High-order oligomerization is required for the function of the H-NS family member MvaT in Pseudomonas aeruginosa

Molecular Microbiology

Volumn 78, Issue 4, 2010, Pages 916-931

  Castang, Sandra ^a   Dove, Simon L ^a  

^a BOSTON CHILDREN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DIMER; DNA; HISTONE LIKE NUCLEOID STRUCTURING PROTEIN; MVAT PROTEIN; OLIGOMER; UNCLASSIFIED DRUG;

ARTICLE; DNA BINDING; ENTEROBACTERIACEAE; GENE SILENCING; MUTANT; NONHUMAN; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; PSEUDOMONAS AERUGINOSA;

BACTERIAL PROTEINS; DNA, BACTERIAL; MUTANT PROTEINS; MUTATION, MISSENSE; PROTEIN BINDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN INTERACTION MAPPING; PROTEIN MULTIMERIZATION; PSEUDOMONAS AERUGINOSA; TRANS-ACTIVATORS;

ENTEROBACTERIACEAE; PSEUDOMONAS AERUGINOSA;

EID: 78349236998     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2010.07378.x     Document Type: Article

References (54)

1. Badaut, C., Williams, R., Arluison, V., Bouffartigues, E., Robert, B., Buc, H., and Rimsky, S. (2002) The degree of oligomerization of the H-NS nucleoid structuring protein is related to specific binding to DNA. J Biol Chem 277: 41657-41666.
2. Baehler, E., De Werra, P., Wick, L.Y., Pechy-Tarr, M., Mathys, S., Maurhofer, M., and Keel, C. (2006) Two novel MvaT-like global regulators control exoproduct formation and biocontrol activity in root-associated Pseudomonas fluorescens CHA0. Mol Plant Microbe Interact 19: 313-329.
3. Bloch, V., Yang, Y., Margeat, E., Chavanieu, A., Auge, M.T., Robert, B., et al. (2003) The H-NS dimerization domain defines a new fold contributing to DNA recognition. Nat Struct Biol 10: 212-218.
4. 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.
5. Castang, S., McManus, H.R., Turner, K.H., and Dove, S.L. (2008) H-NS family members function coordinately in an opportunistic pathogen. Proc Natl Acad Sci USA 105: 18947-18952.
6. Chen, J.M., Ren, H., Shaw, J.E., Jing Wang, Y., Li, M., Leung, A.S., et al. (2008) Lsr2 of Mycobacterium tuberculosis is a DNA-bridging protein. Nucleic Acids Res 36: 2123-2135.
7. 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.
8. 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.
9. Diggle, S.P., Winzer, K., Lazdunski, A., Williams, P., and Camara, P. (2002) Advancing the quorum in Pseudomonas aeruginosa: MvaT and the regulation of N-acylhomoserine lactone production and virulence gene expression. J Bacteriol 184: 2576-2586.
10. Dillon, S.C., and Dorman, C.J. (2010) Bacterial nucleoid-associated proteins, nucleoid structure and gene expression. Nat Rev Microbiol 8: 185-195.
11. Dorman, C.J. (2004) H-NS: a universal regulator for a dynamic genome. Nat Rev Microbiol 2: 391-400.
12. Dorman, C.J. (2007) H-NS, the genome sentinel. Nat Rev Microbiol 5: 157-161.
13. Dorman, C.J., and Kane, K.A. (2009) DNA bridging and antibridging: a role for bacterial nucleoid-associated proteins in regulating the expression of laterally acquired genes. FEMS Microbiol Rev 33: 587-592.
14. Dove, S.L., and Hochschild, A. (1998) Conversion of the omega subunit of Escherichia coli RNA polymerase into a transcriptional activator or an activation target. Genes Dev 12: 745-754.
15. Dove, S.L., and Hochschild, A. (2004) A bacterial two-hybrid system based on transcription activation. Methods Mol Biol 261: 231-246.
16. Dove, S.L., Joung, J.K., and Hochschild, A. (1997) Activation of prokaryotic transcription through arbitrary protein-protein contacts. Nature 386: 627-630.
