Cytolocalization of the PhoP response regulator in Salmonella enterica: Modulation by extracellular Mg2+ and by the SCV environment

Molecular Microbiology

Volumn 70, Issue 2, 2008, Pages 479-493

  Sciara, Mariela I ^a   Spagnuolo, Carla ^b   Jares Erijman, Elizabeth ^b   García Véscovi, Eleonora ^a  

^a UNIVERSIDAD NACIONAL DE ROSARIO   (Argentina)

^b DEPARTAMENTO DE QUÍMICA ORGÁNICA   (Argentina)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; MAGNESIUM ION; MUTANT PROTEIN; PHOP PROTEIN; PROTEIN PHOQ; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL VACUOLE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOPLASM; FLUORESCENCE MICROSCOPY; IN VITRO STUDY; MACROPHAGE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; SALMONELLA ENTERICA; TRANSCRIPTION INITIATION;

ANIMALS; BACTERIAL PROTEINS; CELL LINE; CYTOPLASM; MACROPHAGES; MAGNESIUM; MICE; MICROSCOPY, FLUORESCENCE; SALMONELLA ENTERICA;

BACTERIA (MICROORGANISMS); SALMONELLA; SALMONELLA ENTERICA; STRAWBERRY CRINKLE VIRUS;

EID: 52649121903     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2008.06427.x     Document Type: Article

References (69)

