The two-component sensor kinase KdpD is required for Salmonella typhimurium colonization of Caenorhabditis elegans and survival in macrophages

Cellular Microbiology

Volumn 13, Issue 10, 2011, Pages 1618-1637

  Alegado, Rosanna A ^a,d   Chin, Chui Yoke ^b   Monack, Denise M ^a   Tan, Man Wah ^a,c  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITI KEBANGSAAN MALAYSIA   (Malaysia)

^c GENENTECH INC   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PHOSPHOTRANSFERASE; PROTEIN KDPD; UNCLASSIFIED DRUG; VIRULENCE FACTOR;

ANIMAL CELL; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL VIRULENCE; CAENORHABDITIS ELEGANS; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; GENE LOCUS; MACROPHAGE; NEMATODE; NONHUMAN; OXIDATIVE STRESS; PATHOGENESIS; PERSISTENT INFECTION; PRIORITY JOURNAL; SALMONELLA ENTERICA; SALMONELLA TYPHIMURIUM; SEROTYPE; TISSUE CULTURE;

ANIMALS; BACTERIAL PROTEINS; CAENORHABDITIS ELEGANS; CELL LINE; GASTROINTESTINAL TRACT; GENE KNOCKOUT TECHNIQUES; GENETIC TESTING; MACROPHAGES; MICE; MICROBIAL VIABILITY; PROTEIN KINASES; SALMONELLA TYPHIMURIUM; VIRULENCE; VIRULENCE FACTORS;

BACTERIA (MICROORGANISMS); CAENORHABDITIS ELEGANS; METAZOA; MURINAE; SALMONELLA; SALMONELLA ENTERICA SUBSP. ENTERICA SEROVAR TYPHIMURIUM; SALMONELLA TYPHIMURIUM;

EID: 80052822475     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/j.1462-5822.2011.01645.x     Document Type: Article

References (137)

1. Aballay, A., Yorgey, P., and Ausubel, F.M. (2000) Salmonella typhimurium proliferates and establishes a persistent infection in the intestine of Caenorhabditis elegans. Curr Biol 10: 1539-1542.
2. Ahmer, B.M., van Reeuwijk, J., Watson, P.R., Wallis, T.S., and Heffron, F. (1999) Salmonella SirA is a global regulator of genes mediating enteropathogenesis. Mol Microbiol 31: 971-982.
3. Alegado, R.A., and Tan, M.W. (2008) Resistance to antimicrobial peptides contributes to persistence of Salmonella typhimurium in the C. elegans intestine. Cell Microbiol 10: 1259-1273.
4. Allman, E., Johnson, D., and Nehrke, K. (2009) Loss of the apical V-ATPase a-subunit VHA-6 prevents acidification of the intestinal lumen during a rhythmic behavior in C. elegans. Am J Physiol Cell Physiol 297: C1071-C1081.
5. Altendorf, K., Voelkner, P., and Puppe, W. (1994) The sensor kinase KdpD and the response regulator KdpE control expression of the kdpFABC operon in Escherichia coli. Res Microbiol 145: 374-381.
6. Altier, C., Suyemoto, M., Ruiz, A.I., Burnham, K.D., and Maurer, R. (2000) Characterization of two novel regulatory genes affecting Salmonella invasion gene expression. Mol Microbiol 35: 635-646.
7. Altschul, S.F., Gish, W., Miller, W., Myers, E.W., and Lipman, D.J. (1990) Basic local alignment search tool. J Mol Biol 215: 403-410.
8. Arlehamn, C.S., Petrilli, V., Gross, O., Tschopp, J., and Evans, T.J. (2010) The role of potassium in inflammasome activation by bacteria. J Biol Chem 285: 10508-10518.
9. Asakura, H., Panutdaporn, N., Kawamoto, K., Igimi, S., Yamamoto, S., and Makino, S. (2004) Isolation of mini-Tn5Km2 insertion mutants of Salmonella enterica serovar Oranienburg sensitive to NaCl-induced osmotic stress. Microbiol Immunol 48: 981-984.
10. Asha, H., and Gowrishankar, J. (1993) Regulation of kdp operon expression in Escherichia coli: evidence against turgor as signal for transcriptional control. J Bacteriol 175: 4528-4537.
