Characterization of the mycobacterial NER system reveals novel functions of the uvrDl helicase

Journal of Bacteriology

Volumn 191, Issue 2, 2009, Pages 555-562

  Güthlein, Carolin ^a   Wanner, Roger M ^a   Sander, Peter ^a,b   Davis, Elaine O ^c   Bosshard, Martin ^a   Jiricny, Josef ^a,d   Böttger, Erik C ^a,b   Springer, Burkhard ^a,b,e  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b Nationales Zentrum fur Mykobakterien   (Switzerland)

^c NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

^d ETH ZURICH   (Switzerland)

^e MEDICAL UNIVERSITY OF GRAZ   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL DNA; EXCINUCLEASE; HELICASE; NUCLEASE; OXIDIZING AGENT; RIFAMPICIN; UNCLASSIFIED DRUG; UVRB HELICASE; UVRD1 HELICASE;

ARTICLE; BACTERIAL MUTATION; CONTROLLED STUDY; CROSS LINKING; DNA DAMAGE; DNA REPAIR; EXCISION REPAIR; GENE CONVERSION; GENE FUNCTION; GENE INACTIVATION; KNOCKOUT GENE; MINIMUM INHIBITORY CONCENTRATION; MOLECULAR RECOGNITION; MYCOBACTERIUM; MYCOBACTERIUM SMEGMATIS; NITROSATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROCESSING;

BACTERIAL PROTEINS; BASE PAIR MISMATCH; DNA HELICASES; DNA REPAIR; GENE CONVERSION; MUTATION; MYCOBACTERIUM SMEGMATIS; ULTRAVIOLET RAYS;

CORYNEBACTERINEAE; MYCOBACTERIUM SMEGMATIS;

EID: 58649089147     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.00216-08     Document Type: Article

References (56)

