Vascular endothelial cadherin-mediated cell-cell adhesion regulated by a small GTPase, Rap1.

Vascular endothelial cadherin (VE-cadherin), which belongs to the classical cadherin family, is localized at adherens junctions exclusively in vascular endothelial cells. Biochemical and biomechanical cues regulate the VE-cadherin adhesive potential by triggering the intracellular signals. VE-cadherin-mediated cell adhesion is required for cell survival and endothelial cell deadhesion is required for vascular development. It is therefore crucial to understand how VE-cadherin-based cell adhesion is controlled. This review summarizes the inter-endothelial cell adhesions and introduces our recent advance in Rap1-regulated VE-cadherin adhesion. A further analysis of the VE-cadherin recycling system will aid the understanding of cell adhesion/deadhesion mechanisms mediated by VE-cadherin in response to extracellular stimuli during development and angiogenesis.

[1]  D. Rohra,et al.  Regulation of human coronary vascular tone: further evidence must be sought before ruling out the direct role of ATP-sensitive potassium channels in regulation of coronary vasculature. , 2006, Circulation research.

[2]  N. Mochizuki,et al.  MAGI-1 is required for Rap1 activation upon cell-cell contact and for enhancement of vascular endothelial cadherin-mediated cell adhesion. , 2005, Molecular biology of the cell.

[3]  William I. Weis,et al.  Deconstructing the Cadherin-Catenin-Actin Complex , 2005, Cell.

[4]  William I. Weis,et al.  α-Catenin Is a Molecular Switch that Binds E-Cadherin-β-Catenin and Regulates Actin-Filament Assembly , 2005, Cell.

[5]  M. Broman,et al.  Cdc42 Regulates Adherens Junction Stability and Endothelial Permeability by Inducing α-Catenin Interaction With the Vascular Endothelial Cadherin Complex , 2005, Circulation research.

[6]  G. Davis,et al.  This Review Is Part of a Thematic Series on Vascular Cell Diversity, Which Includes the following Articles: Heart Valve Development: Endothelial Cell Signaling and Differentiation Molecular Determinants of Vascular Smooth Muscle Cell Diversity Endothelial/pericyte Interactions Endothelial Extracellu , 2022 .

[7]  E. Dejana,et al.  p120-Catenin regulates clathrin-dependent endocytosis of VE-cadherin. , 2005, Molecular biology of the cell.

[8]  M. Corada,et al.  Epac1 regulates integrity of endothelial cell junctions through VE‐cadherin , 2005, FEBS letters.

[9]  D. Cheresh,et al.  Tyrosine Phosphorylation of VE-cadherin Prevents Binding of p120- and β-Catenin and Maintains the Cellular Mesenchymal State* , 2005, Journal of Biological Chemistry.

[10]  Yang Luo,et al.  N-cadherin acts upstream of VE-cadherin in controlling vascular morphogenesis , 2005, The Journal of cell biology.

[11]  D. Stengel,et al.  Platelet‐activating factor increases VE‐cadherin tyrosine phosphorylation in mouse endothelial cells and its association with the PtdIns3′‐kinase , 2005, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[12]  P. Casey,et al.  Rap1 GTPase Inhibits Leukocyte Transmigration by Promoting Endothelial Barrier Function* , 2005, Journal of Biological Chemistry.

[13]  T. Mayadas,et al.  Regulation of vascular endothelial barrier function by Epac, a cAMP-activated exchange factor for Rap GTPase. , 2005, Blood.

[14]  G. Christé,et al.  Vascular Endothelial–Cadherin Tyrosine Phosphorylation in Angiogenic and Quiescent Adult Tissues , 2005, Circulation research.

[15]  M. Matsuda,et al.  Involvement of the c-Src-Crk-C3G-Rap1 Signaling in the Nectin-induced Activation of Cdc42 and Formation of Adherens Junctions* , 2005, Journal of Biological Chemistry.

[16]  N. Mochizuki,et al.  Cyclic AMP Potentiates Vascular Endothelial Cadherin-Mediated Cell-Cell Contact To Enhance Endothelial Barrier Function through an Epac-Rap1 Signaling Pathway , 2005, Molecular and Cellular Biology.

[17]  M. Mareel,et al.  Implication of the MAGI‐1b/PTEN signalosome in stabilization of adherens junctions and suppression of invasiveness , 2005, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[18]  G. Sarosi,et al.  NADPH oxidase mediates vascular endothelial cadherin phosphorylation and endothelial dysfunction. , 2004, Blood.

