Mycobacterium tuberculosis nucleoid-associated DNA-binding protein H-NS binds with high-affinity to the holliday junction and inhibits strand exchange promoted by RecA protein

Nucleic Acids Research

Volumn 38, Issue 11, 2010, Pages 3555-3569

  Sharadamma, N ^a   Harshavardhana, Y ^a   Singh, Pawan ^a   Muniyappa, K ^a  

^a INDIAN INSTITUTE OF SCIENCE   (India)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE; BACTERIAL DNA; CROSSOVER JUNCTION ENDODEOXYRIBONUCLEASE; DOUBLE STRANDED DNA; GUANOSINE; HISTONE LIKE NUCLEOID STRUCTURING PROTEIN; RECA PROTEIN;

ARTICLE; BACTERIAL GENETICS; BINDING AFFINITY; CONTROLLED STUDY; DNA CONTENT; DNA REPAIR; DNA REPLICATION; DNA STRAND; ESCHERICHIA COLI; HOLLIDAY JUNCTION; HOMOLOGOUS RECOMBINATION; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; BASE COMPOSITION; DNA, BACTERIAL; DNA, CRUCIFORM; DNA, SUPERHELICAL; DNA-BINDING PROTEINS; ESCHERICHIA COLI PROTEINS; FIMBRIAE PROTEINS; MOLECULAR SEQUENCE DATA; MYCOBACTERIUM TUBERCULOSIS; REC A RECOMBINASES; SEQUENCE HOMOLOGY, AMINO ACID;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI HS; MYCOBACTERIUM TUBERCULOSIS;

EID: 77954359116     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkq064     Document Type: Article

References (76)

1. Travers,A. and Muskhelishvili,G. (2005) Bacterial chromatin. Curr. Opin. Genet. Dev., 15, 507-514.
2. Rouviere-Yaniv,J. and Gros,F. (1975) Characterization of a novel, low-molecular-weight DNA-binding protein from Escherichia coli. Proc. Natl Acad. Sci. USA, 72, 3428-3432.
3. Drlica,K. and Rouviere-Yaniv,J. (1987) Histone-like proteins of bacteria. Microbiol. Rev., 51, 301-319.
4. Dame,R.T. (2005) The role of nucleoid-associated proteins in the organization and compaction of bacterial chromatin. Mol. Microbiol., 56, 858-870.
5. Luijsterburg,M.S., White,M.F., van Driel,R. and Dame,R.T. (2008) The major architects of chromatin: architectural proteins in bacteria, archaea and eukaryotes. Crit. Rev. Biochem. Mol. Biol., 43, 393-418.
6. Dorman,C.J. and Deighan,P. (2003) Regulation of gene expression by histone-like proteins in bacteria. Curr. Opin. Genet. Dev., 13, 179-184.
7. Azam,T.A. and Ishihama,A. (1999) Twelve species of the nucleoid-associated protein from Escherichia coli. Sequence recognition specificity and DNA binding affinity. J. Biol. Chem., 274, 33105-33113.
8. Dorman,C.J. (2004) H-NS: a universal regulator for a dynamic genome. Nat. Rev. Microbiol., 2, 391-400.
9. Dorman,C.J. (2007) H-NS, the genome sentinel. Nat. Rev. Microbiol., 5, 157-161.
10. Rimsky,S. (2004) Structure of the histone-like protein H-NS and its role in regulation and genome superstructure. Curr. Opin. Microbiol., 7, 109-114.
11. Luijsterburg,M.S., Noom,M.C., Wuite,G.J. and Dame,R.T. (2006) The architectural role of nucleoid-associated proteins in the organization of bacterial chromatin: a molecular perspective. J. Struct. Biol., 156, 262-272.
12. Williams,R.M. and Rimsky,S. (1997) Molecular aspects of the E. coli nucleoid protein, H-NS: a central controller of gene regulatory networks. FEMS Microbiol Lett., 156, 175-185.
