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PMID: 1327298 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Epidermal growth factor disrupts gap-junctional communication and induces phosphorylation of connexin43 on serine.

Molecular biology of the cell ·Vol. 3 ·No. 8 ·1992-08-00 ·Pages 865-74

Lau AF, Kanemitsu MY, Kurata WE, Danesh S, Boynton AL

Abstract

Growth factors regulate cellular proliferation and differentiation by activating plasma membrane tyrosine kinase receptors and triggering a cascade of events mediated by intracellular signaling proteins. The mechanism underlying growth factor modification of cellular functions, such as gap-junctional communication (gjc), has not been established clearly. Addition of epidermal growth factor (EGF) to T51B rat liver epithelial cells resulted in the rapid activation of EGF receptor tyrosine kinase activity followed by a transient dose-dependent disruption of gjc. This change did not result from the gross disturbance of membrane gap junction plaques as measured by immunofluorescence microscopy, but instead correlated with markedly elevated phosphorylation of the connexin43 (cx43) gap junction protein, a profound shift to predominantly phosphorylated forms of cx43, and the appearance of a novel phosphorylated cx43 protein. These changes in cx43 phosphorylation involved only serine residues. On restoration of gjc, these alterations in cx43 phosphorylation reverted to the pre-EGF treatment state. Both events were inhibited by the serine/threonine protein phosphatase inhibitor, okadaic acid. Therefore, unlike the case for pp60v-src, EGF-induced disruption of gjc is not associated with tyrosine phosphorylation of cx43, but instead may result from phosphorylation of cx43 by activated intracellular signaling serine protein kinase(s).