[19]  Y. Takai,et al.  Biology and pathology of nectins and nectin-like molecules. , 2004, Current opinion in cell biology.

[20]  S. Butz,et al.  Endothelial adhesion molecule ESAM binds directly to the multidomain adaptor MAGI-1 and recruits it to cell contacts , 2004 .

[21]  John G. Collard,et al.  Rap1 Regulates E-cadherin-mediated Cell-Cell Adhesion* , 2004, Journal of Biological Chemistry.

[22]  W. Birchmeier,et al.  Rap1 Regulates the Formation of E-Cadherin-Based Cell-Cell Contacts , 2004, Molecular and Cellular Biology.

[23]  M. Fortini,et al.  Functional reconstitution of γ‐secretase through coordinated expression of presenilin, nicastrin, Aph‐1, and Pen‐2 , 2004, Journal of neuroscience research.

[24]  J. Stow,et al.  The ins and outs of E-cadherin trafficking. , 2004, Trends in cell biology.

[25]  E. Devilard,et al.  DNAM-1 and PVR Regulate Monocyte Migration through Endothelial Junctions , 2004, The Journal of experimental medicine.

[26]  P. Vincent,et al.  VE-cadherin: adhesion at arm's length. , 2004, American journal of physiology. Cell physiology.

[27]  Elisabetta Dejana,et al.  Endothelial cell–cell junctions: happy together , 2004, Nature Reviews Molecular Cell Biology.

[28]  N. Himes,et al.  Src blockade stabilizes a Flk/cadherin complex, reducing edema and tissue injury following myocardial infarction. , 2004, The Journal of clinical investigation.

[29]  G. Borisy,et al.  p120 catenin associates with kinesin and facilitates the transport of cadherin–catenin complexes to intercellular junctions , 2003, The Journal of cell biology.

[30]  G. Bazzoni The JAM family of junctional adhesion molecules. , 2003, Current opinion in cell biology.

[31]  Keith R. Johnson,et al.  Cadherin-mediated cellular signaling. , 2003, Current opinion in cell biology.

[32]  Celeste M Nelson,et al.  VE-cadherin simultaneously stimulates and inhibits cell proliferation by altering cytoskeletal structure and tension , 2003, Journal of Cell Science.

[33]  J. Bos Epac: a new cAMP target and new avenues in cAMP research , 2003, Nature Reviews Molecular Cell Biology.

[34]  R. Parton,et al.  Characterization of E-cadherin Endocytosis in Isolated MCF-7 and Chinese Hamster Ovary Cells , 2003, Journal of Biological Chemistry.

[35]  M. Ueno,et al.  Abnormal blood vessel development in mice lacking presenilin-1 , 2003, Mechanisms of Development.

[36]  P. Newman,et al.  Signal transduction pathways mediated by PECAM-1: new roles for an old molecule in platelet and vascular cell biology. , 2003, Arteriosclerosis, thrombosis, and vascular biology.

[37]  M. Corada,et al.  Contact inhibition of VEGF-induced proliferation requires vascular endothelial cadherin, β-catenin, and the phosphatase DEP-1/CD148 , 2003, The Journal of cell biology.

[38]  A. Malik,et al.  VE-cadherin-induced Cdc42 Signaling Regulates Formation of Membrane Protrusions in Endothelial Cells* , 2003, The Journal of Biological Chemistry.

[39]  Y. Takai,et al.  Nectin and afadin: novel organizers of intercellular junctions , 2003, Journal of Cell Science.

[40]  Doo Yeon Kim,et al.  Nectin-1α, an Immunoglobulin-like Receptor Involved in the Formation of Synapses, Is a Substrate for Presenilin/γ-Secretase-like Cleavage* , 2002, The Journal of Biological Chemistry.

[41]  M. Matsuda,et al.  Adaptor protein Crk is required for ephrin-B1-induced membrane ruffling and focal complex assembly of human aortic endothelial cells. , 2002, Molecular biology of the cell.

[42]  W. Seeger,et al.  Adrenomedullin Reduces Endothelial Hyperpermeability , 2002, Circulation research.

[43]  P. Campochiaro,et al.  Angiopoietin-2 is required for postnatal angiogenesis and lymphatic patterning, and only the latter role is rescued by Angiopoietin-1. , 2002, Developmental cell.

