Mycobacterium tuberculosis UvrD1 and UvrA proteins suppress DNA strand exchange promoted by cognate and noncognate RecA proteins

Biochemistry

Volumn 49, Issue 23, 2010, Pages 4872-4883

  Singh, Pawan ^a   Patil, K Neelakanteshwar ^a   Khanduja, Jasbeer Singh ^a   Kumar, P Sanjay ^a   Williams, Alan ^c   Rossi, Franca ^b   Rizzi, Menico ^b   Davis, Elaine O ^c   Muniyappa, K ^a  

^a INDIAN INSTITUTE OF SCIENCE   (India)

^b UNIVERSITY OF EASTERN PIEDMONT   (Italy)

^c NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ATP-ASE ACTIVITY; DELETERIOUS EFFECTS; DNA HELICASES; DNA METABOLISM; DNA STRANDS; E. COLI; EXPERIMENTAL EVIDENCE; HELICASES; HOMOLOGOUS RECOMBINATION; IN-PROCESS; IN-VIVO; M. TUBERCULOSIS; MOLECULAR MECHANISM; MYCOBACTERIAL; MYCOBACTERIUM SMEGMATIS; MYCOBACTERIUM TUBERCULOSIS; NUCLEOPROTEIN FILAMENTS; PHYSICAL INTERACTIONS; REACTION CATALYZED; RECA PROTEINS; RECOMBINATION INTERMEDIATES;

DISSOLUTION; DNA; ESCHERICHIA COLI; GENES; NUCLEIC ACIDS;

PROTEINS;

ADENOSINE TRIPHOSPHATASE; HELICASE; MUTANT PROTEIN; RECA PROTEIN; UNCLASSIFIED DRUG; UVRA PROTEIN; UVRD1 PROTEIN;

ARTICLE; CONTROLLED STUDY; DNA STRAND; ENZYME ACTIVITY; ESCHERICHIA COLI; GENETIC RECOMBINATION; MYCOBACTERIUM SMEGMATIS; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION;

AMINO ACID SUBSTITUTION; BACTERIAL PROTEINS; DNA HELICASES; DNA, BACTERIAL; ENDODEOXYRIBONUCLEASES; ESCHERICHIA COLI PROTEINS; MYCOBACTERIUM SMEGMATIS; MYCOBACTERIUM TUBERCULOSIS; REC A RECOMBINASES; RECOMBINATION, GENETIC; STRUCTURAL HOMOLOGY, PROTEIN;

CORYNEBACTERINEAE; ESCHERICHIA COLI; MYCOBACTERIUM SMEGMATIS; MYCOBACTERIUM TUBERCULOSIS;

EID: 77953282252     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi902021d     Document Type: Article

References (75)