Related Genes
MeSH Terms
Animals Cell Communication/physiology Cells, Cultured Connexins Epidermal Growth Factor/physiology Intercellular Junctions/metabolism,physiology Liver/cytology Membrane Proteins/metabolism Microscopy, Fluorescence Phosphorylation Precipitin Tests Protein-Tyrosine Kinases/metabolism Rats Serine/metabolism
Chemicals
Connexins Membrane Proteins Serine Epidermal Growth Factor Protein-Tyrosine Kinases
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Lau A F
Molecular Oncology Program, University of Hawaii, Manoa, Honolulu 96813.
Kanemitsu M Y
Kurata W E
Danesh S
Boynton A L
References (51)
51 references, click to expand
  1. Mechanism of desensitization of the epidermal growth factor receptor protein-tyrosine kinase.
    J Biol Chem. 1992 Jan 15;267(2):1129-40 PMID: 1309762
  2. Selective disruption of gap junctional communication interferes with a patterning process in hydra.
    Science. 1987 Jul 3;237(4810):49-55 PMID: 3037697
  3. ras mediates nerve growth factor receptor modulation of three signal-transducing protein kinases: MAP kinase, Raf-1, and RSK.
    Cell. 1992 Mar 20;68(6):1041-50 PMID: 1312393
  4. Connexin43 in MDCK cells: regulation by a tumor-promoting phorbol ester and Ca2+.
    Eur J Cell Biol. 1992 Feb;57(1):40-50 PMID: 1322299
  5. Pro-Leu-Ser/Thr-Pro is a consensus primary sequence for substrate protein phosphorylation. Characterization of the phosphorylation of c-myc and c-jun proteins by an epidermal growth factor receptor threonine 669 protein kinase.
    J Biol Chem. 1991 Aug 15;266(23):15277-85 PMID: 1651323
  6. Phorbol ester induces phosphorylation and down-regulation of connexin 43 in WB cells.
    Biochim Biophys Acta. 1991 Sep 3;1094(2):243-5 PMID: 1654122
  7. The tumor promoter 12-O-tetradecanoylphorbol-13-acetate and the ras oncogene modulate expression and phosphorylation of gap junction proteins.
    Mol Cell Biol. 1991 Oct;11(10):5364-71 PMID: 1656230
  8. Tumor suppressor genes.
    Science. 1991 Nov 22;254(5035):1138-46 PMID: 1659741
  9. Phosphorylation of connexin43 gap junction protein in uninfected and Rous sarcoma virus-transformed mammalian fibroblasts.
    Mol Cell Biol. 1990 Apr;10(4):1754-63 PMID: 1690850
  10. Multiple components in an epidermal growth factor-stimulated protein kinase cascade. In vitro activation of a myelin basic protein/microtubule-associated protein 2 kinase.
    J Biol Chem. 1991 Mar 5;266(7):4220-7 PMID: 1705548
  11. Tissue-specific distribution of differentially phosphorylated forms of Cx43.
    Mol Cell Biol. 1991 Jan;11(1):363-9 PMID: 1846023
  12. Transfection of C6 glioma cells with connexin 43 cDNA: analysis of expression, intercellular coupling, and cell proliferation.
    Proc Natl Acad Sci U S A. 1991 Mar 1;88(5):1883-7 PMID: 1848013
  13. Positive selection of candidate tumor-suppressor genes by subtractive hybridization.
    Proc Natl Acad Sci U S A. 1991 Apr 1;88(7):2825-9 PMID: 1849277
  14. Tyrosine phosphorylation of a gap junction protein correlates with inhibition of cell-to-cell communication.
    Cell Growth Differ. 1990 Dec;1(12):661-8 PMID: 1963075
  15. Identification of multiple epidermal growth factor-stimulated protein serine/threonine kinases from Swiss 3T3 cells.
    J Biol Chem. 1990 Jul 15;265(20):11487-94 PMID: 2142153
  16. Okadaic acid: a new probe for the study of cellular regulation.
    Trends Biochem Sci. 1990 Mar;15(3):98-102 PMID: 2158158
  17. Signal transduction by receptors with tyrosine kinase activity.
    Cell. 1990 Apr 20;61(2):203-12 PMID: 2158859
  18. Phosphorylation of connexin 32, a hepatocyte gap-junction protein, by cAMP-dependent protein kinase, protein kinase C and Ca2+/calmodulin-dependent protein kinase II.
    Eur J Biochem. 1990 Sep 11;192(2):263-73 PMID: 2170122
  19. Control of myometrial contractility: role and regulation of gap junctions.
    Oxf Rev Reprod Biol. 1988;10:436-90 PMID: 3072507
  20. Cleavage of structural proteins during the assembly of the head of bacteriophage T4.
    Nature. 1970 Aug 15;227(5259):680-5 PMID: 5432063
  21. Relation between colony formation in calcium-deficient medium, colony formation in soft agar, and tumor formation by T51B rat liver cells.
    Cancer Lett. 1984 Jan;21(3):293-302 PMID: 6692347
  22. Junctional intercellular communication and the control of growth.
    Biochim Biophys Acta. 1979 Feb 4;560(1):1-65 PMID: 216404
  23. Phosphorylation of connexin43 in cells containing mutant src oncogenes.
    Oncogene. 1992 May;7(5):999-1003 PMID: 1315016
  24. Recent progress in characterization of protein kinase cascades for phosphorylation of ribosomal protein S6.
    Biochim Biophys Acta. 1991 May 17;1092(3):350-7 PMID: 1646641
  25. Consensus sequences as substrate specificity determinants for protein kinases and protein phosphatases.
    J Biol Chem. 1991 Aug 25;266(24):15555-8 PMID: 1651913
