1. Institut Curie, Centre de Recherche, Laboratoire Trafic, Signalisation et Ciblage Intracellulaires,
2. Laboratoire Physico-Chimie,
3. Laboratoire Structure et Compartiments Membranaires,
4. Laboratoire Chimie Organique (Vectorisation), 26 rue d'Ulm, 75248 Paris Cedex 05, France
5. CNRS UMR144,
6. Université P. et M. Curie/CNRS UMR168,
7. CNRS UMR176,
8. Centre for Vascular Research, University of New South Wales, 2052 Sydney, Australia
9. Department of Haematology, Prince of Wales Hospital, 2031 Sydney, Australia
10. Institut für Organische und Biomolekulare Chemie, Georg-August Universität, Tammannstr. 2, 37077 Göttingen, Germany
11. Laboratoire de Physiologie Cellulaire de la Synapse, CNRS UMR 5091 et Université Bordeaux 2, Institut François Magendie, 33077 Bordeaux, France
12. UMR Gulliver CNRS-ESPCI 7083, 10 rue Vauquelin, 75231 Paris Cedex 05, France

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.

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