Shiga toxin induces tubular membrane invaginations for its uptake into cells

Winfried Römer, Ludwig Berland, Valérie Chambon, Katharina Gaus, Barbara Windschiegl, Danièle Tenza, Mohamed R. E. Aly, Vincent Fraisier, Jean-Claude Florent, David Perrais, Christophe Lamaze, Graça Raposo, Claudia Steinem, Pierre Sens, Patricia Bassereau and Ludger Johannes ()
Additional contact information
Winfried Römer: Institut Curie, Centre de Recherche, Laboratoire Trafic, Signalisation et Ciblage Intracellulaires,
Ludwig Berland: Laboratoire Physico-Chimie,
Valérie Chambon: Institut Curie, Centre de Recherche, Laboratoire Trafic, Signalisation et Ciblage Intracellulaires,
Katharina Gaus: Centre for Vascular Research, University of New South Wales, 2052 Sydney, Australia
Barbara Windschiegl: Institut für Organische und Biomolekulare Chemie, Georg-August Universität, Tammannstr. 2, 37077 Göttingen, Germany
Danièle Tenza: Laboratoire Structure et Compartiments Membranaires,
Mohamed R. E. Aly: Laboratoire Chimie Organique (Vectorisation), 26 rue d’Ulm, 75248 Paris Cedex 05, France
Vincent Fraisier: CNRS UMR144,
Jean-Claude Florent: Laboratoire Chimie Organique (Vectorisation), 26 rue d’Ulm, 75248 Paris Cedex 05, France
David Perrais: Laboratoire de Physiologie Cellulaire de la Synapse, CNRS UMR 5091 et Université Bordeaux 2, Institut François Magendie
Christophe Lamaze: Institut Curie, Centre de Recherche, Laboratoire Trafic, Signalisation et Ciblage Intracellulaires,
Graça Raposo: Laboratoire Structure et Compartiments Membranaires,
Claudia Steinem: Institut für Organische und Biomolekulare Chemie, Georg-August Universität, Tammannstr. 2, 37077 Göttingen, Germany
Pierre Sens: UMR Gulliver CNRS-ESPCI 7083, 10 rue Vauquelin, 75231 Paris Cedex 05, France
Patricia Bassereau: Laboratoire Physico-Chimie,
Ludger Johannes: Institut Curie, Centre de Recherche, Laboratoire Trafic, Signalisation et Ciblage Intracellulaires,

Nature, 2007, vol. 450, issue 7170, 670-675

Abstract: Abstract Clathrin seems to be dispensable for some endocytic processes and, in several instances, no cytosolic coat protein complexes could be detected at sites of membrane invagination. Hence, new principles must in these cases be invoked to account for the mechanical force driving membrane shape changes. Here we show that the Gb3 (glycolipid)-binding B-subunit of bacterial Shiga toxin induces narrow tubular membrane invaginations in human and mouse cells and model membranes. In cells, tubule occurrence increases on energy depletion and inhibition of dynamin or actin functions. Our data thus demonstrate that active cellular processes are needed for tubule scission rather than tubule formation. We conclude that the B-subunit induces lipid reorganization that favours negative membrane curvature, which drives the formation of inward membrane tubules. Our findings support a model in which the lateral growth of B-subunit–Gb3 microdomains is limited by the invagination process, which itself is regulated by membrane tension. The physical principles underlying this basic cargo-induced membrane uptake may also be relevant to other internalization processes, creating a rationale for conceptualizing the perplexing diversity of endocytic routes.

Date: 2007
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DOI: 10.1038/nature05996

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