Signal-specific temporal response by the SalmonellaPhoP/PhoQ regulatory system

Molecular Microbiology

Volumn 91, Issue 1, 2014, Pages 135-144

  Park, Sun Yang ^a,b,c   Groisman, Eduardo A ^a,b,c  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^c YALE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; POLYMYXIN B; POLYPEPTIDE ANTIBIOTIC AGENT; PROTEIN MGTA; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR PHOP; TRANSCRIPTION FACTOR PHOQ; UNCLASSIFIED DRUG; ADENOSINE TRIPHOSPHATASE; C18G PEPTIDE; CARRIER PROTEIN; MAGNESIUM; MGTA PROTEIN, BACTERIA; PEPTIDE; PHOP PROTEIN, BACTERIA; PHOQ PROTEIN, BACTERIA;

ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL GROWTH; BACTERIAL STRAIN; CONTROLLED STUDY; ENZYME ACTIVATION; HEAT TOLERANCE; NONHUMAN; OPEN READING FRAME; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; SALMONELLA TYPHIMURIUM; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; BIOLOGICAL MODEL; CYTOPLASM; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PH; SALMONELLA ENTERICA SUBSP. ENTERICA SEROVAR TYPHIMURIUM; TIME;

SALMONELLA ENTERICA SUBSP. ENTERICA SEROVAR TYPHIMURIUM;

ADENOSINE TRIPHOSPHATASES; BACTERIAL PROTEINS; DRUG RESISTANCE, BACTERIAL; GENE EXPRESSION REGULATION, BACTERIAL; HYDROGEN-ION CONCENTRATION; MAGNESIUM; MEMBRANE TRANSPORT PROTEINS; MODELS, BIOLOGICAL; PEPTIDES; PERIPLASM; POLYMYXIN B; SALMONELLA TYPHIMURIUM; TIME FACTORS;

EID: 84891147511     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.12449     Document Type: Article

References (50)