1. Kuzminov, A. (1999) Recombinational repair of DNA damage in Escherichia coli and bacteriophage-Microbiol. Mol. Biol. Rev. 63, 751-813
2. Cox, M. M. (2007) Regulation of bacterial RecA protein function Crit. Rev. Biochem. Mol. Biol. 42, 41-63
3. Spies, M. and Kowalczykowski, S. C. (2005) Homologous recombination by the RecBCD and RecF pathways, in The Bacterial Chromosome (Higgins, N. P., Ed.) pp 389-403, ASM Press, Washington, DC.
4. West, S. C. (2003) Molecular views of recombination proteins and their control Nat. Rev. Mol. Cell Biol. 4, 435-445
5. Bzymek, M. and Lovett, S. T. (2001) Instability of repetitive DNA sequences: The role of replication in multiple mechanisms Proc. Natl. Acad. Sci. U.S.A. 98, 8319-8325
6. Modrich, P. and Lahue, R. (1996) Mismatch repair in replication fidelity, genetic recombination, and cancer biology Annu. Rev. Biochem. 65, 101-133
7. Cole, S. T., Brosch, R., Parkhill, J., Garnier, T., Churcher, C., Harris, D., Gordon, S. V., Eiglmeier, K., Gas, S., Barry, C. E., III, Tekaia, F., Badcock, K., Basham, D., Brown, D., Chillingworth, T., Connor, R., Davies, R., Devlin, K., Feltwell, T., Gentles, S., Hamlin, N., Holroyd, S., Hornsby, T., Jagels, K., Krogh, A., McLean, J., Moule, S., Murphy, L., Oliver, K., Osborne, J., Quail, M. A., Rajandream, M. A., Rogers, J., Rutter, S., Seeger, K., Skelton, J., Squares, R., Squares, S., Sulston, J. E., Taylor, K., Whitehead, S., and Barrell, B. G. (1998) Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence Nature 393, 537-544
8. Monot, M., Honoré, N., Garnier, T., Zidane, N., Sherafi, D., Paniz-Mondolfi, A., Matsuoka, M., Taylor, G. M., Donoghue, H. D., Bouwman, A., Mays, S., Watson, C., Lockwood, D., Khamispour, A., Dowlati, Y., Jianping, S., Rea, T. H., Vera-Cabrera, L., Stefani, M. M., Banu, S., Macdonald, M., Sapkota, B. R., Spencer, J. S., Thomas, J., Harshman, K., Singh, P., Busso, P., Gattiker, A., Rougemont, J., Brennan, P. J., and Cole, S. T. (2009) Comparative genomic and phylogeographic analysis of Mycobacterium leprae Nat. Genet. 41, 1282-1289
9. Garnier, T., Eiglmeier, K., Camus, J. C., Medina, N., Mansoor, H., Pryor, M., Duthoy, S., Grondin, S., Lacroix, C., Monsempe, C., Simon, S., Harris, B., Atkin, R., Doggett, J., Mayes, R., Keating, L., Wheeler, P. R., Parkhill, J., Barrell, B. G., Cole, S. T., Gordon, S. V., and Hewinson, R. G. (2003) The complete genome sequence of Mycobacterium bovis Proc. Natl. Acad. Sci. U.S.A. 100, 7877-7882
10. Dillingham, M. S. and Kowalczykowski, S. C. (2008) RecBCD enzyme and the repair of double-stranded DNA breaks Microbiol. Mol. Biol. Rev. 72, 642-671
11. Persky, N. S. and Lovett, S. T. (2008) Mechanisms of recombination: lessons from E. coli Crit. Rev. Biochem. Mol. Biol. 43, 347-370
12. Kunkel, T. A. and Erie, D. A. (2005) DNA mismatch repair Annu. Rev. Biochem. 74, 681-710
13. Kumura, K., Sekiguchi, M., Steinum, A.-L., and Seeberg, E. (1985) Stimulation of the UvrABC enzyme-catalyzed repair rections by the UvrD protein (DNA helicase II) Nucleic Acids Res. 13, 1483-1492
14. Matson, S. W. and Robertson, A. B. (2006) The UvrD helicase and its modulation by the mismatch repair protein MutL Nucleic Acids Res. 34, 4089-4097
15. Jiricny, J. (2006) The multifaceted mismatch-repair system Nat. Rev. Mol. Cell Biol. 7, 335-346
16. Zieg, J., Maples, V. F., and Kushner, S. R. (1978) Recombinant levels of Escherichia coli K-12 mutants deficient in various replication, recombination, or repair genes J. Bacteriol. 134, 958-966
17. Arthur, H. M. and Lloyd, R. G. (1980) Hyper-recombination in uvrD mutants of Escherichia coli K-12 Mol. Gen. Genet. 180, 185-191
