Molecular dissection of transjunctional voltage dependence in the connexin-32 and connexin-43 junctions

Biophysical Journal

Volumn 77, Issue 3, 1999, Pages 1374-1383

  Revilla, Ana ^a   Castro, Carmen ^a   Barrio, Luis C ^a  

^a HOSPITAL RAMÓN Y CAJAL   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

CONNEXIN 32; CONNEXIN 43; MUTANT PROTEIN;

ANIMAL CELL; ARTICLE; CHANNEL GATING; CONDUCTANCE; GAP JUNCTION; MEMBRANE POTENTIAL; MODEL; NONHUMAN; VOLTAGE CLAMP; XENOPUS;

ANIMALIA;

EID: 0032838486     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-3495(99)76986-9     Document Type: Article

References (57)

1. Amstrong, C., and B. Hille. 1998. Voltage-gated ion channels and electrical excitability. Neuron. 20:371-380.
2. Banach, K., S. V. Ramanan, and P. R. Brink. 1998. Homotypic hCx37 and rCx43 and their heterotypic form. In Gap Junctions. R. Werner, editor. IOS Press, Amsterdam. 76-80.
3. Banach, K., and R. Weingart. 1996. Connexin43 gap junctions exhibit asymmetrical gating properties. Pfliiger Arch Eur. J. Physiol. 432: 775-785.
4. Barrio, L. C., J. Capel, J. A. Jarillo, C. Castro, and A. Revilla. 1997. Species-specific voltage-gating properties of connexin-45 junctions expressed in Xenopus oocytes. Biophys. J. 73:757-769.
5. Barrio, L. C., J. A. Jarillo, J. C. Sáez, and E. C. Beyer. 1995. Comparison of voltage dependence of chick connexin 45 and 42 channels expressed in pairs of Xenopus oocytes. In Progress in Cell Research: Gap Junctions, Vol. 4. Y. Kanno, K. Kataoka, Y. Shiba, Y. Shibata, and T. Shimazu, editors. Elvesier, Amsterdam. 391-394.
6. Barrio, L. C., A. Revilla, J. M. Gómez-Hemadez, M. DeMiguel, and D. Gonzalez. 1999. Membrane potential dependence of gap junctions in vertebrates. In Current Topics in Membranes: Gap Junctions - Molecular Basis of Cell Communication in Health and Disease. C. Pericchia, editor. Academic Press, San Diego, (in press)
7. Barrio, L. C., T. 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. Sei. USA. 88:8410-8414.
8. Bennett, M. V. L., L. C. Barrio, T. A. Bargiello, D. C. Spray, E. Hertzberg, and J. C. Sdez. 1991. Gap junctions: new tools, new answers, new questions. Neuron. 6:305-320.
9. Bennett, M. V. L., and V. K. Verselis. 1992. Biophysics of gap junctions. Semin. Cell Biol. 3:29-47.
10. Beyer, E. C., D. L. Paul, and D. A. Goodenough. 1987. Connexin 43: a protein from rat heart homologous to a gap junction protein from liver. J. Cell Biol. 105:2621-2629.
11. Bone, L. J., N. Dahl, M. W. Lensch, P. F. Chance, T. Kelly, E. Le Guem, S. Magi, G. Parry, H. Shapiro, S. Wang, and K. H. Fischbeck. 1995. New connexin32 mutations associated with X-linked dominant CharcotMarie-Tooth disease. Neurology. 45:1863-1866.
12. Bruzzone, R., J.-A. Haefliger, R. L. Gimlich, and D. L. Paul. 1993. Connexin40, a component of gap junctions in vascular endothelium, is restricted in its ability to interact with other connexins. Mol. Biol. Cell. 4:7-20.
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. 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.
15. Dunham, B., S. Liu, S. Taffet, E. Trabda-Janik, M. Delmar, R. Tetryshyn, S. Zheng, R. Perzova, and M. L. Vallano. 1992. Immunolocalization and expression of functional and nonfunctional cell-to-cell channels from wild-type and mutant rat heart connexin43 cDNA. Circ. Res. 70: 1233-1243.
16. Ebihara, L., E. C. Beyer, K. I. Swenson, D. L. Paul, and D. A. Goodenough. 1989. Cloning and expression of a Xenopus embryonic gap junction. Science. 243:1194-1195.
17. Ek, J. F., M. Delmar, R. Perzova, and S. M. Taffet. 1994. Role of histidine 95 on pH gating of the cardiac 'gap junction protein connexin43. Circ. Res. 74:1058-1064.
