Gap junction channel gating modulated through protein phosphorylation

Progress in Biophysics and Molecular Biology

Volumn 94, Issue 1-2, 2007, Pages 107-119

  Moreno, Alonso P ^a   Lau, Alan F ^b  

^a UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF HAWAII CANCER CENTER   (United States)

Author keywords

Cell to cell coupling; Gap junction; Gating; Protein phosphorylation; Serine protein kinase; Tyrosine protein kinase

Indexed keywords

GAP JUNCTION PROTEIN; PROTEIN TYROSINE KINASE;

BIOLOGICAL MODEL; CELL COMMUNICATION; CELL JUNCTION; CHANNEL GATING; CHEMICAL MODEL; CHEMISTRY; METABOLISM; PHOSPHORYLATION; PROTEIN CONFORMATION; REVIEW;

CELL COMMUNICATION; CONNEXINS; GAP JUNCTIONS; ION CHANNEL GATING; MODELS, BIOLOGICAL; MODELS, CHEMICAL; PHOSPHORYLATION; PROTEIN CONFORMATION; PROTEIN-TYROSINE KINASES;

EID: 34249014302     PISSN: 00796107     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pbiomolbio.2007.03.004     Document Type: Review

References (79)

1. Abrams C.K., and Bennett M.V.L. Hereditary human diseases caused by connexin mutations. In: Peracchia C. (Ed). Gap Junctions. Molecular Basis of Cell Communication in Health and Disease (2000), Academic Press, New York 423-459
2. Anumonwo J.M., Taffet S., Gu H., Chanson M., Moreno A.P., and Delmar M. The carboxyl terminal domain regulates the unitary conductance and voltage dependence of connexin40 gap junction channels. Circ. Res. 88 (2001) 666-673
3. Atkinson M.M., Anderson S.K., and Sheridan J.D. Modification of gap junctions in cells transformed by a temperature-sensitive mutant of Rous sarcoma virus. J. Membr. Biol. 91 (1986) 53-64
4. Azarnia R., Reddy S., Kmiecik T.E., Shalloway D., and Loewenstein W.R. The cellular src gene product regulates junctional cell-to-cell communication. Science 239 (1988) 398-401
5. Barrio L.C., Castro C., and Gómez-Hernández J.M. Altered assembly of gap junction channels caused by COOH-terminal connexin32 mutants of CMTX. Ann. NY Acad. Sci. 883 (1999) 526-529
6. Boulven I., Robin P., Desmyter C., Harbon S., and Leiber D. Differential involvement of Src family kinases in pervanadate-mediated responses in rat myometrial cells. Cell Signal 14 (2002) 341-349
7. Bruzzone R., Hormuzdi S.G., Barbe M.T., Herb A., and Monyer H. Pannexins a family of gap junction proteins expressed in brain. Proc. Nord. Aroma. Symp. 100 (2003) 13644-13649
8. Bukauskas F.F., and Verselis V.K. Gap junction channel gating. Biochim. Biophys. Acta 1662 (2004) 42-60 (Review, 110 refs.)
9. Bukauskas F.F., and Weingart R. Voltage-dependent gating of single gap junction channels in an insect cell line. Biophys. J. 67 (1994) 613-625
10. Bukauskas F.F., Elfgang C., Willecke K., and Weingart R. Biophysical properties of gap junction channels formed by mouse connexin40 in induced pairs of transfected human HeLa cells. Biophys. J. 68 (1995) 2289-2298
11. Burt J.M., and Spray D.C. Inotropic agents modulate gap junctional conductance between cardiac myocytes. Am. J. Physiol. 254 (1988) H1206-H1210
12. Chanson M., White M.M., and Garber S.S. cAMP promotes gap junctional coupling in T84 cells. Am. J. Physiol. 271 (1996) C533-C539
13. Cheng H.L., and Louis C.F. Functional effects of casein kinase I-catalyzed phosphorylation on lens cell-to-cell coupling. J. Membr. Biol. 181 (2001) 21-30
