The PhoQ histidine kinases of Salmonella and Pseudomonas spp. are structurally and functionally different: Evidence that pH and antimicrobial peptide sensing contribute to mammalian pathogenesis

Molecular Microbiology

Volumn 69, Issue 2, 2008, Pages 503-519

  Prost, Lynne R ^a   Daley, Margaret E ^a   Bader, Martin W ^a   Klevit, Rachel E ^a   Miller, Samuel I ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; CATION; POLYPEPTIDE ANTIBIOTIC AGENT; PROTEIN HISTIDINE KINASE; PSEUDOMONAS PHOQ PROTEIN; SALMONELLA TYPHIMURIUM PHOQ PROTEIN;

ARTICLE; BACTERIAL VIRULENCE; CONTROLLED STUDY; MAMMAL; MOUSE; NONHUMAN; PATHOGENESIS; PH; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN STRUCTURE; PSEUDOMONAS; SALMONELLA;

AMINO ACID SEQUENCE; ANIMALS; ANTIMICROBIAL CATIONIC PEPTIDES; BACTERIAL PROTEINS; BINDING SITES; CATIONS, DIVALENT; DNA MUTATIONAL ANALYSIS; FEMALE; GENE DELETION; GENETIC COMPLEMENTATION TEST; HYDROGEN-ION CONCENTRATION; MAGNETIC RESONANCE SPECTROSCOPY; MICE; MICE, INBRED BALB C; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; PROTEIN KINASES; PSEUDOMONAS AERUGINOSA; SALMONELLA INFECTIONS, ANIMAL; SALMONELLA TYPHIMURIUM; SEQUENCE ALIGNMENT; VIRULENCE;

ANIMALIA; MAMMALIA; PSEUDOMONAS; PSEUDOMONAS AERUGINOSA; SALMONELLA; SALMONELLA TYPHIMURIUM;

EID: 47249120854     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2008.06303.x     Document Type: Article

References (33)