11. Avery, L., and Shtonda, B.B. (2003) Food transport in the C. elegans pharynx. J Exp Biol 206: 2441-2457.
12. Ballal, A., Basu, B., and Apte, S.K. (2007) The Kdp-ATPase system and its regulation. J Biosci 32: 559-568.
13. Banyai, L., and Patthy, L. (1998) Amoebapore homologs of Caenorhabditis elegans. Biochim Biophys Acta 1429: 259-264.
14. Begun, J., Sifri, C.D., Goldman, S., Calderwood, S.B., and Ausubel, F.M. (2005) Staphylococcus aureus virulence factors identified by using a high-throughput Caenorhabditis elegans-killing model. Infect Immun 73: 872-877.
15. Bell, B.L., Mohapatra, N.P., and Gunn, J.S. (2010) Regulation of virulence gene transcripts by the Francisella novicida orphan response regulator PmrA: role of phosphorylation and evidence of MglA/SspA interaction. Infect Immun 78: 2189-2198.
16. Benjamin, W.H., Jr, Hall, P., and Briles, D.E. (1991) A hemA mutation renders Salmonella typhimurium avirulent in mice, yet capable of eliciting protection against intravenous infection with S. typhimurium. Microb Pathog 11: 289-295.
17. Bijlsma, J.J., and Groisman, E.A. (2005) The PhoP/PhoQ system controls the intramacrophage type three secretion system of Salmonella enterica. Mol Microbiol 57: 85-96.
18. Brenner, S. (1974) The genetics of Caenorhabditis elegans. Genetics 77: 71-94.
19. Brodsky, I.E., and Monack, D. (2009) NLR-mediated control of inflammasome assembly in the host response against bacterial pathogens. Semin Immunol 21: 199-207.
20. Brown, N.F., Vallance, B.A., Coombes, B.K., Valdez, Y., Coburn, B.A., and Finlay, B.B. (2005) Salmonella pathogenicity island 2 is expressed prior to penetrating the intestine. PLoS Pathog 1: e32.
21. Burns-Guydish, S.M., Olomu, I.N., Zhao, H., Wong, R.J., Stevenson, D.K., and Contag, C.H. (2005) Monitoring age-related susceptibility of young mice to oral Salmonella enterica serovar Typhimurium infection using an in vivo murine model. Pediatr Res 58: 153-158.
22. Callewaert, L., Aertsen, A., Deckers, D., Vanoirbeek, K.G., Vanderkelen, L., Van Herreweghe, J.M., etal. (2008) A new family of lysozyme inhibitors contributing to lysozyme tolerance in gram-negative bacteria. PLoS Pathog 4: e1000019.
23. Chan, K., Kim, C.C., and Falkow, S. (2005) Microarray-based detection of Salmonella enterica serovar Typhimurium transposon mutants that cannot survive in macrophages and mice. Infect Immun 73: 5438-5449.
24. Chang, A.C., and Cohen, S.N. (1978) Construction and characterization of amplifiable multicopy DNA cloning vehicles derived from the P15A cryptic miniplasmid. J Bacteriol 134: 1141-1156.
25. Chaudhuri, R.R., Peters, S.E., Pleasance, S.J., Northen, H., Willers, C., Paterson, G.K., etal. (2009) Comprehensive identification of Salmonella enterica serovar Typhimurium genes required for infection of BALB/c mice. PLoS Pathog 5: e1000529.
26. Chavez, V., Mohri-Shiomi, A., Maadani, A., Vega, L.A., and Garsin, D.A. (2007) Oxidative stress enzymes are required for DAF-16-mediated immunity due to generation of reactive oxygen species by Caenorhabditis elegans. Genetics 176: 1567-1577.
27. Chen, L.M., Kaniga, K., and Galan, J.E. (1996) Salmonella spp. are cytotoxic for cultured macrophages. Mol Microbiol 21: 1101-1115.
28. Choi, J., Shin, D., Yoon, H., Kim, J., Lee, C.R., Kim, M., etal. (2010) Salmonella pathogenicity island 2 expression negatively controlled by EIIANtr-SsrB interaction is required for Salmonella virulence. Proc Natl Acad Sci USA 107: 20506-20511.
