Hemichannels: New pathways for gliotransmitter release

Neuroscience

Volumn 286, Issue , 2015, Pages 45-59

  Montero, T D ^a   Orellana, J A ^a  

^a PONTIFICIA UNIVERSIDAD CATÓLICA DE CHILE   (Chile)

Author keywords

Astrocyte; Connexin; Hemichannel; Microglia; Neuron; Pannexin

Indexed keywords

ACID SENSING ION CHANNEL; ADENOSINE TRIPHOSPHATE; AMYLOID BETA PROTEIN; AQUAPORIN; CONNEXIN 26; CONNEXIN 30; CONNEXIN 32; CONNEXIN 43; GAP JUNCTION PROTEIN; GLIOTRANSMITTER; GLUCOSE; GLUTAMIC ACID; GLUTAMINE; GLYCYRRHETINIC ACID DERIVATIVE; HEMICHANNEL; INI 06032; LACTIC ACID; MEMBRANE PROTEIN; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NEUROTRANSMITTER; PANNEXIN 1; PANNEXIN 2; PURINERGIC P2X7 RECEPTOR; PURINERGIC P2Y1 RECEPTOR; UNCLASSIFIED DRUG;

ALZHEIMER DISEASE; AMYLOID PLAQUE; ARTERIAL CARBON DIOXIDE TENSION; BRAIN ISCHEMIA; CALCIUM TRANSPORT; CELL COMMUNICATION; CHANNEL GATING; CHEMORECEPTOR; DEGENERATIVE DISEASE; ENERGY BALANCE; GAP JUNCTION; GLIA CELL; GLIOTRANSMITTER RELEASE; HUMAN; MEDIOBASAL HYPOTHALAMUS; MEDULLA OBLONGATA; MICROGLIA; NEUROFIBRILLARY TANGLE; NEUROTRANSMITTER RELEASE; NONHUMAN; RESPIRATION CONTROL; REVIEW; SENILE PLAQUE; SPATIAL LEARNING; SYNAPTIC TRANSMISSION; ANIMAL; BRAIN; GLIA; METABOLISM; NERVE CELL; SECRETION (PROCESS); SIGNAL TRANSDUCTION;

ADENOSINE TRIPHOSPHATE; ANIMALS; BRAIN; CONNEXINS; HUMANS; NEUROGLIA; NEURONS; SIGNAL TRANSDUCTION; SYNAPTIC TRANSMISSION;

EID: 84916887253     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2014.11.048     Document Type: Review

References (164)

