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J Biol Chem, Vol. 274, Issue 13, 8405-8410, March 26, 1999
Inactivation of the dlt Operon in
Staphylococcus aureus Confers Sensitivity to Defensins,
Protegrins, and Other Antimicrobial Peptides
Andreas
Peschel ,
Michael
Otto ,
Ralph W.
Jack¶,
Hubert
Kalbacher ,
Günther
Jung¶, and
Friedrich
Götz
From Mikrobielle Genetik, Universität
Tübingen, Waldhäuser Straße 70/8, 72076 Tübingen,
Germany, ¶ Organische Chemie, Universität
Tübingen, 72076 Tübingen, Germany, ECHAZ
Microcollections®, Sindelfingerstraße 3, 72070 Tübingen,
Germany, and Physiologische Chemie, Universität
Tübingen, Ob dem Himmelreich 7, 72074 Tübingen,
Germany
Positively charged antimicrobial peptides with
membrane-damaging activity are produced by animals and humans as
components of their innate immunity against bacterial infections and
also by many bacteria to inhibit competing microorganisms.
Staphylococcus aureus and Staphylococcus
xylosus, which tolerate high concentrations of several
antimicrobial peptides, were mutagenized to identify genes responsible
for this insensitivity. Several mutants with increased sensitivity were
obtained, which exhibited an altered structure of teichoic acids, major
components of the Gram-positive cell wall. The mutant teichoic acids
lacked D-alanine, as a result of which the cells carried an
increased negative surface charge. The mutant cells bound fewer
anionic, but more positively charged proteins. They were sensitive to
human defensin HNP1-3, animal-derived protegrins, tachyplesins, and
magainin II, and to the bacteria-derived peptides gallidermin and
nisin. The mutated genes shared sequence similarity with the
dlt genes involved in the transfer of D-alanine into teichoic acids from other Gram-positive bacteria. Wild-type strains bearing additional copies of the dlt operon
produced teichoic acids with higher amounts of D-alanine
esters, bound cationic proteins less effectively and were less
sensitive to antimicrobial peptides. We propose a role of the
D-alanine-esterified teichoic acids which occur in many
pathogenic bacteria in the protection against human and animal defense systems.
Copyright © 1999 by The American Society for Biochemistry and Molecular Biology, Inc.

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A. Grundling and O. Schneewind
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S. A. Loutet, R. S. Flannagan, C. Kooi, P. A. Sokol, and M. A. Valvano
A Complete Lipopolysaccharide Inner Core Oligosaccharide Is Required for Resistance of Burkholderia cenocepacia to Antimicrobial Peptides and Bacterial Survival In Vivo
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N. Fisher, L. Shetron-Rama, A. Herring-Palmer, B. Heffernan, N. Bergman, and P. Hanna
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A. S. Bayer, P. McNamara, M. R. Yeaman, N. Lucindo, T. Jones, A. L. Cheung, H.-G. Sahl, and R. A. Proctor
Transposon Disruption of the Complex I NADH Oxidoreductase Gene (snoD) in Staphylococcus aureus Is Associated with Reduced Susceptibility to the Microbicidal Activity of Thrombin-Induced Platelet Microbicidal Protein 1
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R. A. Dorschner, B. Lopez-Garcia, A. Peschel, D. Kraus, K. Morikawa, V. Nizet, and R. L. Gallo
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C. Weidenmaier, A. Peschel, V. A. J. Kempf, N. Lucindo, M. R. Yeaman, and A. S. Bayer
DltABCD- and MprF-Mediated Cell Envelope Modifications of Staphylococcus aureus Confer Resistance to Platelet Microbicidal Proteins and Contribute to Virulence in a Rabbit Endocarditis Model
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C. M. A. Linde, S. Grundstrom, E. Nordling, E. Refai, P. J. Brennan, and M. Andersson
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V. Dartois, J. Sanchez-Quesada, E. Cabezas, E. Chi, C. Dubbelde, C. Dunn, J. Granja, C. Gritzen, D. Weinberger, M. R. Ghadiri, et al.
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B. Fournier and D. J. Philpott
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K. Ouhara, H. Komatsuzawa, S. Yamada, H. Shiba, T. Fujiwara, M. Ohara, K. Sayama, K. Hashimoto, H. Kurihara, and M. Sugai
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A. Resch, R. Rosenstein, C. Nerz, and F. Gotz
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M. Pietiainen, M. Gardemeister, M. Mecklin, S. Leskela, M. Sarvas, and V. P. Kontinen
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H. Zhang, K. Morikawa, T. Ohta, and Y. Kato
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J. Xue, I. Hunter, T. Steinmetz, A. Peters, B. Ray, and K. W. Miller
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R. Leonardi, S. Chohnan, Y.-M. Zhang, K. G. Virga, R. E. Lee, C. O. Rock, and S. Jackowski
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K. M. Mason, R. S. Munson Jr., and L. O. Bakaletz
A Mutation in the sap Operon Attenuates Survival of Nontypeable Haemophilus influenzae in a Chinchilla Model of Otitis Media
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M. Sieprawska-Lupa, P. Mydel, K. Krawczyk, K. Wojcik, M. Puklo, B. Lupa, P. Suder, J. Silberring, M. Reed, J. Pohl, et al.
