Different ionic selectivities for connexins 26 and 32 produce rectifying gap junction channels

Biophysical Journal

Volumn 77, Issue 6, 1999, Pages 2968-2987

  Suchyna, Thomas M ^a   Nitsche, Johannes M ^b   Chilton, Mark ^c   Harris, Andrew L ^d   Veenstra, Richard D ^c   Nicholson, Bruce J ^a  

^a UNIVERSITY AT BUFFALO   (United States)

^b State University of New York   (United States)

^c SUNY UPSTATE MEDICAL UNIVERSITY   (United States)

^d JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CONNEXIN 26; CONNEXIN 32; DNA; GLUTAMIC ACID; POTASSIUM CHLORIDE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL MEMBRANE PERMEABILITY; CONTROLLED STUDY; DIFFUSION; ELECTRIC POTENTIAL; ELECTROPHYSIOLOGY; GAP JUNCTION; ION CONDUCTANCE; ION CURRENT; MALE; MOUSE; NEUROBLASTOMA CELL; NONHUMAN;

EID: 0032764028     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-3495(99)77129-8     Document Type: Article

References (57)

1. Barrio, L. C., T. M. Suchyna, T. Bargiello, L. X. Xu, R. S. Roginski, M. V. L. Bennett, and B. J. Nicholson. 1991. Gap junctions formed by connexins 26 and 32 alone and in combination are differently affected by applied voltage. Proc. Natl. Acad. Sci. USA. 88:8410-8414.
2. 3. J. Gen. Physiol. 109:509-522.
3. 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.
4. Brink, P. R., K. Cronin, K. Banach, E Peterson, E. M. Westphale, K. H. Seul, S. V. Ramanan, and E. C. Beyer. 1997. Evidence for heteromeric gap junction channels formed from rat connexin43 and human connexin37. Am. J. Physiol. 273:01386-1396.
5. Brink, P. R., and M. M. Dewey. 1980. Evidence for fixed charge in the nexus. Nature. 285:101-102.
6. Bruzzone, R., T. W. White, and D. L. Paul. 1996. Connections with connexins: the molecular basis of direct intercellular signalling. Eur. J. Biochem. 238:1-27.
7. Bukauskas, F. F., C. Elfgang, K. Willecke, and R. Weingart. 1995. Heterotypic gap junction channels (connexin26-connexin32) violate the paradigm of unitary conductance. Pflugerx Arch. Eur. J. Physiol. 429: 870-872.
8. Cao, F., R. Eckert, C. Elfgang, J. M. Nitsche, S. Snyder, D. F. Hulser, 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.
9. Chen, D. P., V. Barcilon, and R. S. Eisenberg. 1992. Constant fields and constant gradients in open ionic channels. Biophys. J. 61:1372-1393.
10. Chen, D. P., and R. S. Eisenberg. 1993. Flux, coupling, and selectivity in ionic channels of one conformation. Biophys. J. 65:727-746.
11. Dahl, E., D. Manthey, Y. Chen, J. Schwartz, Y. S. Chang, P. A. Lalley, B. J. Nicholson, and K. Willecke. 1996. Mouse Cx30: molecular cloning and functional expression of a gap junction gene highly expressed in adult brain and skin. J. Biol. Chem. 271:17903-17910.
12. Dunlap, K., K. Takeda, and P. Brehm. 1987. Activation of a calcium-dependent photoprotein by chemical signaling through gap junctions. Nature. 325:60-62.
13. Eisenberg, R. S. 1996. Computing the field in proteins and channels. J. Membr. Biol. 150:1-25.
14. 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.
15. Falk, M., L. Buehler, N. Kumar, and N. Gilula. 1997. Cell-free synthesis and assembly of connexins into functional gap junction membrane channels. EMBO J. 16:2703-2716.
16. Flagg-Newton, J., G. Dahl, and W. R. Loewenstein. 1981. Cell junction and cyclic AMP. 1. Upregulation of junctional membrane permeability and junctional membrane particles by administration of cyclic nucleotide or phosphodiesterase inhibitor. J. Membr. Biol. 63:105-121.
17. Frankenhaeuser, B. 1960. Sodium permeability in toad nerve and in squid nerve. J. Physiol. (Lond.). 152:159-166.
