Dissection of the molecular basis of pp60(v-src) induced gating of connexin 43 gap junction channels

Journal of Cell Biology

Volumn 144, Issue 5, 1999, Pages 1033-1045

  Zhou, Lan ^a   Kasperek, Eileen M ^a   Nicholson, Bruce J ^a  

^a UNIVERSITY AT BUFFALO   (United States)

Author keywords

Intercellular coupling; MAP kinase; Phosphorylation; V src; Xenopus oocytes

Indexed keywords

GAP JUNCTION PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN KINASE P60;

AMINO ACID SEQUENCE; ANIMAL CELL; ARTICLE; CELL COMMUNICATION; CELL INTERACTION; CHANNEL GATING; GAP JUNCTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SEQUENCE ANALYSIS;

ANIMALS; BASE SEQUENCE; CA(2+)-CALMODULIN DEPENDENT PROTEIN KINASE; CELL LINE; CONNEXIN 43; DNA PRIMERS; ENZYME ACTIVATION; FEMALE; GAP JUNCTIONS; ION CHANNEL GATING; MUTAGENESIS, SITE-DIRECTED; ONCOGENE PROTEIN PP60(V-SRC); PHOSPHORYLATION; RATS; TYROSINE; XENOPUS;

ANIMALIA; XENOPUS LAEVIS;

EID: 0033535338     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.144.5.1033     Document Type: Article

References (91)

