Connexin 43 hemichannels mediate the Ca2+ influx induced by extracellular alkalinization

American Journal of Physiology - Cell Physiology

Volumn 299, Issue 6, 2010, Pages

  Schalper, Kurt A ^a   Sánchez, Helmuth A ^a   Lee, Sung C ^b   Altenberg, Guillermo A ^b   Nathanson, Michael H ^c   Sáez, Juan C ^a,d  

^a PONTIFICIA UNIVERSIDAD CATÓLICA DE CHILE   (Chile)

^b TEXAS TECH UNIVERSITY HEALTH SCIENCES CENTER SCHOOL OF MEDICINE   (United States)

^c YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d Núcleo Milenio de Inmunología e Inmunoterapia ^*  (Chile)

Author keywords

Alkaline pH; Calcium permeability; Connexons; Liposomes

Indexed keywords

CONNEXIN 43; ETHIDIUM; LIPOSOME; PROBENECID;

ALKALINIZATION; ARTICLE; CALCIUM CELL LEVEL; CALCIUM TRANSPORT; CELL PH; CELLULAR DISTRIBUTION; HELA CELL; MEMBRANE PERMEABILITY; PRIORITY JOURNAL; PROTEIN EXPRESSION;

CALCIUM; CALCIUM CHANNELS; CONNEXIN 43; HELA CELLS; HUMANS; HYDROGEN-ION CONCENTRATION; LANTHANUM; PROBENECID; URICOSURIC AGENTS;

EID: 78649653091     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00015.2010     Document Type: Article

References (76)

