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Science 11 April 1997:
Vol. 276. no. 5310, pp. 250 - 253
DOI: 10.1126/science.276.5310.250
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Reports

Regulation of Lipid A Modifications by Salmonella typhimurium Virulence Genes phoP-phoQ

Lin Guo, * Kheng B. Lim, * John S. Gunn, Brian Bainbridge, Richard P. Darveau, Murray Hackett, Samuel I. Miller dagger

Bacterial pathogenesis requires proteins that sense host microenvironments and respond by regulating virulence gene transcription. For Salmonellae, one such regulatory system is PhoP-PhoQ, which regulates genes required for intracellular survival and resistance to cationic peptides. Analysis by mass spectrometry revealed that Salmonella typhimurium PhoP-PhoQ regulated structural modifications of lipid A, the host signaling portion of lipopolysaccharide (LPS), by the addition of aminoarabinose and 2-hydroxymyristate. Structurally modified lipid A altered LPS-mediated expression of the adhesion molecule E-selectin by endothelial cells and tumor necrosis factor-alpha expression by adherent monocytes. Thus, altered responses to environmentally induced lipid A structural modifications may represent a mechanism for bacteria to gain advantage within host tissues.

L. Guo, J. S. Gunn, S. I. Miller, Departments of Medicine and Microbiology, University of Washington, Seattle, WA 98195, USA.
K. B. Lim and M. Hackett, Department of Medicinal Chemistry, University of Washington, Seattle, WA 98195, USA.
B. Bainbridge and R. P. Darveau, Inflammation Department, Bristol-Myers Squibb Pharmaceutical Research Institute, Seattle, WA 98121, USA.
*   These authors contributed equally to this report.

dagger    To whom correspondence should be addressed. E-mail: millersi{at}u.washington.edu

