Platelet-derived growth factor-induced disruption of gap junctional communication and phosphorylation of connexin43 involves protein kinase C and mitogen-activated protein kinase

Journal of Cellular Physiology

Volumn 176, Issue 2, 1998, Pages 332-341

  Hossain, Mohammad Z ^a   Ao, Peng ^a   Boynton, Alton L ^a  

^a NORTHWEST HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; CALPHOSTIN C; CONNEXIN 43; CYCLOHEXIMIDE; MITOGEN ACTIVATED PROTEIN KINASE; PHORBOL 13 ACETATE 12 MYRISTATE; PLATELET DERIVED GROWTH FACTOR BB; PROTEIN KINASE C;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVATION; GAP JUNCTION; LIVER CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RAT;

ANIMALS; CA(2+)-CALMODULIN DEPENDENT PROTEIN KINASE; CARCINOGENS; CELL COMMUNICATION; CONNEXIN 43; ENZYME INHIBITORS; EPITHELIAL CELLS; GAP JUNCTIONS; LIVER; NAPHTHALENES; PHOSPHORYLATION; PLATELET-DERIVED GROWTH FACTOR; PROTEIN KINASE C; RATS; TETRADECANOYLPHORBOL ACETATE;

ANIMALIA;

EID: 0031824861     PISSN: 00219541     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1097-4652(199808)176:2<332::AID-JCP11>3.0.CO;2-5     Document Type: Article

References (87)

1. Akimoto, K., Takahashi, R., Moriya, S., Nishioka, N., Takayanagi, J., Kimura, K., Fukui, Y., Osada, Si., Mizuno, K., Hirai, Si., Kazlauskas, A., and Ohno, S. (1996) EGF or PDGF receptors activate atypical PKC lambda through phosphatidylinositol 3-kinase. EMBO J., 15:788-798.
2. Berthoud, V.M., Rook, M.B., Traub, O., Hertzberg, E.L., and Saez, J.C. (1993) On the mechanisms of cell uncoupling induced by a tumor promoter phorbol ester in clone 9 cells, a rat liver epithelial cell line. Eur. J. Cell Biol., 61:384-396.
3. Beyer, E.C., Paul, D.L., and Goodenough, D.A. (1990) Connexin family of gap junction proteins. J. Membr. Biol., 116:187-194.
4. Bohmer, F.D., Bohmer, A., Obermeier, A., and Ullrich, A. (1995) Use of selective tyrosine kinase blockers to monitor growth factor receptor dephosphorylation in intact cells. Anal. Biochem., 228:267-273.
5. Boynton, A.L., Kleine, L.P., and Whitfield, J.F. (1984) Relation between colony formation in calcium-deficient medium, colony formation in soft agar, and tumor formation by rat T51B cells. Cancer Lett., 21:293-302.
6. Brooks, G., Goss, M.W., and Hart, I.R. (1992) Differential induction of 12-O-tradecanoylphorbol-13-acetate sequence gene expression in murine melanocytes and melanoma cells. Mol. Carcinog., 5:328-333.
7. Bruzzone, R., White, T.W., and Paul, D.L. (1996) Connection with connexins: The molecular basis of direct intercellular signalling. Eur. J. Biochem., 238:1-27.
8. Burack, W.R., and Sturgill, T.W. (1997) The activating dual phosphorylation of MAPK by MEK is nonprocessive. Biochemistry, 36:5929-5933.
9. Cai, H., Smola, U., Wixler, V., Eisenmann-Tappe, I., Diaz-Meco, M.T., Moscat, J., Rapp, U., and Cooper, G.M. (1997) Role of diacylglycerol-regulated protein kinase C isotypes in growth factor activation of the raf-1 protein kinase. Mol. Cell. Biol., 17:732-741.
10. Chen, S.C., Pelletier, D.E., Ao, P., and Boynton, A.L. (1995) Connexin43 reverses the phenotype of transformed cells and alters their expression of cyclin/cyclin-dependent kinases. Cell Growth Differ., 6:681-690.