29. Cirillo, D.M., Valdivia, R.H., Monack, D.M., and Falkow, S. (1998) Macrophage-dependent induction of the Salmonella pathogenicity island 2 type III secretion system and its role in intracellular survival. Mol Microbiol 30: 175-188.
30. Coburn, B., Li, Y., Owen, D., Vallance, B.A., and Finlay, B.B. (2005) Salmonella enterica serovar Typhimurium pathogenicity island 2 is necessary for complete virulence in a mouse model of infectious enterocolitis. Infect Immun 73: 3219-3227.
31. Coombes, B.K., Coburn, B.A., Potter, A.A., Gomis, S., Mirakhur, K., Li, Y., and Finlay, B.B. (2005a) Analysis of the contribution of Salmonella pathogenicity islands 1 and 2 to enteric disease progression using a novel bovine ileal loop model and a murine model of infectious enterocolitis. Infect Immun 73: 7161-7169.
32. Coombes, B.K., Wickham, M.E., Lowden, M.J., Brown, N.F., and Finlay, B.B. (2005b) Negative regulation of Salmonella pathogenicity island 2 is required for contextual control of virulence during typhoid. Proc Natl Acad Sci USA 102: 17460-17465.
33. 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.
34. De Groote, M.A., Ochsner, U.A., Shiloh, M.U., Nathan, C., McCord, J.M., Dinauer, M.C., etal. (1997) Periplasmic superoxide dismutase protects Salmonella from products of phagocyte NADPH-oxidase and nitric oxide synthase. Proc Natl Acad Sci USA 94: 13997-14001.
35. Deiwick, J., Nikolaus, T., Erdogan, S., and Hensel, M. (1999) Environmental regulation of Salmonella pathogenicity island 2 gene expression. Mol Microbiol 31: 1759-1773.
36. Epstein, W., and Davies, M. (1970) Potassium-dependant mutants of Escherichia coli K-12. J Bacteriol 101: 836-843.
37. Fellenius, E., Berglindh, T., Sachs, G., Olbe, L., Elander, B., Sjostrand, S.E., and Wallmark, B. (1981) Substituted benzimidazoles inhibit gastric acid secretion by blocking (H++ K+)ATPase. Nature 290: 159-161.
38. Finlay, B.B., and Falkow, S. (1997) Common themes in microbial pathogenicity revisited. Microbiol Mol Biol Rev 61: 136-169.
39. Frymier, J.S., Reed, T.D., Fletcher, S.A., and Csonka, L.N. (1997) Characterization of transcriptional regulation of the kdp operon of Salmonella typhimurium. J Bacteriol 179: 3061-3063.
40. Galan, J.E. (1996) Molecular genetic bases of Salmonella entry into host cells. Mol Microbiol 20: 263-271.
41. Garsin, D.A., Sifri, C.D., Mylonakis, E., Qin, X., Singh, K.V., Murray, B.E., etal. (2001) A simple model host for identifying Gram-positive virulence factors. Proc Natl Acad Sci USA 98: 10892-10897.
42. Garsin, D.A., Mylonakis, E., Calderwood, S.B., and Ausubel, F.M. (2002) Identifying Enterococcus faecalis virulence factors by screening for avirulent mutants in Caenorhabditis elegans. Abstr Gen Meet Am Soc Microbiol 102: 58.
43. Garvis, S., Munder, A., Ball, G., de Bentzmann, S., Wiehlmann, L., Ewbank, J.J., etal. (2009) Caenorhabditis elegans semi-automated liquid screen reveals a specialized role for the chemotaxis gene cheB2 in Pseudomonas aeruginosa virulence. PLoS Pathog 5: e1000540.
44. Geiszt, M., Witta, J., Baffi, J., Lekstrom, K., and Leto, T.L. (2003) Dual oxidases represent novel hydrogen peroxide sources supporting mucosal surface host defense. FASEB J 17: 1502-1504.
45. Gowrishankar, J. (1985) Identification of osmoresponsive genes in Escherichia coli: evidence for participation of potassium and proline transport systems in osmoregulation. J Bacteriol 164: 434-445.
46. 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.
47. 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.
