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J. Biol. Chem., Vol. 278, Issue 46, 45216-45223, November 14, 2003

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Pore Formation by Equinatoxin II, a Eukaryotic Protein Toxin, Occurs by Induction of Nonlamellar Lipid Structures^*

Gregor Anderluh, Mauro Dalla Serra, Gabriella Viero, Graziano Guella¶, Peter Maek, and Gianfranco Menestrina||

From the Department of Biology, Biotechnical Faculty, University of Ljubljana, Vena pot 111, 1000 Ljubljana, Slovenia, ITC-CNR, Institute of Biophysics, Section at Trento, Via Sommarive 18, 38050 Povo (Trento) Italy, ^¶Laboratory of Bioorganic Chemistry, Department of Physics, University of Trento, Via Sommarive 14, 38050 Povo (Trento), Italy

Pore formation in the target cell membranes is a common mechanism used by many toxins in order to kill cells. Among various described mechanisms, a toroidal pore concept was described recently in the course of action of small antimicrobial peptides. Here we provide evidence that such mechanism may be used also by larger toxins. Membrane-destabilizing effects of equinatoxin II, a sea anemone cytolysin, were studied by various biophysical techniques. ³¹P NMR showed an occurrence of an isotropic component when toxin was added to multilamellar vesicles and heated. This component was not observed with melittin, -staphylococcal toxin, or myoglobin. It does not originate from isolated small lipid structures, since the size of the vesicles after the experiment was similar to the control without toxin. Electron microscopy shows occurrence of a honeycomb structure, previously observed only for some particular lipid mixtures. The analysis of FTIR spectra of the equinatoxin II-lipid complex showed lipid disordering that is consistent with isotropic component observed in NMR. Finally, the cation selectivity of the toxin-induced pores increased in the presence of negatively charged phosphatidic acid, indicating the presence of lipids in the conductive channel. The results are compatible with the toroidal pore concept that might be a general mechanism of pore formation for various membrane-interacting proteins or peptides.

Received for publication, June 5, 2003 , and in revised form, August 26, 2003.

^* This work was supported by grants from Consiglio Nazionale delle Ricerche, Ministero Italiano Università e Ricerca Scientifica, and Istituto Trentino di Cultura (to G. A., M. D. S., G.V., G. G., and G. M.) and the Ministry of Education, Science, and Sport of Slovenia (to G. A. and P. M.). 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 should be addressed. Tel.: 39-0461-314-256; Fax: 39-0461-810-628; E-mail: menes{at}itc.it.

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