Drosophila bloom helicase maintains genome integrity by inhibiting recombination between divergent DNA sequences

Nucleic Acids Research

Volumn 36, Issue 21, 2008, Pages 6907-6917

  Kappeler, Michael ^a   Kranz, Elisabeth ^a   Woolcock, Katrina ^a   Georgiev, Oleg ^a   Schaffner, Walter ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; DOUBLE STRANDED DNA; DROSOPHILA PROTEIN; HELICASE;

ARTICLE; CELL CULTURE; DNA RECOMBINATION; DNA REPAIR; DNA SEQUENCE; DNA STRAND BREAKAGE; DROSOPHILA MELANOGASTER; GENE EXPRESSION REGULATION; GENE FREQUENCY; GENETIC RECOMBINATION; GENETIC VARIABILITY; HOMOLOGOUS RECOMBINATION; IN VIVO STUDY; MISMATCH REPAIR; NONHUMAN; PRIORITY JOURNAL; SACCHAROMYCES CEREVISIAE; SEQUENCE ANALYSIS; SEQUENCE HOMOLOGY;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; BASE SEQUENCE; CELL LINE; DNA BREAKS, DOUBLE-STRANDED; DNA HELICASES; DNA REPAIR; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; GENOME, INSECT; MOLECULAR SEQUENCE DATA; RECOMBINATION, GENETIC; REPETITIVE SEQUENCES, NUCLEIC ACID; SEQUENCE ANALYSIS, DNA;

DROSOPHILA MELANOGASTER; MAMMALIA; SACCHAROMYCES CEREVISIAE;

EID: 57149096230     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkn793     Document Type: Article

References (40)