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M. A. Campos, M. A. Vargas, V. Regueiro, C. M. Llompart, S. Alberti, and J. A. Bengoechea
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V. Vadyvaloo, S. Arous, A. Gravesen, Y. Hechard, R. Chauhan-Haubrock, J. W. Hastings, and M. Rautenbach
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P. Joseph, A. Guiseppi, A. Sorokin, and F. Denizot
Characterization of the Bacillus subtilis YxdJ response regulator as the inducer of expression for the cognate ABC transporter YxdLM
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M. J. Franklin, S. A. Douthit, and M. A. McClure
Evidence that the algI/algJ Gene Cassette, Required for O Acetylation of Pseudomonas aeruginosa Alginate, Evolved by Lateral Gene Transfer
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J. M. Voyich, K. R. Braughton, D. E. Sturdevant, C. Vuong, S. D. Kobayashi, S. F. Porcella, M. Otto, J. M. Musser, and F. R. DeLeo
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L. Wang, J. D. Trawick, R. Yamamoto, and C. Zamudio
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M. Li, M. Guan, X. F. Jiang, F. Y. Yuan, M. Xu, W. Z. Zhang, and Y. Lu
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S. Nouaille, J. Commissaire, J. J. Gratadoux, P. Ravn, A. Bolotin, A. Gruss, Y. Le Loir, and P. Langella
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A. Gravesen, B. Kallipolitis, K. Holmstrom, P. E. Hoiby, M. Ramnath, and S. Knochel
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M. Cao and J. D. Helmann
The Bacillus subtilis Extracytoplasmic-Function {sigma}X Factor Regulates Modification of the Cell Envelope and Resistance to Cationic Antimicrobial Peptides
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U. Pag, M. Oedenkoven, N. Papo, Z. Oren, Y. Shai, and H.-G. Sahl
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F. C. Neuhaus and J. Baddiley
A Continuum of Anionic Charge: Structures and Functions of D-Alanyl-Teichoic Acids in Gram-Positive Bacteria
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C. Heilmann, G. Thumm, G. S. Chhatwal, J. Hartleib, A. Uekotter, and G. Peters
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D. M. Hoover, Z. Wu, K. Tucker, W. Lu, and J. Lubkowski
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S. Katzif, D. Danavall, S. Bowers, J. T. Balthazar, and W. M. Shafer
The Major Cold Shock Gene, cspA, Is Involved in the Susceptibility of Staphylococcus aureus to an Antimicrobial Peptide of Human Cathepsin G
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K. Midorikawa, K. Ouhara, H. Komatsuzawa, T. Kawai, S. Yamada, T. Fujiwara, K. Yamazaki, K. Sayama, M. A. Taubman, H. Kurihara, et al.
Staphylococcus aureus Susceptibility to Innate Antimicrobial Peptides, {beta}-Defensins and CAP18, Expressed by Human Keratinocytes
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G. Bell and P.-H. Gouyon
Arming the enemy: the evolution of resistance to self-proteins
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E. Wahlstrom, M. Vitikainen, V. P. Kontinen, and M. Sarvas
The extracytoplasmic folding factor PrsA is required for protein secretion only in the presence of the cell wall in Bacillus subtilis
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M. R. Yeaman and N. Y. Yount
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T. Theis, M. Wedde, V. Meyer, and U. Stahl
The Antifungal Protein from Aspergillus giganteus Causes Membrane Permeabilization
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B. Said-Salim, P. M. Dunman, F. M. McAleese, D. Macapagal, E. Murphy, P. J. McNamara, S. Arvidson, T. J. Foster, S. J. Projan, and B. N. Kreiswirth
Global Regulation of Staphylococcus aureus Genes by Rot
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S. A. Kristian, M. Durr, J. A. G. Van Strijp, B. Neumeister, and A. Peschel
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M. Durr and A. Peschel
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T. Koprivnjak, A. Peschel, M. H. Gelb, N. S. Liang, and J. P. Weiss
Role of Charge Properties of Bacterial Envelope in Bactericidal Action of Human Group IIA Phospholipase A2 against Staphylococcus aureus
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H. Ulvatne, H. H. Haukland, O. Samuelsen, M. Kramer, and L. H. Vorland
Proteases in Escherichia coli and Staphylococcus aureus confer reduced susceptibility to lactoferricin B
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Copyright © 1999 by the American Society for Biochemistry and Molecular Biology.
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