RecQ Promotes Toxic Recombination in Cells Lacking Recombination Intermediate-Removal Proteins

Molecular Cell

Volumn 26, Issue 2, 2007, Pages 273-286

  Magner, Daniel B ^a   Blankschien, Matthew D ^a   Lee, Jennifer A ^a   Pennington, Jeanine M ^a   Lupski, James R ^a,b   Rosenberg, Susan M ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b TEXAS CHILDREN S HOSPITAL   (United States)

Author keywords

DNA

Indexed keywords

BACTERIAL PROTEIN; PROTEIN RUV; PROTEIN UVRD; RECA PROTEIN; RECF PROTEIN; RECJ PROTEIN; RECQ HELICASE; SOS PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL CELL; CHROMOSOME REPLICATION; CHROMOSOME SEGREGATION; CONTROLLED STUDY; ESCHERICHIA COLI; EXCISION REPAIR; FLUORESCENCE IN SITU HYBRIDIZATION; GENE INDUCTION; NONHUMAN; PROTEIN FUNCTION;

BACTERIAL PROTEINS; DNA HELICASES; DNA REPAIR; DNA REPLICATION TIMING; DNA-BINDING PROTEINS; ENDODEOXYRIBONUCLEASES; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; EXODEOXYRIBONUCLEASES; IN SITU HYBRIDIZATION, FLUORESCENCE; MODELS, BIOLOGICAL; MUTATION; REC A RECOMBINASES; RECOMBINATION, GENETIC; RECQ HELICASES; TEMPERATURE;

EID: 34247182657     PISSN: 10972765     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molcel.2007.03.012     Document Type: Article

References (55)