13. Dorman,C.J., Hinton,J.C. and Free,A. (1999) Domain organization and oligomerization among H-NS-like nucleoid-associated proteins in bacteria. Trends Microbiol., 7, 124-128.
14. Hinton,J.C., Santos,D.S., Seirafi,A., Hulton,C.S., Pavitt,G.D. and Higgins,C.F. (1992) Expression and mutational analysis of the nucleoid-associated protein H-NS of Salmonella typhimurium. Mol. Microbiol., 6, 2327-2337.
15. Atlung,T. and Ingmer,H. (1997) H-NS: a modulator of environmentally regulated gene expression. Mol. Microbiol., 24, 7-17.
16. Lejeune,P. and Danchin,A. (1990) Mutations in the bglY gene increase the frequency of spontaneous deletions in Escherichia coli K-12. Proc. Natl Acad. Sci. USA, 87, 360-363.
17. Dri,A.M., Moreau,P.L. and Rouvière-Yaniv,J. (1992) Role of the histone-like proteins OsmZ and HU in homologous recombination. Gene, 120, 11-16.
18. Ono,S., Goldberg,M.D., Olsson,T., Esposito,D., Hinton,J.C. and Ladbury,J.E. (2005) H-NS is a part of a thermally controlled mechanism for bacterial gene regulation. Biochem. J., 391, 203-213.
19. Lucchini,S., Rowley,G., Goldberg,M.D., Hurd,D., Harrison,M. and Hinton,J.C.D. (2006) H-NS mediates the silencing of laterally acquired genes in bacteria. PLoS Pathog., 2, 746-752.
20. Navarre,W.W., Porwollik,S., Wang,Y., McClelland,M., Rosen,H., Libby,S.J. and Fang,F.C. (2006) Selective silencing of foreign DNA with low GC content by the H-NS protein in Salmonella. Science, 313, 236-238.
21. Müller,C.M., Dobrindt,U., Nagy,G., Emödy,L., Uhlin,B.E. and Hacker,J. (2006) Role of histone-like proteins H-NS and StpA in expression of virulence determinants of uropathogenic Escherichia coli. J. Bacteriol., 188, 5428-5438.
22. Dame,R.T., Wyman,C. and Goosen,N. (2000) H-NS mediated compaction of DNA visualised by atomic force microscopy. Nucleic Acids Res., 28, 3504-3510.
23. Rimsky,S. (2004) Structure of the histone-like protein H-NS and its role in regulation and genome superstructure. Curr. Opin. Microbiol., 7, 109-114.
24. Oshima,T., Ishikawa,S., Kurokawa,K., Aiba,H. and Ogasawara,N. (2006) Escherichia coli histone-like protein H-NS preferentially binds to horizontally acquired DNA in association with RNA polymerase. DNA Res., 13, 141-153.
25. Amit,R., Oppenheim,A.B. and Stavans,J. (2003) Increased bending rigidity of single DNA molecules by H-NS, a temperature and osmolarity sensor. Biophys. J., 84, 2467-2473.
26. Dame,R.T. and Wuite,G.J.L. (2003) On the role of H-NS in the organization of bacterial chromatin: from bulk to single molecules and back. Biophys. J., 85, 4146-4148.
27. Dame,R.T., Noom,M.C. and Wuite,G.J.L. (2006) Bacterial chromatin organization by H-NS protein unravelled using dual DNA manipulation. Nature, 444, 387-390.
28. Bouffartigues,E., Buckle,M., Badaut,C., Travers,A. and Rimsky,S. (2007) H-NS cooperative binding to high-affinity sites in a regulatory element results in transcriptional silencing. Nat. Struct. Mol. Biol., 14, 441-448.
29. Esposito,D., Petrovic,A., Harris,R., Ono,S., Eccleston,J.F., Mbabaali,A., Haq,I., Higgins,C.F., Hinton,J.C., Driscoll,P.C. et al. (2002) H-NS oligomerization domain structure reveals the mechanism for high order self-association of the intact protein. J. Mol. Biol., 324, 841-850.
