Distinct permeation profiles of the connexin 30 and 43 hemichannels

FEBS Letters

Volumn 588, Issue 8, 2014, Pages 1446-1457

  Hansen, Daniel Bloch ^a   Braunstein, Thomas Hartig ^a   Nielsen, Morten Schak ^a   Macaulay, Nanna ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

ATP; Current; Fluorescent dye; Glutamate; Water permeability

Indexed keywords

ATP; CURRENT; FLUORESCENT DYE; GLUTAMATE; WATER PERMEABILITY;

ACTION POTENTIALS; ADENOSINE TRIPHOSPHATE; ANIMALS; CELL MEMBRANE PERMEABILITY; CONNEXIN 43; CONNEXINS; GAP JUNCTIONS; GLUCOSE; GLUTAMIC ACID; LACTIC ACID; MEMBRANE POTENTIALS; MICE; RATS; WATER; XENOPUS;

EID: 84898880200     PISSN: 00145793     EISSN: 18733468     Source Type: Journal    
DOI: 10.1016/j.febslet.2014.01.036     Document Type: Conference Paper

References (88)

1. G. Sohl, and K. Willecke An update on connexin genes and their nomenclature in mouse and man Cell Commun. Adhes. 10 2003 173 180 (Pubitemid 38081368)
2. A.L. Harris Connexin channel permeability to cytoplasmic molecules Prog. Biophys. Mol. Biol. 94 2007 120 143 (Pubitemid 46782979)
3. R. Dermietzel, E.L. Hertberg, J.A. Kessler, and D.C. Spray Gap junctions between cultured astrocytes: immunocytochemical, molecular, and electrophysiological analysis J. Neurosci. 11 1991 1421 1432
4. D. Gosejacob, P. Dublin, P. Bedner, K. Huttmann, J. Zhang, O. Tress, K. Willecke, F. Pfrieger, C. Steinhauser, and M. Theis Role of astroglial connexin30 in hippocampal gap junction coupling Glia 59 2011 511 519
5. C. Giaume, J.A. Orellana, V. Abudara, and J.C. Saez Connexin-based channels in astrocytes: how to study their properties R. Milner, Astrocytes Methods in Molecular Biology 2012 Springer Protocols 283 303
6. A. Wallraff, R. Kohling, U. Heinemann, M. Theis, K. Willecke, and C. Steinhauser The impact of astrocytic gap junctional coupling on potassium buffering in the hippocampus J. Neurosci. 26 2006 5438 5447 (Pubitemid 44318396)
7. A. Hofer, and R. Dermietzel Visualization and functional blocking of gap junction hemichannels (connexons) with antibodies against external loop domains in astrocytes Glia 24 1998 141 154 (Pubitemid 28370219)
8. Z.C. Ye, M.S. Wyeth, S. Baltan-Tekkok, and B.R. Ransom Functional hemichannels in astrocytes: a novel mechanism of glutamate release J. Neurosci. 23 2003 3588 3596 (Pubitemid 36958466)
9. S. Ramachandran, L.H. Xie, S.A. John, S. Subramaniam, and R. Lal A novel role for connexin hemichannel in oxidative stress and smoking-induced cell injury PLoS ONE 2 2007 e712
10. H. Li, T.F. Liu, A. Lazrak, C. Peracchia, G.S. Goldberg, P.D. Lampe, and R.G. Johnson Properties and regulation of gap junctional hemichannels in the plasma membranes of cultured cells J. Cell Biol. 134 1996 1019 1030 (Pubitemid 26278225)
11. J.A. Orellana, E. Diaz, K.A. Schalper, A.A. Vargas, M.V. Bennett, and J.C. Saez Cation permeation through connexin 43 hemichannels is cooperative, competitive and saturable with parameters depending on the permeant species Biochem. Biophys. Res. Commun. 409 2011 603 609
12. C.E. Stout, J.L. Costantin, C.C. Naus, and A.C. Charles Intercellular calcium signaling in astrocytes via ATP release through connexin hemichannels J. Biol. Chem. 277 2002 10482 10488 (Pubitemid 34968170)
