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PMID: 9566976 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

The juxtamembrane region of the cadherin cytoplasmic tail supports lateral clustering, adhesive strengthening, and interaction with p120ctn.

The Journal of cell biology ·Vol. 141 ·No. 3 ·1998-05-04 ·Pages 779-89

Yap AS, Niessen CM, Gumbiner BM

Abstract

Cadherin cell-cell adhesion molecules form membrane-spanning molecular complexes that couple homophilic binding by the cadherin ectodomain to the actin cytoskeleton. A fundamental issue in cadherin biology is how this complex converts the weak intrinsic binding activity of the ectodomain into strong adhesion. Recently we demonstrated that cellular cadherins cluster in a ligand-dependent fashion when cells attached to substrata coated with the adhesive ectodomain of Xenopus C-cadherin (CEC1-5). Moreover, forced clustering of the ectodomain alone significantly strengthened adhesiveness (Yap, A.S., W.M. Brieher, M. Pruschy, and B.M. Gumbiner. Curr. Biol. 7:308-315). In this study we sought to identify the determinants of the cadherin cytoplasmic tail responsible for clustering activity. A deletion mutant of C-cadherin (CT669) that retained the juxtamembrane 94-amino acid region of the cytoplasmic tail, but not the beta-catenin-binding domain, clustered upon attachment to substrata coated with CEC1-5. Like wild-type C-cadherin, this clustering was ligand dependent. In contrast, mutant molecules lacking either the complete cytoplasmic tail or just the juxtamembrane region did not cluster. The juxtamembrane region was itself sufficient to induce clustering when fused to a heterologous membrane-anchored protein, albeit in a ligand-independent fashion. The CT669 cadherin mutant also displayed significant adhesive activity when tested in laminar flow detachment assays and aggregation assays. Purification of proteins binding to the juxtamembrane region revealed that the major associated protein is p120(ctn). These findings identify the juxtamembrane region of the cadherin cytoplasmic tail as a functionally active region supporting cadherin clustering and adhesive strength and raise the possibility that p120(ctn) is involved in clustering and cell adhesion.