1. Atkinson, M.M., A.S. Menko, R.G. Johnson, J.R. Sheppard, and J.D. Sheridan. 1981. Rapid and reversible reduction of junctional permeability in cells infected with a temperature-sensitive mutant of avian sarcoma virus. J. Cell Biol. 91:573-578.
2. Azarnia, R., S. Reddy, T.E. Kmiecik, D. Shalloway, and W.R. Loewenstein. 1988. The cellular src gene product regulates junctional cell-to-cell communication. Science. 239:398-401.
3. Barrio, L.C., T. Suchyna, T. Bargiello, L.X. Xu, R.S. Roginski, M.V. Bennett, and B.J. Nicholson. 1991. Gap junctions formed by connexins 26 and 32 alone and in combination are differently affected by applied voltage [published erratum appears in Proc. Natl. Acad. Sci. USA. 1992. 89:4220]. Proc. Natl. Acad. Sci. USA. 88:8410-8414.
4. Behrens, J., L. Vakaet, R. Friis, E. Winterhager, F. Van Roy, M.M. Marcel, and W. Birchmeier. 1993. Loss of epithelial differentiation and gain of invasiveness correlates with tyrosine phosphorylation of the E-cadherin/beta-catenin complex in cells transformed with a temperature-sensitive v-src gene. J. Cell Biol. 120:757-766.
5. Bennett, M.V., and V.K. Verselis. 1992. Biophysics of gap junctions. Semin. Cell Biol. 3:29-47.
6. 2+. Eur. J. Cell Biol. 57:40-50.
7. Beyer, E.C., D.L. Paul, and D.A. Goodenough. 1990. Connexin family of gap junction proteins. J. Membr. Biol. 116:187-194.
8. Chang, C.C., J.E. Trosko, H.J. Kung, D. Bombick, and F. Matsumura. 1985. Potential role of the src gene product in inhibition of gap-junctional communication in NIH/3T3 cells. Proc. Natl. Acad. Sci. USA. 82:5360-5364.
9. Crow, D.S., E.C. Beyer, D.L. Paul, S.S. Kobe, and A.F. Lau. 1990. Phosphorylation of connexin43 gap junction protein in uninfected and Rous sarcoma virus-transformed mammalian fibroblasts. Mol. Cell. Biol. 10:1754-1763.
10. Crow, D.S., W.E. Kurata, and A.F. Lau. 1992. Phosphorylation of connexin43 in cells containing mutant src oncogenes. Oncogene. 7:999-1003.
11. Eghbali, B., J.A. Kessler, L.M. Reid, C. Roy, and D.C. Spray. 1991. Involvement of gap junctions in tumorigenesis: transaction of tumor cells with connexin 32 cDNA retards growth in vivo. Proc. Natl. Acad. Sci. USA. 88: 10701-10705.
12. Ek-Vitorin, J.F., G. Calero, G.E. Morley, W. Coombs, S.M. Taffet, and M. Delmar. 1996. PH regulation of connexin43: molecular analysis of the gating particle. Biophys. J. 71:1273-1284.
13. Elvira, M., J.A. Diez, K.K. Wang, and A. Villalobo. 1993. Phosphorylation of connexin-32 by protein kinase C prevents its proteolysis by mu-calpain and m-calpain. J. Biol. Chem. 268:14294-14300.
14. Fallon, R.F., and D.A. Goodenough. 1981. Five-hour half-life of mouse liver gap-junction protein. J. Cell Biol. 90:521-526.
15. Filson, A.J., R. Azarnia, E.C. Beyer, W.R. Loewenstein, and J.S. Brugge. 1990. Tyrosine phosphorylation of a gap junction protein correlates with inhibition of cell-to-cell communication. Cell Growth Differ. 1:661-668.
16. Goldberg, G.S., and A.F. Lau. 1993. Dynamics of connexin43 phosphorylation in pp60v-src-transformed cells. Biochem. J. 295:735-742.
17. Goldberg, G.S., P.D. Lampe, D. Sheedy, C.C. Stewart, B.J. Nicholson, and C.C. Naus. 1998. Direct isolation and analysis of endogenous transjunctional ADP from Cx43 transfected C6 glioma cells. Exp. Cell Res. 239:82-92.
18. Gong, X., E. Li, G. Klier, Q. Huang, Y. Wu, H. Lei, N.M. Kumar, J. Horwitz, and N.B. Gilula. 1997. Disruption of alpha3 connexin gene leads to proteolysis and cataractogenesis in mice. Cell. 91:833-843.