13. J.E. Contreras, H.A. Sanchez, E.A. Eugenin, D. Speidel, M. Theis, K. Willecke, F.F. Bukauskas, M.V. Bennett, and J.C. Saez 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 2002 495 500 (Pubitemid 34060389)
14. S.A. John, R. Kondo, S.Y. Wang, J.I. Goldhaber, and J.N. Weiss Connexin-43 hemichannels opened by metabolic inhibition J. Biol. Chem. 274 1999 236 240 (Pubitemid 29035054)
15. J.M. Garre, M.A. Retamal, P. Cassina, L. Barbeito, F.F. Bukauskas, J.C. Saez, M.V. Bennett, and V. Abudara FGF-1 induces ATP release from spinal astrocytes in culture and opens pannexin and connexin hemichannels Proc. Natl. Acad. Sci. USA 107 2010 22659 22664
16. N. Froger, J.A. Orellana, C.F. Calvo, E. Amigou, M.G. Kozoriz, C.C. Naus, J.C. Saez, and C. Giaume Inhibition of cytokine-induced connexin43 hemichannel activity in astrocytes is neuroprotective Mol. Cell. Neurosci. 45 2010 37 46
17. K.A. Schalper, H.A. Sanchez, S.C. Lee, G.A. Altenberg, M.H. Nathanson, and J.C. Saez Connexin 43 hemichannels mediate the Ca2+ influx induced by extracellular alkalinization Am. J. Physiol. Cell Physiol. 299 2010 C1504 C1515
18. X. Bao, G.A. Altenberg, and L. Reuss Mechanism of regulation of the gap junction protein connexin 43 by protein kinase C-mediated phosphorylation Am. J. Physiol. Cell Physiol. 286 2004 C647 C654
19. J.E. Contreras, J.C. Saez, F.F. Bukauskas, and M.V. Bennett Gating and regulation of connexin 43 (Cx43) hemichannels Proc. Natl. Acad. Sci. USA 100 2003 11388 11393 (Pubitemid 37205945)
20. J.C. Saez, K.A. Schalper, M.A. Retamal, J.A. Orellana, K.F. Shoji, and M.V. Bennett Cell membrane permeabilization via connexin hemichannels in living and dying cells Exp. Cell Res. 316 2010 2377 2389
21. O. Windmuller, U. Lindauer, M. Foddis, K.M. Einhaupl, U. Dirnagl, U. Heinemann, and J.P. Dreier Ion changes in spreading ischaemia induce rat middle cerebral artery constriction in the absence of NO Brain 128 2005 2042 2051 (Pubitemid 41253272)
22. J.P. Dreier The role of spreading depression, spreading depolarization and spreading ischemia in neurological disease Nat. Med. 17 2011 439 447
23. N. Wang, B.M. De, G. Antoons, A.K. Gadicherla, M. Bol, E. Decrock, W.H. Evans, K.R. Sipido, F.F. Bukauskas, and L. Leybaert Connexin mimetic peptides inhibit Cx43 hemichannel opening triggered by voltage and intracellular Ca2+ elevation Basic Res. Cardiol. 107 2012 304
24. J. Kang, N. Kang, D. Lovatt, A. Torres, Z. Zhao, J. Lin, and M. Nedergaard Connexin 43 hemichannels are permeable to ATP J. Neurosci. 28 2008 4702 4711
25. V. Valiunas Cyclic nucleotide permeability through unopposed connexin hemichannels Front Pharmacol. 4 2013 75
26. M. Abbaci, M. Barberi-Heyob, W. Blondel, F. Guillemin, and J. Didelon Advantages and limitations of commonly used methods to assay the molecular permeability of gap junctional intercellular communication Biotechniques 45 2008 33 62
27. I. Simpson, B. Rose, and W.R. Loewenstein Size limit of molecules permeating the junctional membrane channels Science 195 1977 294 296 (Pubitemid 8015334)
