Gating, permselectivity and pH-dependent modulation of channels formed by connexin57, a major connexin of horizontal cells in the mouse retina

Journal of Physiology

Volumn 587, Issue 13, 2009, Pages 3251-3269

  Palacios Prado, Nicolas ^a   Sonntag, Stephan ^b   Skeberdis, Vytenis A ^a   Willecke, Klaus ^b   Bukauskas, Feliksas F ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF BONN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CONNEXIN 43; CONNEXIN 57; GAP JUNCTION PROTEIN; UNCLASSIFIED DRUG; CALCIUM ION; CONNEXIN 45; CONNEXIN 57 PROTEIN; ENHANCED GREEN FLUORESCENT PROTEIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL MEMBRANE CONDUCTANCE; CELL MEMBRANE PERMEABILITY; CHANNEL GATING; CONTROLLED STUDY; CYTOPLASM; FLUORESCENCE IMAGING; GENETIC LINKAGE; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PH; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REGULATORY MECHANISM; RETINA CELL; VOLTAGE CLAMP; ALTERNATIVE MEDICINE; CELL PH; GAP JUNCTION; HELA CELL LINE; INTRACELLULAR TRANSPORT; MOLECULAR WEIGHT; PROTEIN TRANSPORT;

ANIMALS; BIOPHYSICAL PHENOMENA; CELL MEMBRANE PERMEABILITY; CONNEXINS; FLUORESCENT DYES; GAP JUNCTIONS; GREEN FLUORESCENT PROTEINS; HELA CELLS; HUMANS; HYDROGEN-ION CONCENTRATION; ION CHANNEL GATING; MICE; PATCH-CLAMP TECHNIQUES; RECOMBINANT FUSION PROTEINS; RETINAL HORIZONTAL CELLS;

EID: 67650391661     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2009.171496     Document Type: Article

References (77)

