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J. Biol. Chem., Vol. 279, Issue 33, 34209-34216, August 13, 2004

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Lipid Phase Coexistence Favors Membrane Insertion of Equinatoxin-II, a Pore-forming Toxin from Actinia equina^*

Ariana Barli¶, Ion Gutiérrez-Aguirre¶||, José M. M. Caaveiro||**, Antonio Cruz, Maria-Begoña Ruiz-Argüello¶¶, Jesús Pérez-Gil, and Juan M. González-Mañas||||

From the Unidad de Biofísica (Consejo Superior de Investigaciones Científicas-Universidad del País Vasco/Euskal Herriko Unibertsitatea) and Departamento de Bioquímica y Biología Molecular, Universidad del País Vasco, Apdo. 644, 48080 Bilbao, Spain and Departamento de Bioquímica y Biología Molecular I, Facultad de Biología, Universidad Complutense, 28040 Madrid, Spain

Equinatoxin-II is a eukaryotic pore-forming toxin belonging to the family of actinoporins. Its interaction with model membranes is largely modulated by the presence of sphingomyelin. We have used large unilamellar vesicles and lipid monolayers to gain further information about this interaction. The coexistence of gel and liquid-crystal lipid phases in sphingomyelin/phosphatidylcholine mixtures and the coexistence of liquid-ordered and liquid-disordered lipid phases in phosphatidylcholine/cholesterol or sphingomyelin/phosphatidylcholine/cholesterol mixtures favor membrane insertion of equinatoxin-II. Phosphatidylcholine vesicles are not permeabilized by equinatoxin-II. However, the localized accumulation of phospholipase C-generated diacylglycerol creates conditions for toxin activity. By using epifluorescence microscopy of transferred monolayers, it seems that lipid packing defects arising at the interfaces between coexisting lipid phases may function as preferential binding sites for the toxin. The possible implications of such a mechanism in the assembly of a toroidal pore are discussed.

Received for publication, December 17, 2003 , and in revised form, May 10, 2004.

^* This work was supported by University of the Basque Country Grant 042.310-13552/2001 and Dirección General de Educación Superior e Investigación Científica Grant BIO2003-09056. 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.

Recipient of a postdoctoral fellowship associated to the "Programa Movilizador" of the Basque Government.

^¶ These authors contributed equally to this work.

^|| Recipients of predoctoral fellowships from the Basque Government.

^** Present address: Rosenstiel Basic Medical Sciences Research Center, Brandeis University, 415 South St., Waltham, MA 02454.

Present address: Dept. of Medicine, University of Cambridge, Addenbrooke's Hospital, Hills Rd., CB2 2QQ Cambridge, United Kingdom.

^¶¶ Recipient of a predoctoral fellowship from Ministerio de Ciencia y Tecnología.

^|||| To whom correspondence should be addressed. Tel.: 3494-6015379; Fax: 3494-6013500; E-mail: gbpgomaj{at}lg.ehu.es.

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