This Article
Right arrow Full Text
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrowReprints and Permissions
Right arrow Copyright Information
Right arrow Books from ASM Press
Right arrow MicrobeWorld
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Guina, T.
Right arrow Articles by Miller, S. I.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Guina, T.
Right arrow Articles by Miller, S. I.

 Previous Article  |  Next Article 

Journal of Bacteriology, July 2000, p. 4077-4086, Vol. 182, No. 14
0021-9193/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.

A PhoP-Regulated Outer Membrane Protease of Salmonella enterica Serovar Typhimurium Promotes Resistance to Alpha-Helical Antimicrobial Peptides

Tina Guina,1 Eugene C. Yi,2 Houle Wang,2,dagger Murray Hackett,2 and Samuel I. Miller1,3,*

Departments of Microbiology,1 Medicine,3 and Medicinal Chemistry,2 University of Washington, Seattle, Washington 98195

Received 7 March 2000/Accepted 2 May 2000

The outer membrane protein contents of Salmonella enterica serovar Typhimurium strains with PhoP/PhoQ regulon mutations were compared by two-dimensional gel electrophoresis. At least 26 species of outer membrane proteins (OMPs) were identified as being regulated by PhoP/PhoQ activation. One PhoP/PhoQ-activated OMP was identified by semiautomated tandem mass spectrometry coupled with electronic database searching as PgtE, a member of the Escherichia coli OmpT and Yersinia pestis Pla family of outer membrane proteases. Salmonella PgtE expression promoted resistance to alpha-helical cationic antimicrobial peptides (alpha -CAMPs). Strains expressing PgtE cleaved C18G, an 18-residue alpha -CAMP present in culture medium, indicating that protease activity is likely to be the mechanism of OmpT-mediated resistance to alpha -CAMPs. PhoP/PhoQ did not regulate the transcription or export of PgtE, indicating that another PhoP/PhoQ-dependent mechanism is required for PgtE outer membrane localization. PgtE is a posttranscriptionally regulated component of the PhoP/PhoQ regulon that contributes to Salmonella resistance to innate immunity.


* Corresponding author. Mailing address: Dept. of Microbiology, University of Washington, HSB K-140, Box 357710, Seattle, WA 98195. Phone: (206) 616-5107. Fax: (206) 616-4295. E-mail: millersi{at}u.washington.edu.

dagger Present address: Bruker Daltonics, Billerica, MA 01821.


Journal of Bacteriology, July 2000, p. 4077-4086, Vol. 182, No. 14
0021-9193/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.



This article has been cited by other articles:

  • Pilonieta, M. C., Erickson, K. D., Ernst, R. K., Detweiler, C. S. (2009). A Protein Important for Antimicrobial Peptide Resistance, YdeI/OmdA, Is in the Periplasm and Interacts with OmpD/NmpC. J. Bacteriol. 191: 7243-7252 [Abstract] [Full Text]  
  • Bourret, T. J., Song, M., Vazquez-Torres, A. (2009). Codependent and Independent Effects of Nitric Oxide-Mediated Suppression of PhoPQ and Salmonella Pathogenicity Island 2 on Intracellular Salmonella enterica Serovar Typhimurium Survival. Infect. Immun. 77: 5107-5115 [Abstract] [Full Text]  
  • Adams, M. D., Nickel, G. C., Bajaksouzian, S., Lavender, H., Murthy, A. R., Jacobs, M. R., Bonomo, R. A. (2009). Resistance to Colistin in Acinetobacter baumannii Associated with Mutations in the PmrAB Two-Component System. Antimicrob. Agents Chemother. 53: 3628-3634 [Abstract] [Full Text]  
  • Haiko, J., Kukkonen, M., Ravantti, J. J., Westerlund-Wikstrom, B., Korhonen, T. K. (2009). The Single Substitution I259T, Conserved in the Plasminogen Activator Pla of Pandemic Yersinia pestis Branches, Enhances Fibrinolytic Activity. J. Bacteriol. 191: 4758-4766 [Abstract] [Full Text]  
  • Thwaite, J. E., Humphrey, S., Fox, M. A., Savage, V. L., Laws, T. R., Ulaeto, D. O., Titball, R. W., Atkins, H. S. (2009). The cationic peptide magainin II is antimicrobial for Burkholderia cepacia-complex strains. J Med Microbiol 58: 923-929 [Abstract] [Full Text]  
  • Haiko, J., Suomalainen, M., Ojala, T., Lahteenmaki, K., Korhonen, T. K. (2009). Invited review: Breaking barriers -- attack on innate immune defences by omptin surface proteases of enterobacterial pathogens. Innate Immunity 15: 67-80 [Abstract]  
  • Stromstedt, A. A., Pasupuleti, M., Schmidtchen, A., Malmsten, M. (2009). Evaluation of Strategies for Improving Proteolytic Resistance of Antimicrobial Peptides by Using Variants of EFK17, an Internal Segment of LL-37. Antimicrob. Agents Chemother. 53: 593-602 [Abstract] [Full Text]  
  • Yun, T. H., Cott, J. E., Tapping, R. I., Slauch, J. M., Morrissey, J. H. (2009). Proteolytic inactivation of tissue factor pathway inhibitor by bacterial omptins. Blood 113: 1139-1148 [Abstract] [Full Text]  
  • Llobet, E., Tomas, J. M., Bengoechea, J. A (2008). Capsule polysaccharide is a bacterial decoy for antimicrobial peptides. Microbiology 154: 3877-3886 [Abstract] [Full Text]  
  • Pranting, M., Negrea, A., Rhen, M., Andersson, D. I. (2008). Mechanism and Fitness Costs of PR-39 Resistance in Salmonella enterica Serovar Typhimurium LT2. Antimicrob. Agents Chemother. 52: 2734-2741 [Abstract] [Full Text]  
  • Galvan, E. M., Lasaro, M. A. S., Schifferli, D. M. (2008). Capsular Antigen Fraction 1 and Pla Modulate the Susceptibility of Yersinia pestis to Pulmonary Antimicrobial Peptides Such as Cathelicidin. Infect. Immun. 76: 1456-1464 [Abstract] [Full Text]  
  • Schmidt, R. L., Trejo, T. R., Plummer, T. B., Platt, J. L., Tang, A. H. (2008). Infection-induced proteolysis of PGRP-LC controls the IMD activation and melanization cascades in Drosophila. FASEB J. 22: 918-929 [Abstract] [Full Text]  
  • Eswarappa, S. M., Panguluri, K. K., Hensel, M., Chakravortty, D. (2008). The yejABEF operon of Salmonella confers resistance to antimicrobial peptides and contributes to its virulence. Microbiology 154: 666-678 [Abstract] [Full Text]  
  • Jose, J., Meyer, T. F. (2007). The Autodisplay Story, from Discovery to Biotechnical and Biomedical Applications. Microbiol. Mol. Biol. Rev. 71: 600-619 [Abstract] [Full Text]  
  • Murata, T., Tseng, W., Guina, T., Miller, S. I., Nikaido, H. (2007). PhoPQ-Mediated Regulation Produces a More Robust Permeability Barrier in the Outer Membrane of Salmonella enterica Serovar Typhimurium. J. Bacteriol. 189: 7213-7222 [Abstract] [Full Text]  
  • Masi, M., Vuong, P., Humbard, M., Malone, K., Misra, R. (2007). Initial Steps of Colicin E1 Import across the Outer Membrane of Escherichia coli. J. Bacteriol. 189: 2667-2676 [Abstract] [Full Text]  
  • Alaniz, R. C., Cummings, L. A., Bergman, M. A., Rassoulian-Barrett, S. L., Cookson, B. T. (2006). Salmonella typhimurium Coordinately Regulates FliC Location and Reduces Dendritic Cell Activation and Antigen Presentation to CD4+ T cells. J. Immunol. 177: 3983-3993 [Abstract] [Full Text]  