11. Choudhury, G.G., Biswas, P., Grandaliano, G., and Abboud, H.E. (1993) Involvement of PKC-alpha in PDGF-mediated mitogenic signaling in human mesangial cells. Am. J. Physiol., 265:F634-642.
12. Claesson-Welsh, L. (1995) Platelet-derived growth factor receptor signals. J. Biol. Chem., 269:32023-32026.
13. Cmarik, J.L., Herschman, H., and Colburn, N.H. (1994) Preferential primary-response gene expression in promotion-resistant versus promotion-sensitive JB6 cells. Mol. Carcinog., 11:115-124.
14. Cobb, M.H., and Goldsmith, E.J. (1995) How MAP kinases are regulated. J. Biol. Chem., 270:14843-14846.
15. 2+-dependent signal pathways in Rat-1 cells. J. Biol. Chem., 272:13309-13319.
16. Crow, D.S., Beyer, E.C., Paul, D.L., Kobe, S.S., and Lau, A.F. (1990) Phosphorylation of Cx43 gap junction protein in uninfected and Rous sarcoma virus-transformed mammalian fibroblasts. Mol. Cell. Biol., 10:1754-1763.
17. Dean, N.M., McKay, R., Condon, T.P., and Bennett, C.F. (1994) Inhibition of protein kinase C-alpha expression in human A549 cells by antisense oligonucleotides inhibits induction of intercellular adhesion molecule 1 (ICAM-1) mRNA by phorbol esters. J. Biol. Chem., 269:16416-16424.
18. Dudley, D.T., Pang, L., Decker, S.J., Bridges, A.J., and Saltiel, A.R. (1995) A synthetic inhibitor of the mitogen-activated protein kinase cascade. Proc. Natl. Acad. Sci. USA, 92:7686-7689.
19. Duff, J.L., Monia, B.P., and Berk, B.C. (1995) Mitogen-activated protein (MAP) kinase is regulated by the MAP kinase phosphatase (MKP-1) in vascular smooth muscle cells. Effect of actinomycin D and antisense oligonucleotides. J. Biol. Chem., 270:7161-7166.
20. Eghbali, B., Kessler, J.A., Reid, L.M., Roy, C., and Spray, D.C. (1991) Involvement of gap junctions in tumorigenesis: Transaction of hepatoma cells with connexin32 retards growth in vivo. Proc. Natl. Acad. Sci. USA, 88:10701-10705.
21. k and NRK cells. J. Membr. Biol., 155:275-287.
22. Finbow, M.E., Harrison, M., and Jones, P. (1995) Ductin - a proton pump component, a gap junction channel and a neurotransmitter release channel. Bioessays, 17:247-255.
23. Golard, A., Role, L.W., and Siegelbaum, S.A. (1993) Protein kinase C blocks somatostatin-induced modulation of calcium current in chick sympathetic neurons. J. Neurophysiol., 70:1639-1643.
24. Goppelt-Struebe, M., Stroebel, M., and Hoppe, J. (1996) Regulation of platelet-derived growth factor isoform-mediated expression of prostaglandin G/H synthase in mesangial cells. Kidney Int., 50:71-78.
25. Gotoh, N., Toyoda, M., and Shibuya, M. (1997) Tyrosine phosphorylation sites at amino acids 239 and 240 of shc are involved in epidermal growth factor-induced mitogenic signaling that is distinct from ras/mitogen-activated protein kinase kinase activation. Mol. Cell. Biol., 17:1824-1831.
26. Graves, L.M., Bornfeld, K.E., Raines, E.W., Potts, B.C., Macdonald, S.G., Rossa, R., and Krebs, E.G. (1993) Protein kinase A antagonizes platelet-derived growth factor-induced signalling by mitogen-activated protein kinase in human arterial smooth muscle cells. Proc. Natl. Acad. Sci. USA, 90:10300-10304.
