Regulation of Salmonella typhimurium virulence gene expression by cationic antimicrobial peptides

Molecular Microbiology

Volumn 50, Issue 1, 2003, Pages 219-230

  Bader, Martin W ^a   Navarre, William Wiley ^a   Shiau, Whitney ^b   Nikaido, Hiroshi ^b   Frye, Jonathan G ^c   McClelland, Michael ^c   Fang, Ferric C ^a   Miller, Samuel I ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c SIDNEY KIMMEL CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIINFECTIVE AGENT; CATION; CYCLIC AMP; HYDROGEN PEROXIDE; PEPTIDE DERIVATIVE; PROTEIN HISTIDINE KINASE;

ALPHA HELIX; ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL FLAGELLUM; BACTERIAL GENE; BACTERIAL GENETICS; BACTERIAL GROWTH; BACTERIAL VIRULENCE; CELL INVASION; CELL PROTECTION; CONCENTRATION (PARAMETERS); GENE EXPRESSION REGULATION; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; REGULATORY MECHANISM; REGULON; SALMONELLA TYPHIMURIUM; SECRETION; TRANSCRIPTION REGULATION;

ALKALINE PHOSPHATASE; ANTI-BACTERIAL AGENTS; ANTIMICROBIAL CATIONIC PEPTIDES; BACTERIAL PROTEINS; BETA-GALACTOSIDASE; DRUG RESISTANCE, BACTERIAL; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, BACTERIAL; GENES, BACTERIAL; GENES, REPORTER; OXIDATIVE STRESS; PEPTIDE MAPPING; POLYMYXINS; PROTEOME; REGULON; SALMONELLA TYPHIMURIUM; SIGMA FACTOR; SIGNAL TRANSDUCTION; VIRULENCE;

ANIMALIA; BACTERIA (MICROORGANISMS); NEGIBACTERIA; SALMONELLA TYPHIMURIUM;

EID: 0141818919     PISSN: 0950382X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-2958.2003.03675.x     Document Type: Article

References (50)

