Co-regulation of Salmonella enterica genes required for virulence and resistance to antimicrobial peptides by SlyA and PhoP/PhoQ

Molecular Microbiology

Volumn 56, Issue 2, 2005, Pages 492-508

  Navarre, William Wiley ^a   Halsey, Thomas A ^b   Walthers, Don ^c   Frye, Jonathan ^d   McClelland, Michael ^d   Potter, Jennifer L ^b   Kenney, Linda J ^c   Gunn, John S ^e   Fang, Ferric C ^a   Libby, Stephen J ^a,b  

^a UNIVERSITY OF WASHINGTON   (United States)

^b NORTH CAROLINA STATE UNIVERSITY   (United States)

^c UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^d SIDNEY KIMMEL CANCER CENTER   (United States)

^e OHIO STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; PEPTIDE; TRANSCRIPTOME;

ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL GENE; BACTERIAL GENOME; BACTERIAL MEMBRANE; BACTERIAL VIRULENCE; BINDING SITE; CONTROLLED STUDY; GENE CONTROL; GENE EXPRESSION; MIG 14 GENE; NONHUMAN; PAGC GENE; PAGD GENE; PAGJ GENE; PAGK GENE; PGTE GENE; PHON GENE; PHOP GENE; PIPB2 GENE; PRIORITY JOURNAL; PROMOTER REGION; SALMONELLA ENTERICA; SALMONELLA TYPHIMURIUM; SLYA GENE; SOPD2 GENE; UGTL GENE; VIRK GENE;

ANTIMICROBIAL CATIONIC PEPTIDES; BACTERIAL PROTEINS; DRUG RESISTANCE, BACTERIAL; GENE EXPRESSION REGULATION, BACTERIAL; SALMONELLA ENTERICA; VIRULENCE;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; SALMONELLA; SALMONELLA ENTERICA; SALMONELLA ENTERICA SUBSP. ENTERICA SEROVAR TYPHIMURIUM; TYPHIMURIUM;

EID: 20244365945     PISSN: 0950382X     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2005.04553.x     Document Type: Article

References (80)

