Divalent cations regulate connexin hemichannels by modulating intrinsic voltage-dependent gating

Journal of General Physiology

Volumn 132, Issue 3, 2008, Pages 315-327

  Verselis, Vytas K ^a   Srinivas, Miduturu ^b  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^b STATE UNIVERSITY OF NEW YORK   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GAP JUNCTION PROTEIN; MAGNESIUM; MAGNESIUM CHLORIDE;

ANIMAL CELL; ARTICLE; CHANNEL GATING; CONTROLLED STUDY; ELECTROPHYSIOLOGY; HYPERPOLARIZATION; NONHUMAN; OOCYST; PROTEIN EXPRESSION; XENOPUS;

ANIMALS; CATIONS; CELLS, CULTURED; CONNEXINS; ION CHANNEL GATING; MEMBRANE POTENTIALS; OOCYTES; XENOPUS LAEVIS;

EID: 50449110491     PISSN: 00221295     EISSN: 00221295     Source Type: Journal    
DOI: 10.1085/jgp.200810029     Document Type: Article

References (45)

1. Baumgartner, W., L. Islas, and F.J. Sigworth. 1999. Two-microelectrode voltage clamp of Xenopus oocytes: voltage errors and compensation for local current flow. Biophys. J. 77:1980-1991.
2. Bukauskas, F.F., and V.K. Verselis. 2004. Gap junction channel gating. Biochim. Biophys. Acta. 1662:42-60.
3. Contreras, J.E., H.A. Sanchez, E.A. Eugenin, D. Speidel, M. Theis, K. Willecke, F.F. Bukauskas, M.V. Bennett, and J.C. Saez. 2002. Metabolic inhibition induces opening of unapposed connexin 43 gap junction hemichannels and reduces gap junctional communication in cortical astrocytes in culture. Proc. Natl. Acad. Sci. USA. 99:495-500.
4. Draber, S., and R. Schultze. 1994. Detection of jumps in single-channel data containing subconductance levels. Biophys. J. 67:1404-1413.
5. 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.
6. Ebihara, L., X. Liu, and J.D. Pal. 2003. Effect of external magnesium and calcium on human connexin46 hemichannels. Biophys. J. 84:277-286.
7. Evans, W.H., E. De Vuyst, and L. Leybaert. 2006. The gap junction cellular internet: connexin hemichannels enter the signalling limelight. Biochem. J. 397:1-14.
8. Genetos, D.C., C.J. Kephart, Y. Zhang, C.E. Yellowley, and H.J. Donahue. 2007. Oscillating fluid flow activation of gap junction hemichannels induces ATP release from MLO-Y4 osteocytes. J. Cell. Physiol. 212:207-214.
9. Gomez-Hernandez, J.M., M. deMiguel, B. Larrosa, D. Gonzalez, and L.C. Barrio. 2003. Molecular basis of calcium regulation in connexin-32 hemichannels. Proc. Natl. Acad. Sci. USA. 100:16030-16035.
10. Hille, B., C.M. Armstrong, and R. MacKinnon. 1999. Ion channels: from idea to reality. Nat. Med. 5:1105-1109.
11. Huang, Y.J., Y. Maruyama, G. Dvoryanchikov, E. Pereira, N. Chaudhari, and S.D. Roper. 2007. The role of pannexin 1 hemichannels in ATP release and cell-cell communication in mouse taste buds. Proc. Natl. Acad. Sci. USA. 104:6436-6441.
12. John, S.A., R. Kondo, S.Y. Wang, J.I. Goldhaber, and J.N. Weiss. 1999. Connexin-43 hemichannels opened by metabolic inhibition. J. Biol. Chem. 274:236-240.
13. Kamermans, M., and I. Fahrenfort. 2004. Ephaptic interactions within a chemical synapse: hemichannel-mediated ephaptic inhibition in the retina. Curr. Opin. Neurobiol. 14:531-541.
14. Kamermans, M., I. Fahrenfort, K. Schultz, U. Janssen-Bienhold, T. Sjoerdsma, and R. Weiler. 2001. Hemichannel-mediated inhibition in the outer retina. Science. 292:1178-1180.
15. Kronengold, J., E.B. Trexler, F.F. Bukauskas, T.A. Bargiello, and V.K. Verselis. 2003a. Pore-lining residues identified by single channel SCAM studies in Cx46 hemichannels. Cell Commun. Adhes. 10:193-199.
16. Kronengold, J., E.B. Trexler, F.F. Bukauskas, T.A. Bargiello, and V.K. Verselis. 2003b. Single-channel SCAM identifies pore-lining residues in the first extracellular loop and first transmembrane domains of Cx46 hemichannels. J. Gen. Physiol. 122:389-405.
17. Locovei, S., J. Wang, and G. Dahl. 2006. Activation of pannexin 1 channels by ATP through P2Y receptors and by cytoplasmic calcium. FEBS Lett. 580:239-244.
18. Lurtz, M.M., and C.F. Louis. 2007. Intracellular calcium regulation of connexin43. Am. J. Physiol. Cell Physiol. 293:C1806-C1813.