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   Abstract »    Full Text »    PDF »
Salmonella typhimurium Strains Carrying Independent Mutations Display Similar Virulence Phenotypes Yet Are Controlled by Distinct Host Defense Mechanisms.
B. Raupach, N. Kurth, K. Pfeffer, and S. H. E. Kaufmann (2003)
J. Immunol. 170, 6133-6140
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Characterization of Brucella abortus O-Polysaccharide and Core Lipopolysaccharide Mutants and Demonstration that a Complete Core Is Required for Rough Vaccines To Be Efficient against Brucella abortus and Brucella ovis in the Mouse Model.
D. Monreal, M. J. Grillo, D. Gonzalez, C. M. Marin, M. J. De Miguel, I. Lopez-Goni, J. M. Blasco, A Cloeckaert, and I. Moriyon (2003)
Infect. Immun. 71, 3261-3271
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Review: The lipo-oligosaccharides of Haemophilus influenzae: an interesting array of characters.
W. E. Swords, P. A. Jones, and M. A. Apicella (2003)
Innate Immunity 9, 131-144
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Pathogenic Yersinia enterocolitica Strains Increase the Outer Membrane Permeability in Response to Environmental Stimuli by Modulating Lipopolysaccharide Fluidity and Lipid A Structure.
J. A. Bengoechea, K. Brandenburg, M. D. Arraiza, U. Seydel, M. Skurnik, and I. Moriyon (2003)
Infect. Immun. 71, 2014-2021
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Mutational Analysis of the Residue at Position 48 in the Salmonella enterica Serovar Typhimurium PhoQ Sensor Kinase.
S. Sanowar, A. Martel, and H. L. Moual (2003)
J. Bacteriol. 185, 1935-1941
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Quantitative proteomic analysis indicates increased synthesis of a quinolone by Pseudomonas aeruginosa isolates from cystic fibrosis airways.
T. Guina, S. O. Purvine, E. C. Yi, J. Eng, D. R. Goodlett, R. Aebersold, and S. I. Miller (2003)
PNAS 100, 2771-2776
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Enteric Salmonella Infection Inhibits Paneth Cell Antimicrobial Peptide Expression.
N. H. Salzman, M. M. Chou, H. de Jong, L. Liu, E. M. Porter, and Y. Paterson (2003)
Infect. Immun. 71, 1109-1115
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Solution structure and dynamics of the outer membrane enzyme PagP by NMR.
P. M. Hwang, W.-Y. Choy, E. I. Lo, L. Chen, J. D. Forman-Kay, C. R. H. Raetz, G. G. Prive, R. E. Bishop, and L. E. Kay (2002)
PNAS 99, 13560-13565
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Mutational Analysis of the Escherichia coli PhoQ Sensor Kinase: Differences with the Salmonella enterica Serovar Typhimurium PhoQ Protein and in the Mechanism of Mg2+ and Ca2+ Sensing.
A. G. Regelmann, J. A. Lesley, C. Mott, L. Stokes, and C. D. Waldburger (2002)
J. Bacteriol. 184, 5468-5478
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Mycobacterium tuberculosis phoP mutant: lipoarabinomannan molecular structure.
P. Ludwiczak, M. Gilleron, Y. Bordat, C. Martin, B. Gicquel, and G. Puzo (2002)
Microbiology 148, 3029-3037
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mig-14 Is a Salmonella Gene That Plays a Role in Bacterial Resistance to Antimicrobial Peptides.
I. E. Brodsky, R. K. Ernst, S. I. Miller, and S. Falkow (2002)
J. Bacteriol. 184, 3203-3213
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Mycobacterium tuberculosis Genes Induced during Infection of Human Macrophages.
E. Dubnau, P. Fontan, R. Manganelli, S. Soares-Appel, and I. Smith (2002)
Infect. Immun. 70, 2787-2795
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Two msbB Genes Encoding Maximal Acylation of Lipid A Are Required for Invasive Shigella flexneri to Mediate Inflammatory Rupture and Destruction of the Intestinal Epithelium.
H. d'Hauteville, S. Khan, D. J. Maskell, A. Kussak, A. Weintraub, J. Mathison, R. J. Ulevitch, N. Wuscher, C. Parsot, and P. J. Sansonetti (2002)
J. Immunol. 168, 5240-5251
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A Triple Mutant of Escherichia coli Lacking Secondary Acyl Chains on Lipid A.
M. K. Vorachek-Warren, S. Ramirez, R. J. Cotter, and C. R. H. Raetz (2002)
J. Biol. Chem. 277, 14194-14205
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Salmonella enterica Serovar Typhimurium Resistance to Bile: Identification and Characterization of the tolQRA Cluster.
A. M. Prouty, J. C. Van Velkinburgh, and J. S. Gunn (2002)
J. Bacteriol. 184, 1270-1276
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Intracellular Survival of Neisseria gonorrhoeae in Male Urethral Epithelial Cells: Importance of a Hexaacyl Lipid A.
D. M. B. Post, N. J. Phillips, J. Q. Shao, D. D. Entz, B. W. Gibson, and M. A. Apicella (2002)
Infect. Immun. 70, 909-920
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Lipid A Modifications in Polymyxin-resistant Salmonella typhimurium. PMRA-DEPENDENT 4-AMINO-4-DEOXY-L-ARABINOSE, AND PHOSPHOETHANOLAMINE INCORPORATION.
Z. Zhou, A. A. Ribeiro, S. Lin, R. J. Cotter, S. I. Miller, and C. R. H. Raetz (2001)
J. Biol. Chem. 276, 43111-43121
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An Inner Membrane Enzyme in Salmonella and Escherichia coli That Transfers 4-Amino-4-deoxy-L-arabinose to Lipid A. INDUCTION IN POLYMYXIN-RESISTANT MUTANTS AND ROLE OF A NOVEL LIPID-LINKED DONOR.
M. S. Trent, A. A. Ribeiro, S. Lin, R. J. Cotter, and C. R. H. Raetz (2001)
J. Biol. Chem. 276, 43122-43131
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Accumulation of a Polyisoprene-linked Amino Sugar in Polymyxin-resistant Salmonella typhimurium and Escherichia coli. STRUCTURAL CHARACTERIZATION AND TRANSFER TO LIPID A IN THE PERIPLASM.
M. S. Trent, A. A. Ribeiro, W. T. Doerrler, S. Lin, R. J. Cotter, and C. R. H. Raetz (2001)
J. Biol. Chem. 276, 43132-43144
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Identification of Proteus mirabilis Mutants with Increased Sensitivity to Antimicrobial Peptides.
A. J. McCoy, H. Liu, T. J. Falla, and J. S. Gunn (2001)
Antimicrob. Agents Chemother. 45, 2030-2037
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Invited review: Bacterial lipopolysaccharides and innate immunity.
C. Alexander and E. Th. Rietschel (2001)
Innate Immunity 7, 167-202
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