The first extracellular loop domain is a major determinant of charge selectivity in connexin46 channels

Biophysical Journal

Volumn 79, Issue 6, 2000, Pages 3036-3051

  Trexler, E Brady ^a   Bukauskas, Feliksas F ^a   Kronengold, Jack ^a   Bargiello, Thaddeus A ^a   Verselis, Vytas K ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANION; CATION; CONNEXIN 46; GAP JUNCTION PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; GAP JUNCTION; HELA CELL; HUMAN; HUMAN CELL; ION CONDUCTANCE; ION PERMEABILITY; MULTIGENE FAMILY; NONHUMAN; PROTEIN DOMAIN; XENOPUS;

ANIMALIA;

EID: 0033636361     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-3495(00)76539-8     Document Type: Article

References (68)

1. Adams, D. J., T. M. Dwyer, and B. Hille. 1980. The permeability of endplate channels to monovalent and divalent metal cations. J. Gen. Physiol. 75:493-510.
2. Andersen, O. S., and R. E. Koeppe, II. 1992. Molecular determinants of channel function. Physiol Rev. 72:S89-S158.
3. Beblo, D. A., and R. D. Veenstra. 1997. Monovalent cation permeation through the connexin40 gap junction channel: Cs, Rb, K, Na, Li, TEA, TMA, TBA, and effects of anions Br, Cl, F, acetate, aspartate, glutamate, and NO3. J. Gen. Physiol. 109:509-522.
4. Bennett, M. V., L. C. Barrio, T. A. Bargiello, D. C. Spray, E. Hertzberg, and J. C. Saez. 1991. Gap junctions: new tools, new answers, new questions. Neuron. 6:305-320.
5. Bennett, M. V., M. E. Spira, and D. C. Spray. 1978. Permeability of gap junctions between embryonic cells of Fundulus: a reevaluation. Dev. Biol. 65:114-125.
6. Bennett, M. V., X. Zheng, and M. L. Sogin. 1994. The connexins and their family tree. Soc Gen Physiol Ser. 49:223-233.
7. Bevans, C. G., M. Kordel, S. K. Rhee, and A. L. Harris. 1998. Isoform composition of connexin channels determines selectivity among second messengers and uncharged molecules. J. Biol. Chem. 273:2808-2816.
8. Beyer, E. C., and K. Willecke. 2000. Gap junction genes and their regulation. In Advances in Molecular and Cell Biology. E. L. Hertzberg, editor. JAI press, Stamford, CT. 1-30.
9. Bezrukov, S. M., and I. Vodyanoy. 1993. Probing alamethicin channels with water-soluble polymers: effect on conductance of channel states. Biophys. J. 64:16-25.
10. Boitano, S., E. R. Dirksen, and M. J. Sanderson. 1992. Intercellular propagation of calcium waves mediated by inositol trisphosphate. Science. 258:292-295.
11. Brink, P. R. 1983. Effect of deuterium oxide on junctional membrane channel permeability. J Membr Biol. 71:79-87.
12. Brink, P. R., and M. M. Dewey. 1980. Evidence for fixed charge in the nexus. Nature. 285:101-102.
13. Bruzzone, R., T. W. White, and D. L. Paul. 1996. Connections with connexins: the molecular basis of direct intercellular signaling. Eur J Biochem. 238:1-27.
14. Bukauskas, F. F., C. Elfgang, K. Willecke, and R. Weingart. 1995a. Biophysical properties of gap junction channels formed by mouse connexin40 in induced pairs of transfected human HeLa cells. Biophys. J. 68:2289-2298.
15. Bukauskas, F. F., C. Elfgang, K. Willecke, and R. Weingart. 1995b. Heterotypic gap junction channels (connexin26-connexin32) violate the paradigm of unitary conductance. Pflug. Arch. 429:870-872.