30. Badaut,C., Williams,R., Arluison,V., Bouffartigues,E., Robert,B., Buc,H. and Rimsky,S. (2002) The degree of oligomerization of the HNS nucleoid structuring protein is related to specific binding to DNA. J. Biol. Chem., 277, 41657-41666.
31. Dame,R.T., Luijsterburg,M.S., Krin,E., Bertin,P.N., Wagner,R. and Wuite,G.J. (2005) DNA bridging: a property shared among H-NS like proteins. J. Bacteriol., 187, 1845-1848.
32. Barth,M., Marschall,C., Muffler,A., Fischer,D. and Hengge-Aronis,R. (1995) Role for the histone-like protein H-NS in growth phase-dependent and osmotic regulation of sS and many sS-dependent genes in Escherichia coli. J. Bacteriol., 177, 3455-3464.
33. Dersch,P., Kneip,S. and Bremer,E. (1994) The nucleoid-associated DNA-binding protein H-NS is required for the efficient adaptation of Escherichia coli K-12 to cold environment. Mol. Gen. Genet., 245, 255-259.
34. Hommais,F., Krin,E., Laurent-Winter,C., Soutourina,O., Malpertuy,A., Le Caer,J.P., Danchin,A. and Bertin,P. (2001) Large-scale monitoring of pleiotropic regulation of gene expression by the prokaryotic nucleoid-associated protein, H-NS. Mol. Microbiol., 40, 20-36.
35. McGovern,V., Higgins,N.P., Chiz,R.S. and Jaworski,A. (1994) H-NS over-expression induces an artificial stationary phase by silencing global transcription. Biochimie, 76, 1019-1029.
36. Ghosh,A., Paul,K. and Chowdhury,R. (2006) Role of the histone-like nucleoid structuring protein in colonization, motility, and bile-dependent repression of virulence gene expression in Vibrio cholerae. Infect. Immun., 74, 3060-3064.
37. Yamashino,T., Ueguchi,C. and Mizuno,T. (1995) Quantitative control of the stationary phase-specific sigma factor, sigma S, in Escherichia coli: involvement of the nucleoid protein, H-NS. EMBO J., 14, 594-602.
38. Shanado,Y., Hanada,K. and Ikeda,H. (2001) Suppression of gamma ray-induced illegitimate recombination in Escherichia coli by the DNA-binding protein H-NS. Mol. Gen. Genet., 265, 242-248.
39. Navarre,W.W., McClelland,M., Libby,S.J. and Fang,F.C. (2007) Silencing of xenogeneic DNA by H-NS-facilitation of lateral gene transfer in bacteria by a defense system that recognizes foreign DNA. Genes Dev., 21, 1456-1471.
40. Stoebel,D.M., Free,A. and Dorman,C.J. (2008) Anti-silencing: overcoming H-NS-mediated repression of transcription in Gram-negative enteric bacteria. Microbiology, 154, 2533-2545. 41.
41. Prabhakar,S., Annapurna,P.S., Jain,N.K., Dey,A.B., Tyagi,J.S. and Prasad,H.K. (1998) Identification of an immunogenic histone-like protein (HLPMt) of Mycobacterium tuberculosis. Tuber. Lung Dis., 79, 43-53.
42. Lee,B.H., Murugasu-Oei,B. and Dick,T. (1998) Upregulation of a histone-like protein in dormant Mycobacterium smegmatis. Mol. Gen. Genet., 260, 475-479.
43. Mukherjee,A., Bhattacharyya,G. and Grove,A. (2008) The C-terminal domain of HU-related histone-like protein Hlp from Mycobacterium smegmatis mediates DNA end-joining. Biochemistry, 47, 8744-8753.
44. Shires,K. and Steyn,L. (2001) The cold-shock stress response in Mycobacterium smegmatis induces the expression of a histone-like protein. Mol Microbiol., 39, 994-1009.
