Substrate specificity of the MUS81-EME2 structure selective endonuclease

Nucleic Acids Research

Volumn 42, Issue 6, 2014, Pages 3833-3845

  Pepe, Alessandra ^a   West, Stephen C ^a  

^a IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID SEQUENCE; DNA-BINDING PROTEINS; ENDODEOXYRIBONUCLEASES; ENDONUCLEASES; HEK293 CELLS; HUMANS; MOLECULAR SEQUENCE DATA; PROTEIN ISOFORMS; RECOMBINATION, GENETIC; SEQUENCE ALIGNMENT; SUBSTRATE SPECIFICITY;

EID: 84898965087     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkt1333     Document Type: Article

References (40)

1. Dendouga, N., Gao, H., Moechars, D., Janicot, M., Vialard, J. and McGowan, C. H. (2005) Disruption of murine Mus81 increases genomic instability and DNA damage sensitivity but does not promote tumorigenesis. Mol. Cell. Biol., 25, 7569-7579.
2. McPherson, J. P., Lemmers, B., Chahwan, R., Pamidi, A., Migon, E., Maytysiak-Zablocki, E., Moynahan, M. E., Essers, J., Hanada, K., Poonepalli, A. et al. (2004) Involvement of mammalian Mus81 in genome integrity and tumor suppression. Science, 304, 1822-1826.
3. Hanada, K., Budzowska, M., Modesti, M., Maas, A., Wyman, C., Essers, J. and Kanaar, R. (2006) The structure-specific endonuclease MUS81-EME1 promotes conversion of interstrand crosslinks into double-strand breaks. EMBO J., 25, 4921-4932.
4. 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. (2007) The structure-specific endonuclease MUS81 contributes to replication restart by generating double-strand DNA breaks. Nat. Struct. Mol. Biol., 14, 1096-1104.
5. Shimura, T., Torres, M. J., Martin, M. M., Rao, V. A., Pommier, Y., Katsura, M., Miyagawa, K. and Aladjerm, M. I. (2008) Bloom's syndrome helicase and MUS81 are required to induce transient double-strand DNA breaks in response to DNA replication stress. J. Mol. Biol., 375, 1152-1164.
6. Ying, S. M., Minocherhomji, S., Chan, K. L., Palmai-Pallag, T., Chu, W. K., Wass, T., Mankouri, H. W., Liu, Y. and Hickson, I. D. (2013) MUS81 promotes common fragile site expression. Nat. Cell Biol., 15, 1001-1007.
7. Fugger, K., Chu, W. K., Haahr, P., Kousholt, A. N., Beck, H., Payne, M. J., Hanada, K., Hickson, I. D. and Sorensen, C. S. (2013) FBH1 co-operates with MUS81 in inducing DNA double-strand breaks and cell death following replication stress. Nat. Commun., 4, 1423.
8. Wechsler, T., Newman, S. and West, S. C. (2011) Aberrant chromosome morphology in human cells defective for Holliday junction resolution. Nature, 471, 642-646.
9. 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.
10. Castor, D., Nair, N., Déclais, A. C., Lachaud, C., Toth, R., Macartney, T. J., Lilley, D. M. J., Arthur, J. S. and Rouse, J. (2013) Cooperative control of Holliday junction resolution and DNA repair by the SLX1 and MUS81-EME1 nucleases. Mol. Cell, 52, 221-233.
11. Garner, E., Kim, Y., Lach, F. P., Kottemann, M. C. and 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, 207-215.
12. 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.
13. 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 G(2)/M checkpoints and promotes rereplication in human cells. Nucleic Acids Res., 34, 880-892.
14. Zeng, S. C. and Yang, Q. (2009) The MUS81 endonuclease is essential for telomerase negative cell proliferation. Cell Cycle, 8, 2157-2160.
15. Boddy, M. N., Gaillard, P. H. L., 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.
16. Osman, F., Dixon, J., Doe, C. L. and Whitby, M. C. (2003) Generating crossovers by resolution of nicked Holliday junctions: a role of Mus81-Eme1 in meiosis. Mol. Cell, 12, 761-774.