1. Alpuche-Aranda, C.M., Swanson, J.A., Loomis, W.P. Miller, S.I. (1992) Salmonella typhimurium activates virulence gene transcription within acidified macrophage phagosomes. PNAS 89 : 10079 10083.
2. Bader, M.W., Sanowar, S., Daley, M.E., Schneider, A.R., Cho, U., Xu, W., et al. (2005) Recognition of antimicrobial peptides by a bacterial sensor kinase. Cell 122 : 461 472.
3. Belden, W.J. Miller, S.I. (1994) Further characterization of the PhoP regulon: identification of new PhoP-activated virulence loci. Infect Immun 62 : 5095 5101.
4. Bott, M. (1997) Anaerobic citrate metabolism and its regulation in enterobacteria. Arch Microbiol 167 : 78 88.
5. Bryson, K., McGuffin, L.J., Marsden, R.L., Ward, J.J., Sodhi, J.S. Jones, D.T. (2005) Protein structure prediction servers at University College London. Nucleic Acids Res 33 (Web server issue W36 38.
6. Cho, U.S., Bader, M.W., Amaya, M.F., Daley, M.E., Klevit, R.E. Miller, S.I. (2006) Metal bridges between the PhoQ sensor domain and the membrane regulate transmembrane signaling. J Mol Biol 356 : 1193 1206.
7. Darveau, R., Blake, J., Seachord, C.L., Cosand, W.L., Cunningham, M.D., Cassiano-Clough, L. Maloney, G. (1992) Peptides related to the carboxyl terminus of human platelet factor IV with antibacterial activity. J Clin Invest 90 : 447 455.
8. Delaglio, F., Grzesiek, S., Vuister, G.W., Zhu, G., Pfeifer, J. Bax, A. (1995) NMRPipe - a multidimensional spectral processing system based on UNIX pipes. J Biomol NMR 6 : 277 293.
9. Derzelle, S., Turlin, E., Duchaud, E., Pages, S., Kunst, F., Givaudun, A. Danchin, A. (2004) The PhoP-PhoQ two-component system of Photorhabdus luminescens is essential for virulence in insects. J Bacteriol 186 : 1270 1279.
10. Ernst, R.K., Yi, E.C., Guo, L., Lim, K.B., Burns, J.L., Hackett, M. Miller, S.I. (1999) Specific lipopolysaccharide found in cystic fibrosis airway Pseudomonas aearuginosa. Science 286 : 1561 1565.
11. Fields, P.I., Groisman, E.A. Heffron, F. (1989) A Salmonella locus that controls resistance to microbicidal proteins from phagocytic cells. Science 243 : 1059 1062.
12. Foster, J.W. Hall, H.K. (1990) Adaptive acidification tolerance response of Salmonella typhimurium. J Bacteriol 172 : 771 778.
13. 2+. JBC 272 : 1440 1443.
14. 2+ as an extracellular signal: environmental regulation of Salmonella virulence. Cell 84 : 165 174.
15. Johnson, B.A. Blevins, R.A. (1994) NMRView - a computer program for the visualization and analysis of NMR data. J Biomol NMR 4 : 603 614.
16. Jones, D.T. (1999) Protein secondary structure prediction based on position-specific scoring matrices. J Mol Biol 292 : 195 202.
17. Lee, L. Sykes, B.D. (1983) Use of lanthanide-induced nuclear magnetic resonance shifts for determination of protein structure in solution: EF calcium binding site of carp parvalbumin. Biochemistry 22 : 4366 4373.
18. Lesley, J.A. Waldburger, C.D. (2001) Comparison of the Pseudomonas aeruginosa and Escherichia coli PhoQ sensor domains. J Biol Chem 276 : 30827 30833.
19. Llama-Palacios, A., Lopez-Solanilla, E., Poza-Carrion, C., Garcia-Olmeda, F. Rodriguez-Palenzuela, P. (2003) The Erwinia chrysanthemi phoP-phoQ operon plays an important role in growth at low pH, virulence and bacterial survival in plant tissue. Mol Microbiol 49 : 347 357.
20. Macfarlane, E.L.A., Kwasnicka, A., Ochs, M.M. Hancock, R.E.W. (1999) PhoP-PhoQ homologues in Pseudomonas aeruginosa regulate expression of the outer-membrane protein OprH and polymyxin B resistance. Mol Microbiol 34 : 305 316.
21. Martin-Orozco, N., Touret, N., Zaharik, M.L., Park, E., Kopelman, R., Miller, S.I., et al. (2006) Visualization of vacuolar acidification-induced transcription of genes of pathogens inside macrophages. Mol Biol Cell 17 : 498 510.
22. McPhee, J.B., Lewenza, S. Hancock, R.E.W. (2003) Cationic antimicrobial peptides activate a two-component regulatory system, PmrA-PmrB, that regulates resistance to polymyxin B and cationic antimicrobial peptides in Pseudomonas aeruginosa. Mol Microbiol 50 : 205 217.
23. Miller, S.I., Kukral, A.M. Mekalanos, J.J. (1989) A two-component regulatory system (phoP phoQ) controls Salmonella typhimurium virulence. PNAS 86 : 5054 5058.
24. Miller, S.I., Pulkkinen, W.S., Selsted, M.E. Mekalanos, J.J. (1990) Characterization of defensin resistance phenotypes associated with mutations in the phoP virulence regulon of Salmonella typhimurium. Infect Immun 58 : 3706 3710.
25. Moss, J.E., Fisher, P.E., Vick, B., Groisman, E.A. Zychlinsky, A. (2000) The regulatory protein PhoP controls susceptibility to the host inflammatory response in Shigella flexneri. Cell Microbiol 2 : 443 452.
26. Nelson, D.L. Kennedy, E.P. (1971) Magnesium transport in E. coli: inhibition by cobaltous ion. J Biol Chem 246 : 3042 3049.
27. Oyston, P.C., Dorrell, N., Williams, K., Li, S.R., Green, M., Titball, R.W. Wren, B.W. (2000) The response regulator PhoP is important for survival under conditions of macrophage-induced stress and virulence in Yersinia pestis. Infect Immun 68 : 3419 3425.
28. Prost, L.R. Miller, S.I. (2008) The Salmonellae PhoQ sensor: mechanisms of detection of phagosome signals. Cell Micro 10 : 576 582.
29. Prost, L.R., Daley, M.E., Le Sage, V., Bader, M.W., Le Moual, H., Klevit, R.E. Miller, S.I. (2007) Activation of the bacterial sensor kinase PhoQ by acidic pH. Mol Cell 26 : 165 174.
30. Reinelt, S., Hofmann, E., Gerharz, T., Bott, M. Madden, D.R. (2003) The structure of the periplasmic ligand-binding domain of the sensor kinase CitA reveals the first extracellular PAS domain. J Biol Chem 278 : 39189 39196.
31. Soncini, F.C., Garcia-Vescovi, E., Solomon, F. Groisman, E.A. (1996) Molecular basis of the magnesium deprivation response in Salmonella typhimurium: identification of PhoP-regulated genes. J Bacteriol 178 : 5092 5099.
32. Ulrich, L.E., Koonin, E.V. Zhulin, I.B. (2005) One-component systems dominate signal transduction in prokaryotes. TRENDS Microbiol 13 : 52 56.
33. West, A.H. Stock, A.M. (2001) Histidine kinases and response regulator proteins in two-component systems. TRENDS Biochem Sci 26 : 369 376.