18. Fulbridge, R. C., S. M. Fine, E. R. Unanue, and D. D. Chaplin. 1988. Expression of membrane interleukin 1 by fibroblasts transfected with murine prointerleukin lα cDNA. Proc. Natl. Acad. Sci. USA. 85: 5649-5653.
19. Goldman, D. E. 1943. Potential, impedance and rectification in membranes. J. Gen. Physiol. 27:37-60.
20. Harris, A., A. Walter, D. Paul, D. Goodenough, and J. Zimmerberg. 1992. Ion channels in single bilayers induced by rat connexin 32. Brain Res. Mol. Brain Res. 15:269-280.
21. Hennemann, H., T. M. Suchyna, H. Lichtenberg-Frate, S. Jungbluth, E. Dahl, J. Schwarz, B. J. Nicholson, and K. Willecke. 1992. Molecular cloning and functional expression of mouse connexin40, a second gap junction gene preferentially expressed in lung. J. Cell Biol. 117: 1299-1310.
22. Hiemenz, P. C. 1986. Principles of Colliod and Surface Chemistry, 2nd ed. Marcel Dekker, New York.
23. Hille, B. 1992. Selective permeability: independence. In Ionic Channels of Excitable Membranes, 2nd Ed. Sinauer Associates, Sunderland, MA. 348-361.
24. Hodgkin, A. L., and B. Katz., 1949. The effect of sodium ions on the electrical activity of the giant axon of the squid. J. Physiol. (Lond.). 108:37-77.
25. Horan, P. K., M. J. Melnicoff, B. D. Jensen, and S. E. Slezak. 1990. Fluorescent cell labeling for in vivo and in vitro tracking. Methods Enzymol. 33:469-490.
26. Horn, R. 1998. Run, don't hop, through the nearest calcium channel. Biophys. J. 75:1142-1143.
27. Jaslove, S., and P. R. Brink. 1986. The mechanism of rectification at the electronic motor synapse of the crayfish. Nature. 232:63-65.
28. Jiang, J. X., and D. A. Goodenough. 1996. Heterotypic connexons in lens gap junction channels. Proc. Natl. Acad. Sci. USA. 93:1287-1291.
29. Kumar, N. M., and N. B. Gilula. 1996. The gap junction communication channel. Cell. 84:381-388.
30. Levitt, D. G. 1991. General continuum theory for multi-ion channels. II. Application to acetylcholine channel. Biophys. J. 59:278-288.
31. Makowski, L., D. L. Casper, W. C. Philips, and D. A. Goodenough. 1984. Gap junction structures. V. Structural chemistry inferred from x-ray diffraction measurements on sucrose sucrose accessibility and trypsin susceptibility. J. Mol Biol 174:449-481.
32. Moreno, A. P., B. Eghbali, and D. C. Spray. 1991. Connexin32 gap junction channels in stably transfected cells: unitary conductance. Biophys. J. 60:1254-1266.
33. Nevue, M. J., J. R. Hully, K. L. Babcock, E. L. Hertzberg, B. J. Nicholson, D. L. Paul, and H. C. Pilot. 1994. Multiple mechanisms are responsible for altered expression of gap junction genes during oncogenesis in rat liver. J. Cell Sci. 107:83-95.
34. Nicholson, B. J., R. Dermietzel, D. Teplow, O. Trauh, K. Willecke, and J. P. Revel. 1987. Two homologous proteins of hepatic gap junctions. Nature. 329:732-734.
35. Nicholson, B. J., T. M. Suchyna, L. X. Xu, P. Hammernick, F. L. Cao, C. Fourtner, L. Barrio, and M. V. L. Bennett. 1993. Divergent properties of different connexins expressed in Xenopus oocytes. In Progress in Cell Research: Gap Junctions, Vol. 3. J. E. Hall, G. A. Zampighi, and R. M. Davis, editors. Elsevier Science Publishers, New York. 3-13.
36. Nonner, W., and R. S. Eisenberg. 1998. Ion permeation and glutamate residues linked by Poisson-Nernst-Planck theory in L-type calcium channels. Biophys. J. 75:1287-1305.
37. Paul, D. L. 1986. Molecular cloning of cDNA for rat liver gap junction protein. J. Cell Biol. 103:123-134.
38. Reed, K. E., E. M. Westpale, D. M. Larson, H.-Z. Wang, R. D. Veenstra, and E. C. Beyers. 1993. Molecular cloning and functional expression of human connexin37, an endothelial cell gap junction protein. J. Clin. Invest. 91:997-1004.