27. Heldin, C.H. (1995) Dimerization of cell surface receptors in signal transduction. Cell, 80:213-223.
28. Herschman, H.R., Kujubu, D.A., Fletcher, B.S., Ma, Q., Varnum, B.C., Gilbert, R.S., and Reddy, S.T. (1994) The tis genes, primary response genes induced by growth factors and tumor promoters in 3T3 cells. Prog. Nucleic Acid Res. Mol. Biol., 47:113-148.
29. Hii, C.S., Oh, S.Y., Schmidt, S.A., Clark, K.J., and Murray, A.W. (1994) Lysophosphatidic acid inhibits gap junctional communication and stimulates phosphorylation of connexin43 in WB cells: Possible involvement of the mitogen-activated protein kinase cascade. Biochem. J., 303:475-479.
30. Hii, C.S., Ferrante, A., Edwards, Y.S., Huang, Z.H., Hartfield, P.J., Rathjen, D.A., Poulos, A., and Murray, A.W. (1995a) Activation of mitogen-activated protein kinase by arachidonic acid in rat liver epithelial WB cells by a protein kinase C-dependent mechanism. J. Biol. Chem., 270:4201-4204.
31. Hii, C.S., Ferrante, A., Schmidt, S., Rathjen, D.A., Robinson, B.S., Poulos, A., and Murray, A.W. (1995b) Inhibition of gap junctional communication by polyunsaturated fatty acids in WB cells: Evidence that connexin43 is not hyperphosphorylated. Carcinogenesis, 16:1505-1511.
32. Hill, T.D., Dean, N.M., Mordan, L.J., Lau, A.F., Kanemitsu, M.Y., and Boynton, A.L. (1990) PDGF-induced activation of phospholipase C is not required for induction of DNA synthesis. Science, 248:1660-1663.
33. Hossain, M.Z., Wilkens, L.R., Mehta, P.P., Loewenstein, W.R., and Bertram, J.S. (1989) Enhancement of gap junctional communication by retinoids correlates with their ability to inhibit neoplastic transformation. Carcinogenesis, 10:1743-1748.
34. Hossain, M.Z., Murphy, L.J., Hertzberg, E.L., and Nagy, J.I. (1994) Phosphorylated forms of connexin43 predominate in rat brain: Demonstration by rapid inactivation of brain metabolism. J. Neurochem., 62:2394-2403.
35. Hossain, M.Z., Ernst, L.A., and Nagy, J.I. (1995) Utility of intensely fluorescent cyanin dyes (Cy3) for assay of gap junctional communication by dye-transfer. Neurosci. Lett., 184:71-74.
36. Hossain, M.Z., Ao, P., and Boynton, A.L. (1998) Rapid disruption of gap junctional communication and phosphorylation of connexin43 by platelet-derived growth factor in T51B rat liver epithelial cells expressing PDGF receptor. J. Cell. Physiol. 174:66-77.
37. Huang, R.P., Wu, J.X., Fan, Y., and Adamson, E.D. (1996) UV activates growth factor receptors via reactive oxygen intermediates. J. Cell Biol., 133:211-220.
38. Kanemitsu, M.Y., and Lau, A.F. (1993) Epidermal growth factor stimulates the disruption of gap junctional communication and connexin43 phosphorylation independent of 12-O-tetradecanoylphorbol 13-acetate-sensitive protein kinase C: The possible involvement of mitogen-activated protein kinase. Mol. Biol. Cell, 4:837-848.
39. Kataoka, S., Alam, R., Dash, P.K., and Yatsu, F.M. (1997) Inhibition of PDGF-mediated proliferation of vascular smooth muscle cells by calcium antagonists. Stroke, 28:364-369.
40. Kazlauskas, A., and Cooper, J.A. (1989) Autophosphorylation of the PDGF receptor in the kinase insert region regulates interaction with cell proteins. Cell, 58:1121-1133.
41. Kazlauskas, A., Durden, D.L., and Cooper, J.A. (1991) Functions of the major tyrosine phosphorylation site of the PDGF receptor β subunit. Cell Regul., 2:413-425.
42. Koo, S.K., Kim, D.Y., Park, S.D., Kang, K.W., and Joe, C.O. (1997) PKC phosphorylation disrupts gap junctional communication at Go/ S phase in clone 9 cells. Mol. Cell. Biochem., 167:41-49.
