Mycobacterium tuberculosis RecG binds and unwinds model DNA substrates with a preference for Holliday junctions

Microbiology (United Kingdom)

Volumn 158, Issue 8, 2012, Pages 1982-1993

  Zegeye, Ephrem Debebe ^a   Balasingham, Seetha V ^a,b   Laerdahl, Jon K ^a,b   Homberset, Håvard ^a   Tønjum, Tone ^a,b  

^a UNIVERSITY OF OSLO   (Norway)

^b OSLO UNIVERSITY HOSPITAL   (Norway)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; COPPER; DEOXYADENOSINE TRIPHOSPHATE; IRON; MAGNESIUM; MANGANESE; OLIGONUCLEOTIDE; POLYTHYMIDYLIC ACID; RECG HELICASE; SINGLE STRANDED DNA;

ARTICLE; D LOOP; DNA BINDING; DNA DENATURATION; DNA METABOLISM; DNA RECOMBINATION; DNA REPAIR; DNA REPLICATION; ENZYME ACTIVITY; ENZYME SPECIFICITY; ENZYME SUBSTRATE; ESCHERICHIA COLI; GREEN ALGA; HOLLIDAY JUNCTION; HYDROLYSIS; MOLECULAR GENETICS; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PRIORITY JOURNAL; R LOOP; REPLICATION FORK; VASCULAR PLANT;

BACTERIAL PROTEINS; DNA HELICASES; DNA, BACTERIAL; DNA, CRUCIFORM; KINETICS; MYCOBACTERIUM TUBERCULOSIS; SUBSTRATE SPECIFICITY;

CHLOROPHYTA; ESCHERICHIA COLI; EUKARYOTA; MYCOBACTERIUM TUBERCULOSIS; TRACHEOPHYTA;

EID: 84865641240     PISSN: 13500872     EISSN: None     Source Type: Journal    
DOI: 10.1099/mic.0.058693-0     Document Type: Article

References (69)

