Mms22p protects Saccharomyces cerevisiae from DNA damage induced by topoisomerase II

Nucleic Acids Research

Volumn 33, Issue 3, 2005, Pages 1021-1030

  Baldwin, E L ^a   Berger, A C ^b   Corbett, A H ^b   Osheroff, Neil ^a  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMSACRINE; DNA TOPOISOMERASE (ATP HYDROLYSING); DOUBLE STRANDED DNA; ETOPOSIDE; NUCLEAR PROTEIN; PROTEIN MMS22P; UNCLASSIFIED DRUG; CULLIN; MMS22 PROTEIN, S CEREVISIAE; RTT101 PROTEIN, S CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEIN;

ARTICLE; CELL CYCLE; CONTROLLED STUDY; DNA DAMAGE; DNA STRAND BREAKAGE; FUNGAL STRAIN; FUNGUS CULTURE; GENETIC CODE; GENOME; HOMOLOGOUS RECOMBINATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN LOCALIZATION; SACCHAROMYCES CEREVISIAE; WILD TYPE; YEAST; CELL NUCLEUS; CHEMISTRY; DNA REPAIR; DRUG EFFECT; ENZYMOLOGY; GENE DELETION; GENETIC RECOMBINATION; GENETICS; METABOLISM; PHYSIOLOGY;

SACCHAROMYCES CEREVISIAE;

CELL CYCLE; CELL NUCLEUS; CULLIN PROTEINS; DNA DAMAGE; DNA REPAIR; DNA TOPOISOMERASES, TYPE II, EUKARYOTIC; ETOPOSIDE; GENE DELETION; RECOMBINATION, GENETIC; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 14244257657     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gki246     Document Type: Article

References (63)