1. Adams, S.R., Campbell, R.E., Gross, L.A., Martin, B.R., Walkup, G.K., Yao, Y., et al. (2002) New biarsenical ligands and tetracysteine motifs for protein labeling in vitro and in vivo: synthesis and biological applications. J Am Chem Soc 124 : 6063 6076.
2. Alpuche Aranda, C.M., Swanson, J.A., Loomis, W.P. Miller, S.I. (1992) Salmonella typhimurium activates virulence gene transcription within acidified macrophage phagosomes. Proc Natl Acad Sci USA 89 : 10079 10083.
3. Alpuche-Aranda, C.M., Racoosin, E.L., Swanson, J.A. Miller, S.I. (1994) Salmonella stimulates macrophage macropinocytosis and persists within spacious phagosomes. J Exp Med 179 : 601 608.
4. Bader, M.W., Navarre, W.W., Shiau, W., Nikaido, H., Frye, J.G., McClelland, M., et al. (2003) Regulation of Salmonella typhimurium virulence gene expression by cationic antimicrobial peptides. Mol Microbiol 50 : 219 230.
5. Bajaj, V., Lucas, R.L., Hwang, C. Lee, C.A. (1996) Co-ordinate regulation of Salmonella typhimurium invasion genes by environmental and regulatory factors is mediated by control of hilA expression. Mol Microbiol 22 : 703 714.
6. Banno, S., Shiomi, D., Homma, M. Kawagishi, I. (2004) Targeting of the chemotaxis methylesterase/deamidase CheB to the polar receptor-kinase cluster in an Escherichia coli cell. Mol Microbiol 53 : 1051 1063.
7. Batchelor, E. Goulian, M. (2006) Imaging OmpR localization in Escherichia coli. Mol Microbiol 59 : 1767 1778.
8. Bearson, B.L., Wilson, L. Foster, J.W. (1998) A low pH-inducible, PhoPQ-dependent acid tolerance response protects Salmonella typhimurium against inorganic acid stress. J Bacteriol 180 : 2409 2417.
9. Boyd, J.M. (2000) Localization of the histidine kinase PilS to the poles of Pseudomonas aeruginosa and identification of a localization domain. Mol Microbiol 36 : 153 162.
10. 2+ regulation of the sensor protein PhoQ in Salmonella. J Biol Chem 275 : 22948 22954.
11. 2+-sensor in the recognition of its partner PhoP. J Biol Chem 278 : 23579 23585.
12. Chang, H.C., Kaiser, C.M., Hartl, F.U. Barral, J.M. (2005) De novo folding of GFP fusion proteins: high efficiency in eukaryotes but not in bacteria. J Mol Biol 353 : 397 409.
13. Cherepanov, P.P. Wackernagel, W. (1995) Gene disruption in Escherichia coli: TcR and KmR cassettes with the option of Flp-catalyzed excision of the antibiotic-resistance determinant. Gene 158 : 9 14.
14. Collier, J. Shapiro, L. (2007) Spatial complexity and control of a bacterial cell cycle. Curr Opin Biotechnol 18 : 333 340.
15. Datsenko, K.A. 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.
16. Davis, R.W., Bolstein, D. Roth, J.R. (1980) Advanced Bacterial Genetics. Cold Spring Harbor, NY : Cold Spring Harbor Laboratory Press.
17. De Groote, M.A., Ochsner, U.A., Shiloh, M.U., Nathan, C., McCord, J.M., Dinauer, M.C., et al. (1997) Periplasmic superoxide dismutase protects Salmonella from products of phagocyte NADPH-oxidase and nitric oxide synthase. Proc Natl Acad Sci USA 94 : 13997 14001.
18. Elowitz, M.B., Levine, A.J., Siggia, E.D. Swain, P.S. (2002) Stochastic gene expression in a single cell. Science 297 : 1183 1186.
19. Enninga, J., Mounier, J., Sansonetti, P. Tran, V.N. (2005) Secretion of type III effectors into host cells in real time. Nat Methods 2 : 959 965.
20. Flego, D., Marits, R., Eriksson, A.R., Koiv, V., Karlsson, M.B., Heikinheimo, R. Palva, E.T. (2000) A two-component regulatory system, pehR-pehS, controls endopolygalacturonase production and virulence in the plant pathogen Erwinia carotovora subsp. carotovora. Mol Plant Microbe Interact 13 : 447 455.
21. 2+ as an extracellular signal: environmental regulation of Salmonella virulence. Cell 84 : 165 174.
22. 2+. J Biol Chem 272 : 1440 1443.
23. Garvis, S.G., Beuzon, C.R. Holden, D.W. (2001) A role for the PhoP/Q regulon in inhibition of fusion between lysosomes and Salmonella-containing vacuoles in macrophages. Cell Microbiol 3 : 731 744.
24. Goley, E.D., Iniesta, A.A. Shapiro, L. (2007) Cell cycle regulation in Caulobacter: location, location, location. J Cell Sci 120 : 3501 3507.
25. Golubeva, Y.A. Slauch, J.M. (2006) Salmonella enterica serovar Typhimurium periplasmic superoxide dismutase SodCI is a member of the PhoPQ regulon and is induced in macrophages. J Bacteriol 188 : 7853 7861.
26. Griffin, B.A., Adams, S.R., Jones, J. Tsien, R.Y. (2000) Fluorescent labeling of recombinant proteins in living cells with FlAsH. Methods Enzymol 327 : 565 578.
27. 2+ as a regulatory signal. Bioessays 20 : 96 101.
28. Groisman, E.A. Mouslim, C. (2006) Sensing by bacterial regulatory systems in host and non-host environments. Nat Rev Microbiol 4 : 705 709.
29. Groisman, E.A., Chiao, E., Lipps, C.J. Heffron, F. (1989) Salmonella typhimurium phoP virulence gene is a transcriptional regulator. Proc Natl Acad Sci USA 86 : 7077 7081.
30. 2+ environments. J Bacteriol 179 : 7040 7045.
31. Gunn, J.S., Lim, K.B., Krueger, J., Kim, K., Guo, L., Hackett, M. Miller, S.I. (1998) PmrA-PmrB-regulated genes necessary for 4-aminoarabinose lipid A modification and polymyxin resistance. Mol Microbiol 27 : 1171 1182.
32. Guo, L., Lim, K.B., Gunn, J.S., Bainbridge, B., Darveau, R.P., Hackett, M. Miller, S.I. (1997) Regulation of lipid A modifications by Salmonella typhimurium virulence genes phoP-phoQ. Science 276 : 250 253.
33. Hazelbauer, G.L., Falke, J.J. Parkinson, J.S. (2008) Bacterial chemoreceptors: high-performance signaling in networked arrays. Trends Biochem Sci 33 : 9 19.
34. Hensel, M., Shea, J.E., Waterman, S.R., Mundy, R., Nikolaus, T., Banks, G., et al. (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.