19. Goodenough, D.A., J.A. Goliger, and D.L. Paul. 1996. Connexins, connexons, and intercellular communication. Annu. Rev. Biochem. 65:475-502.
20. Guerrero, P.A., R.B. Schuessler, L.M. Davis, E.C. Beyer, C.M. Johnson, K.A. Yamada, and J.E. Saffitz. 1997. Slow ventricular conduction in mice heterozygous for a connexin43 null mutation. J. Clin. Invest. 99:1991-1998.
21. Hamaguchi, M., N. Matsuyoshi, Y. Ohnishi, B. Gotoh, M. Takeichi, and Y. Nagai. 1993. p60v-src causes tyrosine phosphorylation and inactivation of the N-cadherin-catenin cell adhesion system. EMBO (Eur. Mol. Biol. Organ.) J. 12:307-314.
22. Hanks, S.K., and T.R. Polte. 1997. Signaling through focal adhesion kinase. Bioessays. 19:137-145.
23. Harris, A.L., D.C. Spray, and M.V. Bennett. 1981. Kinetic properties of a voltage-dependent junctional conductance. J. Gen. Physiol. 77:95-117.
24. Haubrich, S., H.J. Schwarz, F. Bukauskas, H. Lichtenberg-Frate, O. Traub, R. Weingart, and K. Willecke. 1996. Incompatibility of connexin 40 and 43 Hemichannels in gap junctions between mammalian cells is determined by intracellular domains. Mol. Biol. Cell. 7:1995-2006.
25. Hill, C.S., S.Y. Oh, S.A. Schmidt, K.J. Clark, and A.W. Murray. 1994. Lysophosphatidic acid inhibits gap-junctional communication and stimulates phosphorylation of connexin-43 in WB cells: possible involvement of the mitogen-activated protein kinase cascade. Biochem. J. 303:475-479.
26. Homma, N., J.L. Alvarado, W. Coombs, K. Stergiopoulos, S.M. Taffet, A.F. Lau, and M. Delmar. 1998. A particle-receptor model for the insulin-induced closure of connexin43 channels. Circ. Res. 83:27-32.
27. Hoshi, T., W.N. Zagotta, and R.W. Aldrich. 1990. Biophysical and molecular mechanisms of Shaker potassium channel inactivation. Science. 250:533-538.
28. Hossain, M.Z., P. Ao, and A.L. Boynton. 1998. Rapid disruption of gap junctional communication and phosphorylation of connexin43 by platelet-derived growth factor in T51B rat liver epithelial cells expressing platelet-derived growth factor receptor. J. Cell. Physiol. 174:66-77.
29. Husoy, T., S.O. Mikalsen, and T. Sanner. 1993. Effects of five phorbol esters on gap junctional intercellular communication, morphological transformation and epidermal growth factor binding in Syrian hamster embryo cells. Carcinogenesis. 14:73-77.
30. 2+ in mouse epidermal cells is controlled by E-cadherin. J. Cell Biol. 114:545-555.
31. Kadle, R., J.T. Zhang, and B.J. Nicholson. 1991. Tissue-specific distribution of differentially phosphorylated forms of Cx43. Mol. Cell. Biol. 11:363-369.
32. Kanemitsu, M.Y., and A.F. Lau. 1993. Epidermal growth factor stimulates the disruption of gap junctional communication and connexin43 phosphorylation independent of 12-0-tetradecanoylphorbol 13-acetate-sensitive protein kinase C: the possible involvement of mitogen-activated protein kinase. Mol. Biol. Cell. 4:837-848.
33. Kanemitsu, M.Y., L.W. Loo, S. Simon, A.F. Lau, and W. Eckhart. 1997. Tyrosine phosphorylation of connexin 43 by v-src is mediated by SH2 and SH3 domain interactions. J. Biol. Chem. 272:22824-22831.
34. Keane, R.W., P.P. Mehta, B. Rose, L.S. Honig, W.R. Loewenstein, and U. Rutishauser. 1988. Neural differentiation. NCAM-mediated adhesion, and gap junctional communication in neuroectoderm. A study in vitro. J. Cell Biol. 106:1307-1319.
35. Kirchhoff, S., E. Nelles, A. Hagendorff, O. Kruger, O. Traub, and K. Willecke. 1998. Reduced cardiac conduction velocity and predisposition to arrhythmias in connexin40-deficient mice. Curr. Biol. 8:299-302.