1. Lindahl,T. (1993) Instability and decay of the primary structure of DNA. Nature, 362, 709-715.
2. Jackson,A.L., Newcomb,T.G. and Loeb,L.A. (1998) Origin of multiple mutations in human cancers. Drug Metab. Rev., 30, 285-304.
3. Friedberg,E.C. (2003) DNA damage and repair. Nature, 421, 436-440.
4. Friedberg,E.C., Walker,G.C. and Siede,W. (1995) DNA Repair and Mutagenesis, 2nd edn. American Society for Microbiology Press, Washington, DC.
5. Marnett,L.J. and Plastaras,J.P. (2001) Endogenous DNA damage and mutation. Trends Genet., 117, 214-221.
6. Burden,D.A. and Osheroff,N. (1998) Mechanism of action of eukaryotic topoisomerase II and drugs targeted to the enzyme. Biochim. Biophys. Acta, 1400, 139-154.
7. Wang,J.C. (1998) Moving one DNA double helix through another by a type II DNA topoisomerase: The story of a simple molecular machine. Quart. Rev. Biophys., 31, 107-144.
8. Fortune,J.M. and Osheroff,N. (2000) Topoisomerase II as a target for anticancer drugs: When enzymes stop being nice. Prog. Nucleic Acid Res. Mol. Biol., 64, 221-253.
9. Champoux,J.J. (2001) DNA topoisomerases: Structure, function, and mechanism. Annu. Rev. Biochem., 70, 369-413.
10. Sabourin,M. and Osheroff,N. (2002) Topoisomerases. In Creighton,T. E. (ed.), Encyclopedia of Molecular Medicine. John Wiley & Sons, New York, Vol. 5, pp. 3192-3197.
11. Wilstermann,A.M. and Osheroff,N. (2003) Stabilization of eukaryotic topoisomerase II-DNA cleavage complexes. Curr. Top. Med. Chem., 3, 321-338.
12. Baguley,B.C. and Ferguson,L.R. (1998) Mutagenic properties of topoisomerase-targeted drugs. Biochim. Biophys. Acta, 1400, 213-222.
13. Felix,C.A. (2001) Leukemias related to treatment with DNA topoisomerase II inhibitors. Med. Pediatr. Oncol., 36, 525-535.
14. Wang,J.C. (1996) DNA topoisomerases. Annu. Rev. Biochem., 65 635-692.
15. Nitiss,J.L. (1998) Investigating the biological functions of DNA topoisomerases in eukaryotic cells. Biochim. Biophys. Acta, 1400, 63-81.
16. Berger,J.M., Gamblin,S.J., Harrison,S.C. and Wang,J.C. (1996) Structure and mechanism of DNA topoisomerase II. Nature, 379, 225-232.
17. Sander,M. and Hsieh,T. (1983) Double strand DNA cleavage by type II DNA topoisomerase from Drosophila melanogaster. J. Biol. Chem., 258 8421-8428.
18. Liu,L.F., Rowe,T.C., Yang,L., Tewey,K.M. and Chen,G.L. (1983) Cleavage of DNA by mammalian DNA topoisomerase II. J. Biol. Chem., 258 15365-15370.
19. Zechiedrich,E.L., Christiansen,K., Andersen,A.H., Westergaard,O. and Osheroff,N. (1989) Double-stranded DNA cleavage/religatiion reaction of eukaryotic topoisomerase II: Evidence for a nicked DNA intermediate. Biochemistry, 28, 6229-6236.
20. Holm,C., Covey,J.M., Kerrigan,D. and Pommier,Y. (1989) Differential requirement of DNA replication for the cytotoxicity of DNA topoisomerase I and II inhibitors in Chinese hamster DC3F cells. Cancer Res., 49, 6365-6368.
21. Corbett,A.H. and Osheroff,N. (1993) When good enzymes go bad: Conversion of topoisomerase II to a cellular toxin by antineoplastic drugs. Chem. Res. Toxicol., 6, 585-597.
22. Howard,M.T., Neece,S.H., Matson,S.W. and Kreuzer,K.N. (1994) Disruption of a topoisomerase-DNA cleavage complex by a DNA helicase. Proc. Natl Acad. Sci. USA, 91, 12031-12035.
23. D'Arpa,P. (1994) Determinants of cellular sensitivity to topoisomerase-targeting antitumor drugs. Adv. Pharmacol., 29B 127-143.
24. Chen,A.Y. and Liu,L.F. (1994) DNA topoisomerases: Essential enzymes and lethal targets. Annu. Rev. Pharmacol. Toxicol., 34, 191-218.
25. Kaufmann,S.H. (1998) Cell death induced by topoisomerase-targeted drugs: more questions than answers. Biochim. Biophys. Acta, 1400, 195-211.