35. Hoch, J.A. (2000) Two-component and phosphorelay signal transduction. Curr Opin Microbiol 3 : 165 170.
36. Ignatova, Z. Gierasch, L.M. (2004) Monitoring protein stability and aggregation in vivo by real-time fluorescent labeling. Proc Natl Acad Sci USA 101 : 523 528.
37. Johnson, C.R., Newcombe, J., Thorne, S., Borde, H.A., Eales-Reynolds, L.J., Gorringe, A.R., et al. (2001) Generation and characterization of a PhoP homologue mutant of Neisseria meningitidis. Mol Microbiol 39 : 1345 1355.
38. Kasahara, M., Nakata, A. Shinagawa, H. (1992) Molecular analysis of the Escherichia coli phoP-phoQ operon. J Bacteriol 174 : 492 498.
39. Kentner, D. Sourjik, V. (2006) Spatial organization of the bacterial chemotaxis system. Curr Opin Microbiol 9 : 619 624.
40. Lee, S.W., Jeong, K.S., Han, S.W., Lee, S.E., Phee, B.K., Hahn, T.R. Ronald, P. (2008) The Xanthomonas oryzae pv. oryzae PhoP/Q two-component system is required for AvrXA21 activity, hrpG expression, and virulence. J Bacteriol 190 : 2183 2197.
41. 2+-responsive PhoP-PhoQ regulon in Salmonella enterica. J Bacteriol 185 : 6287 6294.
42. Lejona, S., Castelli, M.E., Cabeza, M.L., Kenney, L.J., Garcia, V.E. Soncini, F.C. (2004) PhoP can activate its target genes in a PhoQ-independent manner. J Bacteriol 186 : 2476 2480.
43. Lybarger, S.R. Maddock, J.R. (2001) Polarity in action: asymmetric protein localization in bacteria. J Bacteriol 183 : 3261 3267.
44. Macfarlane, E.L., Kwasnicka, A., Ochs, M.M. Hancock, R.E. (1999) PhoP-PhoQ homologues in Pseudomonas aeruginosa regulate expression of the outer-membrane protein OprH and polymyxin B resistance. Mol Microbiol 34 : 305 316.
45. Macfarlane, E.L., Kwasnicka, A. Hancock, R.E. (2000) Role of Pseudomonas aeruginosa PhoP-PhoQ in resistance to antimicrobial cationic peptides and aminoglycosides. Microbiology 146 (Part10 2543 2554.
46. Martin-Orozco, N., Touret, N., Zaharik, M.L., Park, E., Kopelman, R., Miller, S., et al. (2006) Visualization of vacuolar acidification-induced transcription of genes of pathogens inside macrophages. Mol Biol Cell 17 : 498 510.
47. Miller, J.H. (1972) Experiments in Molecular Genetics. Cold Spring Harbor, NY : Cold Spring Harbor Laboratory Press.
48. Mo, Y.Y. Mallavia, L.P. (1994) A Coxiella burnetii gene encodes a sensor-like protein. Gene 151 : 185 190.
49. 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.
50. Patel, J.C. Galan, J.E. (2005) Manipulation of the host actin cytoskeleton by Salmonella- all in the name of entry. Curr Opin Microbiol 8 : 10 15.
51. Perez, E., Samper, S., Bordas, Y., Guilhot, C., Gicquel, B. Martin, C. (2001) An essential role for phoP in Mycobacterium tuberculosis virulence. Mol Microbiol 41 : 179 187.
52. Prost, L.R. Miller, S.I. (2008) The Salmonellae PhoQ sensor: mechanisms of detection of phagosome signals. Cell Microbiol 10 : 576 582.
53. Romantsov, T., Helbig, S., Culham, D.E., Gill, C., Stalker, L. Wood, J.M. (2007) Cardiolipin promotes polar localization of osmosensory transporter ProP in Escherichia coli. Mol Microbiol 64 : 1455 1465.
54. Sanchez, A. Kondev, J. (2008) Transcriptional control of noise in gene expression. Proc Natl Acad Sci USA 105 : 5081 5086.
55. Shapiro, L., McAdams, H.H. Losick, R. (2002) Generating and exploiting polarity in bacteria. Science 298 : 1942 1946.
56. Soncini, F.C. Groisman, E.A. (1996) Two-component regulatory systems can interact to process multiple environmental signals. J Bacteriol 178 : 6796 6801.
57. Soncini, F.C., García Véscovi, E. Groisman, E.A. (1995) Transcriptional autoregulation of the Salmonella typhimurium phoPQ operon. J Bacteriol 177 : 4364 4371.
58. Soncini, F.C., García Véscovi, 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.
59. Sourjik, V. (2004) Receptor clustering and signal processing in E. coli chemotaxis. Trends Microbiol 12 : 569 576.
60. Sourjik, V. Berg, H.C. (2000) Localization of components of the chemotaxis machinery of Escherichia coli using fluorescent protein fusions. Mol Microbiol 37 : 740 751.
61. Spagnuolo, C.C., Vermeij, R.J. Jares-Erijman, E.A. (2006) Improved photostable FRET-competent biarsenical-tetracysteine probes based on fluorinated fluoresceins. J Am Chem Soc 128 : 12040 12041.
62. Teng, F., Wang, L., Singh, K.V., Murray, B.E. Weinstock, G.M. (2002) Involvement of PhoP-PhoS homologs in Enterococcus faecalis virulence. Infect Immun 70 : 1991 1996.
63. Thiem, S., Kentner, D. Sourjik, V. (2007) Positioning of chemosensory clusters in E. coli and its relation to cell division. EMBO J 26 : 1615 1623.
64. Vanengelenburg, S.B. Palmer, A.E. (2008) Quantification of real-time Salmonella effector type III secretion kinetics reveals differential secretion rates for SopE2 and SptP. Chem Biol 15 : 619 628.
65. Viollier, P.H. Shapiro, L. (2004) Spatial complexity of mechanisms controlling a bacterial cell cycle. Curr Opin Microbiol 7 : 572 578.
66. Wolanin, P.M., Thomason, P.A. Stock, J.B. (2002) Histidine protein kinases: key signal transducers outside the animal kingdom. Genome Biol 3 : REVIEWS3013.
67. Wren, B.W., Olsen, A.L., Stabler, R. Li, S.R. (1995) Genetic analysis of phoP and ompR from Yersinia enterocolitica, Yersinia pseudotuberculosis and Yersinia pestis. Contrib Microbiol Immunol 13 : 318 320.
68. Zhou, D., Mooseker, M.S. Galan, J.E. (1999) Role of the S. typhimurium actin-binding protein SipA in bacterial internalization. Science 283 : 2092 2095.
69. Zwir, I., Shin, D., Kato, A., Nishino, K., Latifi, T., Solomon, F., et al. (2005) Dissecting the PhoP regulatory network of Escherichia coli and Salmonella enterica. Proc Natl Acad Sci USA 102 : 2862 2867.