Y., Baek, K., Kim, H.Y., and Cho, Y. 1998. The crystal structure of flap endonuclease-1 from Methanococcus jannaschii. Nat. Struct. Biol. 5: 707-713.
26. Kai, M., Boddy, M.N., Russell, P., and Wang, T.S. 2005. Replication checkpoint kinase Cds1 regulates Mus81 to preserve genome integrity during replication stress. Genes & Dev. 19: 919-932.
27. Kaliraman, V., Mullen, J.R., Fricke, W.M., Bastin-Shanower, S.A., and Brill, S.J. 2001. Functional overlap between Sgs1-Top3 and the Mms4-Mus81 endonuclease. Genes & Dev. 15: 2730-2740.
28. Li, X. and Heyer, W.-D. 2008. Homologous recombination in DNA repair and DNA damage tolerance. Cell Res. 18: 99-113.
29. Lilley, D.M. and White, M.F. 2001. The junction-resolving enzymes. Nat. Rev. Mol. Cell Biol. 2: 433-443.
30. McGlynn, P. and Lloyd, R.G. 2003. Recombinational repair and restart of damaged replication forks. Nat. Rev. Mol. Cell Biol. 3: 859-870.
31. Michel, B., Grompone, G., Flores, M.J., and Bidnenko, V. 2004. Multiple pathways process stalled replication forks. Proc. Natl. Acad. Sci. 101: 12783-12788.
32. Mullen, J.R., Kaliraman, V., Ibrahim, S.S., and Brill, S.J. 2001. Requirement for three novel protein complexes in the absence of the Sgs1 DNA helicase in Saccharomyces cerevisiae. 2001. Genetics 157: 103-118.
33. Newman, M., Murray-Rust, J., Lally, J., Rudolf, J., Fadden, A., Knowles, P.P., White, M.F., and McDonald, N.Q. 2005. Structure of an XPF endonuclease with and without DNA suggests a model for substrate recognition. EMBO J. 24: 895-905.
34. Nishino, T., Komori, K., Ishino, Y., and Morikawa, K. 2003. X-ray and biochemical anatomy of an archaeal XPF/Rad1/Mus81 family nuclease: Similarity between its endonuclease domain and restriction enzymes. Structure 11: 445-457.
35. Nishino, T., Komori, K., Ishino, Y., and Morikawa, K. 2005. Structural and functional analyses of an archaeal XPF/Rad1/Mus81 nuclease: Asymmetric DNA binding and cleavage mechanisms. Structure 13: 1183-1192.
36. Odagiri, N., Seki, M., Onoda, F., Yoshimura, A., Watanabe, S., and Enomoto, T. 2003. Budding yeast mms4 is epistatic with rad52 and the function of Mms4 can be replaced by a bacterial Holliday junction resolvase. DNA Repair (Amst.) 2: 347-358.
37. Ogrunc, M. and Sancar, A. 2003. Identification and characterization of human MUS81-MMS4 structure-specific endonuclease. J. Biol. Chem. 278: 21715-21720.
38. Osman, F., Dixon, J., Doe, C.L., and Whitby, M.C. 2003. Generating crossovers by resolution of nicked Holliday junctions: A role for Mus81-Eme1 in meiosis. Mol. Cell 12: 761-774.
39. Otwinowski, Z. and Minor, W. 1997. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276: 307-326.
40. Roberts, J.A. and White, M.F. 2005a. DNA end-directed and processive nuclease activities of the archaeal XPF enzyme. Nucleic Acids Res. 33: 6662-6670.
41. Roberts, J.A. and White, M.F. 2005b. An archaeal endonuclease displays key properties of both eukaryal XPF-ERCC1 and Mus81. J. Biol. Chem. 280: 5924-5928.
42. Rothstein, R., Michel, B., and Gangloff, S. 2000. Replication fork pausing and recombination or 'gimme a break.' Genes & Dev. 14: 1-10.
43. Schneider, T.R. and Sheldrick, G.M. 2002. Substructure solution with SHELXD. Acta Crystallogr. D Biol. Crystallogr. 58: 1772-1779.
44. Schwacha, A. and Kleckner, N. 1995. Identification of double Holliday junctions as intermediates in meiotic recombination. Cell 83: 783-791.
45. Tsodikov, O.V., Enzlin, J.H., Scharer, O.D., and 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.
46. Whitby, M.C., Osman, F., and 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. Wood, R.D. 1997. Nucleotide excision repair in mammalian cells. J. Biol. Chem. 272: 23465-23468.