[44]  K. Fujiwara,et al.  Evidence for a role of platelet endothelial cell adhesion molecule-1 in endothelial cell mechanosignal transduction , 2002, The Journal of cell biology.

[45]  Elisabetta Dejana,et al.  VEGF receptor 2 and the adherens junction as a mechanical transducer in vascular endothelial cells , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[46]  H. Koeppen,et al.  MAGI-1: a widely expressed, alternatively spliced tight junction protein. , 2002, Experimental cell research.

[47]  J. Gutkind,et al.  E-cadherin and Hakai: signalling, remodeling or destruction? , 2002, Nature Cell Biology.

[48]  M. Corada,et al.  Vascular Endothelial Growth Factor Induces Shc Association With Vascular Endothelial Cadherin: A Potential Feedback Mechanism to Control Vascular Endothelial Growth Factor Receptor-2 Signaling , 2002, Arteriosclerosis, thrombosis, and vascular biology.

[49]  E. Kovacs,et al.  E-cadherin Homophilic Ligation Directly Signals through Rac and Phosphatidylinositol 3-Kinase to Regulate Adhesive Contacts* , 2002, The Journal of Biological Chemistry.

[50]  Kozo Kaibuchi,et al.  Rho-family GTPases in cadherin-mediated cell — cell adhesion , 2001, Nature Reviews Molecular Cell Biology.

[51]  C. Kay,et al.  Multiple cadherin extracellular repeats mediate homophilic binding and adhesion , 2001, The Journal of cell biology.

[52]  A. Miyawaki,et al.  Spatio-temporal images of growth-factor-induced activation of Ras and Rap1 , 2001, Nature.

[53]  I. Dobrosotskaya,et al.  Identification of mNET1 as a candidate ligand for the first PDZ domain of MAGI-1. , 2001, Biochemical and biophysical research communications.

[54]  J. Bos,et al.  Rap1 signalling: adhering to new models , 2001, Nature Reviews Molecular Cell Biology.

[55]  N. Hotchin,et al.  RAC1 regulates adherens junctions through endocytosis of E-cadherin. , 2001, Molecular biology of the cell.

[56]  G. Guillemette,et al.  Permeability of endothelial monolayers to albumin is increased by bradykinin and inhibited by prostaglandins. , 2001, American journal of physiology. Lung cellular and molecular physiology.

[57]  Shoichiro Tsukita,et al.  Multifunctional strands in tight junctions , 2001, Nature Reviews Molecular Cell Biology.

[58]  B. Angst,et al.  COMMENTARY The cadherin superfamily: diversity in form and function , 2022 .

[59]  J. Bos,et al.  The role of Rap1 in integrin-mediated cell adhesion. , 2001, Biochemical Society transactions.

[60]  A. Mino,et al.  Membrane‐associated guanylate kinase with inverted orientation (MAGI)‐1/brain angiogenesis inhibitor 1‐associated protein (BAP1) as a scaffolding molecule for Rap small G protein GDP/GTP exchange protein at tight junctions , 2000, Genes to cells : devoted to molecular & cellular mechanisms.

[61]  Stanley J. Wiegand,et al.  Vascular-specific growth factors and blood vessel formation , 2000, Nature.

[62]  K. Kaibuchi,et al.  Identification of a Novel -Catenin-Interacting Protein , 2000 .

[63]  R. Klein,et al.  Eph receptors and ephrin ligands. essential mediators of vascular development. , 2000, Trends in cardiovascular medicine.

[64]  G. James,et al.  MAGI-1 interacts with beta-catenin and is associated with cell-cell adhesion structures. , 2000, Biochemical and biophysical research communications.

[65]  K. Tsuchida,et al.  Identification and Characterization of a PDZ Protein That Interacts with Activin Type II Receptors* , 2000, The Journal of Biological Chemistry.

[66]  M. Woolkalís,et al.  SHP2 Association with VE-Cadherin Complexes in Human Endothelial Cells Is Regulated by Thrombin* , 2000, The Journal of Biological Chemistry.

[67]  B. Gumbiner,et al.  Regulation of Cadherin Adhesive Activity , 2000, The Journal of cell biology.

[68]  N. Rahimi,et al.  A role for cadherin-5 in regulation of vascular endothelial growth factor receptor 2 activity in endothelial cells. , 1999, Molecular biology of the cell.