  • Thwaite, J. E., Hibbs, S., Titball, R. W., Atkins, T. P. (2006). Proteolytic Degradation of Human Antimicrobial Peptide LL-37 by Bacillus anthracis May Contribute to Virulence.. Antimicrob. Agents Chemother. 50: 2316-2322 [Abstract] [Full Text]  
  • Elahi, S., Buchanan, R. M., Attah-Poku, S., Townsend, H. G. G., Babiuk, L. A., Gerdts, V. (2006). The Host Defense Peptide Beta-Defensin 1 Confers Protection against Bordetella pertussis in Newborn Piglets. Infect. Immun. 74: 2338-2352 [Abstract] [Full Text]  
  • Venkatesh, B., Babujee, L., Liu, H., Hedley, P., Fujikawa, T., Birch, P., Toth, I., Tsuyumu, S. (2006). The Erwinia chrysanthemi 3937 PhoQ Sensor Kinase Regulates Several Virulence Determinants.. J. Bacteriol. 188: 3088-3098 [Abstract] [Full Text]  
  • Faucher, Séb. P., Porwollik, S., Dozois, C. M., McClelland, M., Daigle, F. (2006). Transcriptome of Salmonella enterica serovar Typhi within macrophages revealed through the selective capture of transcribed sequences. Proc. Natl. Acad. Sci. USA 103: 1906-1911 [Abstract] [Full Text]  
  • Martin-Orozco, N., Touret, N., Zaharik, M. L., Park, E., Kopelman, R., Miller, S., Finlay, B. B., Gros, P., Grinstein, S. (2006). Visualization of Vacuolar Acidification-induced Transcription of Genes of Pathogens inside Macrophages. Mol. Biol. Cell 17: 498-510 [Abstract] [Full Text]  
  • Merighi, M., Ellermeier, C. D., Slauch, J. M., Gunn, J. S. (2005). Resolvase-In Vivo Expression Technology Analysis of the Salmonella enterica Serovar Typhimurium PhoP and PmrA Regulons in BALB/c Mice. J. Bacteriol. 187: 7407-7416 [Abstract] [Full Text]  
  • Pietila, T. E., Veckman, V., Kyllonen, P., Lahteenmaki, K., Korhonen, T. K., Julkunen, I. (2005). Activation, cytokine production, and intracellular survival of bacteria in Salmonella-infected human monocyte-derived macrophages and dendritic cells. J. Leukoc. Biol. 78: 909-920 [Abstract] [Full Text]  
  • Tzeng, Y.-L., Ambrose, K. D., Zughaier, S., Zhou, X., Miller, Y. K., Shafer, W. M., Stephens, D. S. (2005). Cationic Antimicrobial Peptide Resistance in Neisseria meningitidis. J. Bacteriol. 187: 5387-5396 [Abstract] [Full Text]  
  • Newcombe, J., Jeynes, J. C., Mendoza, E., Hinds, J., Marsden, G. L., Stabler, R. A., Marti, M., McFadden, J. J. (2005). Phenotypic and Transcriptional Characterization of the Meningococcal PhoPQ System, a Magnesium-Sensing Two-Component Regulatory System That Controls Genes Involved in Remodeling the Meningococcal Cell Surface. J. Bacteriol. 187: 4967-4975 [Abstract] [Full Text]  
  • Cummings, L. A., Barrett, S. L. R., Wilkerson, W. D., Fellnerova, I., Cookson, B. T. (2005). FliC-Specific CD4+ T Cell Responses Are Restricted by Bacterial Regulation of Antigen Expression. J. Immunol. 174: 7929-7938 [Abstract] [Full Text]  
  • Bishop, R. E., Kim, S.-H., El Zoeiby, A. (2005). Role of lipid A palmitoylation in bacterial pathogenesis. Innate Immunity 11: 174-180 [Abstract]  
  • Zhang, H., Morikawa, K., Ohta, T., Kato, Y. (2005). In vitro resistance to the CS{alpha}{beta}-type antimicrobial peptide ASABF- is conferred by overexpression of sigma factor sigB in Staphylococcus aureus. J Antimicrob Chemother 55: 686-691 [Abstract] [Full Text]  
  • Bergman, M. A., Cummings, L. A., Barrett, S. L. R., Smith, K. D., Lara, J. C., Aderem, A., Cookson, B. T. (2005). CD4+ T Cells and Toll-Like Receptors Recognize Salmonella Antigens Expressed in Bacterial Surface Organelles. Infect. Immun. 73: 1350-1356 [Abstract] [Full Text]  
  • Mason, K. M., Munson, R. S. Jr., Bakaletz, L. O. (2005). A Mutation in the sap Operon Attenuates Survival of Nontypeable Haemophilus influenzae in a Chinchilla Model of Otitis Media. Infect. Immun. 73: 599-608 [Abstract] [Full Text]  
  • Campos, M. A., Vargas, M. A., Regueiro, V., Llompart, C. M., Alberti, S., Bengoechea, J. A. (2004). Capsule Polysaccharide Mediates Bacterial Resistance to Antimicrobial Peptides. Infect. Immun. 72: 7107-7114 [Abstract] [Full Text]  
  • McCarter, J. D., Stephens, D., Shoemaker, K., Rosenberg, S., Kirsch, J. F., Georgiou, G. (2004). Substrate Specificity of the Escherichia coli Outer Membrane Protease OmpT. J. Bacteriol. 186: 5919-5925 [Abstract] [Full Text]  