1. Arthur, H. M., and R. G. Lloyd. 1980. Hyper-recombination in uvrD mutants of Escherichia coli K-12. Mol. Gen. Genet. 180:185-191.
2. Batty, D. P., and R. D. Wood. 2000. Damage recognition in nucleotide excision repair of DNA. Gene 241:193-204.
3. Burney, S., J. L. Caulfield, J. C. Niles, J. S. Wishnok, and S. R. Tannenbaum. 1999. The chemistry of DNA damage from nitric oxide and peroxynitrite. Mutat. Res. 424:37-49.
4. Centore, R. C., and S. J. Sandler. 2007. UvrD limits the number and intensities of RecA-green fluorescent protein structures in Escherichia coli K-12. J. Bacteriol. 189:2915-2920.
5. Chan, J., Y. Xing, R. S. Magliozzo, and B. R. Bloom. 1992. Killingofvirulent Mycobacterium tuberculosis by reactive nitrogen intermediates produced by activated murine macrophages. J. Exp. Med. 175:1111-1122.
6. Cole, S. T., R. Brosch, J. Parkhill, T. Garnier, C. Churcher, D. Harris, S. V. Gordon, K. Eiglmeier, S. Gas, C. E. Barry III, F. Tekaia, K. Badcock, D. Basham, D. Brown, T. Chillingworth, R. Connor, R. Davies, K. Devlin, T. Feltwell, S. Gentles, N. Hamlin, S. Holroyd, T. Hornsby, K. Jagels, A. Krogh, J. McLean, S. Moule, L. Murphy, K. Oliver, J. Osborne, M. A. Quail, M. A. Rajandream, J. Rogers, S. Rutter, K. Seeger, J. Skelton, R. Squares, S. Squares, J. E. Sulston, K. Taylor, S. Whitehead, and B. G. Barrell. 1998. Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature 393:537-544.
7. Cole, S. T., K. Eiglmeier, J. Parkhill, K. D. James, N. R. Thomson, P. R. Wheeler, N. Honore, T. Garnier, C. Churcher, D. Harris, K. Mungall, D. Basham, D. Brown, T. Chillingworth, R. Connor, R. M. Davies, K. Devlin, S. Duthoy, T. Feltwell, A. Fraser, N. Hamlin, S. Holroyd, T. Hornsby, K. Jagels, C. Lacroix, J. Maclean, S. Moule, L. Murphy, K. Oliver, M. A. Quail, M.-A. Rajandream, K. M. Rutherford, S. Rutter, K. Seeger, S. Simon, M. Simmonds, J. Skelton, R. Squares, S. Squares, K. Stevens, K. Taylor, S. Whitehead, J. R. Woodward, and B. G. Barrell. 2001. Massive gene decay in the leprosy bacillus. Nature 409:1007-1011.
8. Ding, A., C. Nathan, and D. Stuehr. 1988. Release of reactive nitrogen intermediates and reactive oxygen intermediates from mouse peritoneal macrophages. Comparison of activating cytokines and evidence for independent production. J. Immunol. 141:2407-2412.
9. Dohet, C., R. Wagner, and M. Radman. 1985. Repair of defined single base-pair mismatches in Escherichia coli. Proc. Natl. Acad. Sci. USA 82:503-505.
10. Fleck, O., E. Lehmann, P. Schar, and J. Kohli. 1999. Involvement of nucleotide-excision repair in msh2 pms1-independent mismatch repair. Nat. Genet. 21:314-317.
11. Flores, M. J., V. Bidnenko, and B. Michel. 2004. The DNA repair helicase UvrD is essential for replication fork reversal in replication mutants. EMBO Rep. 5:983-988.
12. Flores, M. J., N. Sanchez, and B. Michel. 2005. A fork-clearing role for UvrD. Mol. Microbiol. 57:1664-1675.
13. Friedberg, E. C., Graham C. Walker, Wolfram Siede, Richard D. Wood, Roger A. Schultz, and Tom Ellenberger. 2005. DNA repair and mutagenesis, 2nd ed. ASM Press, Washington, DC.
14. Frischkorn, K., P. Sander, M. Scholz, K. Teschner, T. Prammananan, and E. C. Bottger. 1998. Investigation of mycobacterial recA function: protein introns in the RecA of pathogenic mycobacteria do not affect competency for homologous recombination. Mol. Microbiol. 29:1203-1214.
15. Garnier, T., K. Eiglmeier, J.-C. Camus, N. Medina, H. Mansoor, M. Pryor, S. Duthoy, S. Grondin, C. Lacroix, C. Monsempe, S. Simon, B. Harris, R. Atkin, J. Doggett, R. Mayes, L. Keating, P. R. Wheeler, J. Parkhill, B. G. Barrell, S. T. Cole, S. V. Gordon, and R. G. Hewinson. 2003. The complete genome sequence of Mycobacterium bovis. Proc. Natl. Acad. Sci. USA 100: 7877-7882.
16. Gasc, A. M., A. M. Sicard, and J. P. Claverys. 1989. Repair of single- and multiple-substitution mismatches during recombination in Streptococcus pneumoniae. Genetics 121:29-36.
17. Halliwell, B., and O. I. Aruoma. 1991. DNA damage by oxygen-derived species. Its mechanism and measurement in mammalian systems. FEBS Lett. 281:9-19.
18. Hix, S., S. Morais Mda, and O. Augusto. 1995. DNA methylation by tertbutyl hydroperoxide-iron(II). Free Radic Biol. Med. 19:293-301.
19. Imlay, J. A., and S. Linn. 1987. Mutagenesis and stress responses induced in Escherichia coli by hydrogen peroxide. J. Bacteriol. 169:2967-2976.
20. Iyer, V. N., and W. Szybalski. 1963. A molecular mechanism of mitomycin action: linking of complementary DNA strands. Proc. Natl. Acad. Sci. USA 50:355-362.
21. Jones, M., R. Wagner, and M. Radman. 1987. Repair of a mismatch is influenced by the base composition of the surrounding nucleotide sequence. Genetics 115:605-610.
22. Kang, J., and M. J. Blaser. 2006. UvrD helicase suppresses recombination and DNA damage-induced deletions. J. Bacteriol. 188:5450-5459.
23. Kaufmann, S. H. 2001. How can immunology contribute to the control of tuberculosis? Nat. Rev. Immunol. 1:20-30.
24. Konola, J. T., K. E. Sargent, and J. B. Gow. 2000. Efficient repair of hydrogen peroxide-induced DNA damage by Escherichia coli requires SOS induction of RecA and RuvA proteins. Mutat. Res. 459:187-194.
25. Kramer, B., W. Kramer, and H. J. Fritz. 1984. Different base/base mismatches are corrected with different efficiencies by the methyl-directed DNA mismatch-repair system of E. coli. Cell 38:879-887.