28. G. Schwarzmann, H. Wiegandt, B. Rose, A. Zimmerman, D. Ben-Haim, and W.R. Loewenstein Diameter of the cell-to-cell junctional membrane channels as probed with neutral molecules Science 213 1981 551 553 (Pubitemid 11045318)
29. W.R. Loewenstein Junctional intercellular communication: the cell-to-cell membrane channel Physiol. Rev. 61 1981 829 913
30. A.L. Harris, and D. Locke Permeability of connexin channels A.L. Harris, D. Locke, Connexins A Guide 2009 Humana Press 165 206
31. L. Bahima, J. Aleu, M. Elias, M. Martin-Satue, A. Muhaisen, J. Blasi, J. Marsal, and C. Solsona Endogenous hemichannels play a role in the release of ATP from Xenopus oocytes J. Cell. Physiol. 206 2006 95 102 (Pubitemid 41740721)
32. G.M. Essenfelder, R. Bruzzone, J. Lamartine, A. Charollais, C. Blanchet-Bardon, M.T. Barbe, P. Meda, and G. Waksman Connexin30 mutations responsible for hidrotic ectodermal dysplasia cause abnormal hemichannel activity Hum. Mol. Genet. 13 2004 1703 1714 (Pubitemid 39173440)
33. H.T. Liu, B.A. Tashmukhamedov, H. Inoue, Y. Okada, and R.Z. Sabirov Roles of two types of anion channels in glutamate release from mouse astrocytes under ischemic or osmotic stress Glia 54 2006 343 357 (Pubitemid 44422937)
34. D.C. Spray, Z.C. Ye, and B.R. Ransom Functional connexin "hemichannels": a critical appraisal Glia 54 2006 758 773 (Pubitemid 44629638)
35. Z.C. Ye, N. Oberheim, H. Kettenmann, and B.R. Ransom Pharmacological "cross-inhibition" of connexin hemichannels and swelling activated anion channels Glia 57 2009 258 269
36. A. Li, C.T. Leung, K. Peterson-Yantorno, C.H. Mitchell, and M.M. Civan Pathways for ATP release by bovine ciliary epithelial cells, the initial step in purinergic regulation of aqueous humor inflow Am. J. Physiol. Cell Physiol. 299 2010 C1308 C1317
37. E. Scemes, D.C. Spray, and P. Meda Connexins, pannexins, innexins: novel roles of "hemi-channels" Pflugers Arch. 457 2009 1207 1226
38. V. Valiunas, and R. Weingart Electrical properties of gap junction hemichannels identified in transfected HeLa cells Pflugers Arch. 440 2000 366 379 (Pubitemid 30445710)
39. Q.V. Hoang, H. Qian, and H. Ripps Functional analysis of hemichannels and gap-junctional channels formed by connexins 43 and 46 Mol. Vis. 16 2010 1343 1352
40. H.B. Moeller, R.A. Fenton, T. Zeuthen, and N. MacAulay Vasopressin-dependent short-term regulation of aquaporin 4 expressed in Xenopus oocytes Neuroscience 164 2009 1674 1684
41. T. Jespersen, M. Grunnet, K. Angelo, D.A. Klaerke, and S.P. Olesen Dual-function vector for protein expression in both mammalian cells and Xenopus laevis oocytes Biotechniques 32 536-8 2002 540
42. T.W. White, R. Bruzzone, D.A. Goodenough, and D.L. Paul Mouse Cx50, a functional member of the connexin family of gap junction proteins, is the lens fiber protein MP70 Mol. Biol. Cell 3 1992 711 720 (Pubitemid 23084555)
43. L. Ebihara Xenopus connexin38 forms hemi-gap-junctional channels in the nonjunctional plasma membrane of Xenopus oocytes Biophys. J. 71 1996 742 748 (Pubitemid 26289157)
44. T. Zeuthen, B. Belhage, and E. Zeuthen Water transport by Na+-coupled cotransporters of glucose (SGLT1) and of iodide (NIS). The dependence of substrate size studied at high resolution J. Physiol. 570 2006 485 499