43. Kumar, N.M., and Gilula, N.B. (1996) The gap junction communication channel. Cell, 84:381-388.
44. Kurata, W.E., and Lau, A.F. (1994) p130gag-fps disrupts gap junctional communication and induces phosphorylation of connexin43 in a manner similar to that of pp60v-src. Oncogene, 9:329-335.
45. Kwak, B.R., Hermans, M.M.P., De Jonge, H.R., Lohmann, S.M., Jongsma, H.J., and Chanson, M. (1995) Differential regulation of distinct types of gap junctional channels by similar phosphorylating conditions. Mol. Biol. Cell, 6:1707-1719.
46. Lau, A.F., Hatch-Pigot, V., and Crow, D.S. (1991) Evidence that heart connexin43 is a phosphoprotein. J. Mol. Cell. Cardiol., 23:659-663.
47. Lau, A.F., Kanemitsu, M.Y., Kurata, W.E., Danesh, S., and Boynton, A.L. (1992) Epidermal growth factor disrupts gap junctional communication and induces phosphorylation of connexin43 on serine. Mol. Biol. Cell, 3:865-874.
48. Lau, A.F., Kurata, W.E., Kanetmitsu, M.Y., Loo, L.W.M., Warn-Cramer, B.J., Eckhart, W., and Lampe, P.D. (1996) Regulation of connexin43 function by activated tyrosine protein kinases. J. Bioenerg. Biomembr., 28:359-368.
49. Lazar, D.F., Wiese, R.J., Brady, M.J., Mastick, C.C., Waters, S.B., Yamauchi, K., Pessin, J.E., Cuatrecasas, P., and Saltiel, A.R. (1995) Mitogen-activated protein kinase inhibition does not block the stimulation of glucose utilization by insulin. J. Biol. Chem., 270:20801-20807.
50. Leng, L., Du, B., Consigli, S., and McCaffrey, T.A. (1996) Translocation of protein kinase C-delta by PDGF in cultured vascular smooth muscle cells: inhibition by TGF-beta 1. Artery, 22:140-154.
51. Li, W., Yu, J.C., Michieli, P., Beeler, J.F., Ellmore, N., Heidaran, MA, and Pierce, J.H. (1994) Stimulation of the platelet-derived growth factor beta receptor signaling pathway activates protein kinase kinase C-delta. Mol. Cell. Biol., 14:6727-6735.
52. Liao, D.F., Duff, J.L., Daum, G., Pelech, S.L., and Berk, B.C. (1996) Angiotensin II stimulates MAP kinase kinase activity in vascular smooth muscle cells, role of raf. Circ. Res., 79:1007-1014.
53. Loewenstein, W.R., and Kanno Y. (1966) Intercellular communication and the control of tissue growth: Lack of communication between cancer cells. Nature, 209:1248-1249.
54. Loewenstein, W.R., and Rose, B. (1992) The cell-cell channel in the control of growth. Semin. Cell Biol., 3:59-79.
55. Ma, Y.H., Reusch, H.P., Wilson, E., Escobedo, J.A., Fantl, W.J., Williams, L.T., and Ives, H.E. (1994) Activation of Na+/H+ exchange by platelet-derived growth factor involves phosphatidylinositol 3′-kinase and phospholipase C gamma. J. Biol., Chem., 269:30734-30739.
56. Malarkey, K., Chilvers, E.R., Lawson, M.F., and Plevin, R. (1995) Stimulation by endothelin-1 of mitogen-activated protein kinases and DNA synthesis in bovine tracheal smooth muscle cells. Br. J. Pharmacol., 116:2267-2273.
57. Matesic, D.F., Rupp, H.L., Bonney, W.J., Ruch, R.J., and Trosko, J.E. (1994) Changes in gap junction permeability, phosphorylation, and number mediated by phorbol ester and non-phorbol-ester tumor promoters in rat liver epithelial cells. Mol. Carcinog., 10:226-236.
