Single-channel SCAM identifies pore-lining residues in the first extracellular loop and first transmembrane domains of Cx46 hemichannels

Journal of General Physiology

Volumn 122, Issue 4, 2003, Pages 389-405

  Kronengold, J ^a   Trexler, E B ^b   Bukauskas, F F ^a   Bargiello, T A ^a   Verselis, Vytas K ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

Author keywords

Conductance; Connexin; Cysteine scanning; Gap junctions; Rectification

Indexed keywords

GAP JUNCTION PROTEIN; THIOMESYLIC ACID METHYL ESTER;

ANALYTIC METHOD; ARTICLE; CONDUCTANCE; CONTROLLED STUDY; GAP JUNCTION; ION CURRENT; NONHUMAN; RAT; SUBSTITUTED CYSTEINE ACCESSIBILITY METHOD;

ANIMALS; CONNEXINS; CYSTEINE; ELECTROPHYSIOLOGY; EXTRACELLULAR SPACE; INDICATORS AND REAGENTS; ION CHANNELS; KINETICS; MEMBRANE POTENTIALS; MESYLATES; OOCYTES; PATCH-CLAMP TECHNIQUES; RATS; RECOMBINANT FUSION PROTEINS; RNA, MESSENGER; XENOPUS;

EID: 0141919839     PISSN: 00221295     EISSN: None     Source Type: Journal    
DOI: 10.1085/jgp.200308861     Document Type: Article

References (45)