1. Aboussekhra A., Chanet R., Zgaga Z., Cassier-Chauvat C., Heude M., and Fabre F. RADH, a gene of Saccharomyces cerevisiae encoding a putative DNA helicase involved in DNA repair. Characteristics of radH mutants and sequence of the gene. Nucleic Acids Res. 17 (1989) 7211-7219
2. Abramoff M.D., Magalhães P.J., and Ram S.J. Image processing with ImageJ. Biophotonics Int. 11 (2004) 36-42
3. Addinall S.G., Bi E., and Lutkenhaus J. FtsZ ring formation in fts mutants. J. Bacteriol. 178 (1996) 3877-3884
4. Bachrati C.Z., and Hickson I.D. RecQ helicases: suppressors of tumorigenesis and premature aging. Biochem. J. 374 (2003) 577-606
5. Bates D., and Kleckner N. Chromosome and replisome dynamics in E. coli: loss of sister cohesion triggers global chromosome movement and mediates chromosome segregation. Cell 121 (2005) 899-911
6. Bierne H., Seigneur M., Ehrlich S.D., and Michel B. uvrD mutations enhance tandem repeat deletion in the Escherichia coli chromosome via SOS induction of the RecF recombination pathway. Mol. Microbiol. 26 (1997) 557-567
7. Bjergbaek L., Cobb J.A., Tsai-Pflugfelder M., and Gasser S.M. Mechanistically distinct roles for Sgs1p in checkpoint activation and replication fork maintenance. EMBO J. 24 (2005) 405-417
8. Britton R.A., and Lupski J.R. Partitioning and segregation of the bacterial chromosome. In: de Bruijn F.J., Lupski J.R., and Weinstock G.M. (Eds). Bacterial Genomes, Physical Structure and Analysis (1998), Chapman and Hall, New York 103-111
9. Chen J.C., and Beckwith J. FtsQ, FtsL and FtsI require FtsK, but not FtsN, for co-localization with FtsZ during Escherichia coli cell division. Mol. Microbiol. 42 (2001) 395-413
10. Clark A.J., Chamberlin M., Boyce R.P., and Howard-Flanders P. Abnormal metabolic response to ultraviolet light of a recombination-deficient mutant of Escherichia coli K12. J. Mol. Biol. 19 (1966) 442-454
11. Corette-Bennett S., and Lovett S.T. Enhancement of RecA strand transfer activity by the RecJ exonuclease of Escherichia coli. J. Biol. Chem. 270 (1995) 6881-6885
12. Courcelle J., and Hanawalt P.C. RecQ and RecJ process blocked replication forks prior to the resumption of replication in UV-irradiated Escherichia coli. Mol. Gen. Genet. 262 (1999) 543-551
13. Courcelle J., Carswell-Crumpton C., and Hanawalt P.C. RecF and RecR are required for resumption of replication at DNA replication forks in Escherichia coli. Proc. Natl. Acad. Sci. USA 94 (1997) 3714-3719
14. Doe C.L., and Whitby M.C. The involvement of Srs2 in post-replication repair and homologous recombination in fission yeast. Nucleic Acids Res. 32 (2004) 1480-1491
15. - phenotype by expression of a bacterial Holliday junction resolvase. EMBO J. 19 (2000) 2751-2762
16. Fabre F., Chan A., Heyer W.D., and Gangloff S. 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 (2002) 16887-16892
17. Florés M.J., Bidnenko V., and Michel B. The DNA repair helicase UvrD is essential for replication fork reversal in replication mutants. EMBO Rep. 5 (2004) 983-988
18. Florés M.J., Sanchez N., and Michel B. A fork-clearing role for UvrD. Mol. Microbiol. 57 (2005) 1664-1675
19. Friedberg E.C., Walker G.C., Siede W., Wood R.D., Schultz R.A., and Ellenberger T. DNA Repair and Mutagenesis. Second Edition (2005), ASM Press, Washington, D.C.
20. Gangloff S., Soustelle C., and Fabre F. Homologous recombination is responsible for cell death in the absence of the Sgs1 and Srs2 helicases. Nat. Genet. 25 (2000) 192-194
21. Hanada K., Ukita T., Kohno Y., Saito K., Kato J., and Ikeda H. RecQ DNA helicase is a suppressor of illegitimate recombination in Escherichia coli. Proc. Natl. Acad. Sci. USA 94 (1997) 3860-3865
22. Harmon F.G., and Kowalczykowski S.C. RecQ helicase, in concert with RecA and SSB proteins, initiates and disrupts DNA recombination. Genes Dev. 12 (1998) 1134-1144
23. Harmon F.G., DiGate R.J., and Kowalczykowski S.C. RecQ helicase and topoisomerase III comprise a novel DNA strand passage function: a conserved mechanism for control of DNA recombination. Mol. Cell 3 (1999) 611-620
24. Hendricks E.C., Szerlong H., Hill T., and Kuempel P. Cell division, guillotining of dimer chromosomes and SOS induction in resolution mutants (dif, xerC and xerD) of Escherichia coli. Mol. Microbiol. 36 (2000) 973-981
25. Hishida T., Han Y.W., Shibata T., Kubota Y., Ishino Y., Iwasaki H., and Shinagawa H. Role of the Escherichia coli RecQ DNA helicase in SOS signaling and genome stabilization at stalled replication forks. Genes Dev. 18 (2004) 1886-1897
26. Hu Y., Lu X., Barnes E., Yan M., Lou H., and Luo G. Recql5 and Blm RecQ DNA helicases have nonredundant roles in suppressing crossovers. Mol. Cell. Biol. 25 (2005) 3431-3442
27. Huber M.D., Lee D.C., and Maizels N. G4 DNA unwinding by BLM and Sgs1p: substrate specificity and substrate-specific inhibition. Nucleic Acids Res. 30 (2002) 3954-3961
28. Ira G., Malkova A., Liberi G., Foiani M., and Haber J.E. Srs2 and Sgs1-Top3 suppress crossovers during double-strand break repair in yeast. Cell 115 (2003) 401-411
29. Ishioka K., Fukuoh A., Iwasaki H., Nakata A., and Shinagawa H. Abortive recombination in Escherichia coli ruv mutants blocks chromosome partitioning. Genes Cells 3 (1998) 209-220