18. Fairweather, N., C. Bell, S. Cochrane, J. Chelly, S. Wang, M. L. Mostacciuolo, A. P. Monaco, and N. E. Haites. 1994. Mutations in the connexin 32 gene in X-linked dominant Charcot-Marie-Tooth disease (CMTX1). Hum. Mol. Genet. 3:29-34.
19. Goodenough, D. A., D. L. Paul, and L. Jesaitis. 1988. Topological distribution of two connexin32 antigenic sites in intact and split rodent hepatocyte gap junctions. J. Cell Biol. 107:1817-1824.
20. Gupta, V. K., V. M. Berthoud, N. Atal, J. A. Jarillo, L. C. Barrio, and E. C. Beyer. 1994. Bovine connexin44, a lens gap junction protein: molecular cloning, immunological characterization and functional expression. Invest. Ophthalmol. Vis. Sei. 35:3747-3758.
21. Harris, A., D. C. Spray, and M. V. L. Bennett. 1981. Kinetic properties of a voltage-dependent junctional conductance. J. Gen. Physiol. 77:95-117.
22. Hennemann, H., T. Suckyna, H. Lichtenberg-Fraté, S. Jungbluth, E. Dahl, L.Swarz, 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.
23. r 27,000 liver gap junction protein cytoplasmic localization of the amino and carboxyl termini and a hydrophobic domain which is protease hypersensitive. J. Biol. Chem. 265:2138-2147.
24. Homma, N., J. L. Alvarado, W. Coombs, K. Stergiopoulos, S. M. Taffet, A. F. Lau, and M. Delmar. 1998. A particle-receptor model for insulin-induced closure of connexin43 channels. Circ. Res 83:27-32.
25. Hoshi, T., W. N. Zagotta, and R. W. Aldrich. 1990. Biophysical and molecular mechanisms of Shaker potassium channel inactivation. Science. 250:533-538.
26. lonasescu, V. V., R. lonasescu, and C. Searb. 1996. Correlation between connexin 32 gene mutations and clinical phenotype in X-linked dominant Charcot-Marie-Tooth neuropathy. Am. J. Med. Genet. 63:486-491.
27. Kumar, N. M., and N. B. Gilula. 1986. Cloning and characterization of human and rat liver cDNAs coding for a gap junction protein. J. Cell Biol. 103:767-776.
28. Lal, R., and M. F. Arnsdorf. 1992. Voltage dependent gating and single-channel conductance of adult mammalian atrial gap junctions. Circ. Res. 71:737-743.
29. Liu, S., S. Taffet, L. Stoner, M. Delmar, M. L. Vallano, and J. Jalife. 1993. A structural basis for the unequal sensitivity of the major cardiac and liver gap junctions to intracellular acidification: the carboxyl tail length. Biophys. J. 64:1422-1433.
30. Makowski, L., D. L. Caspar, W. C. Phillips, and D. A. Goodenough. 1977. Gap junction structures. Analysis of the x-ray diffraction data. J. Cell Biol. 74:629-645.
31. Makowski, L., D. L. Caspar, W. C. Phillips, and D. A. Goodenough. 1984. Gap junction structures. V. Structural chemistry inferred from x-ray diffraction measurements on sucrose accessibility and trypsin susceptibility. J. Mol. Biol. 174:449-481.
32. Martin, P. E. M., C. H. George, C. Castro, J. M. Kendall, J. Capel, A. K. Campbell, A. Revilla, L. C. Barrio, and W. H. Evans. 1998. Assembly of chimeric connexin-aequorin proteins into functional gap junction channels. /. Biol. Chem. 273:1719-1726.
33. Milks, L. C., N. M. Kumar, R. Houghton, N. Unwin, and N. B. Gilula. 1988. Topology of the 32-kd liver gap junction determined by sitedirected antibody localizations. EMBO J. 7:2967-2975.
34. Moreno, A. P., G. I. Fishman, E. C. Beyer, and D. C. Spray. 1995. Voltage dependent gating and single channels analysis of heterotypic gap June-tions formed of Cx45 and Cx43. In Progress in Cell Research: Intracellular Communication Through Gap Junctions, Vol 4. Y. Kanno, K. Kataoka, Y. Shiba, Y. Shibata, and T. Shimazu, editors. Elvesier, Amsterdam. 405-408.
35. Moreno, A. P., G. I. Fishman, and D. C. Spray. 1992. Phosphorylation shifts unitary conductance and modifies voltage dependent kinetics of human connexin43 gap junction channels. Biophys, J. 62:51-53.