45. G.A. Zampighi, M. Kreman, K.J. Boorer, D.D. Loo, F. Bezanilla, G. Chandy, J.E. Hall, and E.M. Wright A method for determining the unitary functional capacity of cloned channels and transporters expressed in Xenopus laevis oocytes J. Membr. Biol. 148 1995 65 78
46. H.B. Moeller, N. MacAulay, M.A. Knepper, and R.A. Fenton Role of multiple phosphorylation sites in the COOH-terminal tail of aquaporin-2 for water transport: evidence against channel gating Am. J. Physiol. Renal Physiol. 296 2009 F649 F657
47. F.F. Bukauskas, and V.K. Verselis Gap junction channel gating Biochim. Biophys. Acta 1662 2004 42 60 (Pubitemid 38366512)
48. J.A. Orellana, D.E. Hernandez, P. Ezan, V. Velarde, M.V. Bennett, C. Giaume, and J.C. Saez Hypoxia in high glucose followed by reoxygenation in normal glucose reduces the viability of cortical astrocytes through increased permeability of connexin 43 hemichannels Glia 58 2010 329 343
49. K.A. Schalper, N. Palacios-Prado, M.A. Retamal, K.F. Shoji, A.D. Martinez, and J.C. Saez Connexin hemichannel composition determines the FGF-1-induced membrane permeability and free [Ca2+]i responses Mol. Biol. Cell 19 2008 3501 3513
50. R. Werner, E. Levine, C. Rabadan-Diehl, and G. Dahl Formation of hybrid cell-cell channels Proc. Natl. Acad. Sci. USA 86 1989 5380 5384 (Pubitemid 19185553)
51. G.E. Morley, S.M. Taffet, and M. Delmar Intramolecular interactions mediate pH regulation of connexin43 channels Biophys. J. 70 1996 1294 1302 (Pubitemid 26073042)
52. P.A. Weber, H.C. Chang, K.E. Spaeth, J.M. Nitsche, and B.J. Nicholson The permeability of gap junction channels to probes of different size is dependent on connexin composition and permeant-pore affinities Biophys. J. 87 2004 958 973 (Pubitemid 39095076)
53. L. Ebihara, E.C. Beyer, K.I. Swenson, D.L. Paul, and D.A. Goodenough Cloning and expression of a Xenopus embryonic gap junction protein Science 243 1989 1194 1195 (Pubitemid 19081147)
54. B. Hille Ion Channels of Excitable Membranes 2001 Sinauer Associates Inc. third ed.
55. A.K. Meinild, D.A. Klaerke, and T. Zeuthen Bidirectional water fluxes and specificity for small hydrophilic molecules in aquaporins 0-5 J. Biol. Chem. 273 1998 32446 32451 (Pubitemid 28557617)
56. T. Zeuthen, and N. MacAulay Passive water transport in biological pores Int. Rev. Cytol. 215 2002 203 230 (Pubitemid 34280296)
57. H. Viadiu, T. Gonen, and T. Walz Projection map of aquaporin-9 at 7 A resolution J. Mol. Biol. 367 2007 80 88
58. H. Tsukaguchi, C. Shayakul, U.V. Berger, B. Mackenzie, S. Devidas, W.B. Guggino, A.N. van Hoek, and M.A. Hediger Molecular characterization of a broad selectivity neutral solute channel J. Biol. Chem. 273 1998 24737 24743 (Pubitemid 28454975)
59. R.M. Stroud, D. Savage, L.J. Miercke, J.K. Lee, S. Khademi, and W. Harries Selectivity and conductance among the glycerol and water conducting aquaporin family of channels FEBS Lett. 555 2003 79 84 (Pubitemid 37431101)
60. J. Gao, X. Sun, L.C. Moore, T.W. White, P.R. Brink, and R.T. Mathias Lens intracellular hydrostatic pressure is generated by the circulation of sodium and modulated by gap junction coupling J. Gen. Physiol. 137 2011 507 520
