Home LiteratureArticle Details
PMID: 10657259 Published · ppublish English Journal Article

Vascular endothelial growth factor stimulates dephosphorylation of the catenins p120 and p100 in endothelial cells.

The Biochemical journal ·Vol. 346 Pt 1 ·2000-02-15 ·Pages 209-16

Wong EY, Morgan L, Smales C, Lang P, Gubby SE, Staddon JM

Abstract

Vascular endothelial growth factor (VEGF) is an endothelium-specific mitogen that induces angiogenesis and increases vascular permeability. These processes involve regulation of cell-cell adhesion, but molecular mechanisms have yet to be fully established. p120, also termed p120(ctn), and its variant p100 are catenins which associate with cadherins and localize to adherens junctions. VEGF was reported to stimulate tyrosine phosphorylation of catenins in endothelial cells. In contrast, we have found that VEGF potently stimulated a rapid and dose-dependent decrease in serine/threonine phosphorylation of p120 and p100. VEGF acted via VEGF receptor 2 to achieve this effect which was independent of activation of the extracellular-signal-regulated kinase pathway. Histamine and activators of protein kinase C had a very similar effect to that of VEGF on phosphorylation of p120 and p100, suggesting that these diverse stimuli may converge on a common signalling element regulating p120/p100 serine/threonine phosphorylation. These data raise the possibility that the dephosphorylation of p120 and p100 triggered by VEGF may contribute to mechanisms regulating permeability and/or motility through modulation of cadherin adhesiveness.