17. Esposito, D., Petrovic, A., Harris, R., Ono, S., Eccleston, J.F., Mbabaali, A., 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.
18. Falconi, M., Gualtieri, M.T., La Teana, A., Losso, M.A., and Pon, C.L. (1988) Proteins from the prokaryotic nucleoid: primary and quaternary structure of the 15-kD Escherichia coli DNA binding protein H-NS. Mol Microbiol 2: 323-329.
19. Fang, F.C., and Rimsky, S. (2008) New insights into transcriptional regulation by H-NS. Curr Opin Microbiol 11: 113-120.
20. Grainger, D.C., Hurd, D., Goldberg, M.D., and Busby, S.J.W. (2006) Association of nucleoid proteins with coding and non-coding segments of the Escherichia coli genome. Nucleic Acids Res 34: 4642-4652.
21. Hu, J.C., Kornacker, M.G., and Hochschild, A. (2000) Escherichia coli one- and two-hybrid systems for the analysis and identification of protein-protein interactions. Methods 20: 80-94.
22. Johansson, J., and Uhlin, B.E. (1999) Differential protease-mediated turnover of H-NS and StpA revealed by a mutation altering protein stability and stationary-phase survival of Escherichia coli. Proc Natl Acad Sci USA 96: 10776-10781.
23. Johansson, J., Dagberg, B., Richet, E., and Uhlin, B.E. (1998) H-NS and StpA proteins stimulate expression of the maltose regulon in Escherichia coli. J Bacteriol 180: 6117-6125.
24. Lang, B., Blot, N., Bouffartigues, E., Buckle, M., Geertz, M., Gualerzi, C.O., et al. (2007) High-affinity DNA binding sites for H-NS provide a molecular basis for selective silencing within proteobacterial genomes. Nucleic Acids Res 35: 6330-6337.
25. Lee, P.-C., Stopford, C.M., Svenson, A.G., and Rietsch, A. (2010) Control of effector export by the Pseudomonas aeruginosa type III secretion proteins PcrG and PcrV. Mol Microbiol 75: 924-941.
26. Leonard, P.G., Ono, S., Gor, J., Perkins, S.J., and Ladbury, J.E. (2009) Investigation of the self- association and hetero- association interactions of H-NS and StpA from Enterobacteria. Mol Microbiol 73: 165-179.
27. Li, C., Wally, H., Miller, S.J., and Lu, C.-D. (2009) The multifaceted proteins MvaT and MvaU, members of the H-NS family, control arginine metabolism, pyocyanin synthesis, and prophage activation in Pseudomonas aeruginosa PAO1. J Bacteriol 191: 6211-6218.
28. Liu, Y., Chen, H., Kenney, L.J., and Yan, J. (2010) A divalent switch drives H-NS/DNA-binding conformations between stiffening and bridging modes. Genes Dev 24: 339-344.
29. 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: e81.
30. 38) regulon during exponential growth of Salmonella typhimurium. Mol Microbiol 74: 1169-1186.
31. Meissner, A., Wild, V., Simm, R., Rohde, M., Erck, C., Bredenbruch, F., et al. (2007) Pseudomonas aeruginosa cupA-encoded fimbriae expression is regulated by a GGDEF and EAL domain-dependent modulation of the intracellular level of cyclic diguanylate. Environ Microbiol 9: 2475-2485.
32. 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.
33. 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.
34. Noom, M.C., Navarre, W.W., Oshima, T., Wuite, G.J., and Dame, R.T. (2007) H-NS promotes looped domain formation in the bacterial chromosome. Curr Biol 17: R913-R914.
35. 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.
36. Renzi, F., Rescalli, E., Galli, E., and Bertoni, G. (2010) Identification of genes regulated by the MvaT-like paralogues TurA and TurB of Pseudomonas putida KT2440. Environ Microbiol 12: 254-263.