1. Allard C., Carneiro L., Grall S., Cline B.H., Fioramonti X., Chrétien C., Baba-Aissa F., Giaume C., Pénicaud L., Leloup C. Hypothalamic astroglial connexins are required for brain glucose sensing-induced insulin secretion. J Cereb Blood Flow Metab 2014, 34(2):339-346.
2. Ambrosi C., Gassmann O., Pranskevich J.N., Boassa D., Smock A., Wang J., Dahl G., Steinem C., Sosinsky G.E. Pannexin1 and Pannexin2 channels show quaternary similarities to connexons and different oligomerization numbers from each other. J Biol Chem 2010, 285:24420-24431.
3. Araque A., Carmignoto G., Haydon P.G., Oliet S.H., Robitaille R., Volterra A. Gliotransmitters travel in time and space. Neuron 2014, 81:728-739.
4. Araque A., Parpura V., Sanzgiri R.P., Haydon P.G. Tripartite synapses: glia, the unacknowledged partner. Trends Neurosci 1999, 22:208-215.
5. Arcuino G., Lin J.H., Takano T., Liu C., Jiang L., Gao Q., Kang J., Nedergaard M. Intercellular calcium signaling mediated by point-source burst release of ATP. Proc Natl Acad Sci USA 2002, 99:9840-9845.
6. Ardiles A.O., Flores-Muñoz C., Toro-Ayala G., Cárdenas A.M., Palacios A.G., Muñoz P., Fuenzalida M., Saez J.C., Martinez A.D. Pannexin 1 regulates bidirectional hippocampal synaptic plasticity in adult mice. Front Cell Neurosci 2014, 8. 10.3389/fncel.2014.00326.
7. Bao L., Locovei S., Dahl G. Pannexin membrane channels are mechanosensitive conduits for ATP. FEBS Lett 2004, 572:65-68.
8. Bao L., Samuels S., Locovei S., Macagno E.R., Muller K.J., Dahl G. Innexins form two types of channels. FEBS Lett 2007, 58:5703-5708.
9. Bao Y., Chen Y., Ledderose C., Li L., Junger W.G. Pannexin 1 channels link chemoattractant receptor signaling to local excitation and global inhibition responses at the front and back of polarized neutrophils. J Biol Chem 2013, 288:22650-22657.
10. Baranova A., Ivanov D., Petrash N., Pestova A., Skoblov M., Kelmanson I., Shagin D., Nazarenko S., Geraymovych E., Litvin O., Tiunova A., Born T.L., Usman N., Staroverov D., Lukyanov S., Panchin Y. The mammalian pannexin family is homologous to the invertebrate innexin gap junction proteins. Genomics 2004, 83:706-716.
11. Bargiotas P., Krenz A., Hormuzdi S.G., Ridder D.A., Herb A., Barakat W., Penuela S., von Engelhardt J., Monyer H., Schwaninger M. Pannexins in ischemia-induced neurodegeneration. Proc Natl Acad Sci USA 2011, 108:20772-20777.
12. Bargiotas P., Krenz A., Monyer H., Schwaninger M. Functional outcome of pannexin-deficient mice after cerebral ischemia. Channels (Austin) 2012, 6:453-456.
13. Bargiotas P., Monyer H., Schwaninger M. Hemichannels in cerebral ischemia. Curr Mol Med 2009, 9:186-194.
14. Batra N., Burra S., Siller-Jackson A.J., Gu S., Xia X., Weber G.F., DeSimone D., Bonewald L.F., Lafer E.M., Sprague E., Schwartz M.A., Jiang J.X. Mechanical stress-activated integrin alpha5beta1 induces opening of connexin 43 hemichannels. Proc Natl Acad Sci USA 2012, 109:3359-3364.
15. Bennett M.V., Garre J.M., Orellana J.A., Bukauskas F.F., Nedergaard M., Saez J.C. Connexin and pannexin hemichannels in inflammatory responses of glia and neurons. Brain Res 2012, 1487:3-15.
16. Bezzi P., Gundersen V., Galbete J.L., Seifert G., Steinhauser C., Pilati E., Volterra A. Astrocytes contain a vesicular compartment that is competent for regulated exocytosis of glutamate. Nat Neurosci 2004, 7:613-620.