14. Cottrell G.T., Lin R., Warn-Cramer B.J., Lau A.F., and Burt J.M. Mechanism of v-Src- and mitogen-activated protein kinase-induced reduction of gap junction communication. Am. J. Physiol. Cell Physiol. 284 (2003) C511-C520
15. Crow D.S., Beyer E.C., Paul D.L., Kobe S.S., and Lau A.F. Phosphorylation of connexin43 gap junction protein in uninfected and Rous sarcoma virus-transformed mammalian fibroblasts. Mol. Cell. Biol. 10 (1990) 1754-1763
16. Duncan J.C., and Fletcher W.H. Alpha 1 Connexin (connexin43) gap junctions and activities of cAMP-dependent protein kinase and protein kinase C in developing mouse heart. Dev. Dyn. 223 (2002) 96-107
17. Ek-Vitorin J.F., King T.J., Heyman N.S., Lampe P.D., and Burt J.M. Selectivity of connexin 43 channels is regulated through protein kinase C-dependent phosphorylation. Circ. Res. 98 (2006) 1498-1505
18. Elenes S., Rubart M., and Moreno A.P. Junctional communication between isolated pairs of canine atrial cells is mediated by homogeneous and heterogeneous gap junction channels. J. Cardiovasc. Electrophysiol. 10 (1999) 990-1004
19. Fan C., Li Q., Ross D., and Engelhardt J.F. Tyrosine phosphorylation of IB activates NFB through a redox-regulated and c-Src-dependent mechanism following hypoxia/reoxygenation. J. Biol. Chem. 278 (2003) 2072-2080
20. Filson A.J., Azarnia R., Beyer E.C., Loewenstein W.R., and Brugge J.S. Tyrosine phosphorylation of a gap junction protein correlates with inhibition of cell-to-cell communication. Cell Growth Differ. 1 (1990) 661-668
21. Haubrich S., Schwarz H.J., Bukauskas F., Lichtenberg-Frate H., Traub O., Weingart R., and Willecke K. Incompatibility of connexin 40 and 43 hemichannels in gap junctions between mammalian cells is determined by intracellular domains. Mol. Biol. Cell 7 (1996) 1995-2006
22. Heiska L., and Carpen O. Src phosphorylates ezrin at tyrosine 477 and induces a phosphospecific association between ezrin and kelch-repeat protein family member. J. Biol. Chem. 280 (2005) 10244-10252
23. Herve J.C., Bourmeyster N., and Sarrouilhe D. Diversity in protein-protein interactions of connexins: emerging roles. Biochim. Biophys. Acta 1662 (2004) 22-41
24. Hille B. Ionic Channels of Excitable Membranes (1992), Sinauer Associates, Sunderland, MA
25. John S., Cesario D., and Weiss J.N. Gap junctional hemichannels in the heart. Acta Physiol. Scand. 179 (2003) 23-31
26. Jongsma H., van Rijen H.V.M., Kwak B.R., and Chanson M. Phosphorylation of connexins: consequences for permeability, conductance and kinetics for gap junction channels. Current Topics in Membranes (2000), Academic Press, New York
27. Jordan K., Solan J.L., Dominquez M., Sia M., Hand A., Lampe P.D., and Laird D.W. Trafficking, assembly, and function of a connexin43- green fluorescent protein chimera in live mammalian cells. Mol. Biol. Cell 10 (1999) 2033-2050
28. Kanemitsu M.Y., Loo L.W., Simon S., Lau A.F., and Eckhart W. Tyrosine phosphorylation of connexin 43 by v-Src is mediated by SH2 and SH3 domain interactions. J. Biol. Chem. 272 (1997) 22824-22831
29. Kanno Y., Enamoto T., Shiba Y., and Yamasaki H. Protective effect of cyclic AMP on tumor promoter-mediated inhibition of cell-cell communication (electrical coupling). Exp. Cell. Res. 152 (1984) 31-37
