The mechanism of Mus81-Mms4 cleavage site selection distinguishes it from the homologous endonuclease Rad1-Rad10

Molecular and Cellular Biology

Volumn 23, Issue 10, 2003, Pages 3487-3496

  Bastin Shanower, Suzanne A ^a   Fricke, William M ^a   Mullen, Janet R ^a   Brill, Steven J ^a  

^a RUTGERS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ENDONUCLEASE;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; DNA DAMAGE; ENZYME DEGRADATION; ENZYME SPECIFICITY; ENZYME STRUCTURE; EXCISION REPAIR; GENE REPLICATION; HOMOLOGOUS RECOMBINATION; IN VIVO STUDY; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN STABILITY; SACCHAROMYCES CEREVISIAE; SEQUENCE HOMOLOGY; STRUCTURE ANALYSIS;

BASE SEQUENCE; DIMERIZATION; DNA DAMAGE; DNA-BINDING PROTEINS; DOSE-RESPONSE RELATIONSHIP, DRUG; DOSE-RESPONSE RELATIONSHIP, RADIATION; ENDONUCLEASES; FUNGAL PROTEINS; MOLECULAR SEQUENCE DATA; MUTATION; PLASMIDS; PROTEIN BINDING; RECOMBINANT PROTEINS; RECOMBINATION, GENETIC; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SUBSTRATE SPECIFICITY; TIME FACTORS; TRANS-ACTIVATORS; ULTRAVIOLET RAYS;

SACCHAROMYCES; SACCHAROMYCES CEREVISIAE;

EID: 0037965787     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.23.10.3487-3496.2003     Document Type: Article

References (49)

