Eme1 is involved in DNA damage processing and maintenance of genomic stability in mammalian cells

EMBO Journal

Volumn 22, Issue 22, 2003, Pages 6137-6147

  Abraham, Jacinth ^a,b   Lemmers, Bénédicte ^a,b   Hande, M Prakash ^c   Moynahan, Mary Ellen ^d   Chahwan, Charly ^a   Ciccia, Alberto ^e   Essers, Jeroen ^f   Hanada, Katsuhiro ^f   Chahwan, Richard ^a   Khaw, Aik Kia ^c   McPherson, Peter ^a   Shehabeldin, Amro ^a,b   Laister, Rob ^b   Arrowsmith, Cheryl ^b   Kanaar, Roland ^f   West, Stephen C ^e   Jasin, Maria ^d   Hakem, Razqallah ^a,b  

^a PRINCESS MARGARET HOSPITAL   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^d MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^e IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

^f ERASMUS MEDICAL CENTER   (Netherlands)

Author keywords

DNA repair; Genomic instability; Homologous recombination; Inter strand DNA cross links; Mus81 Eme1

Indexed keywords

CISPLATIN; DNA; ENDONUCLEASE; ESSENTIAL MEIOTIC ENDONUCLEASE 1; HYDROXYUREA; METHYLMETHANESULFONATE SENSITIVE ULTRAVIOLET SENSITIVE 81; MITOMYCIN C; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; COMPLEX FORMATION; CONTROLLED STUDY; DNA CROSS LINKING; DNA DAMAGE; DNA REPAIR; DNA REPLICATION; DRUG SENSITIVITY; EMBRYO; EMBRYO CELL; GENE CONVERSION; GENE TARGETING; GENETIC STABILITY; HOLLIDAY JUNCTION; HOMOLOGOUS RECOMBINATION; HUMAN; HUMAN CELL; IN VITRO STUDY; IONIZING RADIATION; MAMMAL CELL; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEFICIENCY; PROTEIN DEPLETION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; SISTER CHROMATID EXCHANGE; STEM CELL; ULTRAVIOLET RADIATION;

AMINO ACID SEQUENCE; ANIMALS; CHROMOSOMAL INSTABILITY; DNA DAMAGE; DNA REPAIR; DNA-BINDING PROTEINS; ENDODEOXYRIBONUCLEASES; ENDONUCLEASES; GENOMIC INSTABILITY; HUMANS; MICE; MOLECULAR SEQUENCE DATA; SACCHAROMYCES CEREVISIAE PROTEINS; SCHIZOSACCHAROMYCES POMBE PROTEINS; SISTER CHROMATID EXCHANGE; STEM CELLS;

ANIMALIA; MAMMALIA;

EID: 10744231462     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/cdg580     Document Type: Article

References (44)