30. Kwak B.R., and Jongsma H.J. Regulation of cardiac gap junction channel permeability and conductance by several phosphorylating conditions. Mol. Cell. Biochem. 157 (1996) 93-99
31. Kwak B.R., Hermans M.M., De Jonge H.R., Lohmann S.M., Jongsma H.J., and Chanson M. Differential regulation of distinct types of gap junction channels by similar phosphorylating conditions. Mol. Biol. Cell 6 (1995) 1707-1719
32. Kwak B.R., Sáez J.C., Wilders R., Chanson M., Fishman G.I., Hertzberg E.L., Spray D.C., and Jongsma H.J. Effects of cGMP-dependent phosphorylation on rat and human connexin43 gap junction channels. Pfluegers Arch. 430 (1995) 770-778
33. Kwak B.R., van Veen T.A., Analbers L.J., and Jongsma H.J. TPA increases conductance but decreases permeability in neonatal rat cardiomyocyte gap junction channels. Exp. Cell Res. 220 (1995) 456-463
34. Laird D.W. The life cycle of a connexin: gap junction formation, removal, and degradation. J. Bioenerg. Biomembr. 28 (1996) 311-318
35. Laird D.W. Connexin phosphorylation as a regulatory event linked to gap junction internalization and degradation. Biochim. Biophys. Acta 1711 (2005) 172-182
36. Lampe P.D., and Lau A.F. The effects of connexin phosphorylation on gap junctional communication. Int. J. Biochem. Cell Biol. 36 (2004) 1171-1186
37. Lampe P.D., TenBroek E.M., Burt J.M., Kurata W.E., Johnson R.G., and Lau A.F. Phosphorylation of connexin43 on serine368 by protein kinase C regulates gap junctional communication. J. Cell Biol. 149 (2000) 1503-1512
38. Lampe P.D., Cooper C.D., King T.J., and Burt J.M. Analysis of Connexin43 phosphorylated at S325, S328 and S330 in normoxic and ischemic heart. J. Cell Sci. 119 (2006) 3435-3442
39. Landesman Y., White T.W., Starich T.A., Shaw J.E., Goodenough D.A., and Paul D.L. Innexin-3 forms connexin-like intercellular channels. J. Cell Sci. 112 (1999) 2391-2396
40. Lau A.F., Kurata W.E., Kanemitsu M.Y., Loo L.W., Warn-Cramer B.J., Eckhart W., and Lampe P.D. Regulation of connexin43 function by activated tyrosine protein kinases. J. Bioenerg. Biomembr. 28 (1996) 359-368 (Review, 47 refs.)
41. Lin R., Warn-Cramer B.J., Kurata W.E., and Lau A.F. v-Src phosphorylation of connexin 43 on Tyr247 and Tyr265 disrupts gap junctional communication. J. Cell Biol. 154 (2001) 815-827
42. Lin X., Crye M., and Veenstra R.D. Regulation of connexin43 gap junctional conductance by ventricular action potentials. Circ. Res. 93 (2003) e63-e73
43. Locke D., Koreen I.V., and Harris A.L. Isoelectric points and post-translational modifications of connexin26 and connexin32. Fed. Am. Soc. Exp. Biol. 20 (2006) 1221-1223
44. Loo L.W., Berestecky J.M., Kanemitsu M.Y., and Lau A.F. pp60src-mediated phosphorylation of connexin 43, a gap junction protein pp60src-mediated phosphorylation of connexin 43, a gap junction protein. J. Biol. Chem. 270 (1995) 12751-12761
45. Loo L.W., Kanemitsu M.Y., and Lau A.F. In vivo association of pp60v-src and the gap-junction protein connexin 43 in v-src-transformed fibroblasts. Mol. Carcinogen. 25 (1999) 187-195
46. Marquart K.H. So-called annular gap junctions in bone cells of normal mice. Experientia 33 (1977) 270-272
47. Martínez A.D., Hayrapetyan V., Moreno A.P., and Beyer E.C. Connexin43 and connexin45 form heteromeric gap junction channels in which individual components determine permeability and regulation. Circ. Res. 90 (2002) 1100-1107
