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MBC in Press, published online ahead of print November 15, 2006
Mol. Biol. Cell 10.1091/mbc.E06-06-0487

A more recent version of this article appeared on February 1, 2007
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Submitted on June 5, 2006
Revised on October 19, 2006
Accepted on November 2, 2006

Internalization of Large Double-Membrane Intercellular Vesicles by a Clathrin-dependent Endocytic Process

Michelle Piehl,* Corinna Lehmann,*{dagger} Anna Gumpert, Jean-Pierre Denizot,{ddagger} Dominique Segretain,{sect} and Matthias M. Falk

Department of Biological Sciences, Lehigh University, Bethlehem, PA 18015

Monitoring Editor: Asma Nusrat

Beyond its well-documented role in vesicle endocytosis, clathrin has also been implicated in the internalization of large particles such as viruses, pathogenic bacteria, and even latex beads. We have discovered an additional clathrin-dependent endocytic process that results in the internalization of large, double-membrane vesicles at lateral membranes of cells that are coupled by gap junctions (GJs). GJ channels bridge apposing cell membranes to mediate the direct transfer of electrical currents and signaling molecules from cell to cell. Here we report that entire GJ plaques, clusters of GJ channels, can be internalized to form large, double-membrane vesicles previously termed annular gap junctions (AGJs). These internalized AGJ vesicles subdivide into smaller vesicles that are degraded by endo-/lysosomal pathways. Mechanistic analyses revealed that clathrin-dependent endocytosis machinery-components, including clathrin itself, the alternative clathrin-adaptor Dab2, dynamin, myosin-VI, and actin are involved in the internalization, inward movement, and degradation of these large, intercellular double-membrane vesicles. These findings contribute to the understanding of clathrin’s numerous emerging functions.

*These authors contributed equally to this work.

Present addresses: {dagger}Department of Molecular Physiology and Developmental Biology, University of Bonn, Bonn, Germany; {ddagger}Unité de Neurosciences Intégratives et Computationnelles, CNRS UPR 2191, Gif sur Yvette 91198 Cedex, France; {sect}INSERM U670, Université de Paris 5, Paris, France.

Address correspondence to: Matthias M. Falk (MFalk{at}lehigh.edu)




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