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. 2000 Feb;78(2):752–760. doi: 10.1016/S0006-3495(00)76633-1

The influence of surface charges on the conductance of the human connexin37 gap junction channel.

K Banach 1, S V Ramanan 1, P R Brink 1
PMCID: PMC1300678  PMID: 10653788

Abstract

The single-channel conductance of the hCx37 homotypic gap junction channel does not saturate with transjunctional voltages up to +/-75 mV, nor does it depend linearly on the intracellular electrolyte concentration. The average maximum unitary conductances measured in KCl were 175 pS (30 mM), 236 pS (55 mM), 343 pS (110 mM), and 588 pS (270 mM) in the presence of 0.1 mM MgCl(2). The unexpectedly high unitary conductance at low salt concentrations can be explained by fixed charge groups within or near the channel orifice. Fixed cytoplasmic surface charges (3.4 e) positioned adjacent (15 A) to the channel pore adequately model the data (surface charge density of 0.24 e/(nm)(2)). In other experiments, high Mg(2+) reduced the unitary conductance of hCx37 homotypic gap junction channels more than predicted by screening alone, consistent with specific effects of Mg(2+) on the channel.

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Selected References

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  1. Brink P. R., Cronin K., Banach K., Peterson E., Westphale E. M., Seul K. H., Ramanan S. V., Beyer E. C. Evidence for heteromeric gap junction channels formed from rat connexin43 and human connexin37. Am J Physiol. 1997 Oct;273(4 Pt 1):C1386–C1396. doi: 10.1152/ajpcell.1997.273.4.C1386. [DOI] [PubMed] [Google Scholar]
  2. Brink P. R., Dewey M. M. Evidence for fixed charge in the nexus. Nature. 1980 May 8;285(5760):101–102. doi: 10.1038/285101a0. [DOI] [PubMed] [Google Scholar]
  3. Brink P. R. Gap junction channel gating and permselectivity: their roles in co-ordinated tissue function. Clin Exp Pharmacol Physiol. 1996 Dec;23(12):1041–1046. doi: 10.1111/j.1440-1681.1996.tb01166.x. [DOI] [PubMed] [Google Scholar]
  4. Cai M., Jordan P. C. How does vestibule surface charge affect ion conduction and toxin binding in a sodium channel? Biophys J. 1990 Apr;57(4):883–891. doi: 10.1016/S0006-3495(90)82608-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Goodenough D. A., Goliger J. A., Paul D. L. Connexins, connexons, and intercellular communication. Annu Rev Biochem. 1996;65:475–502. doi: 10.1146/annurev.bi.65.070196.002355. [DOI] [PubMed] [Google Scholar]
  6. Green W. N., Andersen O. S. Surface charges and ion channel function. Annu Rev Physiol. 1991;53:341–359. doi: 10.1146/annurev.ph.53.030191.002013. [DOI] [PubMed] [Google Scholar]
  7. Harris A. L., Spray D. C., Bennett M. V. Kinetic properties of a voltage-dependent junctional conductance. J Gen Physiol. 1981 Jan;77(1):95–117. doi: 10.1085/jgp.77.1.95. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Imoto K., Busch C., Sakmann B., Mishina M., Konno T., Nakai J., Bujo H., Mori Y., Fukuda K., Numa S. Rings of negatively charged amino acids determine the acetylcholine receptor channel conductance. Nature. 1988 Oct 13;335(6191):645–648. doi: 10.1038/335645a0. [DOI] [PubMed] [Google Scholar]
  9. MacKinnon R., Latorre R., Miller C. Role of surface electrostatics in the operation of a high-conductance Ca2+-activated K+ channel. Biochemistry. 1989 Oct 3;28(20):8092–8099. doi: 10.1021/bi00446a020. [DOI] [PubMed] [Google Scholar]
  10. Naranjo D., Latorre R., Cherbavaz D., McGill P., Schumaker M. F. A simple model for surface charge on ion channel proteins. Biophys J. 1994 Jan;66(1):59–70. doi: 10.1016/S0006-3495(94)80750-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Neyton J., Trautmann A. Single-channel currents of an intercellular junction. 1985 Sep 26-Oct 2Nature. 317(6035):331–335. doi: 10.1038/317331a0. [DOI] [PubMed] [Google Scholar]
  12. Ohki S., Kurland R. Surface potential of phosphatidylserine monolayers. II. Divalent and monovalent ion binding. Biochim Biophys Acta. 1981 Jul 20;645(2):170–176. doi: 10.1016/0005-2736(81)90187-5. [DOI] [PubMed] [Google Scholar]
  13. Ramanan S. V., Brink P. R., Varadaraj K., Peterson E., Schirrmacher K., Banach K. A three-state model for connexin37 gating kinetics. Biophys J. 1999 May;76(5):2520–2529. doi: 10.1016/S0006-3495(99)77406-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Reed K. E., Westphale E. M., Larson D. M., Wang H. Z., Veenstra R. D., Beyer E. C. Molecular cloning and functional expression of human connexin37, an endothelial cell gap junction protein. J Clin Invest. 1993 Mar;91(3):997–1004. doi: 10.1172/JCI116321. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Simpson I., Rose B., Loewenstein W. R. Size limit of molecules permeating the junctional membrane channels. Science. 1977 Jan 21;195(4275):294–296. doi: 10.1126/science.831276. [DOI] [PubMed] [Google Scholar]
  16. Unger V. M., Kumar N. M., Gilula N. B., Yeager M. Projection structure of a gap junction membrane channel at 7 A resolution. Nat Struct Biol. 1997 Jan;4(1):39–43. doi: 10.1038/nsb0197-39. [DOI] [PubMed] [Google Scholar]
  17. Veenstra R. D., Wang H. Z., Beblo D. A., Chilton M. G., Harris A. L., Beyer E. C., Brink P. R. Selectivity of connexin-specific gap junctions does not correlate with channel conductance. Circ Res. 1995 Dec;77(6):1156–1165. doi: 10.1161/01.res.77.6.1156. [DOI] [PubMed] [Google Scholar]
  18. Veenstra R. D., Wang H. Z., Beyer E. C., Ramanan S. V., Brink P. R. Connexin37 forms high conductance gap junction channels with subconductance state activity and selective dye and ionic permeabilities. Biophys J. 1994 Jun;66(6):1915–1928. doi: 10.1016/S0006-3495(94)80985-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Verselis V. K., Ginter C. S., Bargiello T. A. Opposite voltage gating polarities of two closely related connexins. Nature. 1994 Mar 24;368(6469):348–351. doi: 10.1038/368348a0. [DOI] [PubMed] [Google Scholar]
  20. Verselis V., Brink P. R. The gap junction channel. Its aqueous nature as indicated by deuterium oxide effects. Biophys J. 1986 Nov;50(5):1003–1007. doi: 10.1016/S0006-3495(86)83542-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Wang H. Z., Veenstra R. D. Monovalent ion selectivity sequences of the rat connexin43 gap junction channel. J Gen Physiol. 1997 Apr;109(4):491–507. doi: 10.1085/jgp.109.4.491. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Wilders R., Jongsma H. J. Limitations of the dual voltage clamp method in assaying conductance and kinetics of gap junction channels. Biophys J. 1992 Oct;63(4):942–953. doi: 10.1016/S0006-3495(92)81664-8. [DOI] [PMC free article] [PubMed] [Google Scholar]

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