1. Bardwell, A. J., L. Bardwell, A. E. Tomkinson, and E. C. Friedberg. 1994. Specific cleavage of model recombination and repair intermediates by the yeast Rad1-Rad10 DNA endonuclease. Science 265:2082-2085.
2. Bennett, R. J., M. F. Noirot-Gros, and J. C. Wang. 2000. Interaction between yeast Sgs1 helicase and DNA topoisomerase III. J. Biol. Chem. 275:26898-26905.
3. Boddy, M. N., P. H. Gaillard, W. H. McDonald, P. Shanahan, J. R. Yates III, and P. Russell. 2001. Mus81-Eme1 are essential components of a Holliday junction resolvase. Cell 107:537-548.
4. Boddy, M. N., A. Lopez-Girona, P. Shanahan, H. Interthal, W. D. Heyer, and P. Russell. 2000. Damage tolerance protein Mus81 associates with the FHA1 domain of checkpoint kinase Cds1. Mol. Cell. Biol. 20:8758-8766.
5. Bolt, E. L., and R. G. Lloyd. 2002. Substrate specificity of RusA resolvase reveals the DNA structures targeted by RuvAB and RecG in vivo. Mol. Cell 10:187-198.
6. Chakraverty, R. K., and I. D. Hickson. 1999. Defending genome integrity during DNA replication: a proposed role for RecQ family helicases. Bioessays 21:286-294.
7. Chen, X. B., R. Melchionna, C. M. Denis, P. H. Gaillard, A. Blasina, I. Van de Weyer, M. N. Boddy, P. Russell, J. Vialard, and C. H. McGowan. 2001. Human Mus81-associated endonuclease cleaves Holliday junctions in vitro. Mol. Cell 8:1117-1127.
8. Constantinou, A., X. B. Chen, C. H. McGowan, and S. C. West. 2002. Holliday junction resolution in human cells: two junction endonucleases with distinct substrate specificities. EMBO J. 21:5577-5585.
9. Courcelle, J., C. Carswell-Crumpton, and P. C. Hanawalt. 1997. recF and recR are required for the resumption of replication at DNA replication forks in Escherichia coli. Proc. Natl. Acad. Sci. USA 94:3714-3719.
10. Cox, M. M. 2001. Historical overview: searching for replication help in all of the rec places. Proc. Natl. Acad. Sci. USA 98:8173-8180.
11. de Laat, W. L., E. Appeldoorn, N. G. Jaspers, and J. H. Hoeijmakers. 1998. DNA structural elements required for ERCC1-XPF endonuclease activity. J. Biol. Chem. 273:7835-7842.
12. de los Santos, T., J. Loidl, B. Larkin, and N. M. Hollingsworth. 2001. A role for MMS4 in the processing of recombination intermediates during meiosis in Saccharomyces cerevisiae. Genetics 159:1511-1525.
13. Doe, C. L., J. S. Ahn, J. Dixon, and M. C. Whitby. 2002. Mus81-Eme1 and Rqh1 involvement in processing stalled and collapsed replication forks. J. Biol. Chem. 25:25.
14. - phenotype by expression of a bacterial Holliday junction resolvase. EMBO J. 19:2751-2762.
15. Eng, W. K., L. Faucette, R. K. Johnson, and R. Sternglanz. 1988. Evidence that DNA topoisomerase I is necessary for the cytotoxic effects of camptothecin. Mol. Pharmacol. 34:755-760.
16. Fabre, F., A. Chan, W. D. Heyer, and S. Gangloff. 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.
17. Fricke, W. M., V. Kaliraman, and S. J. Brill. 2001. Mapping the DNA topoisomerase III binding domain of the Sgs1 DNA helicase. J. Biol. Chem. 276:8848-8855.
18. Gangloff, S., B. de Massy, L. Arthur, R. Rothstein, and F. Fabre. 1999. The essential role of yeast topoisomerase III in meiosis depends on recombination. EMBO J. 18:1701-1711.
19. Gangloff, S., J. P. McDonald, C. Bendixen, L. Arthur, and R. Rothstein. 1994. The yeast type I topoisomerase Top3 interacts with Sgs1, a DNA helicase homolog: a potential eukaryotic reverse gyrase. Mol. Cell. Biol. 14:8391-8398.
20. Goldstein, A. L., and J. H. McCusker. 1999. Three new dominant drug resistance cassettes for gene disruption in Saccharomyces cerevisiae. Yeast 15:1541-1553.
21. Guldener, U., S. Heck, T. Fielder, J. Beinhauer, and J. H. Hegemann. 1996. A new efficient gene disruption cassette for repeated use in budding yeast. Nucleic Acids Res. 24:2519-2524.
22. Higgins, N. P., K. Kato, and B. Strauss. 1976. A model for replication repair in mammalian cells. J. Mol. Biol. 101:417-425.
23. Interthal, H., and W. D. Heyer. 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. Johnson, F. B., D. B. Lombard, N. F. Neff, M. A. Mastrangelo, W. Dewolf, N. A. Ellis, R. A. Marciniak, Y. Yin, R. Jaenisch, and L. Guarente. 2000. Association of the Bloom syndrome protein with topoisomerase IIIα in somatic and meiotic cells. Cancer Res. 60:1162-1167.
25. Kadyk, L. C., and L. H. Hartwell. 1993. Replication-dependent sister chromatid recombination in rad1 mutants of Saccharomyces cerevisiae. Genetics 133:469-487.