26. Kumar, S., R. Lipman, and M. Tomasz. 1992. Recognition of specific DNA sequences by mitomycin C for alkylation. Biochemistry 31:1399-1407.
27. Kunkel, T. A., and D. A. Erie. 2005. DNA mismatch repair. Annu. Rev. Biochem. 74:681-710.
28. Kunz, C., and O. Fleck. 2001. Role of the DNA repair nucleases Rad13, Rad2 and Uve1 of Schizosaccharomyces pombe in mismatch correction. J. Mol. Biol. 313:241-253.
29. Lefevre, J. C., P. Mostachfi, A. M. Gasc, E. Guillot, F. Pasta, and M. Sicard. 1989. Conversion of deletions during recombination in pneumococcal transformation. Genetics 123:455-464.
30. Lestini, R., and B. Michel. 2007. UvrD controls the access of recombination proteins to blocked replication forks. EMBO J. 26:3804-3814.
31. Marra, G., and P. Schär. 1999. Recognition of DNA alterations by the mismatch repair system. Biochem. J. 338:1-13.
32. Matic, I., C. Rayssiguier, and M. Radman. 1995. Interspecies gene exchange in bacteria: the role of SOS and mismatch repair systems in evolution of species. Cell 80:507-515.
33. Minton, K. W. 1994. DNA repair in the extremely radioresistant bacterium Deinococcus radiodurans. Mol. Microbiol. 13:9-15.
34. Mizrahi, V., and S. J. Andersen. 1998. DNA repair in Mycobacterium tuberculosis. What have we learnt from the genome sequence? Mol. Microbiol. 29:1331-1339.
35. Nathan, C., and M. U. Shiloh. 2000. Reactive oxygen and nitrogen intermediates in the relationship between mammalian hosts and microbial pathogens. Proc. Natl. Acad. Sci. USA 97:8841-8848.
36. Nowosielska, A., S. A. Smith, B. P. Engelward, and M. G. Marinus. 2006. Homologous recombination prevents methylation-induced toxicity in Escherichia coli. Nucleic Acids Res. 34:2258-2268.
37. Parker, B. O., and M. G. Marinus. 1992. Repair of DNA heteroduplexes containing small heterologous sequences in Escherichia coli. Proc. Natl. Acad. Sci. USA 89:1730-1734.
38. Petit, M. A., and D. Ehrlich. 2002. Essential bacterial helicases that counteract the toxicity of recombination proteins. EMBO J. 21:3137-3147.
39. + aminoglycosides. J. Mol. Biol. 346:467-475.
40. Pfister, P., S. Jenni, J. Poehlsgaard, A. Thomas, S. Douthwaite, N. Ban, and E. C. Biöttger. 2004. The structural basis of macrolide-ribosome binding assessed using mutagenesis of 23S rRNA positions 2058 and 2059. J. Mol. Biol. 342:1569-1581.
41. Rayssiguier, C., D. S. Thaler, and M. Radman. 1989. The barrier to recombination between Escherichia coli and Salmonella typhimurium is disrupted in mismatch-repair mutants. Nature 342:396-401.
42. Samson, L., J. Thomale, and M. F. Rajewsky. 1988. Alternative pathways for the in vivo repair of O6-alkylguanine and O4-alkylthymine in Escherichia coli: the adaptive response and nucleotide excision repair. EMBO J. 7:2261-2267.
43. Sancar, A. 1996. DNA excision repair. Annu. Rev. Biochem. 65:43-81.
44. +: a dominant selectable marker for gene replacement in mycobacteria. Mol. Microbiol. 16:991-1000.
45. Sander, P., T. Prammananan, and E. C. Böttger. 1996. Introducing mutations into a chromosomal rRNA gene using a genetically modified eubacterial host with a single rRNA operon. Mol. Microbiol. 22:841-848.
46. Schofield, M. J., and P. Hsieh. 2003. DNA mismatch repair: molecular mechanisms and biological function. Annu. Rev. Microbiol. 57:579-608.
47. Sicard, N., J. Oreglia, and A. M. Estevenon. 1992. Structure of the gene complementing uvr-402 in Streptococcus pneumoniae: homology with Escherichia coli uvrB and the homologous gene in Micrococcus luteus. J. Bacteriol. 174:2412-2415.
48. Sidorkina, O., M. Saparbaev, and J. Laval. 1997. Effects of nitrous acid treatment on the survival and mutagenesis of Escherichia coli cells lacking baseexcisionrepair(hypoxanthine-DNAglycosylase- ALKAprotein)and/or nucleotide excision repair. Mutagenesis 12:23-28.
49. Sinha, K. M., N. C. Stephanou, F. Gao, M. S. Glickman, and S. Shuman. 2007. Mycobacterial UvrD1 is a Ku-dependent DNA helicase that plays a role in multiple DNA repair events, including double-strand break repair. J. Biol. Chem. 282:15114-15125.
50. Spek, E. J., T. L. Wright, M. S. Stitt, N. R. Taghizadeh, S. R. Tannenbaum, M. G. Marinus, and B. P. Engelward. 2001. Recombinational repair is critical for survival of Escherichia coli exposed to nitric oxide. J. Bacteriol. 183:131-138.
51. Springer, B., P. Sander, L. Sedlacek, W.-D. Hardt, V. Mizrahi, P. Schar, and E. C. Böttger. 2004. Lack of mismatch correction facilitates genome evolution in mycobacteria. Mol. Microbiol. 53:1601-1609.
52. Van Houten, B., D. L. Croteau, M. J. DellaVecchia, H. Wang, and C. Kisker. 2005. 'Close-fitting sleeves': DNA damage recognition by the UvrABC nuclease system. Mutat. Res. 577:92-117.
53. Veaute, X., S. Delmas, M. Selva, J. Jeusset, E. Le Cam, I. Matic, F. Fabre, and M. A. Petit. 2005. UvrD helicase, unlike Rep helicase, dismantles RecA nucleoprotein filaments in Escherichia coli. EMBO J. 24:180-189.
54. Veaute, X., J. Jeusset, C. Soustelle, S. C. Kowalczykowski, E. Le Cam, and F. Fabre. 2003. The Srs2 helicase prevents recombination by disrupting Rad51 nucleoprotein filaments. Nature 423:309-312.
55. Washburn, B. K., and S. R. Kushner. 1991. Construction and analysis of deletions in the structural gene (uvrD) for DNA helicase II of Escherichia coli. J. Bacteriol. 173:2569-2575.
56. Worth, L., Jr., S. Clark, M. Radman, and P. Modrich. 1994. Mismatch repair proteins MutS and MutL inhibit RecA-catalyzed strand transfer between diverged DNAs. Proc. Natl. Acad. Sci. USA 91:3238-3241.