61. A.P. Quist, S.K. Rhee, H. Lin, and R. Lal Physiological role of gap-junctional hemichannels. Extracellular calcium-dependent isosmotic volume regulation J. Cell Biol. 148 2000 1063 1074
62. D.L. Paul, L. Ebihara, L.J. Takemoto, K.I. Swenson, and D.A. Goodenough Connexin46, a novel lens gap junction protein, induces voltage-gated currents in nonjunctional plasma membrane of Xenopus oocytes J. Cell Biol. 115 1991 1077 1089 (Pubitemid 21909955)
63. S. Eskandari, G.A. Zampighi, D.W. Leung, E.M. Wright, and D.D. Loo Inhibition of gap junction hemichannels by chloride channel blockers J. Membr. Biol. 185 2002 93 102 (Pubitemid 34095240)
64. F. Anselmi, V.H. Hernandez, G. Crispino, A. Seydel, S. Ortolano, S.D. Roper, N. Kessaris, W. Richardson, G. Rickheit, M.A. Filippov, H. Monyer, and F. Mammano ATP release through connexin hemichannels and gap junction transfer of second messengers propagate Ca2+ signals across the inner ear Proc. Natl. Acad. Sci. USA 105 2008 18770 18775
65. C. Stout, and A. Charles Modulation of intercellular calcium signaling in astrocytes by extracellular calcium and magnesium Glia 43 2003 265 273 (Pubitemid 37047682)
66. E. De Vuyst, E. Decrock, B.M. De, H. Yamasaki, C.C. Naus, W.H. Evans, and L. Leybaert Connexin hemichannels and gap junction channels are differentially influenced by lipopolysaccharide and basic fibroblast growth factor Mol. Biol. Cell 18 2007 34 46 (Pubitemid 46066708)
67. M.L. Cotrina, J.H. Lin, A. Alves-Rodrigues, S. Liu, J. Li, H. Azmi-Ghadimi, J. Kang, C.C. Naus, and M. Nedergaard Connexins regulate calcium signaling by controlling ATP release Proc. Natl. Acad. Sci. USA 95 1998 15735 15740 (Pubitemid 29018769)
68. R.A. Pearson, N. Dale, E. Llaudet, and P. Mobbs ATP released via gap junction hemichannels from the pigment epithelium regulates neural retinal progenitor proliferation Neuron 46 2005 731 744 (Pubitemid 40733129)
69. H. Takeuchi, S. Jin, J. Wang, G. Zhang, J. Kawanokuchi, R. Kuno, Y. Sonobe, T. Mizuno, and A. Suzumura Tumor necrosis factor-alpha induces neurotoxicity via glutamate release from hemichannels of activated microglia in an autocrine manner J. Biol. Chem. 281 2006 21362 21368 (Pubitemid 44115475)
70. T. Fellin, T. Pozzan, and G. Carmignoto Purinergic receptors mediate two distinct glutamate release pathways in hippocampal astrocytes J. Biol. Chem. 281 2006 4274 4284 (Pubitemid 43847857)
71. D. Manthey, K. Banach, T. Desplantez, C.G. Lee, C.A. Kozak, O. Traub, R. Weingart, and K. Willecke Intracellular domains of mouse connexin26 and -30 affect diffusional and electrical properties of gap junction channels J. Membr. Biol. 181 2001 137 148 (Pubitemid 32466639)
72. M. Beltramello, M. Bicego, V. Piazza, C.D. Ciubotaru, F. Mammano, and P. D'Andrea Permeability and gating properties of human connexins 26 and 30 expressed in HeLa cells Biochem. Biophys. Res. Commun. 305 2003 1024 1033 (Pubitemid 36597866)
73. J. Sun, S. Ahmad, S. Chen, W. Tang, Y. Zhang, P. Chen, and X. Lin Cochlear gap junctions coassembled from Cx26 and 30 show faster intercellular Ca2+ signaling than homomeric counterparts Am. J. Physiol. Cell Physiol. 288 2005 C613 C623
