Heterotypic connexin50/connexin50 mutant gap junction channels reveal interactions between two hemichannels during transjunctional voltage-dependent gating

Journal of Physiology

Volumn 590, Issue 20, 2012, Pages 5037-5052

  Xin, Li ^a   Sun, Yiguo ^a   Bai, Donglin ^a  

^a UNIVERSITY OF WESTERN ONTARIO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CONNEXIN 50; GAP JUNCTION PROTEIN; MUTANT PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CHANNEL GATING; CHIMERA; CONTROLLED STUDY; INTRACELLULAR RECORDING; MEMBRANE CONDUCTANCE; MOLECULAR INTERACTION; MOUSE; NEUROBLASTOMA CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; STEADY STATE; TRANSJUNCTIONAL VOLTAGE DEPENDENT GATING; VOLTAGE CLAMP;

EID: 84867452381     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2012.235507     Document Type: Article

References (43)

1. Anumonwo JM, Taffet SM, Gu H, Chanson M, Moreno AP & Delmar M (2001). The carboxyl terminal domain regulates the unitary conductance and voltage dependence of connexin40 gap junction channels. Circ Res 88, 666-673.
2. Bai D, del Corsso C, Srinivas M & Spray DC (2006). Block of specific gap junction channel subtypes by 2-aminoethoxydiphenyl borate (2-APB). J Pharmacol Exp Ther 319, 1452-1458.
3. Barrio LC, Suchyna T, Bargiello T, Xu LX, Roginski RS, Bennett MV & Nicholson BJ (1991). Gap junctions formed by connexins 26 and 32 alone and in combination are differently affected by applied voltage. Proc Natl Acad Sci U S A 88, 8410-8414.
4. Bukauskas FF, Angele AB, Verselis VK & Bennett MV (2002). 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.
5. Bukauskas FF, Elfgang C, Willecke K & Weingart R (1995). Biophysical properties of gap junction channels formed by mouse connexin40 in induced pairs of transfected human HeLa cells. Biophys J 68, 2289-2298.
6. 2-sensitive and voltage-sensitive. Biophys J 72, 2137-2142.
7. Bukauskas FF & Verselis VK (2004). Gap junction channel gating. Biochim Biophys Acta 1662, 42-60.
8. Chen-Izu Y, Moreno AP & Spangler RA (2001). Opposing gates model for voltage gating of gap junction channels. Am J Physiol Cell Physiol 281, C1604-C1613.
9. del Corsso C, Srinivas M, Urban-Maldonado M, Moreno AP, Fort AG, Fishman GI & Spray DC (2006). Transfection of mammalian cells with connexins and measurement of voltage sensitivity of their gap junctions. Nat Protoc 1, 1799-1809.
10. Dong L, Liu X, Li H, Vertel BM & Ebihara L (2006). Role of the N-terminus in permeability of chicken connexin45.6 gap junctional channels. J Physiol 576, 787-799.
11. Elenes S, Martinez AD, Delmar M, Beyer EC & Moreno AP (2001). Heterotypic docking of Cx43 and Cx45 connexons blocks fast voltage gating of Cx43. Biophys J 81, 1406-1418.
12. Goldberg GS, Lampe PD & Nicholson BJ (1999). Selective transfer of endogenous metabolites through gap junctions composed of different connexins. Nat Cell Biol 1, 457-459.
13. Gonzalez D, Gomez-Hernandez JM & Barrio LC (2007). Molecular basis of voltage dependence of connexin channels: an integrative appraisal. Prog Biophys Mol Biol 94, 66-106.
14. Goodenough DA, Goliger JA & Paul DL (1996). Connexins, connexons, and intercellular communication. Annu Rev Biochem 65, 475-502.
15. Harris AL (2001). Emerging issues of connexin channels: biophysics fills the gap. Q Rev Biophys 34, 325-472.
16. Harris AL, Spray DC & Bennett MV (1981). Kinetic properties of a voltage-dependent junctional conductance. J Gen Physiol 77, 95-117.
17. r 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.
18. Kreuzberg MM, Sohl G, Kim JS, 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.
19. Maeda S, Nakagawa S, Suga M, Yamashita E, Oshima A, Fujiyoshi Y & Tsukihara T (2009). Structure of the connexin 26 gap junction channel at 3.5 Å resolution. Nature 458, 597-602.
20. Moreno AP, Chanson M, Elenes S, Anumonwo J, Scerri I, Gu H, Taffet SM & Delmar M (2002). Role of the carboxyl terminal of connexin43 in transjunctional fast voltage gating. Circ Res 90, 450-457.