  26. Biochemical analysis of connexin43 intracellular transport, phosphorylation, and assembly into gap junctional plaques.
    J Cell Biol. 1991 Dec;115(5):1357-74 PMID: 1659577
  27. Incorporation of the gene for a cell-cell channel protein into transformed cells leads to normalization of growth.
    J Membr Biol. 1991 Dec;124(3):207-25 PMID: 1664859
  28. SH2 and SH3 domains: elements that control interactions of cytoplasmic signaling proteins.
    Science. 1991 May 3;252(5006):668-74 PMID: 1708916
  29. Turnover and phosphorylation dynamics of connexin43 gap junction protein in cultured cardiac myocytes.
    Biochem J. 1991 Jan 1;273(Pt 1):67-72 PMID: 1846532
  30. Identification, purification, and characterization of a novel serine/threonine protein phosphatase from bovine brain.
    J Biol Chem. 1991 Apr 5;266(10):6614-9 PMID: 1848859
  31. Tyrosine phosphorylation of the gap junction protein connexin43 is required for the pp60v-src-induced inhibition of communication.
    Cell Regul. 1990 Dec;1(13):989-1002 PMID: 1966893
  32. Evidence for an epidermal growth factor-stimulated protein kinase cascade in Swiss 3T3 cells. Activation of serine peptide kinase activity by myelin basic protein kinases in vitro.
    J Biol Chem. 1990 Jul 15;265(20):11495-501 PMID: 2142154
  33. Expression of the gap junction protein connexin43 in embryonic chick lens: molecular cloning, ultrastructural localization, and post-translational phosphorylation.
    J Membr Biol. 1990 Jun;116(2):163-75 PMID: 2166164
  34. Differential phosphorylation of the gap junction protein connexin43 in junctional communication-competent and -deficient cell lines.
    J Cell Biol. 1990 Nov;111(5 Pt 1):2077-88 PMID: 2172261
  35. The hormone-induced regulation of contact-dependent cell-cell communication by phosphorylation.
    Endocr Rev. 1990 May;11(2):302-25 PMID: 2194784
  36. Altered regulation of intercellular communication by epidermal growth factor, transforming growth factor-beta and peptide hormones in normal human keratinocytes.
    Carcinogenesis. 1989 Jan;10(1):13-20 PMID: 2463113
  37. Evidence that pp42, a major tyrosine kinase target protein, is a mitogen-activated serine/threonine protein kinase.
    Proc Natl Acad Sci U S A. 1989 Sep;86(18):6940-3 PMID: 2550926
  38. Further evidence for the involvement of gap-junctional intercellular communication in induction and maintenance of transformed foci in BALB/c 3T3 cells.
    Cancer Res. 1988 Jun 15;48(12):3490-5 PMID: 2836057
  39. Growth factors modulate junctional cell-to-cell communication.
    J Membr Biol. 1988 Dec;106(3):203-10 PMID: 2854164
  40. Cyclic adenosine monophosphate stimulates biosynthesis and phosphorylation of the 26 kDa gap junction protein in cultured mouse hepatocytes.
    Eur J Cell Biol. 1987 Feb;43(1):48-54 PMID: 3032632
  41. The role of gap junctions in development.
    Annu Rev Physiol. 1985;47:319-35 PMID: 3888077
  42. Ras is essential for nerve growth factor- and phorbol ester-induced tyrosine phosphorylation of MAP kinases.
    Cell. 1992 Mar 20;68(6):1031-40 PMID: 1312392
  43. Epidermal growth factor.
    J Biol Chem. 1990 May 15;265(14):7709-12 PMID: 2186024
  44. Growth inhibition of transformed cells correlates with their junctional communication with normal cells.
    Cell. 1986 Jan 17;44(1):187-96 PMID: 2416473
  45. Phosphotyrosine-containing 120,000-dalton protein coimmunoprecipitated with pp60v-src from Rous sarcoma virus-transformed mammalian cells.
    Virology. 1986 May;151(1):86-99 PMID: 2421483
  46. Acid and base hydrolysis of phosphoproteins bound to immobilon facilitates analysis of phosphoamino acids in gel-fractionated proteins.
    Anal Biochem. 1989 Jan;176(1):22-7 PMID: 2540676
  47. Phosphorylation of the 27-kDa gap junction protein by protein kinase C in vitro and in rat hepatocytes.
    J Biochem. 1989 Oct;106(4):723-7 PMID: 2558115
  48. Connexin43: a protein from rat heart homologous to a gap junction protein from liver.
    J Cell Biol. 1987 Dec;105(6 Pt 1):2621-9 PMID: 2826492
  49. Epidermal growth factor-stimulated DNA synthesis requires an influx of extracellular calcium.
    J Cell Biochem. 1988 Oct;38(2):137-44 PMID: 2851595
  50. cAMP increases junctional conductance and stimulates phosphorylation of the 27-kDa principal gap junction polypeptide.
    Proc Natl Acad Sci U S A. 1986 Apr;83(8):2473-7 PMID: 3010311
  51. Junctional intercellular communication: the cell-to-cell membrane channel.
    Physiol Rev. 1981 Oct;61(4):829-913 PMID: 6270711
Article Info
Journal
Molecular biology of the cell
Abbr.
Mol Biol Cell
ISSN
1059-1524
Published
1992-08-00
Pages
865-74
Language
English
Region
United States
NLM ID
9201390
PMCID
PMC275645
Subset
IM
Grants
NCI NIH HHS · CA 57064 · United States
NCI NIH HHS · CA39745 · United States
NCI NIH HHS · CA52098 · United States
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