45. Chen,J.M., Ren,H., Shaw,J.E., Wang,Y.J., Li,M., Leung,A.S., Tran,V., Berbenetz,N.M., Kocíncová,D., Yip,C.M. et al. (2008) Lsr2 of Mycobacterium tuberculosis is a DNA-bridging protein. Nucleic Acids Res., 36, 2123-2135.
46. 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.
47. Tripathi,P., Anuradha,S., Ghosal,G. and Muniyappa,K. (2006) Selective binding of meiosis-specific yeast Hop1 protein to the Holliday junctions distorts the DNA structure and its implications for junction migration and resolution. J. Mol. Biol., 364, 599-611.
48. Cole,S.T., Brosch,R., Parkhill,J., Garnier,T., Churcher,C., Harris,D., Gordon,S.V., Eiglmeier,K., Gas,S., Barry,C.E. III et al. (1998) Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature, 393, 537-544.
49. Sette,M., Spurio,R., Trotta,E., Brandizi,C., Brandi,A., Pon,C.L., Barbato,G., Boelens,R. and Gualerzi,C.O. (2009) Sequence-specific recognition of DNA by the C-terminal domain of nucleoid-associated protein H-NS. J. Biol. Chem., 284, 30453-30462.
50. Del Portillo,P., Reyes,A., Salazar,L., del Carmen Menéndez,M. and García,M.J. (2007) Genomics and proteomics, Chapter 4. In Ritacco,V., Leão,S.C. and Palomino,J.C. (eds), Tuberculosis 2007, A Medical Text Book. Pitman Medical and Scientific Publishing Co. Ltd, London, pp. 113-156.
51. 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.
52. Mukherjee,A., Sokunbi,A.O. and Grove,A. (2008) DNA protection by histone-like protein HU from the hyperthermophilic eubacterium Thermotoga maritime. Nucleic Acids Res., 36, 3956-3968.
53. Werlang,I.C.R., Schneider,C.Z., Mendonc,J.D., Palma,M.S., Luiz,A., Basso,L.A. and Santos,D.S. (2009) Identification of Rv3852 as a nucleoid-associated protein in Mycobacterium tuberculosis. Microbiology, 155, 2652-2663.
54. Prakash,P., Aruna,B., Sardesai,A.A. and Hasnain,S.E. (2005) Purified recombinant hypothetical protein coded by open reading frame Rv1885c of Mycobacterium tuberculosis exhibits a mono-functional AroQ class of periplasmic chorismate mutase activity. J. Biol. Chem., 280, 19641-19648.
55. Sasso,S., Ramakrishnan,C., Gamper,M., Hilvert,D. and Kast,P. (2005) Characterization of the secreted chorismate mutase from the pathogen Mycobacterium tuberculosis. FEBS Lett., 272, 375-389.
56. Qamra,R., Prakash,P., Aruna,B., Hasnain,S.E. and Mande,S.C. (2006) The 2.15 A crystal structure of Mycobacterium tuberculosis chorismate mutase reveals an unexpected gene duplication and suggests a role in host-pathogen interactions. Biochemistry, 45, 6997-700.
57. Argyrides Argyrou,A., Jin,L., Siconilfi-Baez,L., Angeletti,R.H. and Blanchard,J.S. (2006) Proteome-wide profiling of isoniazid targets in Mycobacterium tuberculosis. Biochemistry, 45, 13947-13953.
58. Tendeng,C. and Bertin,P.N. (2003) H-NS in Gram-negative bacteria: a family of multifaceted proteins. Trends Microbiol., 11, 511-518.
59. Tendeng,C., Soutourina,O.A., Danchin,A. and Bertin,P.N. (2003) MvaT proteins in Pseudomonas spp.: a novel class of H-NS-like proteins. Microbiology, 149, 3047-3050.
60. Gordon,B.R.G., Imperial,R., Wang,L., Navarre,W.W. and Liu,J. (2008) Lsr2 of Mycobacterium represents a novel class of H-NS-like proteins. J. Bacteriol., 190, 7052-7059.