16. Cao, F., R. Eckert, C. Elfgang, J. M. Nitsche, S. A. Snyder, H. D. F., K. Willecke, and B. J. Nicholson. 1998. A quantitative analysis of connexin-specific permeability differences of gap junctions expressed in HeLa transfectants and Xenopus oocytes. J Cell Sci. 111:31-43.
17. Chen, D., J. Lear, and B. Eisenberg. 1997. Permeation through an open channel: Poisson-Nernst-Planck theory of a synthetic ionic channel. Biophys. J. 72:97-116.
18. Chen, D. P., L. Xu, A. Tripathy, G. Meissner, and B. Eisenberg. 1999. Selectivity and permeation in calcium release channel of cardiac muscle: alkali metal ions. Biophys. J. 76:1346-1366.
19. D' Andrea, P., and F. Vittur. 1996. Gap junctions mediate intercellular calcium signalling in cultured articular chondrocytes. Cell Calcium. 20:389-397.
20. + conduction and selectivity [see comments]. Science. 280:69-77.
21. Ebihara, L., and E. Steiner. 1993. Properties of a nonjunctional current expressed from a rat connexin46 cDNA in Xenopus oocytes. J. Gen. Physiol. 102:59-74.
22. Eisenman, G., and R. Horn. 1983. Ionic selectivity revisited: the role of kinetic and equilibrium processes in ion permeation through channels. J Membr. Biol. 76:197-225.
23. Elfgang, C., R. Eckert, H. Lichtenberg-Frate, A. Butterweck, O. Traub, R. A. Klein, D. F. Hulser, and K. Willecke. 1995. Specific permeability and selective formation of gap junction channels in connexin-transfected HeLa cells. J Cell Biol. 129:805-817.
24. Finkbeiner, S. 1992. Calcium waves in astrocytes: filling in the gaps. Neuron. 8:1101-1108.
25. Flagg-Newton, J., I. Simpson, and W. R. Loewenstein. 1979. Permeability of the cell-to-cell membrane channels in mammalian cell junction. Science. 205:404-407.
26. Green, W. N., and O. S. Andersen. 1991. Surface charges and ion channel function. Annu. Rev. Physiol. 53:341-359.
27. Hu, X., and G. Dahl. 1999. Exchange of conductance and gating properties between gap junction hemichannels. FEBS Lett. 451:113-117.
28. Imoto, K., C. Busch, B. Sakmann, M. Mishina, T. Konno, J. Nakai, H. Bujo, Y. Mori, K. Fukuda, and S. Numa. 1988. Rings of negatively charged amino acids determine the acetylcholine receptor channel conductance. Nature. 335:645-648.
29. Kienker, P. K., W. F. DeGrado, and J. D. Lear. 1994. A helical-dipole model describes the single-channel current rectification of an uncharged peptide ion channel. Proc. Natl. Acad. Sci. U.S.A. 91:4859-4863.
30. Kienker, P. K., and J. D. Lear. 1995. Charge selectivity of the designed uncharged peptide ion channel Ac-(LSSLLSL)3-CONH2. Biophys. J. 68:1347-1358.
31. Kohen, E., C. Kohen, B. Thorell, D. H. Mintz, and A. Rabinovitch. 1979. Intercellular communication in pancreatic islet monolayer cultures: a microfluorometric study. Science. 204:862-865.
32. Lawrence, T. S., W. H. Beers, and N. B. Gilula. 1978. Transmission of hormonal stimulation by cell-to-cell communication. Nature. 272: 501-506.
33. Lo, C. W. 1999. Genes, gene knockouts, and mutations in the analysis of gap junctions. Dev. Genet. 24:1-4.
34. Mills, S. L., and S. C. Massey. 1995. Differential properties of two gap junctional pathways made by All amacrine cells [see comments]. Nature. 377:734-737.
