Mycobacterium tuberculosis RuvA induces two distinct types of structural distortions between the homologous and heterologous holliday junctions

Biochemistry

Volumn 48, Issue 1, 2009, Pages 27-40

  Khanduja, Jasbeer Singh ^a   Tripathi, Pankaj ^a   Muniyappa, K ^a  

^a INDIAN INSTITUTE OF SCIENCE   (India)

Author keywords

[No Author keywords available]

Indexed keywords

BASE PAIRINGS; BRANCH MIGRATION; DNA DAMAGING AGENTS; DNA MOLECULES; DNA REPAIR; E. COLI; GENOTOXIC STRESSES; HOLLIDAY JUNCTIONS; IN-VITRO; IN-VIVO; LOCAL DISTORTIONS; MYCOBACTERIUM TUBERCULOSIS (MTAHPC); PROTEIN BINDS; PROTEIN COMPLEXES;

DNA; ESCHERICHIA COLI; GENES; NUCLEIC ACIDS; PROBABILITY DENSITY FUNCTION;

ORGANIC ACIDS;

BACTERIAL PROTEIN; PROTEIN SUBUNIT; RUVA PROTEIN; RUVB PROTEIN; RUVC PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; COMPLEX FORMATION; DNA DAMAGE; DNA REPAIR; ESCHERICHIA COLI; GENETIC RECOMBINATION; HOLLIDAY JUNCTION; HOMOLOGOUS RECOMBINATION; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; SEQUENCE HOMOLOGY;

BACTERIAL PROTEINS; BASE PAIRING; CLONING, MOLECULAR; CRYSTALLOGRAPHY, X-RAY; DNA DAMAGE; DNA HELICASES; DNA, CRUCIFORM; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; MUTATION; MYCOBACTERIUM TUBERCULOSIS; PROTEIN BINDING; RECOMBINATION, GENETIC;

ESCHERICHIA COLI; MYCOBACTERIUM TUBERCULOSIS;

EID: 58549087167     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi8016526     Document Type: Article

References (62)