17. Bolborea M., Dale N. Hypothalamic tanycytes: potential roles in the control of feeding and energy balance. Trends Neurosci 2013, 36:91-100.
18. Bonansco C., Couve A., Perea G., Ferradas C.A., Roncagliolo M., Fuenzalida M. Glutamate released spontaneously from astrocytes sets the threshold for synaptic plasticity. Eur J Neurosci 2011, 33:1483-1492.
19. Bond S.R., Naus C.C. The pannexins: past and present. Front Physiol 2014, 5:58.
20. Bruzzone R., Hormuzdi S.G., Barbe M.T., Herb A., Monyer H. Pannexins, a family of gap junction proteins expressed in brain. Proc Natl Acad Sci USA 2003, 100:13644-13649.
21. + fluxes in intact cells. FASEB J 2001, 15:10-12.
22. Clarke L.E., Barres B.A. Emerging roles of astrocytes in neural circuit development. Nat Rev Neurosci 2013, 14:311-321.
23. Contreras J.E., Saez J.C., Bukauskas F.F., Bennett M.V. Gating and regulation of connexin 43 (Cx43) hemichannels. Proc Natl Acad Sci USA 2003, 100:11388-11393.
24. Contreras J.E., Sánchez H.A., Eugenin E.A., Speidel D., Theis M., Willecke K., Bukauskas F.F., Bennett M.V.L., Sáez J.C. 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 2002, 99:495-500.
25. Cotrina M.L., Lin J.H., Alves-Rodrigues A., Liu S., Li J., Azmi-Ghadimi H., Kang J., Naus C.C., Nedergaard M. Connexins regulate calcium signaling by controlling ATP release. Proc Natl Acad Sci USA 1998, 95:15735-15740.
26. Cotrina M.L., Lin J.H., Nedergaard M. Adhesive properties of connexin hemichannels. Glia 2008, 56:1791-1798.
27. Cherian P.P., Siller-Jackson A.J., Gu S., Wang X., Bonewald L.F., Sprague E., Jiang J.X. Mechanical strain opens connexin 43 hemichannels in osteocytes: a novel mechanism for the release of prostaglandin. Mol Biol Cell 2005, 16:3100-3106.
28. Dahl G., Keane R.W. Pannexin: from discovery to bedside in 11±4 years?. Brain Res 2012, 1487:150-159.
29. Davidson J.O., Green C.R., Bennet L., Nicholson L.F., Danesh-Meyer H., O'Carroll S.J., Gunn A.J. A key role for connexin hemichannels in spreading ischemic brain injury. Curr Drug Targets 2013, 14:36-46.
30. De Bock M., Culot M., Wang N., Bol M., Decrock E., De Vuyst E., da Costa A., Dauwe I., Vinken M., Simon A.M., Rogiers V., De Ley G., Evans W.H., Bultynck G., Dupont G., Cecchelli R., Leybaert L. Connexin channels provide a target to manipulate brain endothelial calcium dynamics and blood-brain barrier permeability. J Cereb Blood Flow Metab 2011, 31:1942-1957.
31. De Bock M., Vandenbroucke R.E., Decrock E., Culot M., Cecchelli R., Leybaert L. A new angle on blood-CNS interfaces: a role for connexins?. FEBS Lett 2014, 588:1259-1270.
32. De Vuyst E., Boengler K., Antoons G., Sipido K.R., Schulz R., Leybaert L. Pharmacological modulation of connexin-formed channels in cardiac pathophysiology. Br J Pharmacol 2011, 163:469-483.
33. Dobrowolski R., Sasse P., Schrickel J.W., Watkins M., Kim J.S., Rackauskas M., Troatz C., Ghanem A., Tiemann K., Degen J., Bukauskas F.F., Civitelli R., Lewalter T., Fleischmann B.K., Willecke K. The conditional connexin43G138R mouse mutant represents a new model of hereditary oculodentodigital dysplasia in humans. Hum Mol Genet 2008, 17:539-554.
34. Duan S., Anderson C.M., Keung E.C., Chen Y., Swanson R.A. P2X7 receptor-mediated release of excitatory amino acids from astrocytes. J Neurosci 2003, 23:1320-1328.
35. Dunwiddie T.V., Masino S.A. The role and regulation of adenosine in the central nervous system. Annu Rev Neurosci 2001, 24:31-55.
