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J. Biol. Chem., Vol. 278, Issue 49, 49469-49477, December 5, 2003

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Maturation of Lipoproteins by Type II Signal Peptidase Is Required for Phagosomal Escape of Listeria monocytogenes^*

Hélène Réglier-Poupet, Claude Frehel, Iharilalao Dubail, Jean-Luc Beretti, Patrick Berche, Alain Charbit, and Catherine Raynaud, Supported by a fellowship from the "Fondation pour la Recherche Médicale."

From the INSERM U570, Faculté de Médecine Necker-Enfants Malades, 156 rue de Vaugirard, 75730 Paris cedex 15, France

Lipoproteins of Gram-positive bacteria are involed in a broad range of functions such as substrate binding and transport, antibiotic resistance, cell signaling, or protein export and folding. Lipoproteins are also known to initiate both innate and adaptative immune responses. However, their role in the pathogenicity of intracellular microorganisms is yet poorly understood. In Listeria monocytogenes, a Gram-positive facultative intracellular human pathogen, surface proteins have important roles in the interactions of the microorganism with the host cells. Among the putative surface proteins of L. monocytogenes, lipoproteins constitute the largest family. Here, we addressed the role of the signal peptidase (SPase II), responsible for the maturation of lipoproteins in listerial pathogenesis. We identified a gene, lsp, encoding a SPase II in the genome of L. monocytogenes and constructed a lsp chromosomal deletion mutant. The mutant strain fails to process several lipoproteins demonstrating that lsp encodes a genuine SPase II. This defect is accompanied by a reduced efficiency of phagosomal escape during infection of eucaryotic cells, and leads to an attenuated virulence. We show that lsp gene expression is strongly induced when bacteria are still entrapped inside phagosomes of infected macrophages. The data presented establish, thus, that maturation of lipoproteins is critical for efficient phagosomal escape of L. monocytogenes, a process temporally controlled by the regulation of Lsp production in infected cells.

Received for publication, July 22, 2003 , and in revised form, September 5, 2003.

^* This work was supported in part by CNRS, INSERM, and the Université Paris V. 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.

To whom correspondence may be addressed. Tel.: 33-1-40-61-53-79; Fax: 33-1-40-61-55-92; E-mail: charbit{at}necker.fr. To whom correspondence may be addressed. E-mail: cathraynaud{at}yahoo.fr.

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