  • Derzelle, S., Turlin, E., Duchaud, E., Pages, S., Kunst, F., Givaudan, A., Danchin, A. (2004). The PhoP-PhoQ Two-Component Regulatory System of Photorhabdus luminescens Is Essential for Virulence in Insects. J. Bacteriol. 186: 1270-1279 [Abstract] [Full Text]  
  • Newcombe, J., Eales-Reynolds, L.-J., Wootton, L., Gorringe, A. R., Funnell, S. G. P., Taylor, S. C., McFadden, J. J. (2004). Infection with an Avirulent phoP Mutant of Neisseria meningitidis Confers Broad Cross-Reactive Immunity. Infect. Immun. 72: 338-344 [Abstract] [Full Text]  
  • Nikaido, H. (2003). Molecular Basis of Bacterial Outer Membrane Permeability Revisited. Microbiol. Mol. Biol. Rev. 67: 593-656 [Abstract] [Full Text]  
  • Lejona, S., Aguirre, A., Cabeza, M. L., Vescovi, E. G., Soncini, F. C. (2003). Molecular Characterization of the Mg2+-Responsive PhoP-PhoQ Regulon in Salmonella enterica. J. Bacteriol. 185: 6287-6294 [Abstract] [Full Text]  
  • Gibson, R. L., Burns, J. L., Ramsey, B. W. (2003). Pathophysiology and Management of Pulmonary Infections in Cystic Fibrosis. Am. J. Respir. Crit. Care Med. 168: 918-951 [Abstract] [Full Text]  
  • Zhou, L., Lei, X.-H., Bochner, B. R., Wanner, B. L. (2003). Phenotype MicroArray Analysis of Escherichia coli K-12 Mutants with Deletions of All Two-Component Systems. J. Bacteriol. 185: 4956-4972 [Abstract] [Full Text]  
  • Chen, H., Schifferli, D. M. (2003). Construction, Characterization, and Immunogenicity of an Attenuated Salmonella enterica Serovar Typhimurium pgtE Vaccine Expressing Fimbriae with Integrated Viral Epitopes from the spiC Promoter. Infect. Immun. 71: 4664-4673 [Abstract] [Full Text]  
  • Bell, G., Gouyon, P.-H. (2003). Arming the enemy: the evolution of resistance to self-proteins. Microbiology 149: 1367-1375 [Abstract] [Full Text]  
  • Wiese, A., Gutsmann, T., Seydel, U. (2003). Review: Towards antibacterial strategies: studies on the mechanisms of interaction between antibacterial peptides and model membranes. Innate Immunity 9: 67-84 [Abstract]  
  • Guina, T., Purvine, S. O., Yi, E. C., Eng, J., Goodlett, D. R., Aebersold, R., Miller, S. I. (2003). Quantitative proteomic analysis indicates increased synthesis of a quinolone by Pseudomonas aeruginosa isolates from cystic fibrosis airways. Proc. Natl. Acad. Sci. USA 100: 2771-2776 [Abstract] [Full Text]  
  • Yeaman, M. R., Yount, N. Y. (2003). Mechanisms of Antimicrobial Peptide Action and Resistance. Pharmacol. Rev. 55: 27-55 [Abstract] [Full Text]  
  • Ulvatne, H., Haukland, H. H., Samuelsen, O., Kramer, M., Vorland, L. H. (2002). Proteases in Escherichia coli and Staphylococcus aureus confer reduced susceptibility to lactoferricin B. J Antimicrob Chemother 50: 461-467 [Abstract] [Full Text]  
  • Brodsky, I. E., Ernst, R. K., Miller, S. I., Falkow, S. (2002). mig-14 Is a Salmonella Gene That Plays a Role in Bacterial Resistance to Antimicrobial Peptides. J. Bacteriol. 184: 3203-3213 [Abstract] [Full Text]  
  • Hansen-Wester, I., Hensel, M. (2002). Genome-Based Identification of Chromosomal Regions Specific for Salmonella spp.. Infect. Immun. 70: 2351-2360 [Abstract] [Full Text]  
  • Matsunaga, J., Young, T. A., Barnett, J. K., Barnett, D., Bolin, C. A., Haake, D. A. (2002). Novel 45-Kilodalton Leptospiral Protein That Is Processed to a 31-Kilodalton Growth-Phase-Regulated Peripheral Membrane Protein. Infect. Immun. 70: 323-334 [Abstract] [Full Text]  
  • McCoy, A. J., Liu, H., Falla, T. J., Gunn, J. S. (2001). Identification of Proteus mirabilis Mutants with Increased Sensitivity to Antimicrobial Peptides. Antimicrob. Agents Chemother. 45: 2030-2037 [Abstract] [Full Text]  
  • Robey, M., O'Connell, W., Cianciotto, N. P. (2001). Identification of Legionella pneumophila rcp, a pagP-Like Gene That Confers Resistance to Cationic Antimicrobial Peptides and Promotes Intracellular Infection. Infect. Immun. 69: 4276-4286 [Abstract] [Full Text]  
  • Ganz, T. (2001). Fatal Attraction Evaded: How Pathogenic Bacteria Resist Cationic Polypeptides. JEM 193: f31-f34 [Full Text]  
  • Groisman, E. A. (2001). The Pleiotropic Two-Component Regulatory System PhoP-PhoQ. J. Bacteriol. 183: 1835-1842 [Full Text]  
  • Gunn, J. S. (2001). Bacterial modification of LPS and resistance to antimicrobial peptides. Innate Immunity 7: 57-62 [Abstract]