36. Ebihara L., Steiner E. Properties of a nonjunctional current expressed from a rat connexin46 cDNA in Xenopus oocytes. J Gen Physiol 1993, 102:59-74.
37. Essenfelder G.M., Bruzzone R., Lamartine J., Charollais A., Blanchet-Bardon C., Barbe M.T., Meda P., Waksman G. Connexin30 mutations responsible for hidrotic ectodermal dysplasia cause abnormal hemichannel activity. Hum Mol Genet 2004, 13:1703-1714.
38. Fasciani I., Temperan A., Perez-Atencio L.F., Escudero A., Martinez-Montero P., Molano J., Gomez-Hernandez J.M., Paino C.L., Gonzalez-Nieto D., Barrio L.C. Regulation of connexin hemichannel activity by membrane potential and the extracellular calcium in health and disease. Neuropharmacology 2013, 75:479-490.
39. Frayling C., Britton R., Dale N. ATP-mediated glucosensing by hypothalamic tanycytes. J Physiol 2011, 589:2275-2286.
40. Funk G.D. The 'connexin' between astrocytes, ATP and central respiratory chemoreception. J Physiol 2010, 588:4335-4337.
41. Garré J.M., Retamal M.A., Cassina P., Barbeito L., Bukauskas F.F., Sáez J.C., Bennett M.V.L., Abudara V. FGF-1 induces ATP release from spinal astrocytes in culture and opens pannexin and connexin hemichannels. Proc Natl Acad Sci USA 2010, 107:22659-22664.
42. Giaume C., Leybaert L., Naus C.C., Saez J.C. Connexin and pannexin hemichannels in brain glial cells: properties, pharmacology, and roles. Front Pharmacol 2013, 4:88.
43. Gonzalez D., Gomez-Hernandez J.M., Barrio L.C. Species specificity of mammalian connexin-26 to form open voltage-gated hemichannels. FASEB J 2006, 20:2329-2338.
44. Gourine A.V., Llaudet E., Dale N., Spyer K.M. ATP is a mediator of chemosensory transduction in the central nervous system. Nature 2005, 436:108-111.
45. Gourine A.V., Llaudet E., Dale N., Spyer K.M. Release of ATP in the ventral medulla during hypoxia in rats: role in hypoxic ventilatory response. J Neurosci 2005, 25:1211-1218.
46. Halassa M.M., Fellin T., Haydon P.G. Tripartite synapses: roles for astrocytic purines in the control of synaptic physiology and behavior. Neuropharmacology 2009, 57:343-346.
47. Hamilton N., Vayro S., Kirchhoff F., Verkhratsky A., Robbins J., Gorecki D.C., Butt A.M. Mechanisms of ATP- and glutamate-mediated calcium signaling in white matter astrocytes. Glia 2008, 56:734-749.
48. Hansen D.B., Braunstein T.H., Nielsen M.S., MacAulay N. Distinct permeation profiles of the connexin 30 and 43 hemichannels. FEBS Lett 2014, 588:1446-1457.
49. Harris A.L. Connexin channel permeability to cytoplasmic molecules. Prog Biophys Mol Biol 2007, 94:120-143.
50. Hervé J.-C., Derangeon M. Gap-junction-mediated cell-to-cell communication. Cell Tissue Res 2013, 352:21-31.
51. Hofer A., Dermietzel R. Visualization and functional blocking of gap junction hemichannels (connexons) with antibodies against external loop domains in astrocytes. Glia 1998, 24:141-154.
52. Hofer A.M., Brown E.M. Extracellular calcium sensing and signalling. Nat Rev Mol Cell Biol 2003, 4:530-538.
53. 2-dependent opening of connexin 26 and related β connexins. J Physiol 2010, 588:3921-3931.
54. 2-dependent release of ATP in the medulla oblongata contributes to central respiratory chemosensitivity. J Physiol 2010, 588:3901-3920.
55. Iglesias R., Dahl G., Qiu F., Spray D.C., Scemes E. Pannexin 1: the molecular substrate of astrocyte "hemichannels". J Neurosci 2009, 29:7092-7097.
