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J. Biol. Chem., Vol. 280, Issue 47, 39104-39114, November 25, 2005

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Truncation of the Lipopolysaccharide Outer Core Affects Susceptibility to Antimicrobial Peptides and Virulence of Actinobacillus pleuropneumoniae Serotype 1^*

Mahendrasingh Ramjeet, Vincent Deslandes, Frank St. Michael, Andrew D. Cox, Marylène Kobisch¶, Marcelo Gottschalk, and Mario Jacques1

From the Groupe de Recherche sur les Maladies Infectieuses du Porc and the Département de Pathologie et Microbiologie, Faculté de Médecine Vétérinaire, Université de Montréal, St-Hyacinthe, Quebec J2S 7C6, Canada, Institute for Biological Sciences, National Research Council, Ottawa, Ontario K1A OR6, Canada, and the ^¶Unité de Recherche de Mycoplasmologie et Bactériologie, Agence Française de Sécurité Sanitaire des Aliments, BP 53, 22440 Ploufragan, France

We reported previously that the core oligosaccharide region of the lipopolysaccharide (LPS) is essential for optimal adhesion of Actinobacillus pleuropneumoniae, an important swine pathogen, to respiratory tract cells. Rough LPS and core LPS mutants of A. pleuropneumoniae serotype 1 were generated by using a mini-Tn10 transposon mutagenesis system. Here we performed a structural analysis of the oligosaccharide region of three core LPS mutants that still produce the same O-antigen by using methylation analyses and mass spectrometry. We also performed a kinetic study of proinflammatory cytokines production such as interleukin (IL)-6, tumor necrosis factor-, IL1-, MCP-1, and IL8 by LPS-stimulated porcine alveolar macrophages, which showed that purified LPS of the parent strain, the rough LPS and core LPS mutants, had the same ability to stimulate the production of cytokines. Most interestingly, an in vitro susceptibility test of these LPS mutants to antimicrobial peptides showed that the three core LPS mutants were more susceptible to cationic peptides than both the rough LPS mutant and the wild type parent strain. Furthermore, experimental pig infections with these mutants revealed that the galactose (Gal I) and D,D-heptose (Hep IV) residues present in the outer core of A. pleuropneumoniae serotype 1 LPS are important for adhesion and overall virulence in the natural host, whereas deletion of the terminal GalNAc-Gal II disaccharide had no effect. Our data suggest that an intact core-lipid A region is required for optimal protection of A. pleuropneumoniae against cationic peptides and that deletion of specific residues in the outer LPS core results in the attenuation of the virulence of A. pleuropneumoniae serotype 1.

Received for publication, March 15, 2005 , and in revised form, August 29, 2005.

^* This work was supported in part by the Natural Sciences and Engineering Research Council of Canada Grant DGPIN3428 (to M. J.) and Fonds pour la Formation de Chercheurs et l'Aide à la Recherche Grant 2002-ER-71900. The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

¹ To whom correspondence should be addressed: Groupe de Recherche sur les Maladies Infectieuses du Porc, Faculté de Médecine Vétérinaire, Université de Montréal, St-Hyacinthe, Quebec J2S 7C6, Canada. Tel.: 450-773-8521 (ext. 18348); E-mail: mario.jacques{at}umontreal.ca.

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