1. Baldridge WH, Ball AK & Miller RG (1987). Dopaminergic regulation of horizontal cell gap junction particle density in goldfish retina. J Comp Neurol 265, 428-436.
2. Becker D, Bonness VV & Mobbs P (1998). Cell coupling in the retina: patterns and purpose. Cell Biol Intern 22, 781-792.
3. Bennett MV, Barrio LC, Bargiello TA, Spray DC, Hertzberg E & Saez JC (1991). Gap junctions: New tools, new answers, new questions. Neuron 6, 305-320.
4. Bukauskas FF, Bukauskiene A, Bennett MV & Verselis VK (2001). Gating properties of gap junction channels assembled from connexin43 and connexin43 fused with green fluorescent protein. Biophys J 81, 137-152.
5. Bukauskas FF, Bukauskiene A & Verselis VK (2002a). Conductance and permeability of the residual state of connexin43 gap junction channels. J Gen Physiol 119, 171-186.
6. Bukauskas FF, Bukauskiene A, Verselis VK & Bennett MVL (2002 b). Coupling asymmetry of heterotypic connexin 45/connexin 43-EGFP gap junctions: Properties of fast and slow gating mechanisms. Proc Natl Acad Sci U S A 99, 7113-7118.
7. Bukauskas FF, Jordan K, Bukauskiene A, Bennett MV, Lampe PD, Laird DW & Verselis VK (2000). Clustering of connexin 43-enhanced green fluorescent protein gap junction channels and functional coupling in living cells. Proc Natl Acad Sci U S A 97, 2556-2561.
8. Bukauskas FF, Kreuzberg M, Rackauskas M, Bukauskiene A, Bennett MVL, Verselis VK & Willecke K (2006). Properties of mouse connexin 30.2 and human connexin 31.9 hemichannels: Implications for atrioventricular conduction in the heart. Proc Natl Acad Sci U S A 103, 9726-9731.
9. Bukauskas FF & Verselis VK (2004). Gap junction channel gating. Biochim Biophys Acta 1662, 42-60.
10. Cadetti L & Thoreson WB (2006). Feedback effects of horizontal cell membrane potential on cone calcium currents studied with simultaneous recordings. J Neurophysiol 95, 1992-1995.
11. Caspar DL, Goodenough DA, Makowski L & Phillips WC (1977). Gap junction structures. I. Correlated electron microscopy and x-ray diffraction. J Cell Biol 74, 605-628.
12. Chesler M (2003). Regulation and modulation of pH in the brain. Physiol Rev 83, 1183-1221.
13. Ciolofan C, Lynn BD, Wellershaus K, Willecke K & Nagy JI (2007). Spatial relationships of connexin36, connexin57 and zonula occludens-1 in the outer plexiform layer of mouse retina. J Neurosci 148, 473-488.
14. Contreras JE, Saez JC, Bukauskas FF & Bennett MV (2003). Gating and regulation of connexin 43 (Cx43) hemichannels. Proc Natl Acad Sci U S A 100, 11388-11393.
15. Davenport CM, Detwiler PB & Dacey DM (2008). Effects of pH buffering on horizontal and ganglion cell light responses in primate retina: evidence for the proton hypothesis of surround formation. J Neurosci 28, 456-464.
16. Deans MR & Paul DL (2001). Mouse horizontal cells do not express connexin26 or connexin36. Cell Commun Adhes 8, 361-366.
17. Dedek K, Pandarinath C, Alam NM, Wellershaus K, Schubert T, Willecke K, Prusky GT, Weiler R & Nirenberg S (2008). Ganglion cell adaptability: Does the coupling of horizontal cells play a role? PLoS ONE 3, e1714.
18. Delmar M, Coombs W, Sorgen P, Duffy HS & Taffet SM (2004). Structural bases for the chemical regulation of Connexin43 channels. Cardiovasc Res 62, 268-275.
19. DeVries SH & Schwartz EA (1989). Modulation of an electrical synapse between solitary pairs of catfish horizontal cells by dopamine and second messengers. J Physiol 414, 351-375.
20. DeVries SH & Schwartz EA (1992). Hemi-gap-junction channels in solitary horizontal cells of the catfish retina. J Physiol 445, 201-230.
21. Dixon DB, Takahashi K, Bieda M & Copenhagen DR (1996). Quinine, intracellular pH and modulation of hemi-gap junctions in catfish horizontal cells. Vision Res 36, 3925-3931.
22. Dobrowolski R, Sommershof A & Willecke K (2007). Some oculodentodigital dysplasia-associated Cx43 mutations cause increased hemichannel activity in addition to deficient gap junction channels. J Membr Biol 219, 9-17.
23. Ek-Vitorin JF & Burt JM (2005). Quantification of gap junction selectivity. Am J Physiol Cell Physiol 289, C1535-1546.
24. Gallemore RP, Li JD, Govardovskii VI & Steinberg RH (1994). Calcium gradients and light-evoked calcium changes outside rods in the intact cat retina. Vis Neurosci 11, 753-761.
25. Gu H, Ek-Vitorin JF, Taffet SM & Delmar M (2000). Coexpression of connexins 40 and 43 enhances the pH sensitivity of gap junctions: A model for synergistic interactions among connexins. Circ Res 86, E98-E103.