56. Iglesias R., Locovei S., Roque A., Alberto A.P., Dahl G., Spray D.C., Scemes E. P2X7 receptor-Pannexin1 complex: pharmacology and signaling. Am J Physiol Cell Physiol 2008, 295:C752-C760.
57. Iglesias R., Spray D.C., Scemes E. Mefloquine blockade of Pannexin1 currents: resolution of a conflict. Cell Commun Adhes 2009, 16:131-137.
58. Imura Y., Morizawa Y., Komatsu R., Shibata K., Shinozaki Y., Kasai H., Moriishi K., Moriyama Y., Koizumi S. Microglia release ATP by exocytosis. Glia 2013, 61:1320-1330.
59. Irani B.G., Le Foll C., Dunn-Meynell A., Levin B.E. Effects of leptin on rat ventromedial hypothalamic neurons. Endocrinology 2008, 149:5146-5154.
60. Ishikawa M., Iwamoto T., Nakamura T., Doyle A., Fukumoto S., Yamada Y. Pannexin 3 functions as an ER Ca(2+) channel, hemichannel, and gap junction to promote osteoblast differentiation. J Cell Biol 2011, 193:1257-1274.
61. Iwabuchi S., Kawahara K. Functional significance of the negative-feedback regulation of ATP release via pannexin-1 hemichannels under ischemic stress in astrocytes. Neurochem Int 2011, 58:376-384.
62. Jiang S., Yuan H., Duan L., Cao R., Gao B., Xiong Y.-F., Rao Z.-R. Glutamate release through connexin 43 by cultured astrocytes in a stimulated hypertonicity model. Brain Res 2011, 1392:8-15.
63. Jiang T., Xu R.X., Zhang A.W., Di W., Xiao Z.J., Miao J.Y., Luo N., Fang Y.N. Effects of transcranial direct current stimulation on hemichannel pannexin-1 and neural plasticity in rat model of cerebral infarction. J Neurosci 2012, 226:421-426.
64. John S.A., Kondo R., Wang S.Y., Goldhaber J.I., Weiss J.N. Connexin-43 hemichannels opened by metabolic inhibition. J Biol Chem 1999, 274:236-240.
65. Kawamura M., Ruskin D.N., Masino S.A. Metabolic autocrine regulation of neurons involves cooperation among pannexin hemichannels, adenosine receptors, and KATP channels. J Neurosci 2010, 30:3886-3895.
66. Kienitz M.C., Bender K., Dermietzel R., Pott L., Zoidl G. Pannexin 1 constitutes the large conductance cation channel of cardiac myocytes. J Biol Chem 2011, 286:290-298.
67. Kim J.E., Kang T.C. The P2X7 receptor-pannexin-1 complex decreases muscarinic acetylcholine receptor-mediated seizure susceptibility in mice. J Clin Invest 2011, 121:2037-2047.
68. Kimelberg H.K., Goderie S.K., Higman S., Pang S., Waniewski R.A. Swelling-induced release of glutamate, aspartate, and taurine from astrocyte cultures. J Neurosci 1990, 10:1583-1591.
69. Klaassen L.J., Sun Z., Steijaert M.N., Bolte P., Fahrenfort I., Sjoerdsma T., Klooster J., Claassen Y., Shields C.R., Ten Eikelder H.M., Janssen-Bienhold U., Zoidl G., McMahon D.G., Kamermans M. Synaptic transmission from horizontal cells to cones is impaired by loss of connexin hemichannels. PLoS Biol 2011, 9:e1001107.
70. Kondo R.P., Wang S.Y., John S.A., Weiss J.N., Goldhaber J.I. Metabolic inhibition activates a non-selective current through connexin hemichannels in isolated ventricular myocytes. J Mol Cell Cardiol 2000, 32:1859-1872.
71. Koulakoff A., Mei X., Orellana J.A., Saez J.C., Giaume C. Glial connexin expression and function in the context of Alzheimer's disease. Biochim Biophys Acta 2012, 1818:2048-2057.
72. Kuchibhotla K.V., Lattarulo C.R., Hyman B.T., Bacskai B.J. Synchronous hyperactivity and intercellular calcium waves in astrocytes in Alzheimer mice. J Neurosci 2009, 323:1211-1215.