21. Moreno AP, Eghbali B & Spray DC (1991). Connexin32 gap junction channels in stably transfected cells. Equilibrium and kinetic properties. Biophys J 60, 1267-1277.
22. Moreno AP, Rook MB, Fishman GI & Spray DC (1994). Gap junction channels: distinct voltage-sensitive and -insensitive conductance states. Biophys J 67, 113-119.
23. Palacios-Prado N & Bukauskas FF (2009). Heterotypic gap junction channels as voltage-sensitive valves for intercellular signaling. Proc Natl Acad Sci U S A 106, 14855-14860.
24. Palacios-Prado N & Bukauskas FF (2012). Modulation of metabolic communication through gap junction channels by transjunctional voltage; synergistic and antagonistic effects of gating and ionophoresis. Biochim Biophys Acta 1818, 1884-1894.
25. Paul DL (1986). Molecular cloning of cDNA for rat liver gap junction protein. J Cell Biol 103, 123-134.
26. Paulauskas N, Pranevicius M, Pranevicius H & Bukauskas FF (2009). A stochastic four-state model of contingent gating of gap junction channels containing two "fast" gates sensitive to transjunctional voltage. Biophys J 96, 3936-3948.
27. 2 sensitivity of voltage gating with D3N mutation of Cx50. Am J Physiol Cell Physiol 288, C1381-C1389.
28. Rackauskas M, Kreuzberg MM, Pranevicius M, Willecke K, Verselis VK & Bukauskas FF (2007). Gating properties of heterotypic gap junction channels formed of connexins 40, 43, and 45. Biophys J 92, 1952-1965.
29. Revilla A, Castro C & Barrio LC (1999). Molecular dissection of transjunctional voltage dependence in the connexin-32 and connexin-43 junctions. Biophys J 77, 1374-1383.
30. Rubin JB, Verselis VK, Bennett MV & Bargiello TA (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 U S A 89, 3820-3824.
31. Rubin JB, Verselis VK, Bennett MV & Bargiello TA (1992b). Molecular analysis of voltage dependence of heterotypic gap junctions formed by connexins 26 and 32. Biophys J 62, 183-193; discussion 193-185.
32. Sigworth FJ & Sine SM (1987). Data transformations for improved display and fitting of single-channel dwell time histograms. Biophys J 52, 1047-1054.
33. Spray DC, Harris AL & Bennett MV (1981). Equilibrium properties of a voltage-dependent junctional conductance. J Gen Physiol 77, 77-93.
34. Srinivas M, Costa M, Gao Y, Fort A, Fishman GI & Spray DC (1999a). Voltage dependence of macroscopic and unitary currents of gap junction channels formed by mouse connexin50 expressed in rat neuroblastoma cells. J Physiol 517, 673-689.
35. Srinivas M, Kronengold J, Bukauskas FF, Bargiello TA & Verselis VK (2005). Correlative studies of gating in Cx46 and Cx50 hemichannels and gap junction channels. Biophys J 88, 1725-1739.
36. Srinivas M, Rozental R, Kojima T, Dermietzel R, Mehler M, Condorelli DF, Kessler JA & Spray DC (1999b). Functional properties of channels formed by the neuronal gap junction protein connexin36. J Neurosci 19, 9848-9855.
37. Vogel R & Weingart R (1998). Mathematical model of vertebrate gap junctions derived from electrical measurements on homotypic and heterotypic channels. J Physiol 510, 177-189.
38. White TW, Bruzzone R, Wolfram S, Paul DL & Goodenough DA (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.
39. 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.
40. Xin L, Gong XQ & Bai D (2010). The role of amino terminus of mouse Cx50 in determining transjunctional voltage- dependent gating and unitary conductance. Biophys J 99, 2077-2086.
41. Xin L, Nakagawa S, Tsukihara T & Bai D (2012). Aspartic acid residue D3 critically determines Cx50 gap junction channel transjunctional voltage-dependent gating and unitary conductance. Biophys J 102, 1022-1031.
42. Xu X, Berthoud VM, Beyer EC & Ebihara L (2002). Functional role of the carboxyl terminal domain of human connexin 50 in gap junctional channels. J Membr Biol 186, 101-112.
43. Yeager M, Unger VM & Falk MM (1998). Synthesis, assembly and structure of gap junction intercellular channels. Curr Opin Struct Biol 8, 517-524.