[69]  P. Carmeliet,et al.  Targeted Deficiency or Cytosolic Truncation of the VE-cadherin Gene in Mice Impairs VEGF-Mediated Endothelial Survival and Angiogenesis , 1999, Cell.

[70]  G. Yancopoulos,et al.  Growth factors acting via endothelial cell-specific receptor tyrosine kinases: VEGFs, angiopoietins, and ephrins in vascular development. , 1999, Genes & development.

[71]  F. Breviario,et al.  Identification of a Novel Cadherin (Vascular Endothelial Cadherin-2) Located at Intercellular Junctions in Endothelial Cells* , 1998, The Journal of Biological Chemistry.

[72]  M. Corada,et al.  Vascular endothelial growth factor induces VE-cadherin tyrosine phosphorylation in endothelial cells. , 1998, Journal of cell science.

[73]  R. Ross,et al.  Cleavage of beta-catenin and plakoglobin and shedding of VE-cadherin during endothelial apoptosis: evidence for a role for caspases and metalloproteinases. , 1998, Molecular biology of the cell.

[74]  E. Dejana,et al.  Differential Localization of VE- and N-Cadherins in Human Endothelial Cells: VE-Cadherin Competes with N-Cadherin for Junctional Localization , 1998, The Journal of cell biology.

[75]  R. Guy,et al.  MAGI-1, a Membrane-associated Guanylate Kinase with a Unique Arrangement of Protein-Protein Interaction Domains* , 1997, The Journal of Biological Chemistry.

[76]  K. Fujiwara,et al.  Platelet endothelial cell adhesion molecule‐1 is a major SH‐PTP2 binding protein in vascular endothelial cells , 1997, FEBS letters.

[77]  D. Jackson,et al.  The Protein-tyrosine Phosphatase SHP-2 Binds Platelet/Endothelial Cell Adhesion Molecule-1 (PECAM-1) and Forms a Distinct Signaling Complex during Platelet Aggregation , 1997, The Journal of Biological Chemistry.

[78]  B. Gumbiner,et al.  A Synthetic Peptide Corresponding to the Extracellular Domain of Occludin Perturbs the Tight Junction Permeability Barrier , 1997, The Journal of cell biology.

[79]  Pamela F. Jones,et al.  Requisite Role of Angiopoietin-1, a Ligand for the TIE2 Receptor, during Embryonic Angiogenesis , 1996, Cell.

[80]  M. Corada,et al.  Inhibition of cultured cell growth by vascular endothelial cadherin (cadherin-5/VE-cadherin). , 1996, The Journal of clinical investigation.

[81]  Janet Rossant,et al.  Failure of blood-island formation and vasculogenesis in Flk-1-deficient mice , 1995, Nature.

[82]  J. Rossant,et al.  Role of the Flt-1 receptor tyrosine kinase in regulating the assembly of vascular endothelium , 1995, Nature.

[83]  B. Geiger,et al.  The molecular organization of endothelial cell to cell junctions: differential association of plakoglobin, beta-catenin, and alpha- catenin with vascular endothelial cadherin (VE-cadherin) , 1995, The Journal of cell biology.

[84]  R. Hynes,et al.  Extrajunctional distribution of N-cadherin in cultured human endothelial cells. , 1992, Journal of cell science.

[85]  V. V. van Hinsbergh,et al.  Norepinephrine and iloprost improve barrier function of human endothelial cell monolayers: role of cAMP. , 1991, The American journal of physiology.

[86]  B. Gumbiner,et al.  Identification of a 160-kDa polypeptide that binds to the tight junction protein ZO-1. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[87]  D. Connolly,et al.  Vascular permeability factor, an endothelial cell mitogen related to PDGF. , 1989, Science.

[88]  W. Weis,et al.  Alpha-catenin is a molecular switch that binds E-cadherin-beta-catenin and regulates actin-filament assembly. , 2005, Cell.

[89]  M. Peifer,et al.  Comment Traffic control : p 120-catenin acts as a gatekeeper to control the fate of classical cadherins in mammalian cells , 2003 .

[90]  A. Blangy,et al.  Biogenesis of N-cadherin-dependent cell-cell contacts in living fibroblasts is a microtubule-dependent kinesin-driven mechanism. , 2002, Molecular biology of the cell.

[91]  K. Kaibuchi,et al.  Identification of a novel beta-catenin-interacting protein. , 2000, Biochemical and biophysical research communications.