18. Bierne, H., Seigneur, M., Ehrlich, S. D., and Michel, B. (1997) uvrD mutations enhance tandem repeat deletion in the Escherichia coli chromosome via SOS induction of the RecF recombination pathway Mol. Microbiol. 26, 557-567
19. Centore, R. C. and Sandler, S. J. (2007) UvrD limits the number and intensities of RecA-green fluorescent protein structures in Escherichia coli K-12 J. Bacteriol. 189, 2915-2920
20. Centore, R. C., Leeson, M. C., and Sandler, S. J. (2009) UvrD303, a hyperhelicase mutant that antagonizes RecA-dependent SOS expression by a mechanism that depends on its C terminus J. Bacteriol. 191, 1429-1438
21. Horii, Z. and Clark, A. J. (1973) Genetic analysis of the recF pathway to genetic recombination in Escherichia coli K12: isolation and characterization of mutants J. Mol. Biol. 80, 327-344
22. Morel, P., Hejna, J. A., Ehrlich, S. D., and Cassuto, E. (1993) Anti-pairing and strand transferase activities of E. coli helicase II (UvrD) Nucleic Acids Res. 21, 3205-3209
23. Veaute, X., Delmas, S., Selva, M., Jeusset, J., Le Cam, E., Matic, I., Fabre, F., and Petit, M. A. (2005) UvrD helicase, unlike Rep helicase, dismantles RecA nucleoprotein filaments in Escherichia coli EMBO J. 24, 180-189
24. Flores, M. J., Sanchez, N., and Michel, B. (2005) A fork-clearing role for UvrD Mol. Microbiol. 57, 1664-1675
25. Michel, B., Boubakri, H., Baharoglu, Z., LeMasson, M., and Lestini, R. (2007) Recombination proteins and rescue of arrested replication forks DNA Repair (Amsterdam) 6, 967-980
26. Aguilera, A. and Klein, H. L. (1988) Genetic control of intrachromosomal recombination in Saccharomyces cerevisiae. Isolation and genetic characterization of hyper-recombination mutations Genetics 119, 779-790
27. Krejci, L., Van Komen, S., Li, Y., Villemain, J., Reddy, M. S., Klein, H., Ellenberger, T., and Sung, P. (2003) DNA helicase Srs2 disrupts the Rad51 presynaptic filament Nature 423, 305-309
28. Veaute, X., Jeusset, J., Soustelle, C., Kowalczykowski, S. C., Le Cam, E., and Fabre, F. (2003) The Srs2 helicase prevents recombination by disrupting Rad51 nucleoprotein filaments Nature 423, 309-312
29. Darwin, K. H. and Nathan, C. F. (2005) Role for nucleotide excision repair in virulence of Mycobacterium tuberculosis Infect. Immun. 73, 4581-4587
30. Boschoff, H. I., Reed, M. B., Barry, C. E., and Mizrahi, V. (2003) DnaE2 polymerase contributes to in vivo survival and the emergence of drug resistance in Mycobacterium tuberculosis Cell 113, 183-193
31. Cirz, R. T., Chin, J. K., Andes, D. R., de Crecy-Lagard, V., Craig, W. A., and Romesberg, F. E. (2005) Inhibition of mutation and combating the evolution of antibiotic resistance PLoS Biol. 3, 1024-1033
32. Vultos, T. D., Mestre, O., Tonjum, T., and Gicquel, B. (2009) DNA repair in Mycobacterium tuberculosis revisited FEMS Microbiol. Rev. 33, 471-487
33. Springer, B., Rand, L., Sander, P., Boettger, E. C., and Davis, E. O. (2004) Abstr. 104th Gen. Meet. Am. Soc. Microbiol., Abstract U-048.
34. Graham, J. E. and Clark-Curtiss, J. E. (1999) Identification of Mycobacterium tuberculosis RNAs synthesized in response to phagocytosis by human macrophages by selective capture of transcribed sequences (SCOTS) Proc. Natl. Acad. Sci. U.S.A. 96, 11554-11559
35. Cabusora, L., Sutton, E., Fulmer, A., and Forst, C. V. (2005) Differential network expression during drug and stress response Bioinformatics 21, 2898-2905
36. Mizrahi, V and Andersen, S. J. (1998) DNA repair in Mycobacterium tuberculosis. What have we learnt from the genome sequence? Mol. Microbiol. 29, 1331-1339
37. Muniyappa, K., Vaze, M. B., Ganesh, N., Reddy, M. S., Guhan, N., and Venkatesh, R. (2000) Comparative genomics of Mycobacterium tuberculosis and Escherichia coli for recombination (rec) genes Microbiology 146, 2093-2095
