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PMID: 9508779 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Differential localization of VE- and N-cadherins in human endothelial cells: VE-cadherin competes with N-cadherin for junctional localization.

The Journal of cell biology ·Vol. 140 ·No. 6 ·1998-03-23 ·Pages 1475-84

Navarro P, Ruco L, Dejana E

Abstract

The two major cadherins of endothelial cells are neural (N)-cadherin and vascular endothelial (VE)- cadherin. Despite similar level of protein expression only VE-cadherin is located at cell-cell contacts, whereas N-cadherin is distributed over the whole cell membrane. Cotransfection of VE-cadherin and N-cadherin in CHO cells resulted in the same distribution as that observed in endothelial cells indicating that the behavior of the two cadherins was not cell specific but related to their structural characteristics. Similar amounts of alpha- and beta-catenins and plakoglobin were associated to VE- and N-cadherins, whereas p120 was higher in the VE-cadherin complex. The presence of VE-cadherin did not affect N-cadherin homotypic adhesive properties or its capacity to localize at junctions when cotransfectants were cocultured with cells transfected with N-cadherin only. To define the molecular domain responsible for the VE-cadherin-dominant activity we prepared a chimeric construct formed by VE-cadherin extracellular region linked to N-cadherin intracellular domain. The chimera lost the capacity to exclude N-cadherin from junctions indicating that the extracellular domain of VE-cadherin alone is not sufficient for the preferential localization of the molecule at the junctions. A truncated mutant of VE-cadherin retaining the full extracellular domain and a short cytoplasmic tail (Arg621-Pro702) lacking the catenin-binding region was able to exclude N-cadherin from junctions. This indicates that the Arg621-Pro702 sequence in the VE-cadherin cytoplasmic tail is required for N-cadherin exclusion from junctions. Competition between cadherins for their clustering at intercellular junctions in the same cell has never been described before. We speculate that, in the endothelium, VE- and N-cadherin play different roles; whereas VE-cadherin mostly promotes the homotypic interaction between endothelial cells, N-cadherin may be responsible for the anchorage of the endothelium to other surrounding cell types expressing N-cadherin such as vascular smooth muscle cells or pericytes.

