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Originally published In Press as doi:10.1074/jbc.M010412200 on February 7, 2001

J. Biol. Chem., Vol. 276, Issue 19, 15736-15740, May 11, 2001
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Clostridium perfringens Epsilon Toxin Induces a Rapid Change of Cell Membrane Permeability to Ions and Forms Channels in Artificial Lipid Bilayers*

Laetitia PetitDagger , Elke Maier§, Maryse GibertDagger , Michel R. PopoffDagger , and Roland Benz§

From Dagger  Centre National de Référence Anaérobies, Institut Pasteur, 28 rue du Dr Roux, 75724 Paris, cedex 15, France and § Lehrstuhl für Biotechnologie, Theodor-Boveri-Institut (Biozentrum) der Universität Würzburg, Am Hubland, D-97074 Würzburg, Germany

Epsilon toxin is a potent toxin produced by Clostridium perfringens types B and D, which are responsible for a rapidly fatal enterotoxemia in animals. One of the main properties of epsilon toxin is the production of edema. We have previously found that epsilon toxin causes a rapid swelling of Madin-Darby canine kidney cells and that the toxin does not enter the cytosol and remains associated with the cell membrane by forming a large complex (Petit, L., Gibert, M., Gillet, D., Laurent-Winter, C., Boquet, P., and Popoff, M. R. (1997) J. Bacteriol. 179, 6480-6487). Here, we report that epsilon toxin induced in Madin-Darby canine kidney cells a rapid decrease of intracellular K+, and an increase of Cl- and Na+, whereas the increase of Ca2+ occurred later. The entry of propidium iodide that was correlated with the loss of cell viability monitored by the 3-(4,5-dimethylthiazol-2-yl)-2,5-diphenyltetrazolium bromide (MTT) test indicates that epsilon toxin formed large pores. In artificial lipid bilayers, epsilon toxin caused current steps with a single-channel conductance of 60 pS in 100 mM KCl, which represented general diffusion pores. The channels were slightly selective for anions, but cations could also penetrate. Epsilon toxin formed wide and water-filled channels permeable to hydrophilic solutes up to a molecular mass of at least 1 kDa, which probably represents the basic mechanism of toxin action on target cells.

* This study was supported in part by grants from the Deutsche Forschungsgemeinschaft (Sonderforschungsbereich 487, Project A5) and the Fonds der Chemischen Industrie and by a Caisse Autonome Nationale d'Assurance Maladíe fellowship (to L. P.).The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

To whom correspondence should be addressed. Tel.: 33 1 45 68 83 07; Fax: 33 1 40 61 31 23; E-mail: mpopoff@pasteur.fr.

Copyright © 2001 by The American Society for Biochemistry and Molecular Biology, Inc.
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