17. de los Santos, T., Hunter, N., Lee, C., Larkin, B., Loidl, J. and Hollingsworth, N. M. (2003) The Mus81/Mms4 endonuclease acts independently of double-Holliday junction resolution to promote a distinct subset of crossovers during meiosis in budding yeast. Genetics, 164, 81-94.
18. Jessop, L. and Lichten, M. (2008) Mus81/Mms4 endonuclease and Sgs1 helicase collborate to ensure proper recombination intermediate metabolism during meiosis. Mol. Cell, 31, 313-323.
19. Oh, S. D., Lao, J. P., Taylor, A. F., Smith, G. R. and Hunter, N. (2008) RecQ helicase, Sgs1, and XPF family endonuclease, Mus81-Mms4, resolve aberrant joint molecules during meiotic recombination. Mol. Cell, 31, 324-336.
20. Zakharyevich, K., Tang, S. M., Ma, Y. M. and Hunter, N. (2012) Delineation of joint molecule resolution pathways in meiosis identifies a crossover-specific resolvase. Cell, 149, 334-347.
21. Holloway, J. K., Booth, J., Edelmann, W., McGowan, C. H. and Cohen, P. E. (2009) MUS81 generates a subset of MLH1-MLH3-independent crossovers in mammalian meiosis. PLoS Genet., 4, e1000186.
22. 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.
23. 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.
24. 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.
25. 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.
26. Ciccia, A., Constantinou, A. and West, S. C. (2003) Identification and characterization of the human MUS81/EME1 endonuclease. J. Biol. Chem., 278, 25172-25178.
27. Taylor, E. R. and McGowan, C. H. (2008) Cleavage mechanism of human MUS81-EME1 acting on Holliday-junction structures. Proc. Natl Acad. Sci. USA, 105, 3757-3762.
28. Matos, J., Blanco, M. G., Maslen, S. L., 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.
29. Matos, J., Blanco, M. G. and West, S. C. (2013) Cell cycle kinases coordinate the resolution of recombination intermediates with chromosome segregation. Cell Rep., 4, 76-86.
30. Szakal, B. and Branzei, D. (2013) Premature Cdk1/Cdc5/Mus81 pathway activation induces aberrant replication and deleterious crossover. EMBO J., 32, 1155-1167.
31. Gallo-Fernandez, M., Sauger, I., Ortiz-Bazan, M. A., Vazquez, M. V. and Tercero, J. A. (2012) Cell cycle-dependent regulation of the nuclease activity of Mus81-Eme1/Mms4. Nucleic Acids Res., 40, 8325-8335.
32. Ciccia, A., McDonald, N. and West, S. C. (2008) Structural and functional relationships of the XPF/MUS81 family of proteins. Ann. Rev. Biochem., 77, 259-287.
33. 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 FANC M. Mol. Cell, 25, 331-343.
34. 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.
35. Rass, U. and West, S. C. (2006) Synthetic junctions as tools to identify and characterise Holliday junction resolvases. In: Campbell, J. L. and Modrich, P. (eds), Methods in Enzymology, Vol. 408. San Diego, Elsevier, pp. 485-501.
36. Deans, A. J. and West, S. C. (2009) FANCM connects the genome instability disorders Bloom's syndrome and Fanconi anemia. Mol. Cell, 36, 943-953.
37. O? grunc, M. and Sancar, A. (2003) Identification and characterization of human MUS81-MMS4 structure-specific endonuclease. J. Biol. Chem., 278, 21715-21720.
38. 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.
39. Griffith, J. D., Comeau, L., Rosenfield, S., Stansel, R. M., Bianchi, A., Moss, H. and de Lange, T. (1999) Mammalian telomeres end in a large duplex loop. Cell, 97, 503-514.
40. Doksani, Y., Wu, J. Y., de Lange, T. and Zhuang, X. (2013) Superresolution fluorescence imaging of telomeres reveals TRF2-dependent T-loop formation. Cell, 155, 345-356.