36. Klaunig, J.E., J.A. Hartnett, R.J. Ruch, C.M. Weghorst, J.A. Hampton, and L.D. Schafer. 1990. Gap junctional intercellular communication in hepatic carcinogenesis. Prog. Clin. Biol. Res. 340D:165-174.
37. Kozak, M. 1986. Point mutations define a sequence flanking the AUG initiator codon that modulates translation by eukaryotic ribosomes. Cell. 44:283-292.
38. v-src. Oncogene. 9:329-335.
39. Laemmli, U.K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 227:680-685.
40. Lampe, P.D. 1994. Analyzing phorhol ester effects on gap junctional communication: a dramatic inhibition of assembly. J. Cell Biol. 127:1895-1905.
41. Lau, A.F., M.Y. Kanemitsu, W.E. Kurata, S. Danesh, and A.L. Boynton. 1992. Epidermal growth factor disrupts gap-junctional communication and induces phosphorylation of connexin43 on serine. Mol. Biol. Cell. 3:865-874.
42. Lau, A.F., W.E. Kurata, M.Y. Kanemitsu, L.W. Loo, B.J. Warn-Cramer, W. Eckhart, and P.D. Lampe. 1996. Regulation of connexin43 function by activated tyrosine protein kinases. J. Bioenerg. Biomembr. 28:359-368.
43. Lim, W.A., and F.M. Richards. 1994. Critical residues in an SH3 domain from Sem-5 suggest a mechanism for proline-rich peptide recognition. Nat. Struct. Biol. 1:221-225.
44. Liu, S., S. Taffet, L. Stoner, M. Delmar, M.L. Vallano, and J. Jalife. 1993. A structural basis for the unequal sensitivity of the major cardiac and liver gap junctions to intracellular acidification: the carboxyl tail length. Biophys. J. 64:1422-1433.
45. Loewenstein, W.R. 1979. Junctional intercellular communication and the control of growth. Biochim. Biophys. Acta. 560:1-65.
46. Loewenstein, W.R. 1981. Junctional intercellular communication: the cell-to-cell membrane channel. Physiol. Rev. 61:829-913.
47. Loewenstein, W.R., and Y. Kanno. 1966. Intercellular communication and the control of tissue growth: lack of communication between cancer cells. Nature. 209:1248-1249.
48. Loo, L.W., J.M. Berestecky, M.Y. Kanemitsu, and A.F. Lau. 1995. pp60src-mediated phosphorylation of connexin 43, a gap junction protein. J. Biol. Chem. 270:12751-12761.
49. c-src. Mol. Cell. Biol. 8:497-501.
50. Maldonado, P.E., B. Rose, and W.R. Loewenstein. 1988. Growth factors modulate junctional cell-to-cell communication. J. Membr. Biol. 106:203-210.
51. Matsuyoshi, N., M. Hamaguchi, S. Taniguchi, A. Nagafuchi, S. Tsukita, and M. Takeichi. 1992. Cadherin-mediated cell-cell adhesion is perturbed by v-src tyrosine phosphorylation in metastatic fibroblasts. J. Cell Biol. 118:703-714.
52. Matus-Leibovitch, N., G. Mengod, and Y. Oron. 1992. Kinetics of the functional loss of different muscarinic receptor isoforms in Xenopus oocytes. Biochem. J. 285:753-758.
53. Mehta, P.P., J.S. Bertram, and W.R. Loewenstein. 1986. Growth inhibition of transformed cells correlates with their junctional communication with normal cells. Cell. 44:187-196.
54. Mehta, P.P., A. Hotz-Wagenblatt, B. Rose, D. Shalloway, and W.R. Loewenstein. 1991. Incorporation of the gene for a cell-cell channel protein into transformed cells leads to normalization of growth. J. Membr. Biol. 124: 207-225.
55. Mensink, A., A. Brouwer, E.H. Van den Burg, S. Geurts, W.M. Jongen, C.M. Lakemond, I. Meijerman, and T. Van der Wijk. 1996. Modulation of intercellular communication between smooth muscle cells by growth factors and cytokines. Eur. J. Pharmacol. 310:73-81.
56. Mesnil, M., V. Krutovskikh, C. Piccoli, C. Elfgang, O. Traub, K. Willecke, and H. Yamasaki. 1995. Negative growth control of HeLa cells by connexin genes: connexin species specificity. Cancer Res. 55:629-639.