MeSH Terms
Cadherins/metabolism Catenins Cell Adhesion Molecules/chemistry,genetics,metabolism Cells, Cultured Dose-Response Relationship, Drug Electrophoresis, Polyacrylamide Gel Endothelial Growth Factors/pharmacology Endothelium, Vascular/cytology,drug effects,enzymology,metabolism Enzyme Activation/drug effects Genetic Variation/genetics Histidine/pharmacology Humans Kinetics Lymphokines/pharmacology Mitogen-Activated Protein Kinases/metabolism Molecular Weight Peptide Mapping Phorbol 12,13-Dibutyrate/pharmacology Phosphoamino Acids/metabolism Phosphoproteins/chemistry,genetics,metabolism Phosphorylation/drug effects Precipitin Tests Protein Kinase C/metabolism Receptor Protein-Tyrosine Kinases/metabolism Receptors, Growth Factor/metabolism Receptors, Vascular Endothelial Growth Factor Signal Transduction/drug effects Vascular Endothelial Growth Factor A Vascular Endothelial Growth Factors
Chemicals
Cadherins Catenins Cell Adhesion Molecules Endothelial Growth Factors Lymphokines Phosphoamino Acids Phosphoproteins Receptors, Growth Factor Vascular Endothelial Growth Factor A Vascular Endothelial Growth Factors delta catenin Phorbol 12,13-Dibutyrate Histidine Receptor Protein-Tyrosine Kinases Receptors, Vascular Endothelial Growth Factor Protein Kinase C Mitogen-Activated Protein Kinases
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Wong E Y
Eisai London Research Laboratories Ltd., Bernard Katz Building, University College London, Gower Street, London WC1E 6BT, U.K.
Morgan L
Smales C
Lang P
Gubby S E
Staddon J M
References (40)
40 references, click to expand
  1. Association of p120, a tyrosine kinase substrate, with E-cadherin/catenin complexes.
    J Cell Biol. 1995 Mar;128(5):949-57 PMID: 7876318
  2. p120(ctn) binds to the membrane-proximal region of the E-cadherin cytoplasmic domain and is involved in modulation of adhesion activity.
    J Biol Chem. 1999 Jul 23;274(30):21409-15 PMID: 10409703
  3. 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
  4. Evidence that tyrosine phosphorylation may increase tight junction permeability.
    J Cell Sci. 1995 Feb;108 ( Pt 2):609-19 PMID: 7769005
  5. p120, a p120-related protein (p100), and the cadherin/catenin complex.
    J Cell Biol. 1995 Jul;130(2):369-81 PMID: 7615637
  6. 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
  7. Peptide mapping by limited proteolysis in sodium dodecyl sulfate and analysis by gel electrophoresis.
    J Biol Chem. 1977 Feb 10;252(3):1102-6 PMID: 320200
  8. Specific proto-oncogenic tyrosine kinases of src family are enriched in cell-to-cell adherens junctions where the level of tyrosine phosphorylation is elevated.
    J Cell Biol. 1991 May;113(4):867-79 PMID: 1709169
  9. Phosphopeptide mapping and phosphoamino acid analysis by two-dimensional separation on thin-layer cellulose plates.
    Methods Enzymol. 1991;201:110-49 PMID: 1943760
  10. Regulation of embryonic cell adhesion by the cadherin cytoplasmic domain.
    Cell. 1992 Apr 17;69(2):225-36 PMID: 1568244
  11. 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
  12. 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
  13. PD 098059 is a specific inhibitor of the activation of mitogen-activated protein kinase kinase in vitro and in vivo.
    J Biol Chem. 1995 Nov 17;270(46):27489-94 PMID: 7499206
  14. Catenin-dependent and -independent functions of vascular endothelial cadherin.
    J Biol Chem. 1995 Dec 29;270(52):30965-72 PMID: 8537353
  15. 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
  16. Cadherin-catenin complex: protein interactions and their implications for cadherin function.
    J Cell Biochem. 1996 Jun 15;61(4):514-23 PMID: 8806074
  17. Similarities and differences between the vascular endothelial growth factor (VEGF) splice variants.
    Cancer Metastasis Rev. 1996 Jun;15(2):153-8 PMID: 8842486
  18. Characterization of vascular endothelial growth factor's effect on the activation of protein kinase C, its isoforms, and endothelial cell growth.
    J Clin Invest. 1996 Nov 1;98(9):2018-26 PMID: 8903320
  19. Cadherin function is required for axon outgrowth in retinal ganglion cells in vivo.
    Neuron. 1996 Nov;17(5):837-48 PMID: 8938117
  20. E-cadherin mediates adhesion and suppresses cell motility via distinct mechanisms.
    J Cell Sci. 1997 Feb;110 ( Pt 3):345-56 PMID: 9057087
  21. Mechanisms of angiogenesis.
    Nature. 1997 Apr 17;386(6626):671-4 PMID: 9109485
  22. The 230 kDa mature form of KDR/Flk-1 (VEGF receptor-2) activates the PLC-gamma pathway and partially induces mitotic signals in NIH3T3 fibroblasts.
    Oncogene. 1997 May 1;14(17):2079-89 PMID: 9160888
  23. Vascular endothelial growth factor stimulates tyrosine phosphorylation and recruitment to new focal adhesions of focal adhesion kinase and paxillin in endothelial cells.
    J Biol Chem. 1997 Jun 13;272(24):15442-51 PMID: 9182576
  24. Tyrosine phosphorylation and cadherin/catenin function.
    Bioessays. 1997 Oct;19(10):883-91 PMID: 9363682
  25. Dephosphorylation of the cadherin-associated p100/p120 proteins in response to activation of protein kinase C in epithelial cells.
    J Biol Chem. 1997 Dec 12;272(50):31894-901 PMID: 9395537
  26. The vascular endothelial growth factor receptor KDR activates multiple signal transduction pathways in porcine aortic endothelial cells.
    J Biol Chem. 1997 Dec 19;272(51):32521-7 PMID: 9405464
  27. Molecular and functional analysis of cadherin-based adherens junctions.
    Annu Rev Cell Dev Biol. 1997;13:119-46 PMID: 9442870
  28. Vascular endothelial growth factor stimulates prostacyclin production and activation of cytosolic phospholipase A2 in endothelial cells via p42/p44 mitogen-activated protein kinase.
    FEBS Lett. 1997 Dec 22;420(1):28-32 PMID: 9450544
  29. The juxtamembrane region of the cadherin cytoplasmic tail supports lateral clustering, adhesive strengthening, and interaction with p120ctn.
    J Cell Biol. 1998 May 4;141(3):779-89 PMID: 9566976
  30. Vascular endothelial growth factor induces VE-cadherin tyrosine phosphorylation in endothelial cells.
    J Cell Sci. 1998 Jul;111 ( Pt 13):1853-65 PMID: 9625748
  31. Molecular cloning of the human p120ctn catenin gene (CTNND1): expression of multiple alternatively spliced isoforms.
    Genomics. 1998 Jun 1;50(2):129-46 PMID: 9653641
  32. Tyrosine phosphorylation of paxillin/pp125FAK and microvascular endothelial barrier function.
    Am J Physiol. 1998 Jul;275(1 Pt 2):H84-93 PMID: 9688899
  33. The membrane-proximal region of the E-cadherin cytoplasmic domain prevents dimerization and negatively regulates adhesion activity.
    J Cell Biol. 1998 Sep 21;142(6):1605-13 PMID: 9744888
  34. Vascular endothelial growth factor regulates endothelial cell survival through the phosphatidylinositol 3'-kinase/Akt signal transduction pathway. Requirement for Flk-1/KDR activation.
    J Biol Chem. 1998 Nov 13;273(46):30336-43 PMID: 9804796
  35. Vascular endothelial growth factor (VEGF) and its receptors.
    FASEB J. 1999 Jan;13(1):9-22 PMID: 9872925
  36. SU5416 is a potent and selective inhibitor of the vascular endothelial growth factor receptor (Flk-1/KDR) that inhibits tyrosine kinase catalysis, tumor vascularization, and growth of multiple tumor types.
    Cancer Res. 1999 Jan 1;59(1):99-106 PMID: 9892193
  37. Structure and function of vascular endothelial growth factor receptor-1 and -2.
    Curr Top Microbiol Immunol. 1999;237:59-83 PMID: 9893346
  38. Dephosphorylation of the catenins p120 and p100 in endothelial cells in response to inflammatory stimuli.
    Biochem J. 1999 Mar 1;338 ( Pt 2):471-8 PMID: 10024525
  39. p120(ctn) acts as an inhibitory regulator of cadherin function in colon carcinoma cells.
    J Cell Biol. 1999 May 3;145(3):551-62 PMID: 10225956
  40. Assembly of the cadherin-catenin complex in vitro with recombinant proteins.
    J Cell Sci. 1994 Dec;107 ( Pt 12):3655-63 PMID: 7706414
Article Info
Journal
The Biochemical journal
Abbr.
Biochem J
ISSN
0264-6021
Published
2000-02-15
Pages
209-16
Language
English
Region
England
NLM ID
2984726R
PMCID
PMC1220842
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com