1. Bianco, P. R., Tracy, R. B., and Kowalczykowski, S. C. (1998) DNA strand exchange proteins: A biochemical and physical comparison. Front. Biosci. 3, D570-D603.
2. Lusetti, S. L., and Cox, M. M. (2002) The bacterial RecA protein and the recombinational DNA repair of stalled replication forks. Annu. Rev. Biochem. 71, 71-100.
3. West, S. C. (2003) Molecular views of recombination proteins and their control. Nat. Rev. Mol. Cell Biol. 4, 435-445.
4. West, S. C. (1997) Processing of recombination intermediates by the RuvABC proteins. Annu. Rev. Genet. 31, 213-244.
5. McGlynn, P., and Lloyd, R. G. (2002) Recombinational repair and restart of damaged replication forks. Nat. Rev. Mol. Cell Biol. 3, 859-870.
6. Yamada, K., Ariyoshi, M., and Morikawa, K. (2004) Three-dimensional structural views of branch migration and resolution in DNA homologous recombination. Curr. Opin. Struct. Biol. 14, 30-137.
7. Kuzminov, A. (1999) Recombinational repair of DNA damage in Escherichia coli and bacteriophage lambda. Microbiol. Mol. Biol. Rev.63, 751-813.
8. Hiom, K., Tsaneva, I. R., and West, S. C. (1996) The directionality of RuvAB-mediated branch migration: In vitro studies with three-armed junctions. Genes Cells 1, 443-451.
9. McGlynn, P., and Lloyd, R. G. (2001) Action of RuvAB at replication fork structures. J. Biol. Chem. 276, 41938-41944.
10. Baharoglu, Z., Petranovic, M., Flores, M., and Michel, B. (2006) RuvAB is essential for replication forks reversal in certain replication mutants. EMBO J. 25, 596-604.
11. Michel, B., Boubakri, H., Baharoglu, Z., LeMasson, M., and Lestini, R. (2007) Recombination proteins and rescue of arrested replication forks. DNA Repair 6, 967-980.
12. Baharoglu, Z., Bradley, A. S., LeMasson, M., Tsaneva, I., and Michel, B. (2008) ruvA mutants that resolve Holliday junctions but do not reverse replication forks. PLoS Genet. 4, e1000012.
13. Donaldson, J. R., Courcelle, C. T., and Courcelle, J. (2004) RuvAB and RecG are not essential for the recovery of DNA synthesis following UV-Induced DNA damage in Escherichia coli. Genetics 166, 1631-1640.
14. Donaldson, J. R., Courcelle, C. T., and Courcelle, J. (2006) RuvABC is required to resolve Holliday junctions that accumulate following replication on damaged templates in Escherichia coli. J. Biol. Chem. 281, 28811-28821.
15. Iwasaki, H., Takahagi, M., Nakata, A., and Shinagawa, H. (1992) Escherichia coli RuvA and RuvB proteins specifically interact with Holliday junctions and promote branch-migration. Genes Dev.6, 2214-2220.
16. Tsaneva, I. R., Müller, B., and West, S. C. (1992) ATP-dependent branch-migration of Holliday junctions promoted by the RuvA and RuvB proteins of E. coli. Cell 69, 1171-1180.
17. Chamberlain, D., Keeley, A., Aslam, M., ArenasLicea, J., Brown, T., Tsaneva, I. R., and Perkins, S. J. (1998) A synthetic Holliday junction is sandwiched between two tetrameric Mycobacterium leprae RuvA structures in solution: New insights from neutron scattering contrast variation and modeling. J. Mol. Biol. 284,385400.
18. Roe, S. M., Barlow, T., Brown, T., Oram, M., Keeley, A., Tsaneva, I. R., and Pearl, L. H. (1998) Crystal structure of an octameric RuvA-Holliday junction complex. Mol. Cell 2, 361-372.
19. Ariyoshi, M., Nishino, T., Iwasaki, H., Shinagawa, H., and Morikawa, K. (2000) Crystal structure of the Holliday junction DNA in complex with a single RuvA tetramer. Proc. Natl. Acad. Sci. U.S.A. 97, 8257-8262.
20. Hargreaves, D., Rice, D. W., Sedelnikova, S. E., Artymiuk, P. J., Lloyd, R. G., and Rafferty, J. B. (1998) Crystal structure of E. coli RuvA with bound DNA Holliday junction at 6 Å resolution. Nat. Struct. Biol. 5, 441-446.
21. Iwasaki, H., Takahagi, M., Shiba, T., Nakata, A., and Shinagawa, H. (1991) Escherichia coli RuvC protein is an endonuclease that resolves the Holliday structure. EMBO J. 10, 4381-4389.