MeSH Terms
Animals CHO Cells/chemistry Cadherins/analysis,biosynthesis,chemistry Cell Adhesion/physiology Cricetinae Cytoskeletal Proteins/analysis,metabolism Endothelium, Vascular/chemistry,cytology Humans Intercellular Junctions/chemistry Phosphorylation Protein Structure, Tertiary Trans-Activators Transfection Tyrosine/metabolism Umbilical Veins/cytology alpha Catenin beta Catenin
Chemicals
CTNNA1 protein, human CTNNB1 protein, human Cadherins Cytoskeletal Proteins Trans-Activators alpha Catenin beta Catenin Tyrosine
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Navarro P
Laboratory of Vascular Biology, Istituto di Ricerche Farmacologiche Mario Negri, Milan, Italy. [email protected]
Ruco L
Dejana E
References (60)
60 references, click to expand
  1. Developmental regulation of a cadherin during the differentiation of skeletal myoblasts.
    Dev Biol. 1990 Oct;141(2):292-8 PMID: 2210038
  2. Expression of N-cadherin by human squamous carcinoma cells induces a scattered fibroblastic phenotype with disrupted cell-cell adhesion.
    J Cell Biol. 1996 Dec;135(6 Pt 1):1643-54 PMID: 8978829
  3. p60v-src causes tyrosine phosphorylation and inactivation of the N-cadherin-catenin cell adhesion system.
    EMBO J. 1993 Jan;12(1):307-14 PMID: 8381351
  4. Cleavage of structural proteins during the assembly of the head of bacteriophage T4.
    Nature. 1970 Aug 15;227(5259):680-5 PMID: 5432063
  5. Tyrosine phosphorylation regulates the adhesions of ras-transformed breast epithelia.
    J Cell Biol. 1995 Jul;130(2):461-71 PMID: 7542250
  6. A potential role for N-cadherin in mediating endothelial cell-smooth muscle cell interactions in the rat vasculature.
    Lab Invest. 1993 Aug;69(2):203-9 PMID: 8350598
  7. Transmembrane control of cadherin-mediated cell adhesion: a 94 kDa protein functionally associated with a specific region of the cytoplasmic domain of E-cadherin.
    Cell Regul. 1989 Nov;1(1):37-44 PMID: 2519616
  8. Developmental defects in mouse embryos lacking N-cadherin.
    Dev Biol. 1997 Jan 1;181(1):64-78 PMID: 9015265
  9. Interendothelial junctions: structure, signalling and functional roles.
    Curr Opin Cell Biol. 1997 Oct;9(5):674-82 PMID: 9330871
  10. Immunoelectron characterisation of the inter-endothelial junctions of human term placenta.
    J Cell Sci. 1993 Apr;104 ( Pt 4):1073-81 PMID: 8314892
  11. HMEC-1: establishment of an immortalized human microvascular endothelial cell line.
    J Invest Dermatol. 1992 Dec;99(6):683-90 PMID: 1361507
  12. A monoclonal antibody disrupting calcium-dependent cell-cell adhesion of brain tissues: possible role of its target antigen in animal pattern formation.
    Proc Natl Acad Sci U S A. 1985 May;82(9):2789-93 PMID: 3857614
  13. Targeted null-mutation in the vascular endothelial-cadherin gene impairs the organization of vascular-like structures in embryoid bodies.
    Proc Natl Acad Sci U S A. 1997 Jun 10;94(12):6273-8 PMID: 9177207
  14. Replacement of insulin receptor tyrosine residues 1162 and 1163 compromises insulin-stimulated kinase activity and uptake of 2-deoxyglucose.
    Cell. 1986 Jun 6;45(5):721-32 PMID: 3518947
  15. Identification of a neural alpha-catenin as a key regulator of cadherin function and multicellular organization.
    Cell. 1992 Jul 24;70(2):293-301 PMID: 1638632
  16. Cell adhesion and signal transduction: the Armadillo connection.
    Trends Cell Biol. 1995 Jun;5(6):224-9 PMID: 14732126
  17. pangolin encodes a Lef-1 homologue that acts downstream of Armadillo to transduce the Wingless signal in Drosophila.
    Nature. 1997 Feb 27;385(6619):829-33 PMID: 9039917
  18. XTcf-3 transcription factor mediates beta-catenin-induced axis formation in Xenopus embryos.
    Cell. 1996 Aug 9;86(3):391-9 PMID: 8756721
  19. A role for cadherins in tissue formation.
    Development. 1996 Oct;122(10):3185-94 PMID: 8898231
  20. Mechanisms of angiogenesis.
    Nature. 1997 Apr 17;386(6626):671-4 PMID: 9109485
  21. Morphogenetic roles of classic cadherins.
    Curr Opin Cell Biol. 1995 Oct;7(5):619-27 PMID: 8573335
  22. A novel endothelial-specific membrane protein is a marker of cell-cell contacts.
    J Cell Biol. 1992 Sep;118(6):1511-22 PMID: 1522121
  23. Perturbation of cell adhesion and microvilli formation by antisense oligonucleotides to ERM family members.
    J Cell Biol. 1994 Jun;125(6):1371-84 PMID: 8207064
  24. Functional properties of human vascular endothelial cadherin (7B4/cadherin-5), an endothelium-specific cadherin.
    Arterioscler Thromb Vasc Biol. 1995 Aug;15(8):1229-39 PMID: 7627717
  25. Cadherins and catenins in development.
    Curr Opin Cell Biol. 1996 Oct;8(5):685-91 PMID: 8939663
  26. Cadherins and catenins: interactions and functions in embryonic development.
    Curr Opin Cell Biol. 1994 Oct;6(5):740-6 PMID: 7833053
  27. DNA sequence analysis with a modified bacteriophage T7 DNA polymerase.
    Proc Natl Acad Sci U S A. 1987 Jul;84(14):4767-71 PMID: 3474623
  28. A soluble chimeric form of the L1 glycoprotein stimulates neurite outgrowth.
    Neuron. 1995 Jan;14(1):57-66 PMID: 7826641
  29. Differential targeting of T- and N-cadherin in polarized epithelial cells.
    J Biol Chem. 1996 Nov 22;271(47):30061-7 PMID: 8939953
  30. The cadherins: cell-cell adhesion molecules controlling animal morphogenesis.