35. Nelles, E., C. Butzler, D. Jung, A. Temme, H. D. Gabriel, U. Dahl, O. Traub, F. Stumpel, K. Jungermann, J. Zielasek, K. V. Toyka, R. Dermietzel, and K. Willecke. 1996. Defective propagation of signals generated by sympathetic nerve stimulation in the liver of connexin32-deficient mice. Proc. Natl. Acad. Sci. U.S.A. 93:9565-9570.
36. Neyton, J., and A. Trautmann. 1985. Single-channel currents of an intercellular junction. Nature. 317:331-335.
37. Niessen, H., H. Harz, P. Bedner, K. Kramer, and K. Willecke. 2000. Selective permeability of different connexin channels to the second messenger inositol 1,4,5-trisphosphate. J Cell Sci. 113:1365-1372.
38. Niessen, H., and K. Willecke. 2000. Strongly decreased gap junctional permeability to inositol 1,4,5-trisphosphate in connexin32 deficient hepatocytes. FEBS Lett. 466:112-114.
39. Nonner, W., D. P. Chen, and B. Eisenberg. 1998. Anomalous mole fraction effect, electrostatics, and binding in ionic channels. Biophys. J. 74: 2327-2334.
40. Nonner, W., and B. Eisenberg. 1998. Ion permeation and glutamate residues linked by Poisson-Nernst-Planck theory in L-type calcium channels. Biophys. J. 75:1287-1305.
41. Oh, S., Y. Ri, M. V. Bennett, E. B. Trexler, V. K. Verselis, and T. A. Bargiello. 1997. Changes in permeability caused by connexin 32 mutations underlie X-linked Charcot-Marie-Tooth disease. Neuron. 19: 927-938.
42. Oh, S., J. B. Rubin, M. V. Bennett, V. K. Verselis, and T. A. Bargiello. 1999. Molecular determinants of electrical rectification of single channel conductance in gap junctions formed by connexins 26 and 32. J. Gen. Physiol. 114:339-364.
43. Paul, D. L., L. Ebihara, L. J. Takemoto, K. I. Swenson, and D. A. Goodenough. 1991. Connexin46, a novel lens gap junction protein, induces voltage-gated currents in nonjunctional plasma membrane of Xenopus oocytes. J. Cell Biol. 115:1077-1089.
44. Pitts, J. D., and J. W. Simms. 1977. Permeability of junctions between animal cells: intercellular transfer of nucleotides but not of macromolecules. Exp. Cell Res. 104:153-163.
45. Roux, B., and M. Karplus. 1994. Molecular dynamics simulations of the gramicidin channel. Annu. Rev. Biophys. Biomol. Struct. 23:731-761.
46. + channel: electrostatic stabilization of monovalent cations [see comments]. Science. 285:100-102.
47. Rubin, J. B., V. K. Verselis, M. V. Bennett, and T. A. Bargiello. 1992a. Molecular analysis of voltage dependence of heterotypic gap junctions formed by connexins 26 and 32. Biophys. J. 62:183-193.
48. Rubin, J. B., V. K. Verselis, M. V. Bennett, and T. A. Bargiello. 1992b. A domain substitution procedure and its use to analyze voltage dependence of homotypic gap junctions formed by connexins 26 and 32. Proc. Natl. Acad. Sci. U.S.A. 89:3820-3824.
49. Saez, J. C., J. A. Connor, D. C. Spray, and M. V. Bennett. 1989. Hepatocyte gap junctions are permeable to the second messenger, inositol 1,4,5-trisphosphate, and to calcium ions. Proc. Natl. Acad. Sci. U.S.A. 86:2708-2712.
50. Schwarzmann, G., H. Wiegandt, B. Rose, A. Zimmerman, D. Ben Haim, and W. R. Loewenstein. 1981. Diameter of the cell-to-cell junctional membrane channels as probed with neutral molecules. Science. 213: 551-553.
51. Sheridan, J. D., M. E. Finbow, and J. D. Pitts. 1979. Metabolic interactions between animal cells through permeable intercellular junctions. Exp. Cell Res. 123:111-117.