26. Hampson EC, Vaney DI & Weiler R (1992). Dopaminergic modulation of gap junction permeability between amacrine cells in mammalian retina. J Neurosci 12, 4911-4922.
27. Hampson EC, Weiler R & Vaney DI (1994). pH-gated dopaminergic modulation of horizontal cell gap junctions in mammalian retina. Proc Biol Sci 255, 67-72.
28. Harris AL (2001). Emerging issues of connexin channels: Biophysics fills the gap. Q Rev Biophys 34, 325-427.
29. Haugh-Scheidt L & Ripps H (1998). pH regulation in horizontal cells of the skate retina. Exp Eye Res 66, 449-463.
30. Hille B (2001). Ionic Channels of Excitable Membranes. Sinauer Associates, Sunderland, MA.
31. 2+ channels. J Gen Physiol 122, 657-671.
32. Hombach S, Janssen-Bienhold U, Söhl G, Schubert T, Büssow H, Ott T, Weiler R & Willecke K (2004). Functional expression of connexin57 in horizontal cells of the mouse retina. Eur J Neurosci 19, 2633-2640.
33. Janssen-Bienhold U, Schultz K, Gellhaus A, Schmidt P, Ammermuller J & Weiler R (2001). Identification and localization of connexin26 within the photoreceptor-horizontal cell synaptic complex. Vis Neurosci 18, 169-178.
34. Janssen-Bienhold U, Trümpler J, Hilgen G, Schultz K, De Sevilla Müller LP, Sonntag S, Dedek K, Dirks P, Willecke K & Weiler R (2009). Connexin57 is expressed in dendro- dendritic and axo-axonal gap junctions of mouse horizontal cells and its distribution is modulated by light. J Comp Neurol 513, 363-374.
35. Jouhou H, Yamamoto K, Homma A, Hara M, Kaneko A & Yamada M (2007a). Depolarization of isolated horizontal cells of fish acidifies their immediate surrounding by activating V-ATPase. J Physiol 585, 401-412.
36. Jouhou H, Yamamoto K, Iwasaki M & Yamada M (2007b). Acidification decouples gap junctions but enlarges the receptive field size of horizontal cells in carp retina. Neurosci Res 57, 203-209.
37. Kamermans M & Fahrenfort I (2004). Ephaptic interactions within a chemical synapse: Hemichannel-mediated ephaptic inhibition in the retina. Curr Opin Neurobiol 14, 531-541.
38. Kamermans M, Fahrenfort I, Schultz K, Janssen-Bienhold U, Sjoerdsma T & Weiler R (2001). Hemichannel-mediated inhibition in the outer retina. Science 292, 1178-1180.
39. Kamermans M & Spekreijse H (1999). The feedback pathway from horizontal cells to cones. A mini review with a look ahead. Vision Res 39, 2449-2468.
40. Kaneko A & Tachibana M (1986). Effects of gamma-aminobutyric acid on isolated cone photoreceptors of the turtle retina. J Physiol 373, 443-461.
41. Kreuzberg MM, Deuchars J, Weiss E, Schober A, Sonntag S, Wellershaus K, Draguhn A & Willecke K (2008). Expression of connexin30.2 in interneurons of the central nervous system in the mouse. Mol Cell Neurosci 37, 119-134.
42. Kreuzberg MM, Sohl G, Kim J, Verselis VK, Willecke K & Bukauskas FF (2005). Functional properties of mouse connexin30.2 expressed in the conduction system of the heart. Circ Res 96, 1169-1177.
43. Kuffler SW (1953). Discharge patterns and functional organization of mammalian retina. J Neurophysiol 16, 37-68.
44. Lal R, John SA, Laird DW & Arnsdorf MF (1995). Heart gap junction preparations reveal hemiplaques by atomic force microscopy. Am J Physiol Cell Physiol 268, C968-C977.
45. Lu C & McMahon DG (1996). Gap junction channel gating at bass retinal electrical synapses. Vis Neurosci 13, 1049-1057.
46. Malchow RP, Qian H & Ripps H (1993). Evidence for hemi-gap junctional channels in isolated horizontal cells of the skate retina. J Neurosci Res 35, 237-245.
47. Manthey D, Bukauskas F, Lee CG, Kozak CA & Willecke K (1999). Molecular cloning and functional expression of the mouse gap junction gene connexin-57 in human HeLa cells. J Biol Chem 274, 14716-14723.
48. Maxeiner S, Dedek K, Janssen-Bienhold U, Ammermuller J, Brune H, Kirsch T, Pieper M, Degen J, Kruger O, Willecke K & Weiler R (2005). Deletion of connexin45 in mouse retinal neurons disrupts the rod/cone signalling pathway between AII amacrine and ON cone bipolar cells and leads to impaired visual transmission. J Neurosci 25, 566-576.
49. McMahon DG (1994). Modulation of electrical synaptic transmission in zebrafish retinal horizontal cells. J Neurosci 14, 1722-1734.
50. McMahon DG, Knapp AG & Dowling JE (1989). Horizontal cell gap junctions: Single-channel conductance and modulation by dopamine. Proc Natl Acad Sci U S A 86, 7639-7643.
51. Mills SL & Massey SC (1995). Differential properties of two gap junctional pathways made by aII amacrine cells. Nature 377, 734-737.
52. i. J Cardiovasc Electrophysiol 8, 939-951.