1. Austin C, Wray S. A quantitative study of the relation between intracellular pH and force in rat mesenteric vascular smooth muscle. Pflügers Arch 427: 270-276, 1994.
2. Bao L, Locovei S, Dahl G. Pannexin membrane channels are mechanosensitive conduits for ATP. FEBS Lett 572: 65-68, 2004.
3. Bao X, Lee SC, Reuss L, Altenberg GA. Change in permeant size selectivity by phosphorylation of connexin 43 gap-junctional hemichannels by PKC. Proc Natl Acad Sci USA 104: 4919-4924, 2007.
4. Bennett MV, Contreras JE, Bukauskas FF, Sáez JC. New roles for astrocytes: gap junction hemichannels have something to communicate. Trends Neurosci 26: 610-617, 2003.
5. Bode HP, Wang L, Cassio D, Leite MF, St-Pierre MV, Hirata K, Okazaki K, Sears ML, Meda P, Nathanson MH, Dufour JF. Expression and regulation of gap junctions in rat cholangiocytes. Hepatology 36: 631-40, 2002.
6. Brañes MC, Contreras JE, Sáez JC. Activation of human polymorphonuclear cells induces formation of functional gap junctions and expression of connexins. Med Sci Monit 8: 313-323, 2002.
7. + fluxes in intact cells. FASEB J 15: 10-12, 2001.
8. Bukauskas FF, Jordan K, Bukauskiene A, Bennett MV, Lampe PD, Laird DW, Verselis VK. Clustering of connexin 43-enhanced green fluorescent protein gap junction channels and functional coupling in living cells. Proc Natl Acad Sci USA 97: 2556-2561, 2000.
9. 2+ overload. Cell Death Differ 13: 1675-1685, 2006.
10. Cherian PP, Siller-Jackson AJ, Gu S, Wang X, Bonewald LF, Sprague E, Jiang JX. Mechanical strain opens connexin 43 hemichannels in osteocytes: a novel mechanism for the release of prostaglandin. Mol Biol Cell 16: 3100-3106, 2005.
11. Contreras JE, Sánchez HA, Eugenín EA, Speidel D, Theis M, Willecke K, Bukauskas FF, Bennett MV, Sáez JC. 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, 2002.
12. Contreras JE, Sáez JC, Bukauskas FF, Bennett MV. Gating and regulation of connexin 43 (Cx43) hemichannels. Proc Natl Acad Sci USA 100: 11388-11393, 2003.
13. 2+-sensing receptor. J Cell Sci 116: 1527-1538, 2003.
14. De Vuyst E, Decrock E, De Bock M, Yamasaki H, Naus CC, Evans WH, Leybaert L. Connexin hemichannels and gap junction channels are differentially influenced by lipopolysaccharide and basic fibroblast growth factor. Mol Biol Cell 18: 34-46, 2007.
15. 2+ regulation of connexin 43 hemichannels in C6 glioma and glial cells. Cell Calcium 46: 176-187, 2009.
16. Delmar M, Coombs W, Sorgen P, Duffy HS, Taffet SM. Structural bases for the chemical regulation of connexin43 channels. Cardiovasc Res 62: 268-275, 2004.
17. Eberhard M, Erne P. Calcium binding to fluorescent calcium indicators: calcium green, calcium orange and calcium crimson. Biochem Biophys Res Commun 180: 09-215, 1991.
18. Ebihara L. New roles for connexons. News Physiol Sci 18: 100-103, 2003.
19. Eisner DA, Kashimura T, Venetucci LA, Trafford AW. From the ryanodine receptor to cardiac arrhythmias. Circ J 73: 1561-1567, 2009.
20. Elfgang C, Eckert R, Lichtenberg-Frate H, Butterweck A, Traub O, Klein RA, Hulser DF, Willecke K. Specific permeability and selective formation of gap junction channels in connexin-transfected HeLa cells. J Cell Biol 129: 805-817, 1995.
21. Evans DF, Pye G, Bramley R, Clark AG, Dyson TJ, Hardcastle JD. Measurement of gastrointestinal pH profiles in normal ambulant human subjects. Gut 29: 1035-1041, 1988.
22. Evans WH, De Vuyst E, Leybaert L. The gap junction cellular internet: connexin hemichannels enter the signalling limelight. Biochem J 397: 1-14, 2006. (Pubitemid 44032830)
23. Faigle M, Seessle J, Zug S, El Kasmi KC, Eltzschig HK. ATP release from vascular endothelia occurs across Cx43 hemichannels and is attenuated during hypoxia. PLoS One 3: 2801, 2008.
24. + and cyclic ADP-ribose in increasing intra-cellular calcium and enhancing cell proliferation of 3T3 fibroblasts. J Biol Chem 276: 21642-21648, 2001.
25. Guttman JA, Lin AE, Li Y, Bechberger J, Naus CC, Vogl AW, Finlay BB. Gap junction hemichannels contribute to the generation of diarrhea during infectious enteric disease. Gut 59: 218-226, 2009.
26. Hawat G, Benderdour M, Rousseau G, Baroudi G. Connexin 43 mimetic peptide Gap26 confers protection to intac heart against myocardial ischemia injury. Pflügers Arch 460: 583-592, 2010.