61. Erard,M., Lakhdar-Ghazal,J. and Amalric,J. (1990) Repeat peptide motifs which contain p-turns and modulate DNA condensation in chromatin. Eur. J. Biochem., 191, 19-25.
62. Khadake,J.R. and Rao,M.R.S. (1997) Condensation of DNA and chromatin by an SPKK-containing octapeptide repeat motif present in the C-terminus of histone H1. Biochemistry, 36, 1041-1051.
63. Kasinsky,H.E., Lewis,J.D., Dacks,J.B. and Ausio,J. (2001) Origin of H1 linker histones. FASEB J., 15, 34-42.
64. Cohavy,O., Harth,G., Horwitz,M., Eggena,M., Landers,C., Sutton,C., Targan,S.R. and Braun,J. (1999) Identification of a novel mycobacterial histone H1 homologue (HupB) as an antigenic target of pANCA monoclonal antibody and serum immunoglobulin A from patients with Crohn's disease. Infect. Immun., 67, 6510-6517.
65. Gowrishankar,J. and Manna,D. (1996) How is osmotic regulation of transcription of the Escherichia coli proU operon achieved: a review and a model. Genetica, 97, 363-378.
66. Rajkumari,K. and Gowrishankar,J. (2001) In vivo expression from the RpoS-dependent P1 promoter of the osmotically regulated proU operon in Escherichia coli and Salmonella enterica serovar Typhimurium: activation by rho and hns mutations and by cold stress. J. Bacteriol., 183, 6543-6550.
67. Owen-Hughes,T.A., Pavitt,G.D., Santos,D.S., Sidebotham,J.M., Hulton,C.S., Hinton,J.C. and Higgins,C.F. (1992) The chromatin-associated protein H-NS interacts with curved DNA to influence DNA topology and gene expression. Cell, 71, 255-265. 68.
68. Kamashev,D. and Rouviere-Yaniv,J. (2000) The histone-like protein HU binds specifically to DNA recombination and repair intermediates. EMBO J., 19, 6527-6535.
69. Groisman,E.A. and Ochman,H. (1996) Pathogenicity islands: bacterial evolution in quantum leaps. Cell, 87, 791-794.
70. Smets,B.F. and Barkay,T. (2005) Horizontal gene transfer: perspectives at a crossroads of scientific disciplines. Nat. Rev. Microbiol., 3, 675-678.
71. Ramdas,J., Mythili,E. and Muniyappa,K. (1989) RecA protein promoted homologous pairing in vitro. Pairing between linear duplex DNA bound to HU Protein (nucleosome cores) and nucleoprotein filaments of recA protein-single-stranded DNA. J. Biol. Chem., 264, 17395-17400.
72. Ennis,D.G., Woodgate,R. and Shi,M. (2006) Selective inhibition of RecA functions by the Hc1 nucleoid condensation protein from Chlamydia trachomatis. FEMS Microbiol. Lett., 182, 279-283.
73. Wardle,S.J., O'Carroll,M., Derbyshire,K.M. and Haniford,D.B. (2005) The global regulator H-NS acts directly on the transpososome to promote Tn10 transposition. Genes Dev., 19, 2224-2235.
74. Falconi,M., McGovern,V., Gualerzi,C., Hillyard,D. and Higgins,N.P. (1991) Mutations altering chromosomal protein H-NS induce mini-Mu transposition. New Biol., 3, 615-625. 75.
75. Cole,C., Barber,J.D. and Barton,G.J. (2008) The Jpred 3 secondary structure prediction server. Nucleic Acids Res., 36(Web Server issue), W197-W201.
76. Waterhouse,A.M., Procter,J.B., Martin,D.M.A., Clamp,M. and Barton,G.J. (2009) Jalview version 2: a multiple sequence alignment and analysis workbench. Bioinformatics, 25, 1189-1191.