53. Paulauskas N, Pranevicius M, Pranevicius H & Bukauskas FF (2009). A four-state model of contingent gating of gap junction channels containing two 'fast'gates sensitive to transjunctional voltage. Biophys J (in press).
54. Peracchia C (1977). Gap junctions. Structural changes after uncoupling procedures. J Cell Biol 72, 628-641.
55. Pottek M, Hoppenstedt W, Janssen-Bienhold U, Schultz K, Perlman I & Weiler R (2003). Contribution of connexin26 to electrical feedback inhibition in the turtle retina. J Comp Neurol 466, 468-477.
56. Qu Y & Dahl G (2002). Function of the voltage gate of gap junction channels: Selective exclusion of molecules. Proc Natl Acad Sci U S A 99, 697-702.
57. Rabl K & Thoreson WB (2002). Calcium-dependent inactivation and depletion of synaptic cleft calcium ions combine to regulate rod calcium currents under physiological conditions. Eur J Neurosci 16, 2070-2077.
58. Rackauskas M, Verselis VK & Bukauskas FF (2007). Permeability of homotypic and heterotypic gap junction channels formed of cardiac connexins mCx30.2, Cx40, Cx43, and Cx45. Am J Physiol Heart Circ Physiol 293, H1729-1736.
59. Saez JC, Berthoud VM, Branes MC, Martinez AD & Beyer EC (2003). Plasma membrane channels formed by connexins: Their regulation and functions. Physiol Rev 83, 1359-1400.
60. Shelley J, Dedek K, Schubert T, Feigenspan A, Schultz K, Hombach S, Willecke K & Weiler R (2006). Horizontal cell receptive fields are reduced in connexin57-deficient mice. Eur J Neurosci 23, 3176-3186.
61. Shields CR, Klooster J, Claassen Y, Ul-Hussain M, Zoidl G, Dermietzel R & Kamermans M (2007). Retinal horizontal cell-specific promoter activity and protein expression of zebrafish connexin 52.6 and connexin 55.5. J Comp Neurol 501, 765-779.
62. Sohl G, Maxeiner S & Willecke K (2005). Expression and functions of neuronal gap junctions. Nat Rev Neurosci 6, 191-200.
63. Stergiopoulos K, Alvarado JL, Mastroianni M, Ek-Vitorin JF, Taffet SM & Delmar M (1999). Hetero-domain interactions as a mechanism for the regulation of connexin channels. Circ Res 84, 1144-1155.
64. Swietach P & Vaughan-Jones RD (2005). Relationship between intracellular pH and proton mobility in rat and guinea-pig ventricular myocytes. J Physiol 566, 793-806.
65. Takahashi K, Dixon DB & Copenhagen DR (1993). Modulation of a sustained calcium current by intracellular pH in horizontal cells of fish retina. J Gen Physiol 101, 695-714.
66. Teranishi T, Negishi K & Kato S (1983). Dopamine modulates S-potential amplitude and dye-coupling between external horizontal cells in carp retina. Nature 301, 243-246.
67. Teranishi T, Negishi K & Kato S (1984). Dye coupling between amacrine cells in carp retina. Neurosci Lett 51, 73-78.
68. Trexler EB, Bukauskas FF, Bennett MVL, Bargiello TA & Verselis VK (1999). Rapid and direct effects of pH on connexins revealed by the connexin46 hemichannel preparation. J Gen Physiol 113, 721-742.
69. Valiunas V (2002). Biophysical properties of connexin-45 gap junction hemichannels studied in vertebrate cells. J Gen Physiol 119, 147-164.
70. Valiunas V, Beyer EC & Brink PR (2002). Cardiac gap junction channels show quantitative differences in selectivity. Circ Res 91, 104-111.
71. Vaney DI & Weiler R (2000). Gap junctions in the eye: Evidence for heteromeric, heterotypic and mixed-homotypic interactions. Brain Res Brain Res Rev 32, 115-120.
72. Verselis V, White RL, Spray DC & Bennett MV (1986). Gap junctional conductance and permeability are linearly related. Science 234, 461-464.
73. Verweij J, Hornstein EP & Schnapf JL (2003). Surround antagonism in macaque cone photoreceptors. J Neurosci 23, 10249-10257.
74. Vessey JP, Stratis AK, Daniels BA, Da Silva N, Jonz MG, Lalonde MR, Baldridge WH & Barnes S (2005). Proton-mediated feedback inhibition of presynaptic calcium channels at the cone photoreceptor synapse. J Neurosci 25, 4108-4117.
75. Weiler R, Pottek M, He S & Vaney DI (2000). Modulation of coupling between retinal horizontal cells by retinoic acid and endogenous dopamine. Brain Res Brain Res Rev 32, 121-129.
76. Wilders R & Jongsma HJ (1992). Limitations of the dual voltage clamp method in assaying conductance and kinetics of gap junction channels. Biophys J 63, 942-953.
77. Zoidl G, Bruzzone R, Weickert S, Kremer M, Zoidl C, Mitropoulou G, Srinivas M, Spray DC & Dermietzel R (2004). Molecular cloning and functional expression of zfCx52.6: A novel connexin with hemichannel-forming properties expressed in horizontal cells of the zebrafish retina. J Biol Chem 279, 2913-2921.