39. Saez, J. C., J. A. Connor, D. C. Spray, and M. V. L. Bennett. 1989, Hrpstocyte gap junctions are permeable to the second messenger, inositol 1:4.5-triphosphate, and to calcium ions. Proc. Natl. Acad Sci. USA. 86:2708-2712.
40. Schwarzmann, G., H. Wiegandt, B. Rose, A. Zimmermann, D. Ben-Haim. and W. R. Loewenstein. 1981. Diameter of a cell-cell junctional membrane channel as probed with neutral molecules. Science. 213:551-553.
41. Spray, D. C., A. L. Harris, and M. V. L. Bennett. 1979. Equilibrium properties of a voltage-dependent junctional conductance. J. Gen. Physiol. 77:77-93.
42. 2-connexin (Cx26) can form heteromeric hemichannels. J. Biol. Chem. 270:6768-6772.
43. Steinberg, T. H., R. Civitelli, S. T. Geist, A. J. Robertson, E. Hick, R. D. Veenstra, H.-Z. Wang, P. M. Marlow, E. M. Westphale, J. Laing, and E. C. Beyer. 1994. Connexin43 and connexin45 form gap junctions with different molecular permeabilities in osteoclastic cells. EMBO J. 4:744-750.
44. Teorell, T. 1953. Transport processes and electrical phenomena in ionic membranes. Prog. Biophys. 3:305-369.
45. Traub, O., J. Look, R. Dermietzel, F. Brunner, D. Hulser, and K. Willecke. 1989. Comparative characterization of the 21 kD and 26 kD gap junction proteins in murine liver and cultured mouse hepatocytes. J. Cell Biol. 108:1039-1051.
46. Tsien, R. W., and R. Weingart. 1976. Ionotropic effect of cyclic AMP in calf ventricular muscle studied by a cut end method. J. Physiol. (Lond.). 260:117-141.
47. Veenstra, R. D. 1996. Size and selectivity of gap junction channels formed from different connexins. J. Bioenerg. Biomembr. 28:327-337.
48. Veenstra, R. D., and P. R. Brink. 1992. Patch clamp analysis of gap junctional currents. In Cell-Cell Interactions: A Practical Approach. B. Stevenson, D. L. Paul, and W. Gallin, editors. IRL Press, Oxford. 167-201.
49. Veenstra, R. D., H. Z. Wang, D. A. Beblo, M. G. Chilton, A. L. Harris, E. C. Beyer, and P. R. Brink. 1995. Selectivity of connexin-specific gap junctions does not correlate with channel conductance. Circ. Res. 77: 1156-1165.
50. Veenstra, R. D., H. Z. Wang, E. C. Beyer, S. V. Ramanan, and P. R. Brink. 1994. Connexin37 forms high conductance gap junctions channels with subconductance state activity and selective dye and ionic permeabilities. Biophys. J. 66:1915-1928.
51. Verselis, R. D., and P. R. Brink. 1986. The gap junction channel. Its aqueous nature as indicated by deuterium oxide effects. Biophys. J. 50:1003-1008.
52. Verselis, V. K., C. S. Ginter, and T. A. Bargiello. 1994. Opposite voltage gating polarities of two closely related connexins. Nature. 368:348-351.
53. Wang, H.-Z., and R. D. Veenstra. 1997. Monovalent cation and anion selectivity sequences of the rat connexin43 gap junction channel. J. Gen. Physiol. 109:491-507.
54. White, T. M. R. Bruzzone, D. A. Goodenough, and D. L. Paul. 1992. Mouse Cx50, a functional member of the connexin family of gap junction proteins, is lens fiber protein MP70. Mol. Biol. Cell. 3:711-720.
55. White, T. W., D. L. Paul, D. A. Goodenough, and R. Bruzzone. 1995. Functional analysis of selective interactions among rodent connexins. Mol. Biol. Cell. 6:459-470.
56. Yeager, M., and B. J. Nicholson. 1996. Structure of gap junction intercellular channels. Curr. Opin. Struct. Cell Biol. 6:183-192.
57. Zhang, J. T., and B. J. Nicholson. 1994. The topological structure of connexin 26 and its distribution compared to connexin 32 in hepatic gap junctions. J. Membr. Biol. 139:15-29.