1. Beahm, D.L., and J.E. Hall. 2002. Hemichannel and junctional properties of connexin 50. Biophys. J. 82:2016-2031.
2. 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.
3. Bera, A.K., M. Chatav, and M.H. Akabas. 2002. GABA(A) receptor M2-M3 loop secondary structure and changes in accessibility during channel gating. J. Biol. Chem. 277:43002-43010.
4. Bergoffen, J., S.S. Scherer, S. Wang, M.O. Scott, L.J. Bone, D.L. Paul, K. Chen, M.W. Lensch, P.F. Chance, and K.H. Fischbeck. 1993. Connexin mutations in X-linked Charcot-Marie-Tooth disease. Science. 262:2039-2042.
5. Castro, C., J.M. Gomez-Hernandez, K. Silander, and L.C. Barrio. 1999. Altered formation of hemichannels and gap junction channels caused by C-terminal connexin-32 mutations. J. Neurosci. 19:3752-3760.
6. Cha, A., and F. Bezanilla. 1998. Structural implications of fluorescence quenching in the Shaker K+ channel. J. Gen. Physiol. 112:391-408.
7. Dahl, G., E. Levine, C. Rabadan Diehl, and R. Werner. 1991. Cell/cell channel formation involves disulfide exchange. Eur. J. Biochem. 197:141-144.
8. Ebihara, L., V.M. Berthoud, and E.C. Beyer. 1995. Distinct behavior of connexin56 and connexin46 gap junctional channels can be predicted from the behavior of their hemi-gap-junctional channels. Biophys. J. 68:1796-1803.
9. 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.
10. Foote, C.I., L. Zhou, X. Zhu, and B.J. Nicholson. 1998. The pattern of disulfide linkages in the extracellular loop regions of connexin 32 suggests a model for the docking interface of gap junctions. J. Cell Biol. 140:1187-1197.
11. Glauner, K.S., L.M. Mannuzzu, C.S. Gandhi, and E.Y. Isacoff. 1999. Spectroscopic mapping of voltage sensor movement in the Shaker potassium channel. Nature. 402:813-817.
12. Harris, A.L. 2001. Emerging issues of connexin channels: biophysics fills the gap. Q. Rev. Biophys. 34:325-472.
13. Hertzberg, E.L., R.M. Disher, A.A. Tiller, Y. Zhou, and R.G. Cook. 1988. Topology of the Mr 27,000 liver gap junction protein. Cytoplasmic localization of amino- and carboxyl termini and a hydrophilic domain which is protease-hypersensitive. J. Biol. Chem. 263:19105-19111.
14. Hu, X., and G. Dahl. 1999. Exchange of conductance and gating properties between gap junction hemichannels. FEBS Lett. 451:113-117.
15. Ionasescu, V., C. Searby, and R. Ionasescu. 1994. Point mutations of the connexin32 (GJB1) gene in X-linked dominant Charcot-Marie-Tooth neuropathy. Hum. Mol. Genet. 3:355-358.
16. Karlin, A. 2001. Scam feels the pinch. J. Gen. Physiol. 117:235-238.
17. Karlin, A., and M.H. Akabas. 1998. Substituted-cysteine accessibility method. Methods Enzymol. 293:123-145.
18. Kelsell, D.P., J. Dunlop, H.P. Stevens, N.J. Lench, J.N. Liang, G. Parry, R.F. Mueller, and I.M. Leigh. 1997. Connexin 26 mutations in hereditary non-syndromic sensorineural deafness. Nature. 387:80-83.
19. Mackay, D., A. Ionides, Z. Kibar, G. Rouleau, V. Berry, A. Moore, A. Shiels, and S. Bhattacharya. 1999. Connexin46 mutations in autosomal dominant congenital cataract. Am. J. Hum. Genet. 64:1357-1364.
20. Oh, S., C.K. Abrams, V.K. Verselis, and T.A. Bargiello. 2000. Stoichiometry of transjunctional voltage-gating polarity reversal by a negative charge substitution in the amino terminus of a connexin32 chimera. J Gen. Physiol. 116:13-31.
21. 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.
22. 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.
23. Paul, D.L. 1986. Molecular cloning of cDNA for rat liver gap junction protein. 1986. J. Cell Biol. 103:123-134.
24. 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.
25. Pfahnl, A., and G. Dahl. 1998. Localization of a voltage gate in connexin46 gap junciton hemichannels. Biophys. J. 75:2323-2331.
26. Richard, G., L.E. Smith, R.A. Bailey, P. Itin, D. Hohl, E.H. Epstein, Jr., J.J. DiGiovanna,J.G. Compton, and S.J. Bale. 1998. Mutations in the human connexin gene GJB3 cause erythrokeratodermia variabilis. Nat. Genet. 20:366-369.
27. Rubin, J.B., V.K. Verselis, M.V. Bennett, and T.A. Bargiello, 1992a. 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. USA. 89:3820-3824.
28. Rubin, J.B., V.K. Verselis, M.V. Bennett, and T.A. Bargiello. 1992b. Molecular analysis of voltage dependence of heterotypic gap junctions formed by connexins 26 and 32. Biophys. J. 62:183-193.
29. Senzel, L., M. Gordon, R.O. Blaustein, K.J. Oh, R.J. Collier, and A. Finkelstein. 2000. Topography of diphtheria Toxin's T domain in the open channel state. J. Gen. Physiol. 115:421-434.
30. Shiels, A., D. Mackay, A. Ionides, V. Berry, A. Moore, and S. Bhattacharya. 1998. A missense mutation in the human connexin50 gene (GJA8) underlies autosomal dominant "zonular pulverulent" cataract, on chromosome 1q. Am. J. Hum. Genet. 62:526-532.
31. Skerrett, I.M., J. Aronowitz, J.H. Shin, G. Cymes, E. Kasperek, F.L. Cao, and B.J. Nicholson. 2002. Identification of amino acid residues lining the pore of a gap junction channel. J. Cell Biol. 159:349-360.
32. Slatin, S.L., X.Q. Qiu, K.S. Jakes, and A. Finkelstein. 1994. Identification of a translocated protein segment in a voltage-dependent channel. Nature. 371:158-161.
33. 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. USA. 93:5836-5841.
34. Trexler, E.B., F.F., Bukauskas, M.V. Bennett, T.A. Bargiello, and V.K. Verselis. 1999. Rapid and direct effects of pH on connexins revealed by the connexin46 hemichannel preparation. J. Gen. Physiol. 113:721-742.
35. Trexler, E.B., F.F. Bukauskas, J. Kronengold, T.A. Bargiello, and V.K. Verselis. 2000. The first extracellular loop domain is a major determinant of charge selectivity in connexin46 channels. Biophys. J. 79:3036-3051.
36. Unger, V.M., N.M. Kumar, N.B. Gilula, and M. Yeager. 1999. Three-dimensional structure of a recombinant gapjunction membrane channel. Science. 283:1176-1180.
37. Valiunas, V. 2002. Biophysical properties of connexin-45 gap junction hemichannels studied in vertebrate cells. J. Gen. Physiol. 119:147-164.
38. Valiunas, V. E.C. Beyer, and P.R. Brink. 2002. Cardiac gap junction channels show quantitative differences in selectivity. Circ. Res. 91:104-111.
39. Valiunas, V., and R. Weingart. 2000. Electrical properties of gap junction hemichannels identified in transfected HeLa cells. Pflugers Arch. 440:366-379.
40. 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.
41. Verselis, V.K., and F.F. Bukauskas. 2002. Connexin-GFPs shed light on regulation of cell-cell communication by gap junctions. Curr. Drug Targets. 3:483-499.
42. Verselis, V.K., E.B. Trexler, and F.F. Bukauskas. 2000. Connexin hemichannels and cell-cell channels: comparison of properties. Braz. J. Med. Biol. Res. 33:379-389.
43. White, T.W., R. Bruzzone, S. Wolfram, D.L. Paul, and D.A. Goodenough. 1994. Selective interactions among the multiple connexin proteins expressed in the vertebrate lens: the second extracellular domain is a determinant of compatibility between connexins. J. Cell Biol. 125:879-892.
44. Willecke, K., J. Eiberger, J. Degen, D. Eckardt, A. Romualdi, M. Guldenagel, U. Deutsch, and G. Sohl. 2002. Structural and functional diversity of connexin genes in the mouse and human genome. Biol. Chem. 383:725-737.
45. Zhou, X.W., A. Pfahnl, R. Werner, A. Hudder, A. Llanes, A. Luebke, and G. Dahl. 1997. Identification of a pore lining segment in gap junction hemichannels. Biophys. J. 72:1946-1953.