1. Ambur, O. H., Davidsen, T., Frye, S. A., Balasingham, S. V., Lagesen, K., Rognes, T. & Tønjum, T. (2009). Genome dynamics in major bacterial pathogens. FEMS Microbiol Rev 33, 453-470.
2. Arabidopsis Genome Initiative (2000). Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408, 796-815.
3. Balasingham, S. V., Zegeye, E. D., Homberset, H., Rossi, M. L., Laerdahl, J. K., Bohr, V. A. & Tønjum, T. (2012). Enzymatic activities and DNA substrate specificity of Mycobacterium tuberculosis DNA helicase XPB. PLoS ONE 7, e36960.
4. Biswas, T., Pero, J. M., Joseph, C. G. & Tsodikov, O. V. (2009). DNA-dependent ATPase activity of bacterial XPB helicases. Biochemistry 48, 2839-2848.
5. Briggs, G. S., Mahdi, A. A., Wen, Q. & Lloyd, R. G. (2005). DNA binding by the substrate specificity (wedge) domain of RecG helicase suggests a role in processivity. J Biol Chem 280, 13921-13927.
6. Brosh, R. M., Jr, Opresko, P. L. & Bohr, V. A. (2006). Enzymatic mechanism of the WRN helicase/nuclease. Methods Enzymol 409, 52-85.
7. Buss, J. A., Kimura, Y. & Bianco, P. R. (2008). RecG interacts directly with SSB: implications for stalled replication fork regression. Nucleic Acids Res 36, 7029-7042.
8. Buttner, K., Nehring, S. & Hopfner, K. P. (2007). Structural basis for DNA duplex separation by a superfamily-2 helicase. Nat Struct Mol Biol 14, 647-652.
9. Cole, S. T., Brosch, R., Parkhill, J., Garnier, T., Churcher, C., Harris, D., Gordon, S. V., Eiglmeier, K., Gas, S. & other authors (1998). Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature 393, 537-544.
10. Curti, E., Smerdon, S. J. & Davis, E. O. (2007). Characterization of the helicase activity and substrate specificity of Mycobacterium tuberculosis UvrD. J Bacteriol 189, 1542-1555.
11. Davis, E. O. & Forse, L. N. (2009). DNA repair: key to survival? In Mycobacteria: Genomics and Molecular Biology, p. 214. Edited by T. Paris & A. Brown. Norwich: Caister Academic Press.
12. Davis, E. O., Springer, B., Gopaul, K. K., Papavinasasundaram, K. G., Sander, P. & Bottger, E. C. (2002). DNA damage induction of recA in Mycobacterium tuberculosis independently of RecA and LexA. Mol Microbiol 46, 791-800.
13. Della, M., Palmbos, P. L., Tseng, H. M., Tonkin, L. M., Daley, J. M., Topper, L. M., Pitcher, R. S., Tomkinson, A. E., Wilson, T. E. & Doherty, A. J. (2004). Mycobacterial Ku and ligase proteins constitute a two-component NHEJ repair machine. Science 306, 683-685.
14. Dos Vultos, T., Mestre, O., Tønjum, T. & Gicquel, B. (2009). DNA repair in Mycobacterium tuberculosis revisited. FEMS Microbiol Rev 33, 471-487.
15. Fonville, N. C., Blankschien, M. D., Magner, D. B. & Rosenberg, S. M. (2010). RecQ-dependent death-by-recombination in cells lacking RecG and UvrD. DNA Repair (Amst) 9, 403-413.
16. Gorna, A. E., Bowater, R. P. & Dziadek, J. (2010). DNA repair systems and the pathogenesis of Mycobacterium tuberculosis: varying activities at different stages of infection. Clin Sci (Lond) 119, 187-202.
17. 2+ as a regulatory signal. Bioessays 20, 96-101.
18. Guo, Y., Bandaru, V., Jaruga, P., Zhao, X., Burrows, C. J., Iwai, S., Dizdaroglu, M., Bond, J. P. & Wallace, S. S. (2010). The oxidative DNA glycosylases of Mycobacterium tuberculosis exhibit different substrate preferences from their Escherichia coli counterparts. DNA Repair (Amst) 9, 177-190.
19. Inoue, H., Hayase, Y., Imura, A., Iwai, S., Miura, K. & Ohtsuka, E. (1987). Synthesis and hybridization studies on two complementary nona(29-O-methyl)ribonucleotides. Nucleic Acids Res 15, 6131-6148.
20. Jaillon, O., Aury, J. M., Noel, B., Policriti, A., Clepet, C., Casagrande, A., Choisne, N., Aubourg, S., Vitulo, N. & other authors (2007). The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature 449, 463-467.
21. Kepple, K. V., Boldt, J. L. & Segall, A. M. (2005). Holliday junctionbinding peptides inhibit distinct junction-processing enzymes. Proc Natl Acad Sci U S A 102, 6867-6872.
22. Khanduja, J. S. & Muniyappa, K. (2012). Functional analysis of DNA replication fork reversal catalyzed by Mycobacterium tuberculosis RuvAB proteins. J Biol Chem 287, 1345-1360.
23. Kim, J. L., Morgenstern, K. A., Griffith, J. P., Dwyer, M. D., Thomson, J. A., Murcko, M. A., Lin, C. & Caron, P. R. (1998). Hepatitis C virus NS3 RNA helicase domain with a bound oligonucleotide: the crystal structure provides insights into the mode of unwinding. Structure 6, 89-100.