1. Bassing, C.H., Swat, W. and Alt, F.W. (2002) The mechanism and regulation of chromosomal V(D)J recombination. Cell, 109, S45-S55.
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. Benson, F.E. and West, S.C. (1994) Substrate specificity of the Escherichia coli RuvC protein. Resolution of three- and four-stranded recombination intermediates. J. Biol. Chem., 269, 5195-5201.
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., McDonald, W.H., Shanahan, P., Yates, J.R., 3rd and Russell, P. (2001) Mus81-Eme1 are essential components of a Holliday junction resolvase. Cell, 107, 537-548.
6. Chakraverty, R.K. and Hickson, I.D. (1999) Defending genome integrity during DNA replication. BioEssays, 21, 286-294.
7. Chen, X.B. et al. (2001) Human Mus81-associated endonuclease cleaver 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. D'Andrea, A.D. and Grompe, M. (2003) The Fanconi anaemia/BRCA pathway. Nat. Rev. Cancer, 3, 23-34.
11. Dasika, G.K., Lin, S.C., Zhao, S., Sung, P., Tomkinson, A. and Lee, E.Y. (1999) DNA damage-induced cell cycle checkpoints and DNA strand break repair in development and tumorigenesis. Oncogene, 18, 7883-7899.
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. Dronkert, M.L. and Kanaar, R. (2001) Repair of DNA interstrand cross-links. Mutat. Res., 486, 217-247.
15. Enzlin, J.H. and Scharer, O.D. (2002) The active site of the DNA repair endonuclease XPF-ERCC1 forms a highly conserved nuclease motif. EMBO J., 21, 2045-2053.
16. Essers, J., Hendriks, R.W., Swagemakers, S.M., Troelstra, C., de Wit, J., Bootsma, D., Hoeijmakers, J.H. and Kanaar, R. (1997) Disruption of mouse RAD54 reduces ionizing radiation resistance and homologous recombination. Cell, 89, 195-204.
17. Essers, J., Hendriks, R.W., Wesoly, J., Beerens, C.E., Smit, B., Hoeijmakers, J.H., Wyman, C., Dronkert, M.L. and Kanaar, R. (2002) Analysis of mouse Rad54 expression and its implications for homologous recombination. DNA Repair, 1, 779-793.
18. 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. USA, 99, 16887-16892.
19. Haber, J.E. and Heyer, W.D. (2001) The fuss about Mus81. Cell, 107, 551-554.
20. Hakem, R. et al. (1998) Differential requirement for caspase 9 in apoptotic pathways in vivo. Cell, 94, 339-352.
21. Hirao, A., Kong, Y.Y., Matsuoka, S., Wakeham, A., Ruland, J., Yoshida, H., Liu, D., Elledge, S.J. and Mak, T.W. (2000) DNA damage-induced activation of p53 by the checkpoint kinase Chk2. Science, 287, 1824-1827.
22. 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.
23. Johnson, R.D. and Jasin, M. (2001) Double-strand-break-induced homologous recombination in mammalian cells. Biochem. Soc. Trans., 29, 196-201.
24. 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.
25. Kaufmann, W.K. (1995) Cell cycle checkpoints and DNA repair preserve the stability of the human genome. Cancer Metastasis Rev., 14, 31-41.
26. Luo, G., Santoro, I.M., McDaniel, L.D., Nishijima, I., Mills, M., Youssoufian, H., Vogel, H., Schultz, R.A. and Bradley, A. (2000) Cancer predisposition caused by elevated mitotic recombination in Bloom mice. Nat. Genet., 26, 424-429.
27. McGlynn, P. and Lloyd, R.G. (2002) Recombinational repair and restart of damaged replication forks. Nat. Rev. Mol. Cell. Biol., 3, 859-870.
28. Moynahan, M.E., Pierce, A.J. and Jasin, M. (2001) BRCA2 is required for homology-directed repair of chromosomal breaks. Mol. Cell, 7, 263-272.
29. 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. Genetics, 157, 103-118.
30. Niedernhofer, L.J., Essers, J., Weeda, G., Beverloo, B., de Wit, J., Muijtjens, M., Odijk, H., Hoeijmakers, J.H., and Kanaar, R. (2001) The structure-specific endonuclease Ercc1-Xpf is required for targeted gene replacement in embryonic stem cells. EMBO J., 20, 6540-6549.
31. Ogrunc, M. and Sancar, A. (2003) Identification and characterization of human MUS81-MMS4 structure-specific endonuclease. J. Biol. Chem., 278, 21715-21720.
32. Pierce, A.J., Johnson, R.D., Thompson, L.H. and Jasin, M. (1999) XRCC3 promotes homology-directed repair of DNA damage in mammalian cells. Genes Dev., 13, 2633-2638.
33. Richardson, C., Moynahan, M.E. and Jasin, M. (1998) Double-strand break repair by interchromosomal recombination: suppression of chromosomal translocations. Genes Dev., 12, 3831-3842.
34. Rooney, S. et al. (2003) Defective DNA repair and increased genomic instability in Artemis-deficient murine cells. J. Exp. Med., 197, 553-565.
35. Roth, D.B. (2002) Amplifying mechanisms of lymphomagenesis. Mol. Cell, 10, 1-2.
36. Rouse, J. and Jackson, S.P. (2002) Interfaces between the detection, signaling and repair of DNA damage. Science, 297, 547-551.
37. Sekiguchi, J. et al. (2001) Genetic interactions between ATM and the nonhomologous end-joining factors in genomic stability and development. Proc. Natl. Acad. Sci. USA, 98, 3243-3248.
38. Sonoda, E., Sasaki, M.S., Morrison, C., Yamaguchi-Iwai, Y., Takata, M. and Takeda, S. (1999) Sister chromatid exchanges are mediated by homologous recombination in vertebrate cells. Mol. Cell. Biol., 19, 5166-5169.
39. te Riele, H., Maandag, E.R., Clarke, A., Hooper, M. and Berns, A. (1990) Consecutive inactivation of both alleles of the pim-1 proto-oncogene by homologous recombination in embryonic stem cells. Nature, 348, 649-651.
40. Wang, W., Seki, M., Narita, Y., Sonoda, E., Takeda, S., Yamada, K., Masuko, T., Katada, T. and Enomoto, T. (2000) Possible association of BLM in decreasing DNA double strand breaks during DNA replication. EMBO J., 19, 3428-3435.
41. Wang, W. et al. (2003) Functional relation among RecQ family helicases RecQL1, RecQL5 and BLM in cell growth and sister chromatid exchange formation. Mol. Cell. Biol., 23, 3527-3535.
42. 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.
43. Xiao, W., Chow, B.L. and Milo, C.N. (1998) Mms4, a putative transcriptional (co)activator, protects Saccharomyces cerevisiae cells from endogenous and environmental DNA damage. Mol. Gen. Genet., 257, 614-623.
44. Zhou, B.B. and Elledge, S.J. (2000) The DNA damage response: putting checkpoints in perspective. Nature, 408, 433-439.