48. Moreno A.P., Fishman G.I., and Spray D.C. Phosphorylation shifts unitary conductance and modifies voltage dependent kinetics of human connexin43 gap junction channels. Biophys. J. 62 (1993) 51-53
49. Moreno A.P., Rook M.B., and Spray D.C. The multiple conductance states of mammalian connexin43. Biophys. J. 64 (1993) A236
50. Moreno A.P., Chanson M., Elenes S., Anumonwo J., Scerri I., Gu H., Taffet S.M., and Delmar M. Role of the carboxyl terminal of connexin43 in transjunctional fast voltage gating. Circ. Res. 90 (2002) 450-457
51. Moreno A.P., Chanson M., Anumonwo J., Scerri I., Gu H., Taffet S.M., and Delmar M. Role of the carboxyl terminal of connexin43 in transjunctional fast voltage gating. Circ. Res. 90 (2002) 450-457
52. Moreno A.P., Hayrapetyan V., Zhong G., Martinez A.D., and Beyer E.C. Homomeric and heteromeric gap junctions. In: Zipes D.P., and Jalife J. (Eds). Cardiac Electrophysiology. From Cell to Bedside (2004), Saunders, Philadelphia 120-126
53. Munster P.N., and Weingart R. Effects of phorbol ester on gap junctions of neonatal rat heart cells. Pfluegers Arch. Eur. J. Physiol. 423 (1993) 181-188
54. Paulson A., Lampe P., Meyer R., TenBroek E., Atkinson M., Walseth T., and Johnson R. Cyclic AMP and LDL trigger a rapid enhancement in gap junction assembly through a stimulation of connexin trafficking. J. Cell Sci. 113 (2001) 3037-3049
55. Purnick P., Benjamin D., Verselis V., Bargiello T., and Dowd T. Structure of the amino terminus of a gap junction protein. Arch. Biochem. Biophys. 381 (2000) 181-190
56. Purnick P.E., Oh S., Abrams C.K., Verselis V.K., and Bargiello T.A. Reversal of the gating polarity of gap junctions by negative charge substitutions in the N-terminus of connexin 32. Biophys. J. 79 (2000) 2403-2415
57. Revilla A., Bennett M.V., and Barrio L.C. Molecular determinants of membrane potential dependence in vertebrate gap junction channels. Proc. Natl. Acad. Sci. USA 97 (2000) 14760-14765
58. Sáez J.C., Spray D.C., Nairn A.C., Hertzberg E., Greengard P., and Bennett M.V. cAMP increases junctional conductance and stimulates phosphorylation of the 27-kDa principal gap junction polypeptide. Proc. Natl. Acad. Sci. USA 83 (1986) 2473-2477
59. Sáez J.C., Nairn A.C., Czernik A.J., Spray D.C., Hertzberg E.L., Greengard P., and Bennett M.V. Phosphorylation of connexin 32, a hepatocyte gap-junction protein, by cAMP-dependent protein kinase, protein kinase C and Ca 2 +/calmodulin-dependent protein kinase II. Eur. J. Biochem. 192 (1990) 263-273
60. Sáez, J.C., Nairn, A.C., Czernik, A.J., Spray, D.C., Hertzberg, E.L., 1993. Rat connexin43: regulation by phosphorylation in heart. In: Hall, J.E., Zampighi, G.A., Davies, R.M. (Eds.), Progress in Cell Research, vol. 3. Elsevier Science Publishers, Netherlands, pp. 275-281.
61. Shi X., Potvin B., Huang T., Hilgard P., Spray D.C., Suadicani S.O., Wolkoff A.W., Stanley P., and Stockert R.J. A novel casein kinase 2 alpha-subunit regulates membrane protein traffic in the human hepatoma cell line HuH-7. J. Biol. Chem. 276 (2001) 2075-2082
62. Solan J.L., and Lampe P.D. Connexin phosphorylation as a regulatory event linked to gap junction channel assembly. Biochim. Biophys. Acta 1711 (2005) 154-163