27. Harris AL. Emerging issues of connexin channels: biophysics fills the gap. Q Rev Biophys 34: 325-472, 2001.
28. Huang Y, Grinspan JB, Abrams CK, Scherer SS. Pannexin1 is expressed by neurons and glia but does not form functional gap junctions. Glia 55: 46-56, 2007.
29. Iacobas DA, Iacobas S, Spray DC. Connexin-dependent transcellular transcriptomic networks in mouse brain. Prog Biophys Mol Biol 94: 169-185, 2007.
30. John SA, Kondo R, Wang SY, Goldhaber JI, Weiss JN. Connexin-43 hemichannels opened by metabolic inhibition. J Biol Chem 274: 236-240, 1999.
31. John S, Cesario D, Weiss JN. Gap junctional hemichannels in the heart. Acta Physiol Scand 179: 23-31, 2003.
32. Kang J, Kang N, Lovatt D, Torres A, Zhao Z, Lin J, Nedergaard M. Connexin 43 hemichannels are permeable to ATP. J Neurosci 28: 4702-4711, 2008.
33. Kanno S, Saffitz JE. The role of myocardial gap junctions in electrical conduction and arrhythmogenesis. Cardiovasc Pathol 10: 169-177, 2001.
34. Kondo RP, Wang SY, John SA, Weiss JN, Goldhaber JI. Metabolic inhibition activates a non-selective current through connexin hemichannels in isolated ventricular myocytes. J Mol Cell Cardiol 32: 1859-1872, 2000.
35. Leaphart CL, Dai S, Gribar SC, Richardson W, Ozolek J, Shi XH, Bruns JR, Branca M, Li J, Weisz OA, Sodhi C, Hackam DJ. Interferon-gamma inhibits enterocyte migration by reversibly displacing connexin43 from lipid rafts. Am J Physiol Gastrointest Liver Physiol 295: G559-G569, 2008.
36. 2+ channels, connecting calcium homeostasis, ageing and uraemia. Nephrol Dial Transplant 7: 1770-1772, 2006.
37. Li H, Liu TF, Lazrak A, Peracchia C, Goldberg GS, Lampe PD, Johnson RG. Properties and regulation of gap junctional hemichannels in the plasma membranes of cultured cells. J Cell Biol 134: 1019-1030, 1996.
38. i in rabbit ventricular myocytes during metabolic inhibition. J Mol Cell Cardiol 33: 2145-2155, 2001.
39. Majima HJ, Oberley TD, Furukawa K, Mattson MP, Yen HC, Szweda LI, St Clair DK. Prevention of mitochondrial injury by manganese superoxide dismutase reveals a primary mechanism for alkaline-induced cell death. J Biol Chem 273: 8217-8224, 1998.
40. Moore EW. Ionized calcium in normal serum, ultrafiltrates, and whole blood determined by ion-exchange electrodes. J Clin Invest 49: 318-334, 1970.
41. Morita M, Saruta C, Kozuka N, Okubo Y, Itakura M, Takahashi M, Kudo Y. Dual regulation of astrocyte gap junction hemichannels by growth factors and a pro-inflammatory cytokine via the mitogen-activated protein kinase cascade. Glia 55: 508-515, 2007.
42. 2+ influx, and response of vascular smooth muscle cells to 5-hydroxytryptamine. Stroke 31: 2500-2507, 2000.
43. Neher E, Sakaba T. Multiple roles of calcium ions in the regulation of neurotransmitter release. Neuron 59: 861-872, 2008.
44. Orellana JA, Hernández DE, Ezan P, Velarde V, Bennett MV, Giaume C, Sáez JC. 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: 329-343, 2010.
45. Palacios-Prado N, Sonntag S, Skeberdis VA, Willecke K, Bukauskas FF. Gating, permselectivity and pH-dependent modulation of channels formed by connexin57, a major connexin of horizontal cells in the mouse retina. J Physiol 587: 3251-3269, 2009.
46. Palacios-Prado N, Briggs SW, Skeberdis VA, Pranevicius M, Bennett MV, Bukauskas FF. pH-dependent modulation of voltage gating in connexin45 homotypic and connexin45/connexin43 heterotypic gap junctions. Proc Natl Acad Sci USA 107: 9897-9902, 2010.
47. Pearson RA, Dale N, Llaudet E, Mobbs P. ATP released via gap junction hemichannels from the pigment epithelium regulates neural retinal progenitor proliferation. Neuron 46: 731-744, 2005.
48. Pelegrin P, Surprenant A. Pannexin-1 mediates large pore formation and interleukin-1β release by the ATP-gated P2X7 receptor. EMBO J 25: 5071-5082, 2006.
49. Peracchia C. Chemical gating of gap junction channels; roles of calcium, pH and calmodulin. Biochim Biophys Acta 1662: 61-80, 2004.
50. Plotkin LI, Manolagas SC, Bellido T. Transduction of cell survival signals by connexin-43 hemichannels. J Biol Chem 277: 8648-8657, 2002.
51. Rana S, Dringen R. Gap junction hemichannel-mediated release of glutathione from cultured rat astrocytes. Neurosci Lett 415: 45-48, 2007.
52. Retamal MA, Cortés CJ, Reuss L, Bennett MV, Sáez JC. S-nitrosylation and permeation through connexin 43 hemichannels in astrocytes: induction by oxidant stress and reversal by reducing agents. Proc Natl Acad Sci USA 103: 4475-4480, 2006.