1. Alekshun, M.N., and Levy, S.B. (1999) Alteration of the repressor activity of MarR, the negative regulator of the Escherichia coli marRAB locus, by multiple chemicals in vitro. J Bacteriol 181: 4669-4672.
2. Ariza, R.R., Cohen, S.P., Bachhawat, N., Levy, S.B., and Demple, B. (1994) Repressor mutations in the marRAB operon that activate oxidative stress genes and multiple antibiotic resistance in Escherichia coli. J Bacteriol 176: 143-148.
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. Berggren, R.E., Wunderlich, A., Ziegler, E., Schleicher, M., Duke, R.C., Looney, D., and Fang, F.C. (1995) HIV gp120-specific cell-mediated immune responses in mice after oral immunization with recombinant Salmonella. J Acquir Immune Defic Syndr 10: 489-495.
5. Blattner, F.R., Plunkett, G., 3rd, Bloch, C.A., Perna, N.T., Burland, V., Riley, M., et al. (1997) The complete genome sequence of Escherichia coli K-12. Science 277: 1453-1474.
6. Brodsky, I.E., Ernst, R.K., Miller, S.I., and Falkow, S. (2002) mig-14 is a Salmonella gene that plays a role in bacterial resistance to antimicrobial peptides. J Bacteriol 184: 3203-3213.
7. Brumell, J.H., Kujat-Choy, S., Brown, N.F., Vallance, B.A., Knodler, L.A., and Finlay, B.B. (2003) SopD2 is a novel type III secreted effector of Salmonella typhimurium that targets late endocytic compartments upon delivery into host cells. Traffic 4: 36-48.
8. Buchmeier, N., Bossie, S., Chen, C.Y., Fang, F.C., Guiney, D.G., and Libby, S.J. (1997) SlyA, a transcriptional regulator of Salmonella typhimurium, is required for resistance to oxidative stress and is expressed in the intracellular environment of macrophages. Infect Immun 65: 3725-3730.
9. Chen, H., and Schifferli, D.M. (2001) Enhanced immune responses to viral epitopes by combining macrophage-inducible expression with multimeric display on a Salmonella vector. Vaccine 19: 3009-3018.
10. Choi, H., Kim, S., Mukhopadhyay, P., Cho, S., Woo, J., Storz, G., and Ryu, S. (2001) Structural basis of the redox switch in the OxyR transcription factor. Cell 105: 103-113.
11. Daniels, J.J., Autenrieth, I.B., Ludwig, A., and Goebel, W. (1996) The gene slyA of Salmonella typhimurium is required for destruction of M cells and intracellular survival but not for invasion or colonization of the murine small intestine. Infect Immun 64: 5075-5084.
12. 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.
13. Deiwick, J., Nikolaus, T., Erdogan, S., and Mensel, M. (1999) Environmental regulation of Salmonella pathogenicity island 2 gene expression. Mol Microbiol 31: 1759-1773.
14. Detweiler, C.S., Monack, D.M., Brodsky, I.E., Mathew, H., and Falkow, S. (2003) virK, somA and rcsC are important for systemic Salmonella enterica serovar Typhimurium infection and cationic peptide resistance. Mol Microbiol 48: 385-400.
15. Eguchi, Y., Okada, T., Minagawa, S., Oshima, T., Mori, H., Yamamoto, K., et al. (2004) Signal transduction cascade between EvgA/EvgS and PhoP/PhoQ two-component systems of Escherichia coli. J Bacteriol 186: 3006-3014.
16. Feng, X., Oropeza, R., and Kenney, L.J. (2003) Dual regulation by phospho-OmpR of ssrA/B gene expression in Salmonella pathogenicity island 2. Mol Microbiol 48: 1131-1143.
17. Feng, X., Walthers, D., Oropeza, R., and Kenney, L.J. (2004) The response regulator SsrB activates transcription and binds to a region overlapping OmpR binding sites at Salmonella pathogenicity island 2. Mol Microbiol 54: 823-835.
18. 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.
19. Galan, B., Kolb, A., Sanz, J.M., Garcia, J.L., and Prieto, M.A. (2003) Molecular determinants of the hpa regulatory system of Escherichia coli: the HpaR repressor. Nucleic Acids Res 31: 6598-6609.