63. Solan J.L., and Lampe P.D. Connexin phosphorylation as a regulatory event linked to gap junction channel assembly. Biochim. Biophys. Acta (BBA) Biomembr. 1711 (2005) 154-163
64. Stergiopoulos K., Alvarado J.L., Mastroianni M., Ek-Vitorin J.F., Taffet S.M., and Delmar M. Hetero-domain interactions as a mechanism for the regulation of connexin channels. Circ. Res. 84 (1999) 1144-1155
65. Suchyna T.M., Nitsche J.M., Chilton M., Harris A.L., Veenstra R.D., and Nicholson B.J. Different ionic selectivities for connexins 26 and 32 produce rectifying gap junction channels. Biophys. J. 77 (2000) 2968-2987
66. Takahashi H., Suzuki K., and Namiki H. Pervanadate-induced reverse translocation and tyrosine phosphorylation of phorbol ester-stimulated protein kinase CII are mediated by Src-family tyrosine kinases in porcine neutrophils. Biochem. Biophys. Res. Commun. 314 (2004) 830-837
67. TakensKwak B.R., and Jongsma H.J. Cardiac gap junctions: three distinct single channel conductances and their modulation by phosphorylating treatments. Pfluegers Arch. 422 (1992) 198-200
68. Traub O., Look J., Dermietzel R., Brummer F., Hulser D., and Willecke K. Comparative characterization of the 21-kD and 26-kD gap junction proteins in murine liver and cultured hepatocytes. J. Cell Biol. 108 (1989) 1039-1051
69. Trexler E.B., Bukauskas F.F., Bennett M.V., Bargiello T.A., and Verselis V.K. Rapid and direct effects of pH on connexins revealed by the connexin46 hemichannel preparation. J. Gen. Physiol. 113 (1999) 721-742
70. van Rijen H.V., van Veen T.A., Hermans M.M., and Jongsma H.J. Human connexin40 gap junction channels are modulated by cAMP. Cardiovasc. Res. 45 (2000) 941-951 (see comments)
71. van Veen T.A., van Rijen H.V., and Jongsma H.J. Electrical conductance of mouse connexin45 gap junction channels is modulated by phosphorylation. Cardiovasc. Res. 46 (2000) 496-510
72. Veenstra R.D. Ion permeation through connexin gap junction channels: effects on conductance and selectivity. Current Topics in Membranes (2000), Academic Press, New York 95-128
73. Veenstra R.D., and DeHaan R.L. Measurement of single channel currents from cardiac gap junctions. Science 233 (1986) 972-974
74. Veenstra R.D., Wang H.Z., Beblo D.A., Chilton M.G., Harris A.L., Beyer E.C., and Brink P.R. Selectivity of connexin-specific gap junctions does not correlate with channel conductance. Circ. Res. 77 (1995) 1156-1165
75. Wang X.G., and Peracchia C. Chemical gating of heteromeric and heterotypic gap junction channels. J. Membr. Biol. 162 (1998) 169-176
76. Warn-Cramer B.J., and Lau A.F. Regulation of gap junctions by tyrosine protein kinases. Biochim. Biophys. Acta. 1662 (2004) 81-95
77. Warn-Cramer B.J., Cottrell G.T., Burt J.M., and Lau A.F. Regulation of connexin-43 gap junctional intercellular communication by mitogen-activated protein kinase. J. Biol. Chem. 273 (1998) 9188-9196
78. Zhong G., Hayrapetyan V., and Moreno A.P. The formation of mono-heteromeric Cx43-Cx45/Cx45 gap junction channels uncovers gating and selectivity properties of their channels. Biophys. J. 82 (2003) 633
79. Zhou L., Kasperek E., and Nicholson B. Dissection of the molecular basis of pp60v-src induced gating of connexin 43 gap junction channels. J. Cell Biol. 144 (1999) 1033-1042