26. Nitiss,J.L., Liu,Y.X., Harbury,P., Jannatipour,M., Wasserman,R. and Wang,J.C. (1992) Amsacrine and etoposide hypersensitivity of yeast cells overexpressing DNA topoisomerase II. Cancer Res., 52, 4467-4472.
27. Nitiss,J.L., Liu,Y.X. and Hsiung,Y. (1993) A temperature sensitive topoisomerase II allele confers temperature dependent drug resistance on amsacrine and etoposide: A genetic system for determining the targets of topoisomerase II inhibitors. Cancer Res., 53, 89-93.
28. Felix,C.A. (1998) Secondary leukemias induced by topoisomerase-targeted drugs. Biochim. Biophys. Acta, 1400, 233-255.
29. Rowley,J.D. (1998) The critical role of chromosome translocations in human leukemias. Annu. Rev. Gen., 32, 495-519.
30. Smith,M.A., Rubinstein,L., Anderson,J.R., Arthur,D., Catalano,P.J., Freidlin,B., Heyn,R., Khayat,A., Krailo,M., Land,V.J., Miser,J., Shuster,J. and Vena,D. (1999) Secondary leukemia or myelodysplastic syndrome after treatment with epipodophyllotoxins. J. Clin. Oncol. 17, 569-577.
31. Ross,J.A., Potter,J.D., Reaman,G.H., Pendergrass,T.W. and Robison,L.L. (1996) Maternal exposure to potential inhibitors of DNA topoisomerase II and infant leukemia (United States): A report from the Children's Cancer Group. Cancer Causes Control, 7, 581-590.
32. Ross,J.A. (1998) Maternal diet and infant leukemia: A role for DNA topoisomerase II inhibitors?. Int. J. Cancer Suppl., 11, 26-28.
33. Lindsey,R.H.,Jr, Bromberg,K.D., Felix,C.A. and Osheroff,N. (2004) 1,4-Benzoquinone is a topoisomerase II poison. Biochemistry, 43 7563-7574.
34. Sabourin,M., Nitiss,J.L., Nitiss,K.C., Tatebayashi,K., Ikeda,H. and Osheroff,N. (2003) Yeast recombination pathways triggered by topoisomerase II-mediated DNA breaks. Nucleic Acids Res., 31 4373-4384.
35. Winzeler,E.A., Shoemaker,D.D., Astromoff,A., Liang,H., Anderson,K., Andre,B., Bangham,R., Benito,R., Boeke,J.D., Bussey,H. et al. (1999) Functional characterization of the S. cerevisiae genome by gene deletion and parallel analysis. Science, 285, 901-906.
36. Nitiss,J. and Wang,J.C. (1988) DNA topoisomerase-targeting antitumor drugs can be studied in yeast. Proc. Natl Acad. Sci. USA, 85 7501-7505.
37. Rothstein,R. (1991) Targeting, disruption, replacement, and allele rescue: Integrative DNA transformation in yeast. Methods Enzymol., 194, 281-301.
38. Yamagata,K., Kato,J., Shimamoto,A., Goto,M., Furuichi,Y. and Ikeda,H. (1998) Bloom's and Werner's syndrome genes suppress hyperrecombination in yeast sgs1 mutant: Implication for genomic instability in human diseases. Proc. Natl Acad. Sci. USA, 95, 8733-8738.
39. Niedenthal,R.K., Riles,L., Johnston,M. and Hegemann,J.H. (1996) Green fluorescent protein as a marker for gene expression and subcellular localization in budding yeast. Yeast, 12, 773-786.
40. Paques,F. and Haber,J.E. (1999) Multiple pathways of recombination induced by double-strand breaks in Saccharomyces cerevisiae. Microbiol. Mol. Biol. Rev., 63, 349-404.
41. Haber,J.E. (2000) Partners and pathways repairing a double-strand break. Trends Genet., 16, 259-264.
42. Dudas,A. and Chovanec,M. (2004) DNA double-strand break repair by homologous recombination. Mutat. Res., 566, 131-167.
43. Hopfner,K.P., Putnam,C.D. and Tainer,J.A. (2002) DNA double-strand break repair from head to tail. Curr. Opin. Struct. Biol., 12, 115-122.
44. Moore,J.K. and Haber,J.E. (1996) Cell cycle and genetic requirements of two pathways of nonhomologous end joining repair of double-strand breaks in Saccharomyces cerevisiae. Mol. Cell. Biol., 16, 2164-2173.
45. Lewis,L.K. and Resnick,M.A. (2000) Tying up loose ends: Nonhomologous end-joining in Saccharomyces cerevisiae. Mutat. Res., 451, 71-89.