19. Muller, D.J., G.M. Hand, A. Engel, and G.E. Sosinsky. 2002. Conformational changes in surface structures of isolated connexin 26 gap junctions. EMBO J. 21:3598-3607.
20. Paemeleire, K., P.E. Martin, S.L. Coleman, K.E. Fogarty, W.A. Carrington, L. Leybaert, R.A. Tuft, W.H. Evans, and M.J. Sanderson. 2000. Intercellular calcium waves in HeLa cells expressing GFP-labeled connexin 43, 32, or 26. Mol. Biol. Cell. 11:1815-1827.
21. Pelegrin, P., and A. Surprenant. 2006. Pannexin-1 mediates large pore formation and interleukin-1β release by the ATP-gated P2X7 receptor. EMBO J. 25:5071-5082.
22. Peracchia, C. 2004. Chemical gating of gap junction channels; roles of calcium, pH and calmodulin. Biochim. Biophys. Acta. 1662:61-80.
23. Pfahnl, A., and G. Dahl. 1998. Localization of a voltage gate in connexin46 gap junction hemichannels. Biophys. J. 75:2323-2331.
24. Pfahnl, A., and G. Dahl. 1999. Gating of cx46 gap junction hemichannels by calcium and voltage. Pflugers. Arch. 437:345-353.
25. Puljung, M.C., V.M. Berthoud, E.C. Beyer, and D.A. Hanck. 2004. Polyvalent cations constitute the voltage gating particle in human connexin37 hemichannels. J. Gen. Physiol. 124:587-603.
26. Purnick, P.E., S. Oh, C.K. Abrams, V.K. Verselis, and T.A. Bargiello. 2000. Reversal of the gating polarity of gap junctions by negative charge substitutions in the N-terminus of connexin 32. Biophys. J. 79:2403-2415.
27. Ramanan, S.V., P.R. Brink, K. Varadaraj, E. Peterson, K. Schirrmacher, and K. Banach. 1999. A three-state model for connexin37 gating kinetics. Biophys. J. 76:2520-2529.
28. Ri, Y., J.A. Ballesteros, C.K. Abrams, S. Oh, V.K. Verselis, H. Weinstein, and T.A. Bargiello. 1999. The role of a conserved proline residue in mediating conformational changes associated with voltage gating of Cx32 gap junctions. Biophys. J. 76:2887-2898.
29. 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. USA. 86:2708-2712.
30. Schock, S.C., D. Leblanc, A.M. Hakim, and C.S. Thompson. 2008. ATP release by way of connexin 36 hemichannels mediates ischemic tolerance in vitro. Biochem. Biophys. Res. Commun. 368:138-144.
31. Srinivas, M., J. Kronengold, F.F. Bukauskas, T.A. Bargiello, and V.K. Verselis. 2005. Corrective studies of gating in Cx46 and Cx50 hemichannels and gap junction channels. Biophys. J. 88:1725-1739.
32. Srinivas, M., D.P. Calderon, J. Kronengold, and V.K. Verselis. 2006. Regulation of connexin hemichannels by monovalent cations. J. Gen. Physiol. 127:67-75.
33. Stout, C.E., J.L. Costantin, C.C. Naus, and A.C. Charles. 2002. Intercellular calcium signaling in astrocytes via ATP release through connexin hemichannels. J. Biol. Chem. 277:10482-10488.
34. Thimm, J., A. Mechler, H. Lin, S. Rhee, and R. Lal. 2005. Calcium-dependent open/closed conformations and interfacial energy maps of reconstituted hemichannels. J. Biol. Chem. 280:10646-10654.
35. Thompson, R.J., N. Zhou, and B.A. MacVicar. 2006. Ischemia opens neuronal gap junction hemichannels. Science. 312:924-927.
36. 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.
37. 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.
38. 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.
39. 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.
40. Verselis, V.K., C.S. Ginter, and T.A. Bargiello. 1994. Opposite voltage gating polarities of two closely related connexins. Nature. 368:348-351.
41. Weissman, T.A., P.A. Riquelme, L. Ivic, A.C. Flint, and A.R. Kriegstein. 2004. Calcium waves propagate through radial glial cells and modulate proliferation in the developing neocortex. Neuron. 43:647-661.
42. 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.
43. Ye, Z.C., M.S. Wyeth, S. Baltan-Tekkok, and B.R. Ransom. 2003. Functional hemichannels in astrocytes: a novel mechanism of glutamate release. J. Neurosci. 23:3588-3596.
44. Zhao, H.B., N. Yu, and C.R. Fleming. 2005. Gap junctional hemichannel-mediated ATP release and hearing controls in the inner ear. Proc. Natl. Acad. Sci. USA. 102:18724-18729.
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.