MeSH Terms
Amino Acid Sequence Animals Binding Sites CHO Cells Cadherins/genetics,metabolism Catenins Cell Adhesion Cell Adhesion Molecules/metabolism Cricetinae Cytoplasm/metabolism Gene Expression Membrane Proteins/metabolism Molecular Sequence Data Mutagenesis Phosphoproteins/metabolism Recombinant Fusion Proteins/genetics,metabolism
Chemicals
Cadherins Catenins Cell Adhesion Molecules Membrane Proteins Phosphoproteins Recombinant Fusion Proteins delta catenin
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Yap A S
Cellular Biochemistry and Biophysics Program, Memorial Sloan-Kettering Cancer Center, New York, 10021, USA.
Niessen C M
Gumbiner B M
References (53)
53 references, click to expand
  1. Selective disruption of E-cadherin function in early Xenopus embryos by a dominant negative mutant.
    Development. 1994 Apr;120(4):901-9 PMID: 7600966
  2. Alpha 1(E)-catenin is an actin-binding and -bundling protein mediating the attachment of F-actin to the membrane adhesion complex.
    Proc Natl Acad Sci U S A. 1995 Sep 12;92(19):8813-7 PMID: 7568023
  3. Single-step purification of polypeptides expressed in Escherichia coli as fusions with glutathione S-transferase.
    Gene. 1988 Jul 15;67(1):31-40 PMID: 3047011
  4. Disruption of gastrulation movements in Xenopus by a dominant-negative mutant for C-cadherin.
    Dev Biol. 1995 Oct;171(2):363-73 PMID: 7556920
  5. Morphogenetic roles of classic cadherins.
    Curr Opin Cell Biol. 1995 Oct;7(5):619-27 PMID: 8573335
  6. Catenin-dependent and -independent functions of vascular endothelial cadherin.
    J Biol Chem. 1995 Dec 29;270(52):30965-72 PMID: 8537353
  7. Binding to cadherins antagonizes the signaling activity of beta-catenin during axis formation in Xenopus.
    J Cell Biol. 1996 Mar;132(6):1105-14 PMID: 8601588
  8. Cell adhesion: the molecular basis of tissue architecture and morphogenesis.
    Cell. 1996 Feb 9;84(3):345-57 PMID: 8608588
  9. Identification of murine p120 isoforms and heterogeneous expression of p120cas isoforms in human tumor cell lines.
    Cancer Res. 1996 Jun 1;56(11):2633-40 PMID: 8653709
  10. Armadillo is required for adherens junction assembly, cell polarity, and morphogenesis during Drosophila embryogenesis.
    J Cell Biol. 1996 Jul;134(1):133-48 PMID: 8698810
  11. Mechanism for transition from initial to stable cell-cell adhesion: kinetic analysis of E-cadherin-mediated adhesion using a quantitative adhesion assay.
    J Cell Biol. 1996 Jul;134(2):549-57 PMID: 8707837
  12. Lateral dimerization is required for the homophilic binding activity of C-cadherin.
    J Cell Biol. 1996 Oct;135(2):487-96 PMID: 8896604
  13. Cadherin function is required for axon outgrowth in retinal ganglion cells in vivo.
    Neuron. 1996 Nov;17(5):837-48 PMID: 8938117
  14. 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
  15. An alpha-E-catenin gene trap mutation defines its function in preimplantation development.
    Proc Natl Acad Sci U S A. 1997 Feb 4;94(3):901-6 PMID: 9023354
  16. E-cadherin mediates adhesion and suppresses cell motility via distinct mechanisms.
    J Cell Sci. 1997 Feb;110 ( Pt 3):345-56 PMID: 9057087
  17. The roles of maternal alpha-catenin and plakoglobin in the early Xenopus embryo.
    Development. 1997 Apr;124(8):1553-60 PMID: 9108371
  18. Uncoupling of XB/U-cadherin-catenin complex formation from its function in cell-cell adhesion.
    J Biol Chem. 1997 May 2;272(18):11856-62 PMID: 9115244
  19. Lateral clustering of the adhesive ectodomain: a fundamental determinant of cadherin function.
    Curr Biol. 1997 May 1;7(5):308-15 PMID: 9133345
  20. Simulation of detachment of specifically bound particles from surfaces by shear flow.
    Biophys J. 1997 Jul;73(1):517-31 PMID: 9199814
  21. Enhanced signaling and morphological transformation by a membrane-localized derivative of the fibroblast growth factor receptor 3 kinase domain.
    Mol Cell Biol. 1997 Oct;17(10):5739-47 PMID: 9315632
  22. Cell confluence regulates tyrosine phosphorylation of adherens junction components in endothelial cells.
    J Cell Sci. 1997 Sep;110 ( Pt 17):2065-77 PMID: 9378757
  23. Tyrosine phosphorylation and cadherin/catenin function.
    Bioessays. 1997 Oct;19(10):883-91 PMID: 9363682
  24. Molecular and functional analysis of cadherin-based adherens junctions.
    Annu Rev Cell Dev Biol. 1997;13:119-46 PMID: 9442870
  25. Interaction of alpha-actinin with the cadherin/catenin cell-cell adhesion complex via alpha-catenin.
    J Cell Biol. 1995 Jul;130(1):67-77 PMID: 7790378
  26. Isolation of monoclonal antibodies specific for human c-myc proto-oncogene product.