22. Dunderdale, H. J., Benson, F. E., Parsons, C. A., Sharples, G. J., Lloyd, R. G., and West, S. C. (1991) Formation and resolution of recombination intermediates by E. coli RecA and RuvC proteins. Nature 354, 506-510.
23. Lloyd, R. G., Benson, F. E., and Shurvinton, C. E. (1984) Effect of ruv mutations on recombination and DNA repair in Escherichia coli K-12. Mol. Gen. Genet. 194, 303-309.
24. Davies, A. A., and West, S. C. (1998) Formation of RuvABC-Holliday junction complexes in vitro. Curr. Biol. 8, 725-727.
25. van Gool, A. J., Hajibagheri, N. M., Stasiak, A., and West, S. C. (1999) Assembly of the Escherichia coli RuvABC resolvasome directs the orientation of Holliday junction resolution. Genes Dev. 13, 1861-1870.
26. Zerbib, D., Mezard, C., George, H., and West, S. C. (1998) Coordinated actions of RuvABC in Holliday junction processing. J. Mol. Biol. 281, 621-630.
27. Muniyappa, K., Vaze, M. B., Ganesh, N., Sreedhar Reddy, M., Guhan, N., and Venkatesh, R. (2000) Comparative genomics of Mycobacterium tuberculosis and Escherichia coli for recombination (rec) genes. Microbiology 146, 2093-2095.
28. Vaze, M. B., and Muniyappa, K. (1999) RecA protein of Myco-bacterium tuberculosis possesses pH-dependent homologous DNA pairing and strand exchange activities: Implications for allele exchange in mycobacteria. Biochemistry 38, 3175-3186.
29. Muniyappa, K., Ganesh, N., Guhan, N., Singh, P., Manjunath, G. P., Datta, S., Chandra, N. R., and Vijayan, M. (2004) Homologous recombination in mycobacteria. Curr. Sci. 86, 141-148.
30. Ganesh, N., and Muniyappa, K. (2003) Characterization of DNA strand transfer promoted by Mycobacterium smegmatis RecA reveals functional diversity with Mycobacterium tuberculosis RecA. Biochemistry 42, 7216-7225.
31. Venkatesh, R., Ganesh, N., Guhan, N., Reddy, M. S., Chan-drasekhar, 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.
32. Hishida, T., Iwasaki, H., Ishioka, K., and Shinagawa, H. ( 1996) Molecular analysis of Pseudomonas aeruginosa genes, ruvA, ruvB and ruvC, involved in processing of homologous recombination intermediates. Gene 182, 63-70.
33. Sambrook, J., Fritsch, E. F., and Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual, 2nd ed., Cold Spring Harbor Laboratory Press, Plainview, NY.
34. 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.
35. Maxam, A. M., and Gilbert, W. (1980) Sequencing end labeled DNA with base-specific chemical cleavages. Methods Enzymol. 65, 499-560.
36. Dèclais, A.-C., and Lilley, D. M. J. (2000) Extensive central disruption of a four-way junction on binding CCE1 resolving enzyme. J. Mol. Biol. 296, 421-433.
37. Sanchez, H., Kidane, D., Reed, P., Curtis, F. A., Cozar, M. C., Graumann, P. L., Sharples, G. J., and Alonso, J. C. (2005) The RuvAB branch migration translocase and RecU Holliday junction resolvase are required for double-stranded DNA break repair in Bacillus subtilis. Genetics 171, 873-883.
38. Parsons, C. A., Kemper, B., and West, S. C. (1990) Interaction of a four-way junction in DNA with T4 endonuclease VII. J. Biol. Chem. 265, 9285-9289.
39. Parsons, C. A., Tsaneva, I., Lloyd, R. G., and West, S. C. (1992) Interaction of Escherichia coli RuvA and RuvB proteins with synthetic Holliday junctions. Proc. Natl. Acad. Sci. U.S.A. 89, 5452-5456.
40. Arenas-Licea, J., van Gool, A. J., Keeley, A. J., Davies, A., West, S. C., and Tsaneva, I. R. (2000) Functional Interactions of Mycobacterium leprae RuvA with Escherichia coli RuvB and RuvC on Holliday Junctions. J. Mol. Biol. 301, 839-850.
41. Rajan Prabu, J., Thamotharan, S., Khanduja, J. S., Alipio, E. Z., Kim, C., Waldo, G. S., Terwilliger, T. C., Segelke, B., Lekin, T., Toppani, D., Hung, L., Yu, M., Bursey, E., Muniyappa, K., Chandra, N. R., and Vijayan, M. (2006) Structure of Mycobacte- rium tuberculosis RuvA, a protein involved in recombination. Acta Crystallogr F62, 731-734.