53. Retamal MA, Schalper KA, Shoji KF, Bennett MV, Sáez JC. Opening of connexin 43 hemichannels is increased by lowering intracellular redox potential. Proc Natl Acad Sci USA 104: 8322-8327, 2007.
54. Retamal MA, Froger N, Palacios-Prado N, Ezan P, Sáez PJ, Sáez JC, Giaume C. Cx43 hemichannels and gap junction channels in astrocytes are regulated oppositely by proinflammatory cytokines released from activated microglia. J Neurosci 27: 13781-13792, 2007.
55. Ripps H, Qian H, Zakevicius J. Properties of connexin26 hemichannels expressed in Xenopus oocytes. Cell Mol Neurobiol 24: 647-665, 2004.
56. Rodrigues MA, Gomes DA, Andrade VA, Leite MF, Nathanson MH. Insulin induces calcium signals in the nucleus of rat hepatocytes. Hepatology 48: 1621-1631, 2008.
57. Romanello M, Pani B, Bicego M, D'Andrea P. Mechanically induced ATP release from human osteoblastic cells. Biochem Biophys Res Commun 289: 1275-1281, 2001.
58. 2+ in transfected HeLa cells. Am J Physiol Cell Physiol 297: C665-C678, 2009.
59. Silverman W, Locovei S, Dahl G. Probenecid, a gout remedy, inhibits pannexin 1 channels. Am J Physiol Cell Physiol 295: C761-C767, 2008.
60. i responses. Mol Biol Cell 19: 3501-3513, 2008.
61. Schalper KA, Palacios-Prado N, Orellana JA, Sáez JC. Currently used methods for identification and characterization of hemichannels. Cell Commun Adhes 15: 207-218, 2008.
62. Schalper KA, Orellana JA, Berthoud VM, Sáez JC. Dysfunctions of the diffusional membrane pathways mediated by hemichannels in inherited and acquired human diseases. Curr Vasc Pharmacol 7: 486-505, 2009.
63. Schock SC, Leblanc D, Hakim AM, Thompson CS. ATP release by way of connexin 36 hemichannels mediates ischemic tolerance in vitro. Biochem Biophys Res Commun 368: 138-144, 2008.
64. Shestopalov VI, Panchin Y. Pannexins and gap junction protein diversity. Cell Mol Life Sci 65: 376-394, 2008.
65. Shintani-Ishida K, Uemura K, Yoshida K. Hemichannels in cardiomyocytes open transiently during ischemia and contribute to reperfusion injury following brief ischemia. Am J Physiol Heart Circ Physiol 293: H1714-H1720, 2007.
66. Sosinsky GE, Solan JL, Gaietta GM, Ngan L, Lee GJ, Mackey MR, Lampe PD. The C-terminus of connexin43 adopts different conformations in the Golgi and gap junction as detected with structure-specific antibodies. Biochem J 408: 375-385, 2007.
67. Stout C, Charles A. Modulation of intercellular calcium signaling in astrocytes by extracellular calcium and magnesium. Glia 43: 265-273, 2003.
68. Thimm J, Mechler A, Lin H, Rhee S, Lal R. Calcium-dependent open/closed conformations and interfacial energy maps of reconstituted hemichannels. J Biol Chem 280: 10646-10654, 2005.
69. Trexler EB, Bukauskas FF, Bennett MV, Bargiello TA, Verselis VK. Rapid and direct effects of pH on connexins revealed by the connexin46 hemichannel preparation. J Gen Physiol 113: 721-742, 1999.
70. Vergara L, Bao X, Cooper M, Bello-Reuss E, Reuss L. Gap-junctional hemichannels are activated by ATP depletion in human renal proximal tubule cells. J Membr Biol 196: 173-184, 2003.
71. Verma V, Hallett MB, Leybaert L, Martin PE, Evans WH. Perturbing plasma membrane hemichannels attenuates calcium signalling in cardiac cells and HeLa cells expressing connexins. Eur J Cell Biol 88: 79-90, 2009.
72. Vinken M, Decrock E, De Vuyst E, De Bock M, Vandenbroucke RE, De Geest BG, Demeester J, Sanders NN, Vanhaecke T, Leybaert L, Rogiers V. Connexin32 hemichannels contribute to the apoptotic-tonecrotic transition during Fas-mediated hepatocyte cell death. Cell Mol Life Sci 67: 907-918, 2009.
73. 2+ entry pathways in vascular endothelial cells. Biochem J 323: 567-573, 1997.
74. Wong CW, Christen T, Roth I, Chadjichristos CE, Derouette JP, Foglia BF, Chanson M, Goodenough DA, Kwak BR. Connexin37 protects against atherosclerosis by regulating monocyte adhesion. Nat Med 12: 950-954, 2006.
75. Ye ZC, Wyeth MS, Baltan-Tekkok S, Ransom BR. Functional hemichannels in astrocytes: a novel mechanism of glutamate release. J Neurosci 23: 3588-3596, 2003.
76. Yu J, Bippes CA, Hand GM, Muller DJ, Sosinsky GE. Aminosulfonate modulated pH-induced conformational changes in connexin26 hemichannels. J Biol Chem 282: 8895-8904, 2007.