58. McGuire, T.F., Corey, S.J., and Sebti, S.M. (1993) Lovastatin inhibits platelet-derived growth factor stimulation of phosphatidylinositol 3-kinase activity as well as association of p85 subunit to tyrosine-phosphorylated PDGF receptor. J. Biol. Chem., 265:22227-22230.
59. Mehta, P.P., Bertram, J.S., and Loewenstein, W.R. (1986) Growth inhibition of transformed cells correlates with their junctional communication with normal cells. Cell, 44:187-196.
60. Moriya, S., Kazlauskas, A., Akimoto, K., Hirai, S., Mizuno, K., Takenawa, T., Fukui, Y., Watanabe, Y., Ozaki, S., and Ohno, S. (1996) Platelet-derived growth factor activates protein kinase C epsilon through redundant and independent signaling pathways involving phospholipase C gamma or phosphatidylinositol 3-kinase. Proc. Natl. Acad. Sci. USA, 93:151-155.
61. Musil, L.S., Cunningham, B.A., Edelman, G.A., and Goodenough, D.A. (1990) Differential phosphorylation of the gap junction protein connexin-43 in communication-competent and -deficient cell lines. J. Cell Biol., 111:2077-2088.
62. Newton, A.C. (1995) Protein kinase C: Structure, function, and regulation. J. Biol. Chem., 270:28495-28498.
63. Oh, S.Y., Grupen, G.S., and Murray, A.W. (1991) Phorbol ester induces phosphorylation and down-regulation of connexin43 in WB cells. Biochim. Biophys. Acta, 1094:243-248.
64. Pang, L., Sawada, T., Decker, S.J., and Saltiel, A.R. (1995) Inhibition of MAP kinase kinase blocks the differentiation of PC-12 cells induced by nerve growth factor. J. Biol. Chem., 270:13585-13588.
65. Pelletier, D.B., and Boynton, A.L. (1994) Dissociation of PDGF receptor tyrosine kinase activity from PDGF-mediated inhibition of gap junctional communication. J. Cell Physiol., 158:427-434.
66. Pukac, L.A., Carter, J.E., Ottlinger, M.E., and Karnovsky, M.J. (1997) Mechanisms of inhibition by heparin of PDGF stimulated MAP kinase activation in vascular smooth muscle cells. J. Cell. Physiol., 172:69-78.
67. Seger, R., Seger, D., Reszka, A.A., Munar, E.S., Eldar-Finkelman, H., Dobrowolska, G., Jensen, A.M., Cambell, J.S., Fischer, E.H., and Krebs, E.G. (1994) Overexpression of mitogen-activated protein kinase kinase (MAPKK) and its mutants in NIH 3T3 cells. Evidence that MAPKK involvement in cellular proliferation is regulated by phosphorylation of serine residues in its kinase subdomains VII and VII. J. Biol. Chem., 269:25699-25709.
68. Seger, R., Biener, Y., Feinstein, R., Hanoch, T., Gazit, A., and Zick, Y. (1995) Differential activation of mitogen-activated protein kinase and S6 kinase signaling pathways by 12-O-tetradecanoylphorbol-13-acetate (TPA) and insulin. Evidence for involvement of a TPA-stimulated protein-tyrosine kinase. J. Biol. Chem., 270:28325-28330.
69. Sozeri, O., Vollmer, K, Liyanage, M., Frith, D., Kour, G., Mark, G.E., III, and Stabel, S. (1992) Activation of the c-raf protein kinase by protein kinase C phosphorylation. Oncogene, 7:2259-2262.
70. Suzuki, M., Asplund, T., Yamashita, H., Heldin, C.H., and Heldin, P. (1995) Stimulation of hyaluronan biosynthesis by platelet-derived growth factor-BB and transforming growth factor-beta 1 involves activation of protein kinase C. Biochem. J., 307:817-821.
71. Swierenga, S.H.H., Whitfield, J.F., Boynton, A.L., MacManus, J.P., Rixon, R.H., Sikorska, M., Tsang, B.K., and Walker, P.R. (1980) Regulation of proliferation of normal and neoplastic rat liver cells by calcium and cyclic AMP. Ann. N.Y. Acad. Sci., 349:294-311.