48. Hamann, K., Zimmann, P., and Altendorf, K. (2008) Reduction of turgor is not the stimulus for the sensor kinase KdpD of Escherichia coli. J Bacteriol 190: 2360-2367.
49. Hansen-Wester, I., and Hensel, M. (2002) Genome-based identification of chromosomal regions specific for Salmonella spp. Infect Immun 70: 2351-2360.
50. Heermann, R., Weber, A., Mayer, B., Ott, M., Hauser, E., Gabriel, G., etal. (2009) The universal stress protein UspC scaffolds the KdpD/KdpE signaling cascade of Escherichia coli under salt stress. J Mol Biol 386: 134-148.
51. Hensel, M., Shea, J.E., Waterman, S.R., Mundy, R., Nikolaus, T., and Banks, G. (1998) Genes encoding putative effector proteins of the type III secretion system of Salmonella Pathogenicity Island 2 are required for bacterial virulence and proliferation in macrophages. Mol Microbiol 30: 163-174.
52. Hershberg, R., Altuvia, S., and Margalit, H. (2003) A survey of small RNA-encoding genes in Escherichia coli. Nucleic Acids Res 31: 1813-1820.
53. Hoiseth, S.K., and Stocker, B.A. (1981) Aromatic-dependent Salmonella typhimurium are non-virulent and effective as live vaccines. Nature 291: 238-239.
54. Isaacson, R.E., and Kinsel, M. (1992) Adhesion of Salmonella typhimurium to porcine intestinal epithelial surfaces: identification and characterization of two phenotypes. Infect Immun 60: 3193-3200.
55. Johnston, C., Pegues, D.A., Hueck, C.J., Lee, A., and Miller, S.I. (1996) Transcriptional activation of Salmonella typhimurium invasion genes by a member of the phosphorylated response-regulator superfamily. Mol Microbiol 22: 715-727.
56. Jones, B.D., Lee, C.A., and Falkow, S. (1992) Invasion by Salmonella typhimurium is affected by the direction of flagellar rotation. Infect Immun 60: 2475-2480.
57. Jung, K., and Altendorf, K. (1998) Truncation of amino acids 12-128 causes deregulation of the phosphatase activity of the sensor kinase KdpD of Escherichia coli. J Biol Chem 273: 17406-17410.
58. Kamath, R.S., Martinez-Campos, M., Zipperlen, P., Fraser, A.G., and Ahringer, J. (2001) Effectiveness of specific RNA-mediated interference through ingested double-stranded RNA in Caenorhabditis elegans. Genome Biol 2: RESEARCH0002.
59. Kato, Y., Aizawa, T., Hoshino, H., Kawano, K., Nitta, K., and Zhang, H. (2002) abf-1 and abf-2, ASABF-type antimicrobial peptide genes in Caenorhabditis elegans. Biochem J 361: 221-230.
60. 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.
61. Kim, Y.M., Talanian, R.V., Li, J., and Billiar, T.R. (1998) Nitric oxide prevents IL-1beta and IFN-gamma-inducing factor (IL-18) release from macrophages by inhibiting caspase-1 (IL-1beta-converting enzyme). J Immunol 161: 4122-4128.
62. Kim, D.H., Feinbaum, R., Alloing, G., Emerson, F.E., Garsin, D.A., Inoue, H., etal. (2002) A conserved p38 MAP kinase pathway in Caenorhabditis elegans innate immunity. Science 297: 623-626.
63. Kothe, M., Antl, M., Huber, B., Stoecker, K., Ebrecht, D., Steinmetz, I., and Eberl, L. (2003) Killing of Caenorhabditis elegans by Burkholderia cepacia is controlled by the cep quorum-sensing system. Cell Microbiol 5: 343-351.
64. Kowarz, L., Coynault, C., Robbe-Saule, V., and Norel, F. (1994) The Salmonella typhimurium katF (rpoS) gene: cloning, nucleotide sequence, and regulation of spvR and spvABCD virulence plasmid genes. J Bacteriol 176: 6852-6860.
65. Kurz, C.L., Chauvet, S., Andres, E., Aurouze, M., Vallet, I., Michel, G.P., etal. (2003) Virulence factors of the human opportunistic pathogen Serratia marcescens identified by in vivo screening. EMBO J 22: 1451-1460.