    Mol Cell Biol. 1985 Dec;5(12):3610-6 PMID: 3915782
  27. Functional correlation between cell adhesive properties and some cell surface proteins.
    J Cell Biol. 1977 Nov;75(2 Pt 1):464-74 PMID: 264120
  28. Cell binding function of E-cadherin is regulated by the cytoplasmic domain.
    EMBO J. 1988 Dec 1;7(12):3679-84 PMID: 3061804
  29. 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
  30. Purification of a 92-kDa cytoplasmic protein tightly associated with the cell-cell adhesion molecule E-cadherin (uvomorulin). Characterization and extractability of the protein complex from the cell cytostructure.
    J Biol Chem. 1991 Mar 5;266(7):4514-20 PMID: 1999432
  31. Cadherin cell adhesion receptors as a morphogenetic regulator.
    Science. 1991 Mar 22;251(5000):1451-5 PMID: 2006419
  32. 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
  33. Regulation of fibronectin receptor distribution.
    J Cell Biol. 1992 Apr;117(2):437-47 PMID: 1373145
  34. Regulation of embryonic cell adhesion by the cadherin cytoplasmic domain.
    Cell. 1992 Apr 17;69(2):225-36 PMID: 1568244
  35. 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
  36. Disruption of epithelial cell-cell adhesion by exogenous expression of a mutated nonfunctional N-cadherin.
    Mol Biol Cell. 1993 Jan;4(1):37-47 PMID: 8443408
  37. Use of mass spectrometric molecular weight information to identify proteins in sequence databases.
    Biol Mass Spectrom. 1993 Jun;22(6):338-45 PMID: 8329463
  38. Distinguishing roles of the membrane-cytoskeleton and cadherin mediated cell-cell adhesion in generating different Na+,K(+)-ATPase distributions in polarized epithelia.
    J Cell Biol. 1993 Oct;123(1):149-64 PMID: 8408194
  39. Controlling signal transduction with synthetic ligands.
    Science. 1993 Nov 12;262(5136):1019-24 PMID: 7694365
  40. Regulation of C-cadherin function during activin induced morphogenesis of Xenopus animal caps.
    J Cell Biol. 1994 Jul;126(2):519-27 PMID: 8034750
  41. Induction of polarized cell-cell association and retardation of growth by activation of the E-cadherin-catenin adhesion system in a dispersed carcinoma line.
    J Cell Biol. 1994 Oct;127(1):247-56 PMID: 7929567
  42. Identification of a new catenin: the tyrosine kinase substrate p120cas associates with E-cadherin complexes.
    Mol Cell Biol. 1994 Dec;14(12):8333-42 PMID: 7526156
  43. Posttranslational regulation of plakoglobin expression. Influence of the desmosomal cadherins on plakoglobin metabolic stability.
    J Biol Chem. 1994 Dec 9;269(49):31214-23 PMID: 7983064
  44. E-cadherin and APC compete for the interaction with beta-catenin and the cytoskeleton.
    J Cell Biol. 1994 Dec;127(6 Pt 2):2061-9 PMID: 7806582
  45. A short core region of E-cadherin is essential for catenin binding and is highly phosphorylated.
    Cell Adhes Commun. 1994 Aug;2(4):319-27 PMID: 7820535
  46. Association of p120, a tyrosine kinase substrate, with E-cadherin/catenin complexes.
    J Cell Biol. 1995 Mar;128(5):949-57 PMID: 7876318
  47. Embryonic axis induction by the armadillo repeat domain of beta-catenin: evidence for intracellular signaling.
    J Cell Biol. 1995 Mar;128(5):959-68 PMID: 7876319
  48. Assembly of the cadherin-catenin complex in vitro with recombinant proteins.
    J Cell Sci. 1994 Dec;107 ( Pt 12):3655-63 PMID: 7706414
  49. In vivo analysis of cadherin function in the mouse intestinal epithelium: essential roles in adhesion, maintenance of differentiation, and regulation of programmed cell death.
    J Cell Biol. 1995 Apr;129(2):489-506 PMID: 7721948
  50. Plasticity in epithelial cell phenotype: modulation by expression of different cadherin cell adhesion molecules.
    J Cell Biol. 1995 Apr;129(2):507-19 PMID: 7536748
  51. High-sensitivity sequencing of large proteins: partial structure of the rapamycin-FKBP12 target.
    Protein Sci. 1994 Dec;3(12):2435-46 PMID: 7756997
  52. Genetic and biochemical dissection of protein linkages in the cadherin-catenin complex.
    Proc Natl Acad Sci U S A. 1995 May 23;92(11):5067-71 PMID: 7761449
  53. p120, a p120-related protein (p100), and the cadherin/catenin complex.
    J Cell Biol. 1995 Jul;130(2):369-81 PMID: 7615637
Article Info
Journal
The Journal of cell biology
Abbr.
J Cell Biol
ISSN
0021-9525
Published
1998-05-04
Pages
779-89
Language
English
Region
United States
NLM ID
0375356
PMCID
PMC2132752
Subset
IM
Grants
NIGMS NIH HHS · GM52717 · United States
NCI NIH HHS · P30-CA-08748 · United States
Analysis Services
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