42. Duckett, D. R., Murchie, A. I., Diekmann, S., von Kitzing, E., Kemper, B., and Lilley, D. M. (1988) The structure of the Holliday junction and its resolution. Cell 55, 79-89.
43. Iida, S., and Hayatsu, H. (1971) The permanganate oxidation of thymidine and thymidylic acid. Biochim. Biophys. Acta 228, 1-8.
44. Sasse-Dwight, S., and Gralla, J. D. (1991) Footprinting protein-DNA complexes in vivo. Methods Enzymol. 206, 146-168.
45. Murchie, A. I. H., Carter, W. A., Portugal, J., and Lilley, D. M. J. (1990) The tertiary structure of the four-way DNA junction affords protection against DNase I cleavage. Nucleic Acids Res. 18, 25992606.
46. Hiom, K., and West, S. C. (1995) Branch migration during homologous recombination: Assembly of a RuvAB-Holliday junction complex in vitro. Cell 80, 787-793.
47. Seigneur, M., Bidnenko, V., Ehrlich, S. D., and Michel, B. (1998) RuvAB acts at arrested replication forks. Cell 95, 419-430.
48. Privezentzev, C. V., Keeley, A., Sigala, B., and Tsaneva, I. R. (2005) The role of RuvA octamerization for RuvAB function in vitro and in vivo. J. Biol. Chem. 280, 3365-3375.
49. Whitby, M. C., Bolt, E. L., Chan, S. N., and Llyod, R. G. (1996) Interactions between RuvA and RuvC at Holliday junctions: Inhibition of junction cleavage and formation of a RuvA-RuvC-DNA complex. J. Mol. Biol. 264, 878-890.
50. Parsons, C. A., Stasiak, A., Bennett, R. J., and West, S. C. (1995) Structure of a multisubunit complex that promotes DNA branch-migration. Nature 374, 375-378.
51. White, M. F., and Lilley, D. M. J. (1997) The resolving enzyme CCE1 of yeast opens the structure of the four-way DNA junction. J. Mol. Biol. 266, 122-134.
52. Giraud-Panis, M.-J. E., and Lilley, D. M. J. (1998) Structural recognition and distortion by the DNA junction resolving enzyme RusA. J. Mol. Biol. 278, 117-133.
53. Gough, G. W., and Lilley, D. M. J. (1985) DNA bending induced by cruciform formation. Nature 313, 154-156.
54. Cooper, J. P., and Hagerman, P. J. (1987) Gel electrophoretic analysis of the geometry of a DNA four-way junction. J. Mol. Biol. 198, 711-719.
55. Ingleston, S. M., Dickman, M. J., Grasby, J. A., Hornby, D. P., Sharples, G. J., and Lloyd, R. G. (2002) Holliday junction binding and processing by the RuvA protein of Mycoplasma pneumoniae. Eur. J. Biochem. 269, 1525-1533.
56. Benson, F. E., Collier, S., and Lloyd, R. G. (1991) Evidence of abortive recombination in ruv mutants of Escherichia coli K-12. Mol. Gen. Genet. 225, 266-272.
57. Sharples, G. J., Benson, F. E., Illing, G. T., and Lloyd, R. G. (1990) Molecular and functional analysis of the ruv region of Escherichia coli K-12 reveals three genes involved in DNA repair and recombination. Mol. Gen. Genet. 221, 219-226.
58. Luisi-DeLuca, C., Lovett, S. T., and Kolodner, R. D. (1989) Genetic and physical analysis of plasmid recombination in recB recC sbcB and recB recC sbcA Escherichia coli K-12 mutants. Genetics 122, 269-278.
59. Eggleston, A. K., Mitchell, A. H., and West, S. C. (1997) In vitro reconstitution of the late steps of genetic recombination in E. coli. Cell 89, 607-617.
60. Lee, Y. C., Flora, R., McCafferty, J. A., Gor, J., Tsaneva, I. R., and Perkins, S. J. (2003) A tetramer-octamer equilibrium in Mycobacterium leprae and Escherichia coli RuvA by analytical ultracentrifugation. J. Mol. Biol. 333, 677-682.
61. Duckett, D. R., Murchie, A. I. H., and Lilley, D. M. J. (1990) The role of metal ions in the conformation of the four-way DNA junction. EMBO J. 9, 583-590.
62. Dèclais, A.-C., and Lilley, D. M. J. (2008) New insight into the recognition of branched DNA structure by junction-resolving enzymes. Curr. Opin. Struct. Biol. 18, 86-95. BI8016526