74. S.W. Yum, J. Zhang, V. Valiunas, G. Kanaporis, P.R. Brink, T.W. White, and S.S. Scherer Human connexin26 and connexin30 form functional heteromeric and heterotypic channels Am. J. Physiol. Cell Physiol. 293 2007 C1032 C1048
75. N.S. Heyman, and J.M. Burt Hindered diffusion through an aqueous pore describes invariant dye selectivity of Cx43 junctions Biophys. J. 94 2008 840 854 (Pubitemid 351162451)
76. H. Ripps, H. Qian, and J. Zakevicius Properties of connexin26 hemichannels expressed in Xenopus oocytes Cell. Mol. Neurobiol. 24 2004 647 665 (Pubitemid 39062428)
77. M. Srinivas, J. Kronengold, F.F. Bukauskas, T.A. Bargiello, and V.K. Verselis Correlative studies of gating in Cx46 and Cx50 hemichannels and gap junction channels Biophys. J. 88 2005 1725 1739 (Pubitemid 40976189)
78. T.W. White, M.R. Deans, J. O'Brien, M.R. Al-Ubaidi, D.A. Goodenough, H. Ripps, and R. Bruzzone Functional characteristics of skate connexin35, a member of the gamma subfamily of connexins expressed in the vertebrate retina Eur. J. Neurosci. 11 1999 1883 1890 (Pubitemid 29240552)
79. G. Hawat, and G. Baroudi Differential modulation of unapposed connexin 43 hemichannel electrical conductance by protein kinase C isoforms Pflugers Arch. 456 2008 519 527
80. M.A. Retamal, N. Froger, N. Palacios-Prado, P. Ezan, P.J. Saez, J.C. Saez, and C. Giaume Cx43 hemichannels and gap junction channels in astrocytes are regulated oppositely by proinflammatory cytokines released from activated microglia J. Neurosci. 27 2007 13781 13792 (Pubitemid 350278255)
81. T.A. Bargiello, Q. Tang, S. Oh, and T. Kwon Voltage-dependent conformational changes in connexin channels Biochim. Biophys. Acta 1818 2012 1807 1822
82. A. Revilla, C. Castro, and L.C. Barrio Molecular dissection of transjunctional voltage dependence in the connexin-32 and connexin-43 junctions Biophys. J. 77 1999 1374 1383 (Pubitemid 29407311)
83. A.P. Moreno, M. Chanson, S. Elenes, J. Anumonwo, I. Scerri, H. Gu, S.M. Taffet, and M. Delmar Role of the carboxyl terminal of connexin43 in transjunctional fast voltage gating Circ. Res. 90 2002 450 457 (Pubitemid 34633915)
84. J.M. Gomez-Hernandez, M.M. de, B. Larrosa, D. Gonzalez, and L.C. Barrio Molecular basis of calcium regulation in connexin-32 hemichannels Proc. Natl. Acad. Sci. USA 100 2003 16030 16035 (Pubitemid 38021109)
85. V.K. Verselis, and M. Srinivas Divalent cations regulate connexin hemichannels by modulating intrinsic voltage-dependent gating J. Gen. Physiol. 132 2008 315 327
86. D.J. Muller, G.M. Hand, A. Engel, and G.E. Sosinsky Conformational changes in surface structures of isolated connexin 26 gap junctions EMBO J. 21 2002 3598 3607 (Pubitemid 34787034)
87. M.J. Allen, J. Gemel, E.C. Beyer, and R. Lal Atomic force microscopy of Connexin40 gap junction hemichannels reveals calcium-dependent three-dimensional molecular topography and open-closed conformations of both the extracellular and cytoplasmic faces J. Biol. Chem. 286 2011 22139 22146
88. X. Liu, L. Sun, M. Torii, and P. Rakic Connexin 43 controls the multipolar phase of neuronal migration to the cerebral cortex Proc. Natl. Acad. Sci. USA 109 2012 8280 8285