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J. Cell Biol. 174 (4): 593-604

Copyright © 2006 by the Rockefeller University Press.


Article

Vascular endothelial cadherin controls VEGFR-2 internalization and signaling from intracellular compartments

Maria Grazia Lampugnani1,2, Fabrizio Orsenigo1, Maria Cristina Gagliani4, Carlo Tacchetti4, , and Elisabetta Dejana1,2,3

1 IFOM, Fondazione Italiana per la Ricerca sul Cancro Institute of Molecular Oncology, 2 Mario Negri Institute for Pharmacological Research, and 3 Department of Biomolecular and Biotechnological Sciences, Faculty of Sciences, University of Milan, 20139 Milan, Italy
4 Department of Experimental Medicine, University of Genova, 16146 Genova, Italy

Correspondence to Elisabetta Dejana: elisabetta.dejana{at}ifom-ieo-campus.it

Abstract: Receptor endocytosis is a fundamental step in controlling the magnitude, duration, and nature of cell signaling events. Confluent endothelial cells are contact inhibited in their growth and respond poorly to the proliferative signals of vascular endothelial growth factor (VEGF). In a previous study, we found that the association of vascular endothelial cadherin (VEC) with VEGF receptor (VEGFR) type 2 contributes to density-dependent growth inhibition (Lampugnani, G.M., A. Zanetti, M. Corada, T. Takahashi, G. Balconi, F. Breviario, F. Orsenigo, A. Cattelino, R. Kemler, T.O. Daniel, and E. Dejana. 2003. J. Cell Biol. 161:793–804). In the present study, we describe the mechanism through which VEC reduces VEGFR-2 signaling. We found that VEGF induces the clathrin-dependent internalization of VEGFR-2. When VEC is absent or not engaged at junctions, VEGFR-2 is internalized more rapidly and remains in endosomal compartments for a longer time. Internalization does not terminate its signaling; instead, the internalized receptor is phosphorylated, codistributes with active phospholipase C–{gamma}, and activates p44/42 mitogen-activated protein kinase phosphorylation and cell proliferation. Inhibition of VEGFR-2 internalization reestablishes the contact inhibition of cell growth, whereas silencing the junction-associated density-enhanced phosphatase-1/CD148 phosphatase restores VEGFR-2 internalization and signaling. Thus, VEC limits cell proliferation by retaining VEGFR-2 at the membrane and preventing its internalization into signaling compartments.

Abbreviations used in this paper: EEA-1, early endosomal antigen-1; DEP-1, density-enhanced phosphatase-1; GSH, glutathione; HUVEC, human umbilical vein endothelial cell; PY, phosphotyrosine; VEC, vascular endothelial cadherin; VEGFR, VEGF receptor.


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