72. Trosko, J.E., Chang, C.C., Madhukar, B.V., and Klaunig, J.E. (1990) Chemical, oncogene and growth factor inhibition of gap junctional intercellular communication: An integrative hypothesis of carcinogenesis. Pathobiology, 58:265-278.
73. Valius, M., and Kazlauskas, A. (1993) Phospholipase C-γ1 and phosphatidylinositol 3 kinase are the downstream mediators of the PDGF receptor's mitogenic signal. Cell, 73:321-334.
74. van der Geer, P., Hunter, T. and Lindberg, R.A. (1994) Receptor protein-tyrosine kinases and their signal transduction pathways. Annu. Rev. Cell Biol., 10:251-337.
75. van Dijk, M.C., Hilkmann, H., and van Blitterswijk, W.J. (1997) Platelet-derived growth factor activation of mitogen-activated protein kinase depends on the sequential activation of phosphatidylcholine-specific phospholipase C, protein kinase C-zeta and raf-1. Biocem. J., 325:303-307.
76. Wang, Y., Mehta, P.P., and Rose, B. (1995) Inhibition of glycosylation induces formation of open connexin-43 cell-to-cell channels and phosphorylation and friton X-100 insolubility of connexin 43. J. Biol. Chem., 270:26581-26585.
77. Warn-Cramer, B.J., Lampe, P.D., Kurata, W.F., Kanemitsu, M.Y., Loo, L.W.M., Eckhart, W., and Lau, A.F. (1996) Characterization of the mitogen-activated protein kinase phosphorylation sites on the connexin-43 gap junction protein. J. Biol. Chem., 271:3779-3786.
78. Xu, J., Rockow, S., Kim, S., Xiong, W., and Li, W. (1994) Interferons block protein kinase C-dependent but not-independent activation of raf-1 and mitogen-activated protein kinases and mitogenesis in NIH 3T3 cells. Mol. Cell. Biol., 14:8018-8027.
79. Xu, J., Zutter, M.M., Santoro, S.A., and Clark, R.A. (1996) PDGF induction of alpha 2 integrin gene expression is mediated by protein kinase C-zeta. J. Cell Biol., 134:1301-1311.
80. Yamasaki, H. (1990) Gap junctional intercellular communication and carcinogenesis. Carcinogenesis, 11:1051-1058.
81. Yamasaki, H., and Naus, C.C.G. (1996) Role of connexin genes in growth control. Carcinogenesis, 17:1199-1213.
82. Yeo, E.J., Kazlauskas, A., and Exton, J.H. (1994) Activation of phospholipase C-gamma is necessary for stimulation of phospholipase D by platelet-derived growth factor. J. Biol. Chem., 269:27823-27826.
83. Yotti, L.P., Chang, C.C., and Trosko, J.E. (1979) Elimination of metabolic cooperation in Chinese hamster cells by a tumor promoter. Science, 206:1089-1091.
84. Zheng, C.F., and Guan, K.L. (1993a) Dephosphorylation and inactivation of the mitogen-activated protein kinase by a mitogen-induced thr/tyr protein phosphatase. J. Biol. Chem., 268:16116-16119.
85. Zheng, C.F., and Guan, K.L. (1993b) Properties of MEKs. the kinases that phosphorylate and activate the extracellular signal-regulated kinases. J. Biol. Chem., 268:23933-23939.
86. Zhang, L-X., Cooney, R.V., and Bertram, J.S. (1991) Carotenoids enhance gap junctional communication and inhibit lipid peroxidation in C3H/10T1/2 cells: Relationship to their cancer chemopreventive action. Carcinogenesis, 12:2109-2114.
87. Zhu, D., Caveney, S., Kidder, G.M., and Naus, C.C.G. (1991) Transfection of C6 glioma cells with connexin43 cDNA: Analysis of expression, intercellular coupling and cell proliferation. Proc. natl. Acad. Sci. USA, 88:1883-1887.