36. Moreno, A. P., M. B. Rook, G. I. Fishman, and D. C. Spray. 1994. Gap junction channels: distinct voltage-sensitive and insensitive conductance states. Biophys. J. 67:113-119.
37. Morley, G. E., S. M. Taffet, and M. Delmar. 1996. Intramolecular interactions mediate the pH regulation of connexin43. Biophys. J. 70: 1294-1302.
38. Nicholson, B. J., T. Suchyna, L. X. Xu, P. Hammernick, F. L. Cao, C. Fourtner, L. C. 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. Elvesier, Amsterdam. 3-13.
39. Nicholson, B. J., L. Zhou, F. Cao, H. Zhiu, and Y. Chen. 1998. Diverse molecular mechanisms of gap junction channel gating. In Gap Junctions. R. Werner, editor. IOS Press, Amsterdam. 3-7.
40. Oh, S., Y. Ri, M. V. L. Bennett, E. B. Trexler, V. K. Verselis, and T. A. Bargiello. 1997. Changes in permeability caused by connexin 32 mutations underlie X-Iinked Charcot-Marie-Tooth disease. Neuron. 19:927-938.
41. Rabadan-Diehl, C., G. Dahl, and R. Werner. 1994. A connexin-32 mutation associated with Charcot-Marie-Tooth disease does not affect channel formation in oocytes. FEBS Lett. 351:90-94.
42. Sosinsky, G. E. 1992. Image analysis of gap junction structures. Electron. Microsc. Rev. 5:59-76.
43. Sosinsky, G. E. 1996. Molecular organization of gap junction membrane channels. J. Bioenerg. Biomembr. 28:297-310.
44. Spray, D. C, A. L. Harris, and M. V. L. Bennett. 1981. Equilibrium properties of a voltage-dependent junctional conductance. J. Gen. Physiol. 77:77-93.
45. Suckyna, T. M., L. Xian-Xu, F. Gao, C. R. Fourtner, and B. J. Nicholson. 1993. Identification of a proline residue as a transduction element involved in voltage gating of gap junctions. Nature. 365:847-849.
46. Unger, V. M., N. M. Kumar, N. B. Gilula, and M. Yeager. 1997. Projection structure of gap junction membrane channel at 7 197 Å resolution. Nature Struct. Biol. 4:39-43.
47. Unwin, P. N. T., and P. D. Ennis. 1984. Two configurations of a channelforming protein. Nature. 307:609-613.
48. Unwin, P. N. T., and G. Zampighi. 1980. Structure of the junctions between communicating cells. Nature. 283:545-549.
49. Valiunas, V., F. F. Bukauskas, and R. Weingart. 1997. Conductances and selective permeability of connexin-43 gap junction channels examined in neonatal heart cells. Circ. Res. 80:708-719.
50. Verselis, V. K., C. S. Ginter, and T. A. Bargiello. 1994. Opposite voltage gating polarities of two closely related connexins. Nature. 368:348-351.
51. Wang, H.-Z., L. Li, F. Lemanski, and R. D. Veenstra. 1992. Gating of mammalian cardiac gap junction channels by transjunctional voltage. Biophys. J. 63:139-151.
52. White, T. W., R. Bruzzone, and D. L. Paul. 1995. The connexin family of intercellular channel forming proteins. Kidney Int. 48:1148-1157.
53. Wilders, R., and H. J. Jongsma. 1992. Limitations of the dual voltage clamp method in assaying conductance and kinetics of gap junction channels. Biophys. J. 63:942-953.
54. Willecke, K., R. Heynkes, E. Dahl, R. Stutenkemper, H. Hennemann, S. Jungbluth, T. Suchyna, and B. J. Nicholson. 1991. Mouse connexin37: cloning and functional expression of a gap junction gene highly expressed in lung. J. Cell Biol. 114:1049-1057.
55. Yancy, S. B., S. A. John, R. Lal, B. J. Austin, and J.-P. Revel. 1989. The 43-kD polypeptide of heart gap junctions: immunolocalization, topology, and functional domains. J. Cell Biol. 108:2241-2254.
56. Yeager, M., and N. B. Gilula. 1992. Membrane topology and quartenary structure of cardiac gap junction ion channels. J. Mol. Biol. 223:929-948.
57. Zimmer, D. B., C. R. Green, W. H. Evans, and N. B. Gilula. 1987. Topological analysis of the major protein in isolated intact rat liver gap junctions and gap junction-derivated single membrane structures. J. Biol. Chem. 262:7751-7763.