24. Kornberg, A., Scott, J. F. & Bertsch, L. L. (1978). ATP utilization by rep protein in the catalytic separation of DNA strands at a replicating fork. J Biol Chem 253, 3298-3304.
25. Kosa, J. L., Zdraveski, Z. Z., Currier, S., Marinus, M. G. & Essigmann, J. M. (2004). RecN and RecG are required for Escherichia coli survival of bleomycin-induced damage. Mutat Res 554, 149-157.
26. Lecointe, F., Sérèna, C., Velten, M., Costes, A., McGovern, S., Meile, J. C., Errington, J., Ehrlich, S. D., Noirot, P. & Polard, P. (2007). Anticipating chromosomal replication fork arrest: SSB targets repair DNA helicases to active forks. EMBO J 26, 4239-4251.
27. Liu, Y. & West, S. C. (2004). Happy Hollidays: 40th anniversary of the Holliday junction. Nat Rev Mol Cell Biol 5, 937-944.
28. Liu, J., Choi, M., Stanenas, A. G., Byrd, A. K., Raney, K. D., Cohan, C. & Bianco, P. R. (2011). Novel, fluorescent, SSB protein chimeras with broad utility. Protein Sci 20, 1005-1020.
29. Lloyd, R. G. & Sharples, G. J. (1993). Dissociation of synthetic Holliday junctions by E. coli RecG protein. EMBO J 12, 17-22.
30. Mahdi, A. A., Briggs, G. S., Sharples, G. J., Wen, Q. & Lloyd, R. G. (2003). A model for dsDNA translocation revealed by a structural motif common to RecG and Mfd proteins. EMBO J 22, 724-734.
31. Masai, H., Tanaka, T. & Kohda, D. (2010). Stalled replication forks: making ends meet for recognition and stabilization. Bioessays 32, 687-697.
32. McGlynn, P. & Lloyd, R. G. (2000). Modulation of RNA polymerase by (p)ppGpp reveals a RecG-dependent mechanism for replication fork progression. Cell 101, 35-45.
33. McGlynn, P. & Lloyd, R. G. (2001). Rescue of stalled replication forks by RecG: simultaneous translocation on the leading and lagging strand templates supports an active DNA unwinding model of fork reversal and Holliday junction formation. Proc Natl Acad Sci U S A 98, 8227-8234.
34. McGlynn, P. & Lloyd, R. G. (2002). Genome stability and the processing of damaged replication forks by RecG. Trends Genet 18, 413-419.
35. McGlynn, P., Al-Deib, A. A., Liu, J., Marians, K. J. & Lloyd, R. G. (1997). The DNA replication protein PriA and the recombination protein RecG bind D-loops. J Mol Biol 270, 212-221.
36. McGlynn, P., Lloyd, R. G. & Marians, K. J. (2001). Formation of Holliday junctions by regression of nascent DNA in intermediates containing stalled replication forks: RecG stimulates regression even when the DNA is negatively supercoiled. Proc Natl Acad Sci U S A 98, 8235-8240.
37. Mirkin, E. V. & Mirkin, S. M. (2007). Replication fork stalling at natural impediments. Microbiol Mol Biol Rev 71, 13-35.
38. Mizrahi, V. & Andersen, S. J. (1998). DNA repair in Mycobacterium tuberculosis. What have we learnt from the genome sequence? Mol Microbiol 29, 1331-1339.
39. Muller, B. & West, S. C. (1994). Processing of Holliday junctions by the Escherichia coli RuvA, RuvB, RuvC and RecG proteins. Experientia 50, 216-222.
40. Niga, T., Yoshida, H., Hattori, H., Nakamura, S. & Ito, H. (1997). Cloning and sequencing of a novel gene (recG) that affects the quinolone susceptibility of Staphylococcus aureus. Antimicrob Agents Chemother 41, 1770-1774.
41. Ochsner, U. A., Vasil, M. L., Alsabbagh, E., Parvatiyar, K. & Hassett, D. J. (2000). Role of the Pseudomonas aeruginosa oxyR-recG operon in oxidative stress defense and DNA repair: OxyR-dependent regulation of katB-ankB, ahpB, and ahpC-ahpF. J Bacteriol 182, 4533-4544.
42. Pyle, A. M. (2008). Translocation and unwinding mechanisms of RNA and DNA helicases. Annu Rev Biophys 37, 317-336.
43. Qiagen (2003). The QIA Expressionist: a Handbook for High-Level Expression and Purification of 66 His-Tagged Proteins. Valencia, CA: Qiagen.
44. Rachman, H., Strong, M., Ulrichs, T., Grode, L., Schuchhardt, J., Mollenkopf, H., Kosmiadi, G. A., Eisenberg, D. & Kaufmann, S. H. (2006). Unique transcriptome signature of Mycobacterium tuberculosis in pulmonary tuberculosis. Infect Immun 74, 1233-1242.
45. Rocak, S. & Linder, P. (2004). DEAD-box proteins: the driving forces behind RNA metabolism. Nat Rev Mol Cell Biol 5, 232-241.