38. Rachman, H., Strong, M., Ulrichs, T., Grode, L., Schuchhardt, J., Mollenkopf, H., Kosmiadi, G. A., Eisenberg, D., and Kaufmann, S. H. (2006) Unique transcriptome signature of Mycobacterium tuberculosis in pulmonary tuberculosis Infect. Immun. 74, 1233-1242
39. Curti, E., Smerdon, S. J., and Davis, E. O. (2007) Characterization of the helicase activity and substrate specificity of Mycobacterium tuberculosis UvrD J. Bacteriol. 189, 1542-1555
40. Sinha, K. M., Stephanou, N. C., Gao, F., Glickman, M. S., and Shuman, S. (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
41. Sinha, K. M., Stephanou, N. C., Unciuleac, M. C., Glickman, M. S., and Shuman, S. (2008) Domain requirements for DNA unwinding by mycobacterial UvrD2, an essential DNA helicase Biochemistry 47, 9355-9364
42. Kumar, R. A., Vaze, M. B., Chandra, N. R., Vijayan, M., and Muniyappa, K. (1996) Functional characterization of the precursor and spliced forms of RecA protein of Mycobacterium tuberculosis Biochemistry 35, 1793-1802
43. Reddy, M. S., Guhan, N., and Muniyappa, K. (2001) Characterization of single-stranded DNA-binding proteins from mycobacteria. The carboxyl-terminal of domain of SSB is essential for stable association with its cognate RecA protein J. Biol. Chem. 276, 45959-45968
44. Vaze, M. B. and Muniyappa, K. (1999) RecA protein of Mycobacterium tuberculosis possesses pH-dependent homologous DNA pairing and strand exchange activities: implications for allele exchange in mycobacteria Biochemistry 38, 3175-3186
45. Ganesh, N. and Muniyappa, K. (2003) Characterization of DNA strand exchange promoted by Mycobacterium smegmatis RecA reveals functional diversity with Mycobacterium tuberculosis RecA Biochemistry 42, 7216-7225
46. Khanduja, J. S., Tripathi, P., and Muniyappa, K. (2009) Mycobacterium tuberculosis RuvA induces two distinct types of structural distortions between the homologous and heterologous Holliday junctions Biochemistry 48, 27-40
47. Venkatesh, R., Ganesh, N., Guhan, N., Reddy, M. S., Chandrasekhar, T., and Muniyappa, K (2002) RecX protein abrogates ATP hydrolysis and strand exchange promoted by RecA: insights into negative regulation of homologous recombination Proc. Natl. Acad. Sci. U.S.A. 99, 12091-12096
48. Güthlein, C., Wanner, R. M., Sander, P., Davis, E. O., Bosshard, M., Jiricny, J., Böttger, E. C., and Springer, B. (2009) Characterization of the mycobacterial NER system reveals novel functions of the uvrD1 helicase J. Bacteriol. 191, 555-562
49. Bradford, M. M. (1976) A rapid and sensitive for the quantitation of microgram quantitites of protein utilizing the principle of protein-dye binding Anal. Biochem. 72, 248-254
50. Ausubel, F. M., Brent, R., Kingston, R. E., Moore, D. D., Seidman, J. G., Smith, J. A., and Struhl, K. (1987) Current Protocols in Molecular Biology, Greene Publishing Associates and Wiley-Interscience, John Wiley & Sons, New York.
51. Dillingham, M. S., Soultanas, P., and Wigley, D. B. (1999) Site-directed mutagenesis of motif III in PcrA helicase reveals a role in coupling ATP hydrolysis to strand separation Nucleic Acids Res. 27, 3310-3317
52. Sinha, K. M., Glickman, M. S., and Shuman, S. (2009) Mutational analysis of mycobacterium UvrD1 identifies functional groups required for ATP hydrolysis, DNA unwinding, and chemomechanical coupling Biochemistry 48, 4019-4030
53. Rosselli, W. and Stasiak, A. (1991) The ATPase activity of RecA is needed to push the DNA strand exchange through heterologous regions EMBO J. 10, 4391-4396
54. Lin, P.-F. and Howard-Flanders, P. (1976) Genetic exchanges caused by ultraviolet photoproducts in phage-DNA molecules: the role of DNA replication Mol. Gen. Genet. 146, 107-115