20. Grkovic, S., Brown, M.H., and Skurray, R.A. (2002) Regulation of bacterial drug export systems. Microbiol Mol Biol Rev 66: 671-701.
21. Groisman, E.A. (2001) The pleiotropic two-component regulatory system PhoP-PhoQ. J Bacteriol 183: 1835-1842.
22. Groisman, E.A., Kayser, J., and Soncini, F.C. (1997) Regulation of polymyxin resistance and adaptation to low-Mg2+ environments. J Bacteriol 179: 7040-7045.
23. Guina, T., Yi, E.C., Wang, H., Hackett, M., and Miller, S.I. (2000) A PhoP-regulated outer membrane protease of Salmonella enterica serovar Typhimurium promotes resistance to alpha-helical antimicrobial peptides. J Bacteriol 182: 4077-4086.
24. 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.
25. Gunn, J.S., Alpuche-Aranda, C.M., Loomis, W.P., Beiden, W.J., and Miller, S.I. (1995) Characterization of the Salmonella typhimurium pagC/pagD chromosomal region. J Bacteriol 177: 5040-5047.
26. Gunn, J.S., Hohmann, E.L., and Miller, S.I. (1996) Transcriptional regulation of Salmonella virulence: a PhoQ periplasmic domain mutation results in increased net phosphotransfer to PhoP. J Bacteriol 178: 6369-6373.
27. Gunn, J.S., Lim, K.B., Krueger, J., Kim, K., Quo, L., Hackett, M., and Miller, S.I. (1998) PmrA-PmrB-regulated genes necessary for 4-aminoarabinose lipid A modification and polymyxin resistance. Mol Microbiol 27: 1171-1182.
28. Heroven, A.K., Nagel, G., Tran, H.J., Parr, S., and Dersch, P. (2004) RovA is autoregulated and antagonizes H-NS-mediated silencing of invasin and rovA expression in Yersinia pseudotuberculosis. Mol Microbiol 53: 871-888.
29. Hmiel, S.P., Snavely, M.D., Miller, G.G., and Maguire, M.E. (1986) Magnesium transport in Salmonella typhimurium: characterization of magnesium influx and cloning of a transport gene. J Bacteriol 168: 1444-1450.
30. 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.
31. Ideker, T., Galitski, T., and Hood, L. (2001) A new approach to decoding life: systems biology. Annu Rev Genomics Hum Genet 2: 343-372.
32. Kaneko, A., Mita, M., Sekiya, K., Matsui, H., Kawahara, K., and Danbara, H. (2002) Association of a regulatory gene, slyA with a mouse virulence of Salmonella serovar Choleraesuis. Microbio Immunol 46: 109-113.
33. Kim, C.C., and Falkow, S. (2004) Delineation of upstream signaling events in the salmonella pathogenicity island 2 transcriptional activation pathway. J Bacteriol 186: 4694-4704.
34. Kim, C.C., Monack, D., and Falkow, S. (2003) Modulation of virulence by two acidified nitrite-responsive loci of Salmonella enterica serovar Typhimurium. Infect Immun 71: 3196-3205.
35. Knodler, L.A., Vallance, B.A., Hensel, M., Jackel, D., Finlay, B.B., and Steele-Mortimer, O. (2003) Salmonella type III effectors PipB and PipB2 are targeted to detergent-resistant microdomains on internal host cell membranes. Mol Microbiol 49: 685-704.
36. Kox, L.F., Wosten, M.M., and Groisman, E.A. (2000) A small protein that mediates the activation of a two-component system by another two-component system. EMBO J 19: 1861-1872.
37. Lee, A.K., Detweiler, C.S., and Falkow, S. (2000) OmpR regulates the two-component system SsrA-ssrB in Salmonella pathogenicity island 2. J Bacteriol 182: 771-781.
38. Lejona, S., Aguirre, A., Cabeza, M.L., Garcia Vescovi, E., and Soncini, F.C. (2003) Molecular characterization of the Mg2+-responsive PhoP-PhoQ regulon in Salmonella enterica. J Bacteriol 185: 6287-6294.
39. Libby, S.J., Goebel, W., Ludwig, A., Buchmeier, N., Bowe, F., Fang, F.C., et al. (1994) A cytolysin encoded by Salmonella is required for survival within macrophages. Proc Natl Acad Sci USA 91: 489-493.
40. McClelland, M., Sanderson, K.E., Spieth, J., Clifton, S.W., Latreille, P., Courtney, L., et al. (2001) Complete genome sequence of Salmonella enterica serovar Typhimurium LT2. Nature 413: 852-856.