57. Moreno, A.P., J.C. Saez, G.I. Fishman, and D.C. Spray. 1994. Human connexin43 gap junction channels. Regulation of unitary conductances by phosphorylation. Circ. Res. 74:1050-1057.
58. Morley, G.E., S.M. Taffet, and M. Delmar. 1996. Intramolecular interactions mediate pH regulation of connexin43 channels. Biophys. J. 70:1294-1302.
59. Musil, L.S., and D.A. Goodenough. 1991. Biochemical analysis of connexin43 intracellular transport, phosphorylation, and assembly into gap junctional plaques. J. Cell Biol. 115:1357-1374.
60. Musil, L.S., and L.M. Roberts. 1998. Functional stabilization of connexins by inhibitors of protein synthesis. In Gap Junctions. R. Werner, editor. IOS Press, Washington, DC. 117-121.
61. Musil, L.S., B.A. Cunningham, G.M. Edelman, and D.A. Goodenough. 1990. Differential phosphorylation of the gap junction protein connexin43 in junctional communication-competent and -deficient cell lines. J. Cell Biol. 111: 2077-2088.
62. Naus, C.C., K. Elisevich, D. Zhu, D.J. Belliveau, and R.F. Del Maestro. 1992. In vivo growth of C6 glioma cells transfected with connexin43 cDNA. Cancer Res. 52:4208-4213.
63. Nelles, E., C. Butzler, D. Jung, A. Temme, H.D. Gabriel, U. Dahl, O. Traub, F. Stumpel, K. Jungermann, J. Zielasek, et al. 1996. Defective propagation of signals generated by sympathetic nerve stimulation in the liver of connexin32-deficient mice. Proc. Natl. Acad. Sci. USA. 93:9565-9570.
64. Nicholson, B.J., L. Zhou, F. Cao, H. Zhu, and Y. Chen. 1998. Diverse molecular mechanism of gap junction channel gating. In Gap Junctions. R. Werner, editor. IOS Press, Washington, DC. 3-7.
65. Oh, S.Y., C.G. Grupen, and A.W. Murray. 1991. Phorbol ester induces phosphorylation and down-regulation of connexin 43 in WB cells. Biochim. Biophys. Acta. 1094:243-245.
66. Oh, S.Y., S.A. Schmidt, and A.W. Murray. 1993. Epidermal growth factor inhibits gap junctional communication and stimulates serine-phosphorylation of connexin43 in WB cells by a protein kinase C-independent mechanism. Cell Adhes. Commun. 1:143-149.
67. Pelicci, G., L. Lanfrancone, F. Grignani, J. McGlade, F. Cavallo, G. Forni, I. Nicoletti, F. Grignani, T. Pawson, and P.G. Pelicci. 1992. A novel transforming protein (SHC) with an SH2 domain is implicated in mitogenic signal transduction. Cell. 70:93-104.
68. Pelletier, D.B., and A.L. Boynton. 1994. Dissociation of PDGF receptor tyrosine kinase activity from PDGF-mediated inhibition of gap junctional communication. J. Cell. Physiol. 158:427-434.
69. Postma, F.R., T. Hengeveld, J. Alblas, B.N. Giepmans, G.C. Zondag, K. Jalink, and W.H. Moolenaar. 1998. Acute loss of cell-cell communication caused by G protein-coupled receptors: a critical role for c-Src. J. Cell Biol. 140:1199-1209.
70. Reaume, A.G., P.A. De Sousa, S. Kulkarni, B.L. Langille, D. Zhu, T.C. Davies, S.C. Juneja, G.M. Kidder, and J. Rossant. 1995. Cardiac malformation in neonatal mice lacking connexin43. Science. 267:1831-1834.
71. Richter, J.D., H.C. Hurst, and N.C. Jones. 1987. Adenovirus E1A requires synthesis of a cellular protein to establish a stable transcription complex in injected Xenopus laevis oocytes. Mol. Cell. Biol. 7:3049-3056.
72. Rose, B., P.P. Mehta, and W.R. Loewenstein. 1993. Gap-junction protein gene suppresses tumorigenicity. Carcinogenesis. 14:1073-1075.
73. Rozakis-Adcock, M., J. McGlade, G. Mbamalu, G. Pelicci, R. Daly, W. Li, A. Batzer, S. Thomas, J. Brugge, P.G. Pelicci, et al. 1992. Association of the Shc and Grb2/Sem5 SH2-containing proteins is implicated in activation of the Ras pathway by tyrosine kinases. Nature. 360:689-692.