46. Bennett,C.B., Lewis,L.K., Karthikeyan,G., Lobachev,K.S., Jin,Y.H., Sterling,J.F., Snipe,J.R. and Resnick,M.A. (2001) Genes required for ionizing radiation resistance in yeast. Nature Genet., 29, 426-434.
47. Araki,Y., Kawasaki,Y., Sasanuma,H., Tye,B.K. and Sugino,A. (2003) Budding yeast mcm10/dna43 mutant requires a novel repair pathway for viability. Genes Cells, 8, 465-480.
48. Chang,M., Bellaoui,M., Boone,C. and Brown,G.W. (2002) A genome-wide screen for methyl methanesulfonate-sensitive mutants reveals genes required for S phase progression in the presence of DNA damage. Proc. Natl Acad. Sci. USA, 99, 16934-16939.
49. Parsons,A.B., Brost,R.L., Ding,H., Li,Z., Zhang,C., Sheikh,B., Brown,G.W., Kane,P.M., Hughes,T.R. and Boone,C. (2004) Integration of chemical-genetic and genetic interaction data links bioactive compounds to cellular target pathways. Nat. Biotechnol., 22, 62-69.
50. Elsea,S.H., Osheroff,N. and Nitiss,J.L. (1992) Cytotoxicity of quinolones toward eukaryotic cells. Identification of topoisomerase II as the primary cellular target for the quinolone CP-115,953 in yeast. J. Biol. Chem., 267, 13150-13153.
51. Byl,J.A., Cline,S.D., Utsugi,T., Kobunai,T., Yamada,Y. and Osheroff,N. (2001) DNA topoisomerase II as the target for the anticancer drug TOP-53: Mechanistic basis for drug action. Biochemistry, 40, 712-718.
52. Hsiung,Y., Elsea,S.H., Osheroff,N. and Nitiss,J.L. (1995) A mutation in yeast TOP2 homologous to a quinolone-resistant mutation in bacteria. Mutation of the amino acid homologous to Ser83 of Escherichia coli gyrA alters sensitivity to eukaryotic topoisomerase inhibitors. J. Biol. Chem., 270, 20359-20364.
53. Ho,Y., Gruhler,A., Heilbut,A., Bader,G.D., Moore,L., Adams,S.L., Millar,A., Taylor,P., Bennett,K., Boutilier,K. et al. (2002) Systematic identification of protein complexes in Saccharomyces cerevisiae by mass spectrometry. Nature, 415, 180-183.
54. Scholes,D.T., Banerjee,M., Bowen,B. and Curcio,M.J. (2001) Multiple regulators of Ty1 transposition in Saccharomyces cerevisiae have conserved roles in genome maintenance. Genetics, 159, 1449-1465.
55. Michel,J.J., McCarville,J.F. and Xiong,Y. (2003) A role for Saccharomyces cerevisiae Cul8 ubiquitin ligase in proper anaphase progression. J. Biol. Chem., 278, 22828-22837.
56. Rouse,J. (2004) Esc4p, a new target of Mec1p (ATR), promotes resumption of DNA synthesis after DNA damage. EMBO J., 23, 1188-1197.
57. Lisby,M. and Rothstein,R. (2004) DNA damage checkpoint and repair centers. Curr. Opin. Cell Biol., 16, 328-334.
58. Lisby,M., Mortensen,U.H. and Rothstein,R. (2003) Colocalization of multiple DNA double-strand breaks at a single Rad52 repair centre. Nature Cell Biol., 5, 572-577.
59. Wolner,B., van Komen,S., Sung,P. and Peterson,C.L. (2003) Recruitment of the recombinational repair machinery to a DNA double-strand break in yeast. Mol. Cell, 12, 221-232.
60. Frei,C. and Gasser,S.M. (2000) The yeast Sgs1p helicase acts upstream of Rad53p in the DNA replication checkpoint and colocalizes with Rad53p in S-phase-specific foci. Genes Dev., 14, 81-96.
61. Pasero,P., Duncker,B.P., Schwob,E. and Gasser,S.M. (1999) A role for the Cdc7 kinase regulatory subunit Dbf4p in the formation of initiation-competent origins of replication. Genes Dev., 13, 2159-2176.
62. Melo,J.A., Cohen,J. and Toczyski,D.P. (2001) Two checkpoint complexes are independently recruited to sites of DNA damage in vivo. Genes Dev., 15, 2809-2821.
63. Tercero,J.A., Longhese,M.P. and Diffley,J.F. (2003) A central role for DNA replication forks in checkpoint activation and response. Mol. Cell, 11, 1323-1336.