41. Martin, R.G., and Rosner, J.L. (2004) Transcriptional and translational regulation of the marRAB multiple antibiotic resistance operon in Escherichia coli. Mol Microbiol 53: 183-191.
42. Miao, E.A., Freeman, J.A., and Miller, S.I. (2002) Transcription of the SsrAB regulon is repressed by alkaline pH and is independent of PhoPQ and magnesium concentration. J Bacteriol 184: 1493-1497.
43. Miller, J. (1972) Experiments in Molecular Genetics. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
44. Miller, S.I., and Mekalanos, J.J. (1990) Constitutive expression of the phoP regulon attenuates Salmonella virulence and survival within macrophages. J Bacteriol 172: 2485-2490.
45. 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.
46. Minagawa, S., Ogasawara, H., Kato, A., Yamamoto, K., Eguchi, Y., Oshima, T., et al. (2003) Identification and molecular characterization of the Mg2+ stimulon of Escherichia coli. J Bacteriol 185: 3696-3702.
47. Nagel, G., Lahrz, A., and Dersch, P. (2001) Environmental control of invasin expression in Yersinia pseudotuberculosis is mediated by regulation of RovA, a transcriptional activator of the SlyA/Hor family. Mol Microbiol 41: 1249-1269.
48. Nasser, W., and Reverchon, S. (2002) H-NS-dependent activation of pectate lyases synthesis in the phytopathogenic bacterium Erwinia chrysanthemi is mediated by the PecT repressor. Mol Microbiol 43: 733-748.
49. Norte, V.A., Stapleton, M.R., and Green, J. (2003) PhoP-responsive expression of the Salmonella enterica serovar Typhimurium slyA gene. J Bacteriol 185: 3508-3514.
50. Porwollik, S., Frye, J., Florea, L.D., Blackmer, F., and McClelland, M. (2003) A non-redundant microarray of genes for two related bacteria. Nucleic Acids Res 31: 1869-1876.
51. Porwollik, S., Boyd, E.F., Choy, C., Cheng, P., Florea, L., Proctor, E., and McClelland, M. (2004) Characterization of Salmonella enterica subspecies I genovars using microarrays. J Bacteriol 186: 5883-5898.
52. Poteete, A.R., and Fenton, A.C. (1984) Lambda red-dependent growth and recombination of phage P22. Virology 134: 161-167.
53. Praillet, T., Reverchon, S., and Nasser, W. (1997) Mutual control of the PecS/PecM couple, two proteins regulating virulence-factor synthesis in Erwinia chrysanthemi. Mol Microbiol 24: 803-814.
54. Prouty, A.M., Brodsky, I.E., Falkow, S., and Gunn, J.S. (2004a) Bile-salt-mediated induction of antimicrobial and bile resistance in Salmonella typhimurium. Microbiology 150: 775-783.
55. Prouty, A.M., Brodsky, I.E., Manos, J., Belas, R., Falkow, S., and Gunn, J.S. (2004b) Transcriptional regulation of Salmonella enterica serovar Typhimurium genes by bile. FEMS Immunol Med Microbiol 41: 177-185.
56. Pulkkinen, W.S., and Miller, S.I. (1991) A Salmonella typhimurium virulence protein is similar to a Yersinia enterocolitica invasion protein and a bacteriophage lambda outer membrane protein. J Bacteriol 173: 86-93.
57. Revell, P.A., and Miller, V.L. (2000) A chromosomally encoded regulator is required for expression of the Yersinia enterocolitica inv gene and for virulence. Mol Microbiol 35: 677-685.
58. Reverchon, S., Nasser, W., and Robert-Baudouy, J. (1994) pecS: a locus controlling pectinase, cellulase and blue pigment production in Erwinia chrysanthemi. Mol Microbiol 11: 1127-1139.
59. Rouanet, C., Reverchon, S., Rodionov, D.A., and Nasser, W. (2004) Definition of a consensus DNA-binding site for PecS, a global regulator of virulence gene expression in Erwinia chrysanthemi and identification of new members of the PecS regulon. J Biol Chem 279: 30158-30167.
60. Schapiro, J.M., Libby, S.J., and Fang, F.C. (2003) Inhibition of bacterial DNA replication by zinc mobilization during nitrosative stress. Proc Natl Acad Sci USA 100: 8496-8501.