30. Khodursky A.B., Peter B.J., Schmid M.B., DeRisi J., Botstein D., Brown P.O., and Cozzarelli N.R. Analysis of topoisomerase function in bacterial replication fork movement: use of DNA microarrays. Proc. Natl. Acad. Sci. USA 97 (2000) 9419-9424
31. Krejci L., Van Komen S., Li Y., Villemain J., Reddy M.S., Klein H., Ellenberger T., and Sung P. DNA helicase Srs2 disrupts the Rad51 presynaptic filament. Nature 423 (2003) 305-309
32. Kuzminov A. Recombinational repair of DNA damage in Escherichia coli and bacteriophage λ. Microbiol. Mol. Biol. Rev. 63 (1999) 751-813
33. Liberi G., Maffioletti G., Lucca C., Chiolo I., Baryshnikova A., Cotta-Ramusino C., Lopes M., Pellicioli A., Haber J.E., and Foiani M. Rad51-dependent DNA structures accumulate at damaged replication forks in sgs1 mutants defective in the yeast ortholog of BLM RecQ helicase. Genes Dev. 19 (2005) 339-350
34. Lopez C.R., Yang S., Deibler R.W., Ray S.A., Pennington J.M., Digate R.J., Hastings P.J., Rosenberg S.M., and Zechiedrich E.L. A role for topoisomerase III in a recombination pathway alternative to RuvABC. Mol. Microbiol. 58 (2005) 80-101
35. Lusetti S.L., Drees J.C., Stohl E.A., Seifert H.S., and Cox M.M. The DinI and RecX proteins are competing modulators of RecA function. J. Biol. Chem. 279 (2004) 55073-55079
36. Mashimo K., Kawata M., and Yamamoto K. Roles of the RecJ and RecQ proteins in spontaneous formation of deletion mutations in the Escherichia coli K12 endogenous tonB gene. Mutagenesis 18 (2003) 355-363
37. McVey M., Larocque J.R., Adams M.D., and Sekelsky J.J. Formation of deletions during double-strand break repair in Drosophila DmBlm mutants occurs after strand invasion. Proc. Natl. Acad. Sci. USA 101 (2004) 15694-15699
38. Miller J.H. A Short Course in Bacterial Genetics (1992), Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
39. Morimatsu K., and Kowalczykowski S.C. RecFOR proteins load RecA protein onto gapped DNA to accelerate DNA strand exchange: a universal step of recombinational repair. Mol. Cell 11 (2003) 1337-1347
40. Myung K., Datta A., Chen C., and Kolodner R.D. SGS1, the Saccharomyces cerevisiae homologue of BLM and WRN, suppresses genome instability and homeologous recombination. Nat. Genet. 27 (2001) 113-116
41. Renzette N., Gumlaw N., and Sandler S.J. DinI and RecX modulate RecA-DNA structures in Escherichia coli K-12. Mol. Microbiol. 63 (2007) 103-115
42. Roth J.R., Benson N., Galitski T., Haack K., Lawrence J.G., and Meisel L. Rearrangements of the bacterial chromosome: formation and applications. In: Neidhardt F.C., Curtiss III R., Ingraham J.L., Lin E.C.C., Low K.B., Magasanik B., Reznikoff W.S., Riley M., Schaechter M., and Umbarger H.E. (Eds). Escherichia coli and Salmonella Cellular and Molecular Biology (1996), ASM Press, Washington, D.C. 2256-2276
43. Saintigny Y., Makienko K., Swanson C., Emond M.J., and Monnat Jr. R.J. Homologous recombination resolution defect in Werner syndrome. Mol. Cell. Biol. 22 (2002) 6971-6978
44. Sangrithi M.N., Bernal J.A., Madine M., Philpott A., Lee J., Dunphy W.G., and Venkitaraman A.R. Initiation of DNA replication requires the RECQL4 protein mutated in Rothmund-Thomson syndrome. Cell 121 (2005) 887-898
45. Sharma S., Stumpo D.J., Balajee A.S., Bock C.B., Lansdorp P.M., Brosh Jr. R.M., and Blackshear P.J. RECQL, a Member of the RecQ family of DNA Helicases, suppresses chromosomal instability. Mol. Cell. Biol. 27 (2006) 1784-1794 10.1128/MCB.01620-06 Published online December 11, 2006
46. Sharples G.J., Ingleston S.M., and Lloyd R.G. Holliday junction processing in bacteria: insights from the evolutionary conservation of RuvABC, RecG, and RusA. J. Bacteriol. 181 (1999) 5543-5550
47. Spell R.M., and Jinks-Robertson S. Examination of the roles of Sgs1 and Srs2 helicases in the enforcement of recombination fidelity in Saccharomyces cerevisiae. Genetics 168 (2004) 1855-1865
48. +, a fission yeast gene related to the Bloom's and Werner's syndrome genes, is required for reversible S-phase arrest. EMBO J. 16 (1997) 2682-2692
49. Veaute X., Jeusset J., Soustelle C., Kowalczykowski S.C., Le Cam E., and Fabre F. The Srs2 helicase prevents recombination by disrupting Rad51 nucleoprotein filaments. Nature 423 (2003) 309-312
50. Veaute X., Delmas S., Selva M., Jeusset J., Le Cam E., Matic I., Fabre F., and Petit M.A. UvrD helicase, unlike Rep helicase, dismantles RecA nucleoprotein filaments in Escherichia coli. EMBO J. 24 (2005) 180-189
51. Volkert M.R., Margossian L.J., and Clark A.J. Evidence that rnmB is the operator of the Escherichia coli recA gene. Proc. Natl. Acad. Sci. USA 78 (1981) 1786-1790
52. Wang X., Liu X., Possoz C., and Sherratt D.J. The two Escherichia coli chromosome arms locate to separate cell halves. Genes Dev. 20 (2006) 1727-1731
53. Washburn B.K., and Kushner S.R. Construction and analysis of deletions in the structural gene (uvrD) for DNA helicase II of Escherichia coli. J. Bacteriol. 173 (1991) 2569-2575
54. Wu L., and Hickson I.D. The Bloom's syndrome helicase suppresses crossing over during homologous recombination. Nature 426 (2003) 870-874
55. Wu L., and Hickson I.D. DNA helicases required for homologous recombination and repair of damaged replication forks. Annu. Rev. Genet. 40 (2006) 279-306