    Development. 1988 Apr;102(4):639-55 PMID: 3048970
  31. Extrajunctional distribution of N-cadherin in cultured human endothelial cells.
    J Cell Sci. 1992 May;102 ( Pt 1):7-17 PMID: 1500442
  32. Cadherin-mediated cell-cell adhesion is perturbed by v-src tyrosine phosphorylation in metastatic fibroblasts.
    J Cell Biol. 1992 Aug;118(3):703-14 PMID: 1639852
  33. A-CAM: a 135-kD receptor of intercellular adherens junctions. I. Immunoelectron microscopic localization and biochemical studies.
    J Cell Biol. 1986 Oct;103(4):1441-50 PMID: 3533954
  34. Tumor-suppressor gene products in cell contacts: the cadherin-APC-armadillo connection.
    Curr Opin Cell Biol. 1994 Oct;6(5):711-6 PMID: 7833051
  35. Endothelial cells: adhesion and tight junctions.
    Curr Opin Cell Biol. 1992 Oct;4(5):830-3 PMID: 1419061
  36. Beta-catenin mediates the interaction of the cadherin-catenin complex with epidermal growth factor receptor.
    J Cell Biol. 1994 Dec;127(5):1375-80 PMID: 7962096
  37. Cell adhesion: the molecular basis of tissue architecture and morphogenesis.
    Cell. 1996 Feb 9;84(3):345-57 PMID: 8608588
  38. Broad spectrum pan-cadherin antibodies, reactive with the C-terminal 24 amino acid residues of N-cadherin.
    J Cell Sci. 1990 Dec;97 ( Pt 4):607-14 PMID: 2077036
  39. Cell confluence regulates tyrosine phosphorylation of adherens junction components in endothelial cells.
    J Cell Sci. 1997 Sep;110 ( Pt 17):2065-77 PMID: 9378757
  40. Endothelial adherens junctions: implications in the control of vascular permeability and angiogenesis.
    J Clin Invest. 1996 Nov 1;98(9):1949-53 PMID: 8903311
  41. Catenin-dependent and -independent functions of vascular endothelial cadherin.
    J Biol Chem. 1995 Dec 29;270(52):30965-72 PMID: 8537353
  42. Spatial and temporal expression pattern of N-cadherin cell adhesion molecules correlated with morphogenetic processes of chicken embryos.
    Dev Biol. 1987 Mar;120(1):215-27 PMID: 3817290
  43. Molecular linkage between cadherins and actin filaments in cell-cell adherens junctions.
    Curr Opin Cell Biol. 1992 Oct;4(5):834-9 PMID: 1419062
  44. Cadherin-catenin complex: protein interactions and their implications for cadherin function.
    J Cell Biochem. 1996 Jun 15;61(4):514-23 PMID: 8806074
  45. Spatial and temporal relationships between cadherins and PECAM-1 in cell-cell junctions of human endothelial cells.
    J Cell Biol. 1994 Jul;126(1):247-58 PMID: 8027182
  46. Expression of N-cadherin adhesion molecules associated with early morphogenetic events in chick development.
    Nature. 1986 Apr 3-9;320(6061):447-9 PMID: 3515198
  47. Activation of the FGF receptor underlies neurite outgrowth stimulated by L1, N-CAM, and N-cadherin.
    Neuron. 1994 Sep;13(3):583-94 PMID: 7917292
  48. N-cadherin expression in developing, adult and denervated chicken neuromuscular system: accumulations at both the neuromuscular junction and the node of Ranvier.
    Development. 1994 Jan;120(1):1-11 PMID: 8119118
  49. Interaction of the adaptor protein Shc and the adhesion molecule cadherin.
    J Biol Chem. 1997 May 23;272(21):13463-6 PMID: 9153187
  50. Uvomorulin-catenin complex formation is regulated by a specific domain in the cytoplasmic region of the cell adhesion molecule.
    Proc Natl Acad Sci U S A. 1990 Jun;87(11):4246-50 PMID: 2349235
  51. From cadherins to catenins: cytoplasmic protein interactions and regulation of cell adhesion.
    Trends Genet. 1993 Sep;9(9):317-21 PMID: 8236461
  52. Functional interaction of beta-catenin with the transcription factor LEF-1.
    Nature. 1996 Aug 15;382(6592):638-42 PMID: 8757136
  53. Submembranous junctional plaque proteins include potential tumor suppressor molecules.
    J Cell Biol. 1993 Dec;123(5):1049-53 PMID: 8245116
  54. The cytoplasmic domain of the cell adhesion molecule uvomorulin associates with three independent proteins structurally related in different species.
    EMBO J. 1989 Jun;8(6):1711-7 PMID: 2788574
  55. The molecular organization of endothelial cell to cell junctions: differential association of plakoglobin, beta-catenin, and alpha-catenin with vascular endothelial cadherin (VE-cadherin).
    J Cell Biol. 1995 Apr;129(1):203-17 PMID: 7698986
  56. c-erbB-2 gene product directly associates with beta-catenin and plakoglobin.
    Biochem Biophys Res Commun. 1995 Mar 28;208(3):1067-72 PMID: 7702605
  57. pac gene as efficient dominant marker and reporter gene in mammalian cells.
    Methods Enzymol. 1992;216:376-85 PMID: 1479910
  58. Molecular cloning and expression of murine vascular endothelial-cadherin in early stage development of cardiovascular system.
    Blood. 1996 Jan 15;87(2):630-41 PMID: 8555485
  59. The body language of cells: the intimate connection between cell adhesion and behavior.
    Cell. 1995 Oct 6;83(1):5-8 PMID: 7553873
  60. Cell binding function of E-cadherin is regulated by the cytoplasmic domain.
    EMBO J. 1988 Dec 1;7(12):3679-84 PMID: 3061804
Article Info
Journal
The Journal of cell biology
Abbr.
J Cell Biol
ISSN
0021-9525
Published
1998-03-23
Pages
1475-84
Language
English
Region
United States
NLM ID
0375356
PMCID
PMC2132661
Subset
IM
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