55. Hanada, K., Iwasaki, M., Ihashi, S., and Ikeda, H. (2000) UvrA and UvrB suppress illegitimate recombination: synergistic action with RecQ helicase Proc. Natl. Acad. Sci. U.S.A. 97, 5989-5994
56. Atkinson, J., Guy, C. P., Cadman, C. J., Moolenaar, G. F., Goosen, N., and McGlynn, P. (2009) Stimulation of UvrD Helicase by UvrAB J. Biol. Chem. 284, 9612-9623
57. Patel, S. S. and Donmez, I. (2006) Mechanisms of helicases J. Biol. Chem. 281, 18265-18268
58. Velankar, S. S., Soultanas, P., Dillingham, M. S., Subramanya, H. S., and Wigley, D. B. (1999) Crystal structures of complexes of PcrA DNA helicase with a DNA substrate indicate an inchworm mechanism Cell 97, 75-84
59. Dillingham, M. S., Wigley, D. B., and Webb, M. R. (2000) Demonstration of unidirectional single-stranded DNA translocation by PcrA helicase: measurement of step size and translocation speed Biochemistry 39, 205-212
60. Soultanas, P. and Wigley, D. B. (2001) Unwinding the "Gordian knot" of helicase action Trends Biochem. Sci. 26, 47-54
61. Tomko, E. J., Fischer, C. J., Niedziela-Majka, A., and Lohman, T. M. (2007) A Non-uniform stepping mechanism for E. coli UvrD monomer translocation along single-stranded DNA Mol. Cell 26, 335-347
62. Lee, J. Y. and Yang, W. (2006) UvrD helicase unwinds DNA one base pair at a time by a two-part power stroke Cell 127, 1349-1360
63. Feinstein, S. I. and Low, K. B. (1986) Hyper-recombining recipient strains in bacterial conjugation Genetics 113, 13-33
64. Kang, J. and Blaser, M. J. (2006) UvrD helicase suppresses recombination and DNA damage-induced deletions J. Bacteriol. 188, 5450-5459
65. 4: implications for decreased ATPase activity and molecular aggregation Nucleic Acids Res. 28, 4964-4973
66. Chang, T. L., Naqvi, A., Anand, S. P., Kramer, M. G., Munshi, R., and Khan, S. A. (2002) Biochemical characterization of the Staphylococcus aureus PcrA helicase and its role in plasmid rolling circle replication J. Biol. Chem. 277, 45880-45886
67. Anand, S. P., Zheng, H., Bianco, P. R., Leuba, S. H., and Khan, S. A. (2007) DNA helicase activity of PcrA is not required for the displacement of RecA protein from DNA or inhibition of RecA-mediated strand exchange J. Bacteriol. 189, 4502-4509
68. Menetski, J. P. and Kowalczykowski, S. C. (1989) Enhancement of Escherichia coli RecA protein enzymatic function by dATP Biochemistry 28, 5871-5881
69. Orren, D. K., Selby, C. P., Hearst, J. E., and Sancar, A. (1992) Post-incision steps of nucleotide excision repair in Escherichia coli. Disassembly of the UvrBC-DNA complex by helicase II and DNA polymerase I J. Biol. Chem. 267, 780-788
70. Hiasa, H. and Marians, K. J. (1992) Differential inhibition of the DNA translocation and DNA unwinding activities of DNA helicases by the Escherichia coli Tus protein J. Biol. Chem. 267, 11379-11385
71. 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. U.S.A. 91, 12031-12035
72. Yancey-Wrona, J. E. and Matson, S. W. (1992) Bound Lac repressor protein differentially inhibits the unwinding reactions catalyzed by DNA helicases Nucleic Acids Res. 20, 6713-6721
73. Burgess, R. C., Lisby, M., Altmannova, V., Krejci, L., Sung, P., and Rothstein, R. (2009) Localization of recombination proteins and Srs2 reveals anti-recombinase function in vivo J. Cell Biol. 185, 969-981
74. Blanck, S., Kobbe, D., Hartung, F., Fengler, K., Focke, M., and Puchta, H. (2009) A SRS2 homolog from Arabidopsis thaliana disrupts recombinogenic DNA intermediates and facilitates single strand annealing Nucleic Acids Res. 37, 7163-7176
75. Rould, E., Muniyappa, K., and Radding, C. M. (1992) Unwinding of heterologous DNA by RecA protein during the search for homologous sequences J. Mol. Biol. 226, 127-139