37. Rescalli, E., Saini, S., Bartocci, C., Rychlewski, L., De Lorenzo, V., and Bertoni, G. (2004) Novel physiological modulation of the Pu promoter of TOL plasmid: negative regulatory role of the TurA protein of Pseudomonas putida in the response to suboptimal growth temperatures. J Biol Chem 279: 7777-7784.
38. 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.
39. Sette, M., Spurio, R., Trotta, E., Brandizi, C., Brandi, A., Pon, C.L., et al. (2009) Sequence-specific recognition of DNA by the C-terminal domain of nucleoid-associated protein H-NS. J Biol Chem 284: 30453-30462.
40. Smyth, C.P., Lundbäck, T., Renzoni, D., Siligardi, G., Beavil, R., Layton, M., et al. (2000) Oligomerization of the chromatin-structuring protein H-NS. Mol Microbiol 36: 962-972.
41. Spurio, R., Durrenberger, M., Falconi, M., La Teana, A., Pon, C.L., and Gualerzi, C.O. (1992) Lethal overproduction of the Escherichia coli nucleoid protein H-NS: ultramicroscopic and molecular autopsy. Mol Gen Genet 231: 201-211.
42. Spurio, R., Falconi, M., Brandi, A., Pon, C.L., and Gualerzi, C.O. (1997) The oligomeric structure of nucleoid protein H-NS is necessary for recognition of intrinsically curved DNA and for DNA bending. EMBO J 16: 1795-1805.
43. Stella, S., Spurio, R., Falconi, M., Pon, C.L., and Gualerzi, C.O. (2005) Nature and mechanism of the in vivo oligomerization of nucleoid protein H-NS. EMBO J 24: 2896-2905.
44. 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.
45. Tendeng, C., and Bertin, P.N. (2003) H-NS in Gram-negative bacteria: a family of multifaceted proteins. Trends Microbiol 11: 511-518.
46. 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.
47. Ueguchi, C., Suzuki, T., Yoshida, T., Tanaka, K., and Mizuno, T. (1996) Systematic mutational analysis revealing the functional domain organization of Escherichia coli nucleoid protein H-NS. J Mol Biol 263: 149-162.
48. Ueguchi, C., Seto, C., Suzuki, T., and Mizuno, T. (1997) Clarification of the dimerization domain and its functional significance for the Escherichia coli nucleoid protein H-NS. J Mol Biol 274: 145-151.
49. Vallet, I., Olson, J.W., Lory, S., Lazdunski, A., and Filloux, A. (2001) The chaperone/usher pathways of Pseudomonas aeruginosa: identification of fimbrial gene clusters (cup) and their involvement in biofilm formation. Proc Natl Acad Sci USA 98: 6911-6916.
50. Vallet, I., Diggle, S.P., Stacey, R.E., Camara, M., Ventre, I., Lory, S., et al. (2004) Biofilm formation in Pseudomonas aeruginosa: fimbrial cup gene clusters are controlled by the transcriptional regulator MvaT. J Bacteriol 186: 2880-2890.
51. Vallet-Gely, I., Donovan, K.E., Fang, R., Joung, J.K., and Dove, S.L. (2005) Repression of phase-variable cup gene expression by H-NS-like proteins in Pseudomonas aeruginosa. Proc Natl Acad Sci USA 102: 11082-11087.
52. Whipple, F.W. (1998) Genetic analysis of prokaryotic and eukaryotic DNA-binding proteins in Escherichia coli. Nucleic Acids Res 26: 3700-3706.
53. Wiggins, P.A., Dame, R.T., Noom, M.C., and Wuite, G.J.L. (2009) Protein-mediated molecular bridging: a key mechanism in biopolymer organization. Biophys J 97: 1997-2003.
54. Williams, R.M., Rimsky, S., and Buc, H. (1996) Probing the structure, function, and interactions of the Escherichia coli H-NS and StpA proteins by using dominant negative derivatives. J Bacteriol 178: 4335-4343.