1. Adams, P., Fowler, R., Kinsella, N., Howell, G., Farris, M., Coote, P., and O'Connor, C.D. (2001) Proteomic detection of PhoPQ- and acid-mediated repression of Salmonella motility. Proteomics 1: 597-607.
2. Alpuche Aranda, C.M., Swanson, J.A., Loomis, W.P., and Miller, S.I. (1992) Salmonella typhimurium activates virulence gene transcription within acidified macrophage phagosomes. Proc Natl Acad Sci USA 89: 10079-10083.
3. Belden, W.J., and Miller, S.I. (1994) Further characterization of the PhoP regulon: identification of new PhoP-activated virulence loci. Infect Immun 62: 5095-5101.
4. Chamnongpol, S., Cromie, M., and Groisman, E.A. (2003) Mg2+ sensing by the Mg2+ sensor PhoQ of Salmonella enterica. J Mol Biol 325: 795-807.
5. Chen, C.Y., Eckmann, L., Libby, S.J., Fang, F.C., Okamoto, S., Kagnoff, M.F., et al. (1996) Expression of Salmonella typhimurium rpoS and rpoS-dependent genes in the intracellular environment of eukaryotic cells. Infect Immun 64: 4739-4743.
6. Csonka, L.N., and Epstein, W. (1996) Osmoregulation. In Escherichia coli and Salmonella typhimurium, Cellular and Molecular Biology. Neidhardt, F.C. (ed.). Washington D.C.: ASM Press, pp. 1210-1223.
7. Darveau, R.P., Blake, J., Seachord, C.L., Cosand, W.L., Cunningham, M.D., Cassiano-Clough, L., and Maloney, G. (1992) Peptides related to the carboxyl terminus of human platelet factor IV with antibacterial activity. J Clin Invest 90: 447-455.
8. Datsenko, K.A., and Wanner, B.L. (2000) One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci USA 97: 6640-6645.
9. Daugelavicius, R., Bakiene, E., and Bamford, D.H. (2000) Stages of polymyxin B interaction with the Escherichia coli cell envelope. Antimicrob Agents Chemother 44: 2969-2978.
10. Ernst, R.K., Guina, T., and Miller, S.I. (2001) Salmonella typhimurium outer membrane remodeling: role in resistance to host innate immunity. Microbes Infect 3: 1327-1334.
11. Fang, F.C., Libby, S.J., Buchmeier, N.A., Loewen, P.C., Switala, J., Harwood, J., and Guiney, D.G. (1992) The alternative sigma factor katF (rpoS) regulates Salmonella virulence. Proc Natl Acad Sci USA 89: 11978-11982.
12. Fields, P.I., Groisman, E.A., and Heffron, F. (1989) A Salmonella locus that controls resistance to microbicidal proteins from phagocytic cells. Science 243: 1059-1062.
13. Garcia Vescovi, E., Soncini, F.C., and Groisman, E.A. (1996) Mg2+ as an extracellular signal: environmental regulation of Salmonella virulence. Cell 84: 165-174.
14. Groisman, E.A., Chiao, E., Lipps, C.J., and Heffron, F. (1989) Salmonella typhimurium phoP virulence gene is a transcriptional regulator. Proc Natl Acad Sci USA 86: 7077-7081.
15. Groisman, E.A., Parra-Lopez, C., Salcedo, M., Lipps, C.J., and Heffron, F. (1992) Resistance to host antimicrobial peptides is necessary for Salmonella virulence. Proc Natl Acad Sci USA 89: 11939-11943.
16. Gunn, J.S., and Miller, S.I. (1996) PhoP-PhoQ activates transcription of pmrAB, encoding a two-component regulatory system involved in Salmonella typhimurium antimicrobial peptide resistance. J Bacteriol 178: 6857-6864.
17. Gunn, J.S., Lim, K.B., Krueger, J., Kim, K., Guo, L., Hackett, M., and Miller, S.I. (1998a) PmrA-PmrB-regulated genes necessary for 4-aminoarabinose lipid A modification and polymyxin resistance. Mol Microbiol 27: 1171-1182.
18. Gunn, J.S., Belden, W.J., and Miller, S.I. (1998b) Identification of PhoP-PhoQ activated genes within a duplicated region of the Salmonella typhimurium chromosome. Microb Pathog 25: 77-90.
19. Gunn, J.S., Ryan, S.S., Van Velkinburgh, J.C., Ernst, R.K., and Miller, S.I. (2000) Genetic and functional analysis of a PmrA-PmrB-regulated locus necessary for lipopolysaccharide modification, antimicrobial peptide resistance, and oral virulence of Salmonella enterica serovar typhimurium. Infect Immun 68: 6139-6146.
20. Guo, L., Lim, K.B., Gunn, J.S., Bainbridge, B., Darveau, R.P., Hackett, M., and Miller, S.I. (1997) Regulation of lipid A modifications by Salmonella typhimurium virulence genes phoP-phoQ. Science 276: 250-253.
21. Guo, L., Lim, K.B., Poduje, C.M, Daniel, M., Gunn, J.S., Hackett, M., and Miller, S.I. (1998) Lipid A acylation and bacterial resistance against vertebrate antimicrobial peptides. Cell 95: 189-198.
22. Hancock, R.E., and Lehrer, R. (1998) Cationic peptides: a new source of antibiotics. Trends Biotechnol 16: 82-88.
23. Hancock, R.E., and Scott, M.G. (2000) The role of antimicrobial peptides in animal defenses. Proc Natl Acad Sci USA 97: 8856-8861.
24. Hengge-Aronis, R. (2002) Signal transduction and regulatory mechanisms involved in control of the sigma (S) (RpoS) subunit of RNA polymerase. Microbiol Mol Biol Rev 66: 373-395.
25. Hengge-Aronis, R., Lange, R., Henneberg, N., and Fischer, D. (1993) Osmotic regulation of rpoS-dependent genes in Escherichia coli. J Bacteriol 175: 259-265.