66. Kwon, Y.M., and Ricke, S.C. (1998) Induction of acid resistance of Salmonella typhimurium by exposure to short-chain fatty acids. Appl Environ Microbiol 64: 3458-3463.
67. Labrousse, A., Chauvet, S., Couillault, C., Kurz, C.L., and Ewbank, J.J. (2000) Caenorhabditis elegans is a model host for Salmonella typhimurium. Curr Biol 10: 1543-1545.
68. Laimins, L.A., Rhoads, D.B., and Epstein, W. (1981) Osmotic control of kdp operon expression in Escherichia coli. Proc Natl Acad Sci USA 78: 464-468.
69. Lawley, T.D., Chan, K., Thompson, L.J., Kim, C.C., Govoni, G.R., and Monack, D.M. (2006) Genome-wide screen for Salmonella genes required for long-term systemic infection of the mouse. PLoS Pathog 2: e11.
70. Ledeboer, N.A., and Jones, B.D. (2005) Exopolysaccharide sugars contribute to biofilm formation by Salmonella enterica serovar Typhimurium on HEp-2 cells and chicken intestinal epithelium. J Bacteriol 187: 3214-3226.
71. Lee, C.A., and Falkow, S. (1990) The ability of Salmonella to enter mammalian cells is affected by bacterial growth state. Proc Natl Acad Sci USA 87: 4304-4308.
72. 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.
73. Li, J., Billiar, T.R., Talanian, R.V., and Kim, Y.M. (1997) Nitric oxide reversibly inhibits seven members of the caspase family via S-nitrosylation. Biochem Biophys Res Commun 240: 419-424.
74. Li, J., Bombeck, C.A., Yang, S., Kim, Y.M., and Billiar, T.R. (1999) Nitric oxide suppresses apoptosis via interrupting caspase activation and mitochondrial dysfunction in cultured hepatocytes. J Biol Chem 274: 17325-17333.
75. Lindgren, S.W., Stojiljkovic, I., and Heffron, F. (1996) Macrophage killing is an essential virulence mechanism of Salmonella typhimurium. Proc Natl Acad Sci USA 93: 4197-4201.
76. de Lorenzo, V., Herrero, M., Jakubzik, U., and Timmis, K.N. (1990) Mini-Tn5 transposon derivatives for insertion mutagenesis, promoter probing, and chromosomal insertion of cloned DNA in gram-negative eubacteria. J Bacteriol 172: 6568-6572.
77. Lovell, M.A., and Barrow, P.A. (1999) Intestinal colonisation of gnotobiotic pigs by Salmonella organisms: interaction between isogenic and unrelated strains. J Med Microbiol 48: 907-916.
78. Luttmann, D., Heermann, R., Zimmer, B., Hillmann, A., Rampp, I.S., Jung, K., and Gorke, B. (2009) Stimulation of the potassium sensor KdpD kinase activity by interaction with the phosphotransferase protein IIA(Ntr) in Escherichia coli. Mol Microbiol 72: 978-994.
79. McClelland, M., Sanderson, K.E., Spieth, J., Clifton, S.W., Latreille, P., Courtney, L., etal. (2001) Complete genome sequence of Salmonella enterica serovar Typhimurium LT2. Nature 413: 852-856.
80. Mahajan-Miklos, S., Tan, M.W., Rahme, L.G., and Ausubel, F.M. (1999) Molecular mechanisms of bacterial virulence elucidated using a Pseudomonas aeruginosa-Caenorhabditis elegans pathogenesis model. Cell 96: 47-56.
81. Maier, K.S., Hubich, S., Liebhart, H., Krauss, S., Kuhn, A., and Facey, S.J. (2008) An amphiphilic region in the cytoplasmic domain of KdpD is recognized by the signal recognition particle and targeted to the Escherichia coli membrane. Mol Microbiol 68: 1471-1484.
82. Mallo, G.V., Kurz, C.L., Couillault, C., Pujol, N., Granjeaud, S., Kohara, Y., and Ewbank, J. (2002) Inducible antibacterial defense system in C. elegans. Curr Biol 12: 1209-1214.
83. Maloy, S.R., Stewart, V.J., and Taylor, R.K. (1996) Genetic Analysis of Pathogenic Bacteria. Plainview, NY: Cold Spring Harbor Laboratory Press.