26. Kadyk, L. C., and L. H. Hartwell. 1992. Sister chromatids are preferred over homologs as substrates for recombinational repair in Saccharomyces cerevisiae. Genetics 132:387-402.
27. Kaliraman, V., J. R. Mullen, W. M. Fricke, S. A. Bastin-Shanower, and S. J. Brill. 2001. Functional overlap between Sgs1-Top3 and the Mms4-Mus81 endonuclease. Genes Dev. 15:2730-2740.
28. Kim, R. A., and J. C. Wang. 1992. Identification of the yeast TOP3 gene product as a single strand-specific DNA topoisomerase. J. Biol. Chem. 267:17178-17185.
29. Klein, H. 2001. Mutations in recombinational repair and in checkpoint control genes suppress the lethal combination of srs2Δ with other DNA repair genes in Saccharomyces cerevisiae. Genetics 157:557-565.
30. Liu, C., J. J. Pouliot, and H. A. Nash. 2002. Repair of topoisomerase I covalent complexes in the absence of the tyrosyl-DNA phosphodiesterase Tdp1. Proc. Natl. Acad. Sci. USA 99:14970-14975.
31. Liu, L. F., P. Duann, C. T. Lin, P. D'Arpa, and J. Wu. 1996. Mechanism of action of camptothecin. Ann. N. Y. Acad. Sci. 803:44-49.
32. Lopes, M., C. Cotta-Ramusino, A. Pellicioli, G. Liberi, P. Plevani, M. Muzi-Falconi, C. S. Newlon, and M. Foiani. 2001. The DNA replication checkpoint response stabilizes stalled replication forks. Nature 412:557-561.
33. Mullen, J. R., V. Kaliraman, and S. J. Brill. 2000. Bipartite structure of the SGS1 DNA helicase in Saccharomyces cerevisiae. Genetics 154:1101-1114.
34. Mullen, J. R., V. Kaliraman, S. S. Ibrahim, and S. J. Brill. 2001. Requirement for three novel protein complexes in the absence of the Sgs1 DNA helicase in Saccharomyces cerevisiae. Genetics 157:103-118.
35. Nitiss, J., and J. C. Wang. 1988. DNA topoisomerase-targeting antitumor drugs can be studied in yeast. Proc. Natl. Acad. Sci. USA 85:7501-7505.
36. Nitiss, J. L., and J. C. Wang. 1996. Mechanisms of cell killing by drugs that trap covalent complexes between DNA topoisomerases and DNA. Mol. Pharmacol. 50:1095-1102.
37. Pouliot, J. J., C. A. Robertson, and H. A. Nash. 2001. Pathways for repair of topoisomerase I covalent complexes in Saccharomyces cerevisiae. Genes Cells 6:677-687.
38. Rose, M. D., F. Winston, and P. Hieter. 1990. Methods in yeast genetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
39. Rothstein, R., B. Michel, and S. Gangloff. 2000. Replication fork pausing and recombination or "gimme a break." Genes Dev. 14:1-10.
40. Seigneur, M., V. Bidnenko, S. D. Ehrlich, and B. Michel. 1998. RuvAB acts at arrested replication forks. Cell 95:419-430.
41. Sijbers, A. M., W. L. de Laat, R. R. Ariza, M. Biggerstaff, Y. F. Wei, J. G. Moggs, K. C. Carter, B. K. Shell, E. Evans, M. C. de Jong, S. Rademakers, J. de Rooij, N. G. Jaspers, J. H. Hoeijmakers, and R. D. Wood. 1996. Xeroderma pigmentosum group F caused by a defect in a structure-specific DNA repair endonuclease. Cell 86:811-822.
42. Tomkinson, A. E., A. J. Bardwell, L. Bardwell, N. J. Tappe, and E. C. Friedberg. 1993. Yeast DNA repair and recombination proteins Rad1 and Rad10 constitute a single-stranded-DNA endonuclease. Nature 362:860-862.
43. Tong, A. H., M. Evangelista, A. B. Parsons, H. Xu, G. D. Bader, N. Page, M. Robinson, S. Raghibizadeh, C. W. Hogue, H. Bussey, B. Andrews, M. Tyers, and C. Boone. 2001. Systematic genetic analysis with ordered arrays of yeast deletion mutants. Science 294:2364-2368.
44. Vance, J. R., and T. E. Wilson. 2002. Yeast Tdp1 and Rad1-Rad10 function as redundant pathways for repairing Top1 replicative damage. Proc. Natl. Acad. Sci. USA 99:13669-13674.
45. Wang, J. C. 1991. DNA topoisomerases: why so many? J. Biol. Chem. 266:6659-6662.
46. White, M. F., and D. M. Lilley. 1996. The structure-selectivity and sequence-preference of the junction-resolving enzyme CCE1 of Saccharomyces cerevisiae. J. Mol. Biol. 257:330-341.
47. Wu, L., S. L. Davies, P. S. North, H. Goulaouic, J. F. Riou, H. Turley, K. C. Gatter, and I. D. Hickson. 2000. The Bloom's syndrome gene product interacts with topoisomerase III. J. Biol. Chem. 275:9636-9644.
48. Xiao, W., B. L. Chow, and C. N. Milo. 1998. Mms4, a putative transcriptional (co)activator, protects Saccharomyces cerevisiae cells from endogenous and environmental DNA damage. Mol. Gen. Genet. 257:614-623.
49. Zou, H., and R. Rothstein. 1997. Holliday junctions accumulate in replication mutants via a RecA homolog-independent mechanism. Cell 90:87-96.