1. Shrivastav,M., De Haro,L.P. and Nickoloff,J.A. (2008) Regulation of DNA double-strand break repair pathway choice. Cell Res., 18, 134-147.
2. Pastink,A., Eeken,J.C. and Lohman,P.H. (2001) Genomic integrity and the repair of double-strand DNA breaks. Mutat. Res., 480, 37-50.
3. Shen,P. and Huang,H.V. (1986) Homologous recombination in Escherichia coli: Dependence on substrate length and homology. Genetics, 112, 441-457.
4. Gonda,D.K. and Radding,C.M. (1983) By searching processively RecA protein pairs DNA molecules that share a limited stretch of homology. Cell, 34, 647-654.
5. Nassif,N. and Engels,W. (1993) DNA homology requirements for mitotic gap repair in Drosophila. Proc. Natl Acad. Sci. USA, 90, 1262-1266.
6. Coveny,A.M., Dray,T. and Gloor,G.B. (2002) The effect of heterologous insertions on gene conversion in mitotically dividing cells in Drosophila melanogaster. Genetics, 161, 249-258.
7. Waldman,A.S. and Liskay,R.M. (1987) Differential effects of base-pair mismatch on intrachromosomal versus extrachromosomal recombination in mouse cells. Proc. Natl Acad. Sci. USA, 84, 5340-5344.
8. Waldman,A.S. and Liskay,R.M. (1988) Dependence of intrachromosomal recombination in mammalian cells on uninterrupted homology. Mol. Cell. Biol., 8, 5350-5357.
9. Matsuo,K., Clay,O., Kunzler,P., Georgiev,O., Urbanek,P. and Schaffner,W. (1994) Short introns interrupting the Oct-2 POU domain may prevent recombination between POU family genes without interfering with potential POU domain 'shuffling' in evolution. Biol. Chem. Hoppe-Seyler, 375, 675-683.
10. Rayssiguier,C., Thaler,D.S. and Radman,M. (1989) The barrier to recombination between Escherichia coli and Salmonella typhimurium is disrupted in mismatch-repair mutants. Nature, 342, 396-401.
11. Datta,A., Adjiri,A., New,L., Crouse,G.F. and Jinks Robertson,S. (1996) Mitotic crossovers between diverged sequences are regulated by mismatch repair proteins in Saccharomyces cerevisiae. Mol. Cell. Biol., 16, 1085-1093.
12. Bailis,A.M. and Rothstein,R. (1990) A defect in mismatch repair in Saccharomyces cerevisiae stimulates ectopic recombination between homeologous genes by an excision repair dependent process. Genetics 126, 535-547.
13. Sugawara,N., Goldfarb,T., Studamire,B., Alani,E. and Haber,J.E. (2004) Heteroduplex rejection during single-strand annealing requires Sgs1 helicase and mismatch repair proteins Msh2 and Msh6 but not Pms1. Proc. Natl Acad. Sci. USA, 101, 9315-9320.
14. Elliott,B. and Jasin,M. (2001) Repair of double-strand breaks by homologous recombination in mismatch repair-defective mammalian cells. Mol. Cell. Biol., 21, 2671-2682.
15. de Wind,N., Dekker,M., Berns,A., Radman,M. and te Riele,H. (1995) Inactivation of the mouse Msh2 gene results in mismatch repair defficiency, methylation tolerance, hyperrecombination, and predisposition to cancer. Cell, 82, 321-330.
16. Hanada,K., Ukita,T., Kohno,Y., Saito,K., Kato,J. and Ikeda,H. (1997) RecQ DNA helicase is a suppressor of illegitimate recombinationin Escherichia coli. Proc. Natl Acad. Sci. USA, 94, 3860-3865.
17. Schmidt,K.H., Wu,J. and Kolodner,R.D. (2006) Control of translocations between highly diverged genes by Sgs1, the Saccharomyces cerevisiae homolog of the Bloom's syndrome protein. Mol. Cell. Biol., 26 5406-5420.
18. Myung,K., Datta,A., Chen,C. and Kolodner,R.D. (2001) SGS1, the Saccharomyces cerevisiae homologue of BLM and WRN, suppresses genome instability and homeologous recombination. Nat. Genet., 27, 113-116.
19. Spell,R.M. and Jinks-Robertson,S. (2004) Examination of the roles of Sgs1 and Srs2 helicases in the enforcement of recombination fidelity in Saccharomyces cerevisiae. Genetics, 168, 1855-1865.
20. Kusano,K., Berres,M.E. and Engels,W.R. (1999) Evolution of the RECQ family of helicases: A drosophila homolog, Dmblm, is similar to the human bloom syndrome gene. Genetics, 151, 1027-1039.
21. Kusano,K., Johnson-Schlitz,D.M. and Engels,W.R. (2001) Sterility of Drosophila with mutations in the Bloom syndrome gene - complementation by Ku70. Science, 291, 2600-2602.
22. Adams,M.D., McVey,M. and Sekelsky,J.J. (2003) Drosophila BLM in double-strand break repair by synthesis-dependent strand annealing. Science, 299, 265-267.
23. Johnson-Schlitz,D. and Engels,W.R. (2006) Template disruptions and failure of double Holliday junction dissolution during double-strand break repair in Drosophila BLM mutants. Proc. Natl Acad. Sci. USA, 103, 16840-16845.
24. McVey,M., Larocque,J.R., Adams,M.D. and Sekelsky,J.J. (2004) Formation of deletions during double-strand break repair in Drosophila DmBlm mutants occurs after strand invasion. Proc. Natl Acad. Sci. USA, 101, 15694-15699.
25. Chaganti,R.S., Schonberg,S. and German,J. (1974) A manyfold increase in sister chromatid exchanges in Bloom's syndrome lymphocytes. Proc. Natl Acad. Sci. USA, 71, 4508-4512.
26. Chester,N., Babbe,H., Pinkas,J., Manning,C. and Leder,P. (2006) Mutation of the murine Bloom's syndrome gene produces global genome destabilization. Mol. Cell. Biol., 26, 6713-6726.
27. Bugreev,D.V., Yu,X., Egelman,E.H. and Mazin,A.V. (2007) Novel pro- and anti-recombination activities of the Bloom's syndrome helicase. Genes Dev., 21, 3085-3094.
28. Wu,L., Bachrati,C.Z., Ou,J., Xu,C., Yin,J., Chang,M., Wang,W., Li,L., Brown,G.W. and Hickson,I.D. (2006) BLAP75/RMI1 promotes the BLM-dependent dissolution of homologous recombination intermediates. Proc. Natl Acad. Sci. USA, 103, 4068-4073.
29. Raynard,S., Bussen,W. and Sung,P. (2006) A double Holliday junction dissolvasome comprising BLM, topoisomerase IIIalpha, and BLAP75. J. Biol. Chem., 281, 13861-13864.
30. Bischof,J., Maeda,R.K., Hediger,M., Karch,F. and Basler,K. (2007) An optimized transgenesis system for Drosophila using germ-line-specific phiC31 integrases. Proc. Natl Acad. Sci. USA, 104, 3312-3317.
31. Schildkraut,E., Miller,C.A. and Nickoloff,J.A. (2005) Gene conversion and deletion frequencies during double-strand break repair in human cells are controlled by the distance between direct repeats. Nucleic Acids Res., 33, 1574-1580.
32. Groth,A.C., Fish,M., Nusse,R. and Calos,M.P. (2004) Construction of Transgenic Drosophila by Using the Site-Specific Integrase From Phage {phi}C31. Genetics, 166, 1775-1782.
33. Wei,D.S. and Rong,Y.S. (2007) A genetic screen for DNA double-strand break repair mutations in Drosophila. Genetics, 177, 63-77.
34. McVey,M., Adams,M., Staeva-Vieira,E. and Sekelsky,J.J. (2004) Evidence for multiple cycles of strand invasion during repair of double-strand gaps in Drosophila. Genetics, 167, 699-705.
35. Flores,C. and Engels,W. (1999) Microsatellite instability in Drosophila spellchecker1 (MutS homolog) mutants. Proc. Natl Acad. Sci. USA, 96, 2964-2969.
36. Korbel,J.O., Urban,A.E., Affourtit,J.P., Godwin,B., Grubert,F., Simons,J.F., Kim,P.M., Palejev,D., Carriero,N.J., Du,L. et al. (2007) Paired-end mapping reveals extensive structural variation in the human genome. Science, 318, 420-426.
37. Kidd,J.M., Cooper,G.M., Donahue,W.F., Hayden,H.S., Sampas,N., Graves,T., Hansen,N., Teague,B., Alkan,C., Antonacci,F. et al. (2008) Mapping and sequencing of structural variation from eight human genomes. Nature, 453, 56-64.
38. Emerson,J.J., Cardoso-Moreira,M., Borevitz,J.O. and Long,M. (2008) Natural selection shapes genome-wide patterns of copy-number polymorphism in Drosophila melanogaster. Science, 320, 1629-1631.
39. Preston,C.R., Sved,J.A. and Engels,W.R. (1996) Flanking duplications and deletions associated with P-induced male recombination in Drosophila. Genetics, 144, 1623-1638.
40. Preston,C.R., Engels,W. and Flores,C. (2002) Efficient repair of DNA breaks in Drosophila: Evidence for single-strand annealing and competition with other repair pathways. Genetics, 161, 711-720.