74. Saez, J.C., V.M. Berthoud, A.P. Moreno, and D.C. Spray. 1993. Gap junctions, Multiplicity of controls in differentiated and undifferentiated cells and possible functional implications. Adv. Second Messenger Phosphoprotein Res. 27: 163-198.
75. Simon, A.M., D.A. Goodenough, E. Li, and D.L. Paul. 1997. Female infertility in mice lacking connexin 37. Nature. 385:525-529.
76. Simon, A.M., D.A. Goodenough, and D.L. Paul. 1998. Mice lacking connexin40 have cardiac conduction abnormalities characteristic of atrioventricular block and bundle branch block. Curr. Biol. 8:295-298.
77. Spray, D.C., A.L. Harris, and M.V. Bennett. 1981. Gap junctional conductance is a simple and sensitive function of intracellular pH. Science. 211:712-715.
78. Stagg, R.B., and W.H. Fletcher. 1990. The hormone-induced regulation of contact-dependent cell-cell communication by phosphorylation. Endocr. Rev. 11:302-325.
79. Suchyna, T.M., L.X. Xu, F. Gao, C.R. Fourtner, and B.J. Nicholson. 1993. Identification of a proline residue as a transduction element involved in voltage gating of gap junctions. Nature. 365:847-849.
80. Swenson, K.I., H. Piwnica-Worms, H. McNamee, and D.L. Paul. 1990. Tyrosine phosphorylation of the gap junction protein connexin43 is required for the pp60v-src-induced inhibition of communication. Cell Regul. 1:989-1002.
81. Takeda, H., A. Nagafuchi, S. Yonemura, S. Tsukita, J. Behrens, W. Birchmeier, and S. Tsukita. 1995. V-src kinase shifts the cadherin-based cell adhesion from the strong to the weak state and beta catenin is not required for the shift. J. Cell Biol. 131:1839-1847.
82. Turin, L., and A. Warner. 1977. Carbon dioxide reversibly abolishes ionic communication between cells of early amphibian embryo. Nature. 270:56-57.
83. Twamley-Stein, G.M., R. Pepperkok, W. Ansorge, and S.A. Courtneidge. 1993. The Src family tyrosine kinases are required for platelet-derived growth factor-mediated signal transduction in NIH 3T3 cells. Proc. Natl. Acad. Sci. USA. 90:7696-7700.
84. Verselis, V.K., C.S. Ginter, and T.A. Bargiello. 1994. Opposite voltage gating polarities of two closely related connexins. Nature. 368:348-351.
85. Warn-Cramer, B.J., P.D. Lampe, W.E. Kurata, M.Y. Kanemitsu, L.W. Loo, W. Eckhart, and A.F. Lau. 1996. Characterization of the mitogen-activated protein kinase phosphorylation sites on the connexin-43 gap junction protein. J. Biol. Chem. 271:3779-3786.
86. Warner, A. 1988. The gap junction. J. Cell Sci. 89:1-7.
87. White, T.W., D.A. Goodenough, and D.L. Paul. 1998. Targeted ablation of connexin50 in mice results in microphthalmia and zonular pulverulent cataracts. J. Cell Biol. 143:815-825.
88. c-src tyrosine kinase, myristylation, and modulatory domains are required for enhanced mitogenic responsiveness to epidermal growth factor seen in cells overexpressing c-src. Mol. Cell. Biol. 9:1536-1544.
89. Xie, H., D.W. Laird, T.H. Chang, and V.W. Hu. 1997. A mitosis-specific phosphorylation of the gap junction protein connexin43 in human vascular cells: biochemical characterization and localization. J. Cell Biol. 137:203-210.
90. Xing, Z., H.C. Chen, J.K. Nowlen, S.J. Taylor, D. Shalloway, and J.L. Guan. 1994. Direct interaction of v-Src with the focal adhesion kinase mediated by the Src SH2 domain. Mol. Biol. Cell. 5:413-421.
91. Yu, H., J.K. Chen, S. Feng, D.C. Dalgarno, A.W. Brauer, and S.L. Schreiber. 1994. Structural basis for the binding of proline-rich peptides to SH3 domains. Cell. 76:933-945.