Human MUS81-EME2 can cleave a variety of DNA structures including intact Holliday junction and nicked duplex

Nucleic Acids Research

Volumn 42, Issue 9, 2014, Pages 5846-5862

  Amangyeld, Tamir ^a   Shin, Yong Keol ^a   Lee, Miju ^a   Kwon, Buki ^a   Seo, Yeon Soo ^a  

^a Korea Advanced Institute of Science and Technology (KAIST)   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

DOUBLE STRANDED DNA; ENDONUCLEASE; ESCHERICHIA COLI PROTEIN; PHOSPHATE; PROTEIN EME2; PROTEIN MUS81; RECOMBINANT PROTEIN; RECOMBINANT PROTEIN EME2; RECOMBINANT PROTEIN MUS81; UNCLASSIFIED DRUG;

5' UNTRANSLATED REGION; ARTICLE; CATALYSIS; CONTROLLED STUDY; DNA CLEAVAGE; DNA STRAND BREAKAGE; DNA STRUCTURE; ENZYME SPECIFICITY; HOLLIDAY JUNCTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN DNA INTERACTION; PROTEIN FUNCTION; PROTEIN ISOLATION; PROTEIN MODIFICATION; RECOMBINATION REPAIR;

DNA BREAKS, DOUBLE-STRANDED; DNA BREAKS, SINGLE-STRANDED; DNA CLEAVAGE; DNA, CRUCIFORM; DNA-BINDING PROTEINS; ENDODEOXYRIBONUCLEASES; ENDONUCLEASES; ESCHERICHIA COLI; HUMANS; KINETICS; MULTIPROTEIN COMPLEXES; PROTEIN SUBUNITS; SUBSTRATE SPECIFICITY;

EID: 84901358862     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gku237     Document Type: Article

References (45)