52. Sneyd, J., M. Wilkins, A. Strahonja, and M. J. Sanderson. 1998. Calcium waves and oscillations driven by an intercellular gradient of inositol (1,4,5)-trisphosphate. Biophys. Chem. 72:101-109.
53. Subak-Sharpe, J. H., R. R. Burk, and J. D. Pitts. 1969. Metabolic cooperation between biochemically marked cells in tissue culture. J. Cell Sci. 4:353-367.
54. Suchyna, T. M., J. M. Nitsche, M. Chilton, A. L. Harris, R. D. Veenstra, and B. J. Nicholson. 1999. Different ionic selectivities for connexins 26 and 32 produce rectifying gap junction channels. Biophys. J. 77: 2968-2987.
55. Trexler, E. B., M. V. Bennett, T. A. Bargiello, and V. K. Verselis. 1996. Voltage gating and permeation in a gap junction hemichannel. Proc. Natl. Acad. Sci. U.S.A. 93:5836-5841.
56. Unger, V. M., N. M. Kumar, N. B. Gilula, and M. Yeager. 1999. Three-dimensional structure of a recombinant gap junction membrane channel. Science. 283:1176-1180.
57. Vaney, D. I., J. C. Nelson, and D. V. Pow. 1998. Neurotransmitter coupling through gap junctions in the retina. J. Neurosci. 18:10594-10602.
58. Veenstra, R. D., H. Z. Wang, E. C. Beyer, and P. R. Brink. 1994a. Selective dye and ionic permeability of gap junction channels formed by connexin45. Circ. Res. 75:483-490.
59. Veenstra, R. D., H. Z. Wang, E. C. Beyer, S. V. Ramanan, and P. R. Brink. 1994b. Connexin37 forms high conductance gap junction channels with subconductance state activity and selective dye and ionic permeabilities. Biophys. Jl. 66:1915-1928.
60. Verselis, V., and P. R. Brink. 1986. The gap junction channel: its aqueous nature as indicated by deuterium oxide effects. Biophys. J. 50: 1003-1007.
61. Verselis, V. K., C. S. Ginter, and T. A. Bargiello. 1994. Opposite voltage gating polarities of two closely related connexins. Nature. 368:348-351.
62. Verselis, V. K., and R. Veenstra. 2000. Gap junction channels: permeability and voltage gating. In Advances in Molecular and Cell Biology, E.L. Hertzberg, editor. JAI press, Stamford, CT. 129-192.
63. Wang, H. Z., and R. D. Veenstra. 1997. Monovalent ion selectivity sequences of the rat connexin43 gap junction channel. J. Gen. Physiol. 109:491-507.
64. White, T. W., and D. L. Paul. 1999. Genetic diseases and gene knockouts reveal diverse connexin functions. Annu. Rev. Physiol. 61:283-310.
65. Willecke, K., S. Kirchhoff, A. Plum, A. Temme, E. Thonnissen, and T. Ott. 1999. Biological functions of connexin genes revealed by human genetic defects, dominant negative approaches and targeted deletions in the mouse. Novartis Found. Symp. 219:76-96.
66. Wilson, G. G., J. M. Pascual, N. Brooijmans, D. Murray, and A. Karlin. 2000. The intrinsic electrostatic potential and the intermediate ring of charge in the acetylcholine receptor channel [In Process Citation]. J. Gen. Physiol. 115:93-106.
67. Young, S. H., H. S. Ennes, and E. A. Mayer. 1996. Propagation of calcium waves between colonic smooth muscle cells in culture. Cell Calcium. 20:257-271.
68. Zhou, X. W., A. Pfahnl, R. Werner, A. Hudder, A. Lianes, A. Luebke, and G. Dahl. 1997. Identification of a pore lining segment in gap junction hemichannels. Biophys. J. 72:1946-1953.