84. Mannick, J.B., Miao, X.Q., and Stamler, J.S. (1997) Nitric oxide inhibits Fas-induced apoptosis. J Biol Chem 272: 24125-24128.
85. Mariathasan, S., Newton, K., Monack, D.M., Vucic, D., French, D.M., Lee, W.P., etal. (2004) Differential activation of the inflammasome by caspase-1 adaptors ASC and Ipaf. Nature 430: 213-218.
86. Mascher, T., Helmann, J.D., and Unden, G. (2006) Stimulus perception in bacterial signal-transducing histidine kinases. Microbiol Mol Biol Rev 70: 910-938.
87. Methner, U., Barrow, P.A., Gregorova, D., and Rychlik, I. (2004) Intestinal colonisation-inhibition and virulence of Salmonella phoP, rpoS and ompC deletion mutants in chickens. Vet Microbiol 98: 37-43.
88. Miller, V.L., and Mekalanos, J.J. (1988) A novel suicide vector and its use in construction of insertion mutations: osmoregulation of outer membrane proteins and virulence determinants in Vibrio cholerae requires toxR. J Bacteriol 170: 2575-2583.
89. 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.
90. Miller, S.I., Pulkkinen, W.S., Selsted, M.E., and 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.
91. Mohri-Shiomi, A., and Garsin, D.A. (2008) Insulin signaling and the heat shock response modulate protein homeostasis in the Caenorhabditis elegans intestine during infection. J Biol Chem 283: 194-201.
92. Monack, D.M., Raupach, B., Hromockyj, A.E., and Falkow, S. (1996) Salmonella typhimurium invasion induces apoptosis in infected macrophages. Proc Natl Acad Sci USA 93: 9833-9838.
93. Monack, D.M., Bouley, D.M., and Falkow, S. (2004) Salmonella typhimurium persists within macrophages in the mesenteric lymph nodes of chronically infected Nramp1+/+ mice and can be reactivated by IFNgamma neutralization. J Exp Med 199: 231-241.
94. Morgan, E., Campbell, J.D., Rowe, S.C., Bispham, J., Stevens, M.P., Bowen, A.J., etal. (2004) Identification ofhost-specific colonization factors of Salmonella enterica serovar Typhimurium. Mol Microbiol 54: 994-1010.
95. Moule, M.G., Monack, D.M., and Schneider, D.S. (2010) Reciprocal analysis of Francisella novicida infections of a Drosophila melanogaster model reveal host-pathogen conflicts mediated by reactive oxygen and imd-regulated innate immune response. PLoS Pathog 6: e1001065.
96. Nakashima, K., Sugiura, A., Momoi, H., and Mizuno, T. (1992) Phosphotransfer signal transduction between two regulatory factors involved in the osmoregulated kdp operon in Escherichia coli. Mol Microbiol 6: 1777-1784.
97. Ochman, H., Soncini, F.C., Solomon, F., and Groisman, E.A. (1996) Identification of a pathogenicity island required for Salmonella survival in host cells. Proc Natl Acad Sci USA 93: 7800-7804.
98. Padalon-Brauch, G., Hershberg, R., Elgrably-Weiss, M., Baruch, K., Rosenshine, I., Margalit, H., and Altuvia, S. (2008) Small RNAs encoded within genetic islands of Salmonella typhimurium show host-induced expression and role in virulence. Nucleic Acids Res 36: 1913-1927.
99. Parra-Lopez, C., Baer, M.T., and Groisman, E.A. (1993) Molecular genetic analysis of a locus required for resistance to antimicrobial peptides in Salmonella typhimurium. EMBO J 12: 4053-4062.
100. Parra-Lopez, C., Lin, R., Aspedon, A., and Groisman, E.A. (1994) A Salmonella protein that is required for resistance to antimicrobial peptides and transport of potassium. EMBO J 13: 3964-3972.
101. Powell, J.R., and Ausubel, F.M. (2008) Models of Caenorhabditis elegans infection by bacterial and fungal pathogens. Methods Mol Biol 415: 403-427.
102. al-Ramadi, B.K., Meissler, J.J., Jr, Huang, D., and Eisenstein, T.K. (1992) Immunosuppression induced by nitric oxide and its inhibition by interleukin-4. Eur J Immunol 22: 2249-2254.