61. Schmieger, H. (1971) A method for detection of phage mutants with altered transducing ability. Mol Gen Genet 110: 378-381.
62. Seoane, A.S., and Levy, S.B. (1995) Characterization of MarR, the repressor of the multiple antibiotic resistance (mar) operon in Escherichia coli. J Bacteriol 177: 3414-3419.
63. Shen-Orr, S.S., Milo, R., Mangan, S., and Alon, U. (2002) Network motifs in the transcriptional regulation network of Escherichia coli. Nat Genet 31: 64-68.
64. Shi, Y., Latifi, T., Cromie, M.J., and Groisman, E.A. (2004a) Transcriptional control of the antimicrobial peptide resistance ugtL gene by the Salmonella PhoP and SlyA regulatory proteins. J Biol Chem 279: 38618-38625.
65. Shi, Y., Cromie, M.J., Hsu, F.F., Turk, J., and Groisman, E.A. (2004b) PhoP-regulated Salmonella resistance to the antimicrobial peptides magainin 2 and polymyxin B. Mol Microbiol 53: 229-241.
66. Soncini, F.C., and Groisman, E.A. (1996) Two-component regulatory systems can interact to process multiple environmental signals. J Bacteriol 178: 6796-6801.
67. 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.
68. Spory, A., Bosserhoff, A., von Rhein, C., Goebel, W., and Ludwig, A. (2002) Differential regulation of multiple proteins of Escherichia coli and Salmonella enterica serovar Typhimurium by the transcriptional regulator SlyA. J Bacteriol 184: 3549-3559.
69. Stapleton, M.R., Norte, V.A., Read, R.C., and Green, J. (2002) Interaction of the Salmonella typhimurium transcription and virulence factor SlyA with target DNA and identification of members of the SlyA regulon. J Biol Chem 277: 17630-17637.
70. Valdivia, R.H., Cirillo, D.M., Lee, A.K., Bouley, D.M., and Falkow, S. (2000) mig-14 is a horizontally acquired, host-induced gene required for Salmonella enterica lethal infection in the murine model of typhoid fever. Infect Immun 68: 7126-7131.
71. Vazquez-Torres, A., Xu, Y., Jones-Carson, J., Holden, D.W., Lucia, S.M., Dinauer, M.C., et al. (2000) Salmonella pathogenicity island 2-dependent evasion of the phagocyte NADPH oxidase. Science 287: 1655-1658.
72. van Velkinburgh, J.C., and Gunn, J.S. (1999) PhoP-PhoQ-regulated loci are required for enhanced bile resistance in Salmonella spp. Infect Immun 67: 1614-1622.
73. Waterman, S.R., and Holden, D.W. (2003) Functions and effectors of the Salmonella pathogenicity island 2 type III secretion system. Cell Microbiol 5: 501-511.
74. Watson, N. (1988) A new revision of the sequence of plasmid pBR322. Gene 70: 399-403.
75. Watson, P.R., Paulin, S.M., Bland, A.P., Libby, S.J., Jones, P.W., and Wallis, T.S. (1999) Differential regulation of enteric and systemic salmonellosis by. Slya Infect Immun 67: 4950-4954.
76. Wosten, M.M., Kox, L.F., Chamnongpol, S., Soncini, F.C., and Groisman, E.A. (2000) A signal transduction system that responds to extracellular iron. Cell 103: 113-125.
77. Wu, R.Y., Zhang, R.G., Zagnitko, O., Dementieva, I., Maltzev, N., Watson, J.D., et al. (2003) Crystal structure of Enterococcus faecalis SlyA-like transcriptional factor. J Biol Chem 278: 20240-20244.
78. Wyborn, N.R., Stapleton, M.R., Norte, V.A., Roberts, R.E., Grafton, J., and Green, J. (2004) Regulation of Escherichia coli hemolysin E expression by H-NS and Salmonella SlyA. J Bacteriol 186: 1620-1628.
79. Xiong, A., Gottman, A., Park, C., Baetens, M., Pandza, S., and Matin, A. (2000) The EmrR protein represses the Escherichia coli emrRAB multidrug resistance operon by directly binding to its promoter region. Antimicrob Agents Chemother 44: 2905-2907.
80. Yamamoto, K., Ogasawara, H., Fujita, N., Utsumi, R., and Ishihama, A. (2002) Novel mode of transcription regulation of divergently overlapping promoters by PhoP, the regulator of two-component system sensing external magnesium availability. Mol Microbiol 45: 423-438.