26. Hill, C.P., Yee, J., Selsted, M.E., and Eisenberg, D. (1991) Crystal structure of defensin HNP-3, an amphiphilic dimer: mechanisms of membrane permeabilization. Science 251: 1461-1465.
27. Ideker, T., Thorsson, V., Siegel, A.F., and Hood, L.E. (2000) Testing for differentially-expressed genes by maximum-likelihood analysis of microarray data. J Comput Biol 7: 805-817.
28. Ideker, T., Galitski, T., and Hood, L. (2001) A new approach to decoding life: systems biology. Annu Rev Genomics Hum Genet 2: 343-372.
29. Kamio, Y., and Nikaido, H. (1976) Outer membrane of Salmonella typhimurium: accessibility of phospholipid head groups to phospholipase c and cyanogen bromide activated dextran in the external medium. Biochemistry 15: 2561-2570.
30. Kokryakov, V.N., Harwig, S.S., Panyutich, E.A., Shevchenko, A.A., Aleshina, G.M., Shamova, O.V., et al. (1993) Protegrins: leukocyte antimicrobial peptides that combine features of corticostatic defensins and tachyplesins. FEBS Microbiol Lett 327: 231-236.
31. Lee, Y.W., Jin, S., Sim, W.S., and Nester, E.W. (1996) The sensing of plant signal molecules by Agrobacterium: genetic evidence for direct recognition of phenolic inducers by the VirA protein. Gene 179: 83-88.
32. Lehrer, R.I., and Ganz, T. (1999) Antimicrobial peptides in mammalian and insect host defence. Curr Opin Immunol 11: 23-27.
33. Lehrer, R.I., Lichtenstein, A.K., and Ganz, T. (1993) Defensins: antimicrobial and cytotoxic peptides of mammalian cells. Annu Rev Immunol 11: 105-128.
34. Macnab, RM. (1992) Genetics and biogenesis of bacterial flagella. Annu Rev Genet 26: 131-158.
35. Miller, S.I., Kukral, A.M., and Mekalanos, J.J. (1989) A two-component regulatory system (phoP phoQ) controls Salmonella typhimurium virulence. Proc Natl Acad Sci USA 86: 5054-5058.
36. Nikaido, H. (1996) In Escherichia coli and Salmonella typhimurium, Cellular and Molecular Biology. Neidhardt, F.C. (ed.). Washington D.C.: ASM Press, pp. 29-47.
37. Rana, F.R., Macias, E.A., Sultany, C.M., Modzrakowski, M.C., and Blazyk, J. (1991) Interactions between magainin 2 and Salmonella typhimurium outer membranes: effect of lipopolysaccharide structure. Biochemistry 30: 5858-5866.
38. Rubenhagen, R., Morbach, S., and Kramer, R. (2001) The osmoreactive betaine carrier BetP from Corynebacterium glutamicum is a sensor for cytoplasmic K+. EMBO J 20: 5412-5420.
39. Sanchez, J.F., Hoh, F., Strub, M.P., Aumelas, A., and Dumas, C. (2002) Structure of the cathelicidin motif of protegrin-3 precursor: structural insights into the activation mechanism of an antimicrobial protein. Structure (Camb) 10: 1363-1370.
40. Sledjeski, D.D., and Gottesman, S. (1996) Osmotic shock induction of capsule synthesis in Escherichia coli K-12. J Bacteriol 178: 1204-1206.
41. Soncini, F.C., Garcia Vescovi, E., Solomon, F., and Groisman, E.A. (1996) Molecular basis of the magnesium deprivation response in Salmonella typhimurium: identification of PhoP-regulated genes. J Bacteriol 178: 5092-5099.
42. Srimal, S., Surolia, N., Balasubramanian, S., and Surolia, A. (1996) Titration calorimetric studies to elucidate the specificity of the interactions of polymyxin B with lipopolysaccharides and lipid A. Biochem J 315: 679-686.
43. Tartera, C., and Metcalf, E.S. (1993) Osmolarity and growth phase overlap in regulation of Salmonella typhi adherence to and invasion of human intestinal cells. Infect Immun 61: 3084-3089.
44. Tossi, A., Sandri, L., and Giangaspero, A. (2000) Amphipathic, alpha-helical antimicrobial peptides. Biopolymers 55: 4-30.
45. Trent, MS., Pabich, W., Raetz, C.R., and Miller, S.I. (2001) A PhoP/PhoQ-induced Lipase (PagL) that catalyzes 3-O-deacylation of lipid A precursors in membranes of Salmonella typhimurium. J Biol Chem 276: 9083-9092.
46. Trisler, P., and Gottesman, S. (1984) Ion transcriptional regulation of genes necessary for capsular polysaccharide synthesis in Escherichia coli K-12. J Bacteriol 160: 184-191.
47. Vaara, M., and Vaara, T. (1981) Outer membrane permeability barrier disruption by polymyxin in polymyxin-susceptible and - resistant Salmonella typhimurium. Antimicrob Agents Chemother 19: 578-583.
48. Vaara, M., and Vaara, T. (1983) Polycations as outer membrane-disorganizing agents. Antimicrob Agents Chemother 24: 114-122.
49. Waldburger, C.D., and Sauer, R.T. (1996) Signal detection by the PhoQ sensor-transmitter. Characterization of the sensor domain and a response-impaired mutant that identifies ligand-binding determinants. J Biol Chem 271: 26630-26636.
50. Winans, S.C., Mantis, N.J., Chen, C.Y., Chang, C.H., and Han, D.C. (1994) Host recognition by the VirA, VirG two-component regulatory proteins of agrobacterium tumefaciens. Res Microbiol 145: 461-473.