103. Reeves, E.P., Lu, H., Jacobs, H.L., Messina, C.G., Bolsover, S., Gabella, G., etal. (2002) Killing activity of neutrophils is mediated through activation of proteases by K+ flux. Nature 416: 291-297.
104. Rhoads, D.B., Waters, F.B., and Epstein, W. (1976) Cation transport in Escherichia coli. VIII. Potassium transport mutants. J Gen Physiol 67: 325-341.
105. Rhoads, D.B., Laimins, L., and Epstein, W. (1978) Functional organization of the kdp genes of Escherichia coli K-12. J Bacteriol 135: 445-452.
106. Rose, R.E. (1988) The nucleotide sequence of pACYC177. Nucleic Acids Res 16: 356.
107. Rychlik, I., and Barrow, P.A. (2005) Salmonella stress management and its relevance to behaviour during intestinal colonisation and infection. FEMS Microbiol Rev 29: 1021.
108. Santiviago, C.A., Reynolds, M.M., Porwollik, S., Choi, S.H., Long, F., Andrews-Polymenis, H.L., and McClelland, M. (2009) Analysis of pools of targeted Salmonella deletion mutants identifies novel genes affecting fitness during competitive infection in mice. PLoS Pathog 5: e1000477.
109. Sardesai, A.A., and Gowrishankar, J. (2001) Trans-acting mutations in loci other than kdpDE that affect kdp operon regulation in Escherichia coli: effects of cytoplasmic thiol oxidation status and nucleoid protein H-NS on kdp expression. J Bacteriol 183: 86-93.
110. Schleussinger, E., Schmid, R., and Bakker, E.P. (2006) New type of kdp region with a split sensor-kinase kdpD gene located within two divergent kdp operons from the thermoacidophilic bacterium Alicyclobacillus acidocaldarius. Biochim Biophys Acta 1759: 437-441.
111. Shea, J.E., Hensel, M., Gleeson, C., and Holden, D.W. (1996) Identification of a virulence locus encoding a second type III secretion system in Salmonella typhimurium. Proc Natl Acad Sci USA 93: 2593-2597.
112. Siegele, D.A. (2005) Universal stress proteins in Escherichia coli. J Bacteriol 187: 6253-6254.
113. Sifri, C.D., Mylonakis, E., Garsin, D.A., Qin, X., Singh, K.V., Murray, B.E., etal. (2001) Evaluation of Enterococcus faecalis fsr quorum-sensing genes for pathogenesis using the Caenorhabditis elegans and mouse peritonitis model systems. Abstr Gen Meet Am Soc Microbiol 101: 95.
114. Sifri, C.D., Begun, J., Ausubel, F.M., and Calderwood, S.B. (2003) Caenorhabditis elegans as a model host for Staphylococcus aureus pathogenesis. Infect Immun 71: 2208-2217.
115. Steyn, A.J., Joseph, J., and Bloom, B.R. (2003) Interaction of the sensor module of Mycobacterium tuberculosis H37Rv KdpD with members of the Lpr family. Mol Microbiol 47: 1075-1089.
116. Su, J., Gong, H., Lai, J., Main, A., and Lu, S. (2009) The potassium transporter Trk and external potassium modulate Salmonella enterica protein secretion and virulence. Infect Immun 77: 667-675.
117. Sutherland, L., Cairney, J., Elmore, M.J., Booth, I.R., and Higgins, C.F. (1986) Osmotic regulation of transcription: induction of the proU betaine transport gene is dependent on accumulation of intracellular potassium. J Bacteriol 168: 805-814.
118. Tan, M.W., Mahajan-Miklos, S., and Ausubel, F.M. (1999a) Killing of Caenorhabditis elegans by Pseudomonas aeruginosa used to model mammalian bacterial pathogenesis. Proc Natl Acad Sci USA 96: 715-720.
119. Tan, M.W., Rahme, L.G., Sternberg, J.A., Tompkins, R.G., and Ausubel, F.M. (1999b) Pseudomonas aeruginosa killing of Caenorhabditis elegans used to identify P. aeruginosa virulence factors. Proc Natl Acad Sci USA 96: 2408-2413.