1. Bader, M.W., Sanowar, S., Daley, M.E., Schneider, A.R., Cho, U., Xu, W., etal. (2005) Recognition of antimicrobial peptides by a bacterial sensor kinase. Cell 122: 461-472.
2. Barbieri, C.M., and Stock, A.M. (2008) Universally applicable methods for monitoring response regulator aspartate phosphorylation both in vitro and in vivo using Phos-tag-based reagents. Anal Biochem 376: 73-82.
3. Battesti, A., Majdalani, N., and Gottesman, S. (2011) The RpoS-mediated general stress response in Escherichia coli. Annu Rev Microbiol 65: 189-213.
4. Blanc-Potard, A.B., and Groisman, E.A. (1997) The Salmonella selC locus contains a pathogenicity island mediating intramacrophage survival. EMBO J 16: 5376-5385.
5. Boulanger, A., Chen, Q., Hinton, D.M., and Stibitz, S. (2013) In vivo phosphorylation dynamics of the Bordetella pertussis virulence-controlling response regulator BvgA. Mol Microbiol 88: 156-172.
6. 2+ regulation of the sensor protein PhoQ in Salmonella. J Biol Chem 275: 22948-22954.
7. Chamnongpol, S., and Groisman, E.A. (2000) Acetyl phosphate-dependent activation of a mutant PhoP response regulator that functions independently of its cognate sensor kinase. J Mol Biol 300: 291-305.
8. 2+ sensor PhoQ of Salmonella enterica. J Mol Biol 325: 795-807.
9. Choi, E., Groisman, E.A., and Shin, D. (2009) Activated by different signals, the PhoP/PhoQ two-component system differentially regulates metal uptake. J Bacteriol 191: 7174-7181.
10. Cotter, P.A., and Jones, A.M. (2003) Phosphorelay control of virulence gene expression in Bordetella. Trends Microbiol 11: 367-373.
11. 2+ transporter MgtA from Salmonella enterica. J Bacteriol 192: 604-607.
12. 2. Cell 125: 71-84.
13. 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.
14. Fujita, M., Gonzalez-Pastor, J.E., and Losick, R. (2005) High- and low-threshold genes in the Spo0A regulon of Bacillus subtilis. J Bacteriol 187: 1357-1368.
15. 2+ as an extracellular signal: environmental regulation of Salmonella virulence. Cell 84: 165-174.
16. Groisman, E.A. (2001) The pleiotropic two-component regulatory system PhoP-PhoQ. J Bacteriol 183: 1835-1842.
17. Groisman, E.A., and Mouslim, C. (2006) Sensing by bacterial regulatory systems in host and non-host environments. Nat Rev Microbiol 4: 705-709.
18. 2+ homeostasis, transport, and virulence. Annu Rev Genet 47: 643-664.
19. Gunn, J.S., Alpuche-Aranda, C.M., Loomis, W.P., Belden, W.J., and Miller, S.I. (1995) Characterization of the Salmonella typhimurium pagC/pagD chromosomal region. J Bacteriol 177: 5040-5047.
20. Gunn, J.S., Belden, W.J., and Miller, S.I. (1998) Identification of PhoP-PhoQ activated genes within a duplicated region of the Salmonella typhimurium chromosome. Microb Pathog 25: 77-90.
21. Hollands, K., Proshkin, S., Sklyarova, S., Epshtein, V., Mironov, A., Nudler, E., and Groisman, E.A. (2012) Riboswitch control of Rho-dependent transcription termination. Proc Natl Acad Sci USA 109: 5376-5381.
22. Kalir, S., McClure, J., Pabbaraju, K., Southward, C., Ronen, M., Leibler, S., etal. (2001) Ordering genes in a flagella pathway by analysis of expression kinetics from living bacteria. Science 292: 2080-2083.
23. Kato, A., Mitrophanov, A.Y., and Groisman, E.A. (2007) A connector of two-component regulatory systems promotes signal amplification and persistence of expression. Proc Natl Acad Sci USA 104: 12063-12068.
24. Kato, A., Chen, H.D., Latifi, T., and Groisman, E.A. (2012) Reciprocal control between a bacterium's regulatory system and the modification status of its lipopolysaccharide. Mol Cell 47: 897-908.
25. 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.
26. Kroos, L. (2007) The Bacillus and Myxococcus developmental networks and their transcriptional regulators. Annu Rev Genet 41: 13-39.
27. Kunkel, B., Kroos, L., Poth, H., Youngman, P., and Losick, R. (1989) Temporal and spatial control of the mother-cell regulatory gene spoIIID of Bacillus subtilis. Genes Dev 3: 1735-1744.
28. Kutsukake, K., Ohya, Y., and Iino, T. (1990) Transcriptional analysis of the flagellar regulon of Salmonella typhimurium. J Bacteriol 172: 741-747.
29. Lippa, A.M., and Goulian, M. (2009) Feedback inhibition in the PhoQ/PhoP signaling system by a membrane peptide. PLoS Genet 5: e1000788.
30. McAdams, H.H., and Shapiro, L. (2003) A bacterial cell-cycle regulatory network operating in time and space. Science 301: 1874-1877.
31. 2+ transport proteins enhances the survival of Salmonella enterica at high temperature. Proc Natl Acad Sci USA 106: 17522-17527.
32. Park, S.Y., Cromie, M.J., Lee, E.J., and Groisman, E.A. (2010) A bacterial mRNA leader that employs different mechanisms to sense disparate intracellular signals. Cell 142: 737-748.
33. Perez, J.C., and Groisman, E.A. (2007) Acid pH activation of the PmrA/PmrB two-component regulatory system of Salmonella enterica. Mol Microbiol 63: 283-293.
34. 2+ homeostasis. PLoS Genet 5: e1000428.
35. Prost, L.R., Daley, M.E., Le Sage, V., Bader, M.W., Le Moual, H., Klevit, R.E., and Miller, S.I. (2007) Activation of the bacterial sensor kinase PhoQ by acidic pH. Mol Cell 26: 165-174.
36. Shi, Y., Cromie, M.J., Hsu, F.F., Turk, J., and Groisman, E.A. (2004) PhoP-regulated Salmonella resistance to the antimicrobial peptides magainin 2 and polymyxin B. Mol Microbiol 53: 229-241.
37. Shin, D., and Groisman, E.A. (2005) Signal-dependent binding of the response regulators PhoP and PmrA to their target promoters in vivo. J Biol Chem 280: 4089-4094.
38. Shin, D., Lee, E.J., Huang, H., and Groisman, E.A. (2006) A positive feedback loop promotes transcription surge that jump-starts Salmonella virulence circuit. Science 314: 1607-1609.
39. 2+ transporter from Bacillus firmus OF4. J Bacteriol 177: 1233-1238.
40. 2+ transport locus of Salmonella typhimurium encodes a P-type ATPase. J Biol Chem 266: 815-823.
41. Soncini, F.C., Vescovi, E.G., and Groisman, E.A. (1995) Transcriptional autoregulation of the Salmonella typhimurium phoPQ operon. J Bacteriol 177: 4364-4371.
42. 2+ in a manner similar to that of the mgtB P-type ATPase. J Bacteriol 177: 2654-2662.
43. Tetsch, L., and Jung, K. (2009) How are signals transduced across the cytoplasmic membrane? Transport proteins as transmitter of information. Amino Acids 37: 467-477.
44. Tu, Y., Shimizu, T.S., and Berg, H.C. (2008) Modeling the chemotactic response of Escherichia coli to time-varying stimuli. Proc Natl Acad Sci USA 105: 14855-14860.
45. 2+. J Biol Chem 272: 1440-1443.
46. Wayne, K.J., Li, S., Kazmierczak, K.M., Tsui, H.C., and Winkler, M.E. (2012) Involvement of WalK (VicK) phosphatase activity in setting WalR (VicR) response regulator phosphorylation level and limiting cross-talk in Streptococcus pneumoniae D39 cells. Mol Microbiol 86: 645-660.
47. 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.
48. Yeo, W.S., Zwir, I., Huang, H.V., Shin, D., Kato, A., and Groisman, E.A. (2012) Intrinsic negative feedback governs activation surge in two-component regulatory systems. Mol Cell 45: 409-421.
49. 2+ facilitates leader peptide translation to induce riboswitch-mediated transcription termination. EMBO J 30: 1485-1496.
50. Zwir, I., Latifi, T., Perez, J.C., Huang, H., and Groisman, E.A. (2012) The promoter architectural landscape of the Salmonella PhoP regulon. Mol Microbiol 84: 463-485.