1. Kuzminov, A. (1995) Collapse and repair of replication forks in Escherichia Coli Mol. Microbiol., 16, 373-384.
2. Fabre, F., Chan, A., Heyer, W.D. and Gangloff, S. (2002) Alternate pathways involving Sgs1/Top3, Mus81/Mms4, and Srs2 prevent formation of toxic recombination intermediates from single-stranded gaps created by DNA replication. Proc. Natl. Acad. Sci. U.S.A., 99, 16887-16892.
3. Cox, M.M., Goodman, M.F., Kreuzer, K.N., Sherratt, D.J., Sandlerk, S.J. and Marians, K.J. (2000) The importance of repairing stalled replication forks. Nature, 404, 37-41. (Pubitemid 30143124
4. Kowalczykowski, S.C. (2000) Initiation of genetic recombination and recombination-dependent replication. Trends Biochem. Sci., 25, 156-165.
5. Higgins, N.P., Kato, K. and Strauss, B. (1976) A model for replication repair in mammalian cells. J. Mol. Biol., 101, 417-425.
6. Seigneu, M., Bidnenko, V., Ehrlich, S.D. and Michel, B. (1998) RuvAB acts at arrested replication forks. Cell, 95, 419-430. (Pubitemid 28507329
7. Lilley, D.M. and White, M.F. (2001) The junction-resolving enzymes. Nat. Rev. Mol. Cell Biol., 433, 433-443.
8. Ralf, C., Hickson, I.D. and Wu, L. (2006) The Bloom's syndrome helicase can promote the regression of a model replication fork. J. Biol. Chem., 32, 22839-22846.
9. Sharples, G.J. (2001) The X philes: Structure-specific endonucleases that resolve Holliday junctions. Mol. Microbiol., 39, 823-834.
10. 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.
11. Takahagi, M., Iwasaki, H. and Shinagawa, H. (1994) Structural requirements of substrate DNA for binding to and cleavage by RuvC, a Holliday junction resolvase. J. Biol. Chem., 269, 15132-15139. (Pubitemid 24198358
12. Whitby, M.C. and Dixon, J. (1998) Substrate specificity of the SpCCE1 Holliday junction resolvase of Schizosaccharomyces pombe. J. Biol. Chem., 273, 35063-35073.
13. Ip, S.C.Y., Rass, U., Blanco, M.G., Flynn, H.R., Skehel, J.M. and West, S.C. (2008) Identification of Holliday junction resolvases from humans and yeast. Nature, 456, 357-361.
14. Rass, U., Compton, S.A., Matos, J., Singleton, M.R., Ip, S.C.Y., Blanco, M.G., Griffith, J.D. and West, S.C. (2010) Mechanism of Holliday junction resolution by the human GEN1 protein. Genes Dev., 24, 1559-1569.
15. Fekairi, S., Scaglione, S., Chahwan, C., Taylor, E.R., Tissier, A., Coulon, S., Dong, M.Q., Ruse, C., Yates, J.R. III, Russell, P. et al. (2009) Human SLX4 is a Holliday junction resolvase subunit that binds multiple DNA repair/recombination endonucleases. Cell, 138, 78-89.
16. Svendsen, J.M., Smogorzewska, A., Sowa, M.E., O'Connell, B.C., Gygi, S.P., Elledge, S.J. and Harper, J.W. (2009) Mammalian BTBD12/SLX4 assembles a Holliday junction resolvase and is required for DNA repair. Cell, 138, 63-77.
17. Andersen, S.L., Bergstralh, D.T., Kohl, K.P., LaRocque, J.R., Moore, C.B. and Sekelsky, J. (2009) Drosophila MUS312 and the vertebrate ortholog BTBD12 interact with DNA structure-specific endonucleases in DNA repair and recombination. Mol. Cell, 35, 128-135.
18. Ciccia, A., McDonald, N. and West, S.C. (2008) Structural and functional relationships of the XPF/MUS81 family of proteins. Annu. Rev. Biochem., 77, 259-287.
19. Ciccia, A., Constantinou, A. and West, S.C. (2003) Identification and characterization of the human Mus81/Eme1 endonuclease. J. Biol. Chem., 278, 25172-25178.
20. Ciccia, A., Ling, C., Coulthard, R., Yan, Z., Xue, Y., Meetei, A.R., Laghmani, E.H., Joenje, H., McDonald, N., de Winter, J.P. et al. (2007) Identification of FAAP24, a Fanconi Anemia core complex protein that interacts with FANCM. Mol. Cell, 25, 331-343.
21. Wu, L. and Hickson, I.D. (2003) The Bloom's syndrome helicase suppresses crossing over during homologous recombination. Nature, 426, 870-874. (Pubitemid 38056876
22. 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.
23. Interthal, H. and Heyer, W.D. (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.
24. 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.
25. 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.
26. 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.
27. Hollingsworth, N.M. and Brill, S.J. (2004) The Mus81 solution to resolution: Generating meiotic crossovers without Holliday junctions. Genes Dev., 18, 117-125. (Pubitemid 38141779
28. 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. (Pubitemid 32988882
29. Kang, M.J., Lee, C.H., Kang, Y.H., Cho, I.T., Nguyen, T.A. and Seo, Y.S. (2010) Genetic and functional interactions between Mus81-Mms4 and Rad27. Nucleic Acids Res., 38, 7611-7625.
30. Ehmsen, K.T. and Heyer, W.D. (2008) Saccharomyces cerevisiae Mus81-Mms4 is a catalytic, DNA structure-selective endonuclease. Nucleic Acids Res., 36, 2182-2195.
31. 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.
32. Shin, Y.K., Amangyeld, T., Nguyen, T.A., Munashingha, P.R. and Seo, Y.S. (2012) Human MUS81 complexes stimulate flap endonuclease 1. FEBS J., 279, 2412-2430.
33. Geuting, V., Kobbe, D., Hartung, F., Durr, J., Focke, M. and Puchta, H. (2009) Two distinct MUS81-EME1 complexes from Arabidopsis process Holliday Junctions. Plant Physiol., 150, 1062-1071.
34. Ehmsen, K.T. and Heyer, W.D., (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.
35. Osman, F., Gaskell, L. and Whitby, M.C. (2009) Efficient second strand cleavage during Holliday junction resolution by RuvC requires both increased junction flexibility and an exposed 5' phosphate. PLoS ONE, 4, e5347.
36. Boddy, M.N., Pierre-Henri, L., Gaillard, McDonald, W.H., Shanahan, P., Yates, J.R. and Russell, P. (2001) Mus81-Eme1 are essential components of a Holliday Junction Resolvase. Cell, 107, 537-548. (Pubitemid 33152788
37. Gaskell, L.J., Osman, F., Gilbert, R.J. and Whitby, M.C. (2007) Mus81 cleavage of Holliday junctions: A failsafe for processing meiotic recombination intermediates? EMBO J., 26, 1891-1901.
38. Taylor, E.R. and McGowan, C.H. (2008) Cleavage mechanism of human Mus81-Eme1 acting on Holliday-junction structures. Proc. Natl. Acad. Sci. U.S.A., 105, 3757-3762.
39. Matos, J., Blanco, M.G., Maslen, S., Skehel, J.M. and West, S.C. (2011) Regulatory control of the resolution of DNA recombination intermediates during meiosis and mitosis. Cell, 147, 158-172.
40. Matos, J., Blanco, M.J. and West, S.C. (2013) Cell-cycle kinases coordinate the resolution of recombination intermediates with chromosome segregation. Cell Rep., 4, 78-86.
41. Wyatt, H.D.M., Sarbajna, S., Matos, J. and West, S.C. (2013) Coordinated actions of SLX1-SLX4 and MUS81-EME1 for Holliday junction resolution in human cells. Mol. Cell, 52, 234-247.
42. Schalbetter, S., Bowles, M., Harris, R., Lally, J., Carr, A.M. and McDonald, N.Q. (2013) A winged helix domain in human MUS81 binds DNA and modulates the endonuclease activity of MUS81 compelxes. Nucleic Acids Res., 41, 9741-9752.
43. White, A., Ding, X., vanderSpek, J.C., Murphy, J.R. and Ringe, D. (1998) Structure of the metal-ion-Activated diphtheria toxin repressor/tox operator complex. Nature, 394, 502-506.
44. Hanada, K., Budzowska, M., Davies, S.L., Drunen, E.V., Onizawa, H., Beverloo, H.B., Mass, A., Essers, J., Hickson, I.D. and Kanaar, R. (2007) The structure-specific endonuclease Mus81 contributes to replication restart by generating double-strand DNA breaks. Nature, 14, 1096-1104. (Pubitemid 350060335
45. 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. (Pubitemid 35231037