120. Tenor, J.L., McCormick, B.A., Ausubel, F.M., and Aballay, A. (2004) Caenorhabditis elegans-based screen identifies Salmonella virulence factors required for conserved host-pathogen interactions. Curr Biol 14: 1018-1024.
121. Timmons, L., Court, D.L., and Fire, A. (2001) Ingestion of bacterially expressed dsRNAs can produce specific and potent genetic interference in Caenorhabditis elegans. Gene 263: 103-112.
122. Tu, X., Latifi, T., Bougdour, A., Gottesman, S., and Groisman, E.A. (2006) The PhoP/PhoQ two-component system stabilizes the alternative sigma factor RpoS in Salmonella enterica. Proc Natl Acad Sci USA 103: 13503-13508.
123. Vaara, M. (1992) Agents that increase the permeability of the outer membrane. Microbiol Rev 56: 395-411.
124. Valdivia, R.H., and Falkow, S. (1996) Bacterial genetics by flow cytometry: rapid isolation of Salmonella typhimurium acid-inducible promoters by differential fluorescence induction. Mol Microbiol 22: 367-378.
125. Vazquez-Torres, A., and Fang, F.C. (2001) Oxygen-dependent anti-Salmonella activity of macrophages. Trends Microbiol 9: 29-33.
126. Vazquez-Torres, A., Jones-Carson, J., Baumler, A.J., Falkow, S., Valdivia, R., Brown, W., etal. (1999) Extraintestinal dissemination of Salmonella by CD18-expressing phagocytes. Nature 401: 804-808.
127. Vazquez-Torres, A., Jones-Carson, J., Mastroeni, P., Ischiropoulos, H., and Fang, F.C. (2000) Antimicrobial actions of the NADPH phagocyte oxidase and inducible nitric oxide synthase in experimental salmonellosis. I. Effects on microbial killing by activated peritoneal macrophages in vitro. J Exp Med 192: 227-236.
128. 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.
129. Voelkner, P., Puppe, W., and Altendorf, K. (1993) Characterization of the KdpD protein, the sensor kinase of the K(+)-translocating Kdp system of Escherichia coli. Eur J Biochem 217: 1019-1026.
130. Walderhaug, M.O., Polarek, J.W., Voelkner, P., Daniel, J.M., Hesse, J.E., Altendorf, K., and Epstein, W. (1992) KdpD and KdpE, proteins that control expression of the kdpABC operon, are members of the two-component sensor-effector class of regulators. J Bacteriol 174: 2152-2159.
131. Wallis, T.S., and Galyov, E.E. (2000) Molecular basis of Salmonella-induced enteritis. Mol Microbiol 36: 997-1005.
132. Waterfield, N.R., Sanchez-Contreras, M., Eleftherianos, I., Dowling, A., Yang, G., Wilkinson, P., etal. (2008) Rapid Virulence Annotation (RVA): identification of virulence factors using a bacterial genome library and multiple invertebrate hosts. Proc Natl Acad Sci USA 105: 15967-15972.
133. Weiss, D.S., Brotcke, A., Henry, T., Margolis, J.J., Chan, K., and Monack, D.M. (2007) In vivo negative selection screen identifies genes required for Francisella virulence. Proc Natl Acad Sci USA 104: 6037-6042.
134. White, A.P., Weljie, A.M., Apel, D., Zhang, P., Shaykhutdinov, R., Vogel, H.J., and Surette, M.G. (2010) A global metabolic shift is linked to Salmonella multicellular development. PLoS ONE 5: e11814.
135. Wood, M.W., Jones, M.A., Watson, P.R., Hedges, S., Wallis, T.S., and Galyov, E.E. (1998) Identification of a pathogenicity island required for Salmonella enteropathogenicity. Mol Microbiol 29: 883-891.
136. Xue, T., You, Y., Hong, D., Sun, H., and Sun, B. (2011) The Staphylococcus aureus KdpDE two-component system couples extracellular K+ sensing and Agr signaling to infection programming. Infect Immun 79: 2154-2167.
137. Zimmann, P., Puppe, W., and Altendorf, K. (1995) Membrane topology analysis of the sensor kinase KdpD of Escherichia coli. J Biol Chem 270: 28282-28288.