46. Rocha, E. P., Cornet, E. & Michel, B. (2005). Comparative and evolutionary analysis of the bacterial homologous recombination systems. PLoS Genet 1, e15.
47. Rudolph, C. J., Upton, A. L., Harris, L. & Lloyd, R. G. (2009a). Pathological replication in cells lacking RecG DNA translocase. Mol Microbiol 73, 352-366.
48. Rudolph, C. J., Upton, A. L. & Lloyd, R. G. (2009b). Replication fork collisions cause pathological chromosomal amplification in cells lacking RecG DNA translocase. Mol Microbiol 74, 940-955.
49. Rudolph, C. J., Mahdi, A. A., Upton, A. L. & Lloyd, R. G. (2010a). RecG protein and single-strand DNA exonucleases avoid cell lethality associated with PriA helicase activity in Escherichia coli. Genetics 186, 473-492.
50. Rudolph, C. J., Upton, A. L., Briggs, G. S. & Lloyd, R. G. (2010b). Is RecG a general guardian of the bacterial genome? DNA Repair (Amst) 9, 210-223.
51. Sayers, E. W., Barrett, T., Benson, D. A., Bolton, E., Bryant, S. H., Canese, K., Chetvernin, V., Church, D. M., Dicuccio, M. & other authors (2012). Database resources of the National Center for Biotechnology Information. Nucleic Acids Res 40 (Database issue), D13-D25.
52. Schnappinger, D., Ehrt, S., Voskuil, M. I., Liu, Y., Mangan, J. A., Monahan, I. M., Dolganov, G., Efron, B., Butcher, P. D. & other authors (2003). Transcriptional adaptation of Mycobacterium tuberculosis within macrophages: insights into the phagosomal environment. J Exp Med 198, 693-704.
53. Sharples, G. J., Ingleston, S. M. & Lloyd, R. G. (1999). Holliday junction processing in bacteria: insights from the evolutionary conservation of RuvABC, RecG, and RusA. J Bacteriol 181, 5543-5550.
54. Singleton, M. R., Scaife, S. & Wigley, D. B. (2001). Structural analysis of DNA replication fork reversal by RecG. Cell 107, 79-89.
55. Slocum, S. L., Buss, J. A., Kimura, Y. & Bianco, P. R. (2007). Characterization of the ATPase activity of the Escherichia coli RecG protein reveals that the preferred cofactor is negatively supercoiled DNA. J Mol Biol 367, 647-664.
56. Stallings, C. L. & Glickman, M. S. (2010). Is Mycobacterium tuberculosis stressed out? A critical assessment of the genetic evidence. Microbes Infect 12, 1091-1101.
57. Sun, Y. H., Exley, R., Li, Y., Goulding, D. & Tang, C. (2005). Identification and characterization of genes required for competence in Neisseria meningitidis. J Bacteriol 187, 3273-3276.
58. Tamae, C., Liu, A., Kim, K., Sitz, D., Hong, J., Becket, E., Bui, A., Solaimani, P., Tran, K. P. & other authors (2008). Determination of antibiotic hypersensitivity among 4,000 single-gene-knockout mutants of Escherichia coli. J Bacteriol 190, 5981-5988.
59. Tanner, N. K. & Linder, P. (2001). DExD/H box RNA helicases: from generic motors to specific dissociation functions. Mol Cell 8, 251-262.
60. Taylor, S. D., Solem, A., Kawaoka, J. & Pyle, A. M. (2010). The NPH-II helicase displays efficient DNA RNA helicase activity and a pronounced purine sequence bias. J Biol Chem 285, 11692-11703.
61. Tuteja, N. & Tuteja, R. (2004). Unraveling DNA helicases. Motif, structure, mechanism and function. Eur J Biochem 271, 1849-1863.
62. Vincent, S. D., Mahdi, A. A. & Lloyd, R. G. (1996). The RecG branch migration protein of Escherichia coli dissociates R-loops. J Mol Biol 264, 713-721.
63. Vissa, V. D. & Brennan, P. J. (2001). The genome of Mycobacterium leprae: a minimal mycobacterial gene set. Genome Biol 2, REVIEWS1023.
64. Warner, D. F. (2010). The role of DNA repair in M. tuberculosis pathogenesis. Drug Discov Today Dis Mech 7, e5-e7.
65. Warner, D. F. & Mizrahi, V. (2006). Tuberculosis chemotherapy: the influence of bacillary stress and damage response pathways on drug efficacy. Clin Microbiol Rev 19, 558-570.
66. Whitby, M. C. & Lloyd, R. G. (1998). Targeting Holliday junctions by the RecG branch migration protein of Escherichia coli. J Biol Chem 273, 19729-19739.
67. Whitby, M. C., Vincent, S. D. & Lloyd, R. G. (1994). Branch migration of Holliday junctions: identification of RecG protein as a junction specific DNA helicase. EMBO J 13, 5220-5228.
68. WHO (2011). Global tuberculosis control report. Geneva: WHO.
69. Wu, Y., Chen, W., Zhao, Y., Xu, H. & Hua, Y. (2009). Involvement of RecG in H2O2-induced damage repair in Deinococcus radiodurans. Can J Microbiol 55, 841-848.