73. Lai C.P.K., Bechberger J.F., Thompson R.J., MacVicar B.A., Bruzzone R., Naus C.C. Tumor-suppressive effects of pannexin 1 in C6 glioma cells. Cancer Res 2007, 67:1545-1554.
74. Lee S., Yoon B.E., Berglund K., Oh S.J., Park H., Shin H.S., Augustine G.J., Lee C.J. Channel-mediated tonic GABA release from glia. J Neurosci 2010, 330:790-796.
75. Li F., Sugishita K., Su Z., Ueda I., Barry W.H. Activation of connexin-43 hemichannels can elevate [Ca(2+)]i and [Na(+)]i in rabbit ventricular myocytes during metabolic inhibition. J Mol Cell Cardiol 2001, 33:2145-2155.
76. Li H., Liu T.F., Lazrak A., Peracchia C., Goldberg G.S., Lampe P.D., Johnson R.G. Properties and regulation of gap junctional hemichannels in the plasma membranes of cultured cells. J Cell Biol 1996, 134:1019-1030.
77. Lin J.H., Lou N., Kang N., Takano T., Hu F., Han X., Xu Q., Lovatt D., Torres A., Willecke K., Yang J., Kang J., Nedergaard M. A central role of connexin 43 in hypoxic preconditioning. J Neurosci 2008, 28:681-695.
78. Liu X., Hashimoto-Torii K., Torii M., Ding C., Rakic P. Gap junctions/hemichannels modulate interkinetic nuclear migration in the forebrain precursors. J Neurosci 2010, 30:4197-4209.
79. Liu X., Sun L., Torii M., Rakic P. Connexin 43 controls the multipolar phase of neuronal migration to the cerebral cortex. Proc Natl Acad Sci USA 2012, 109:8280-8285.
80. Locovei S., Wang J., Dahl G. Activation of pannexin 1 channels by ATP through P2Y receptors and by cytoplasmic calcium. FEBS Lett 2006, 580:239-244.
81. Lohman A.W., Isakson B.E. Differentiating connexin hemichannels and pannexin channels in cellular ATP release. FEBS Lett 2014, 588:1379-1388.
82. Loo D.T., Copani A., Pike C.J., Whittemore E.R., Walencewicz A.J., Cotman C.W. Apoptosis is induced by beta-amyloid in cultured central nervous system neurons. Proc Natl Acad Sci USA 1993, 90:7951-7955.
83. Ma W., Compan V., Zheng W., Martin E., North R.A., Verkhratsky A., Surprenant A. Pannexin 1 forms an anion-selective channel. Pflugers Arch 2012, 463(4):585-592.
84. MacVicar B.A., Thompson R.J. Non-junction functions of pannexin-1 channels. Trends Neurosci 2010, 33:93-102.
85. Mawhinney L.J., de Rivero Vaccari J.P., Dale G.A., Keane R.W., Bramlett H.M. Heightened inflammasome activation is linked to age-related cognitive impairment in Fischer 344 rats. BMC Neurosci 2011, 12:123.
86. Makarenkova H.P., Shestopalov V.I. The role of pannexin hemichannels in inflammation and regeneration. Front Physiol 2014, 5:63.
87. 2+ responses in enteric glia are mediated by connexin-43 hemichannels and modulate colonic transit in mice. Gastroenterology 2014, 146(497-507):e491.
88. Mei X., Ezan P., Giaume C., Koulakoff A. Astroglial connexin immunoreactivity is specifically altered at beta-amyloid plaques in beta-amyloid precursor protein/presenilin1 mice. J Neurosci 2010, 171:92-105.
89. 2 directly modulates connexin 26 by formation of carbamate bridges between subunits. Elife 2013, 2.
90. Moreno A.P., Lau A.F. Gap junction channel gating modulated through protein phosphorylation. Prog Biophys Mol Biol 2007, 94:107-119.
91. Nagy J.I., Li W., Hertzberg E.L., Marotta C.A. Elevated connexin43 immunoreactivity at sites of amyloid plaques in Alzheimer's disease. Brain Res 1996, 717:173-178.
92. Nedergaard M., Verkhratsky A. Artifact versus reality - how astrocytes contribute to synaptic events. Glia 2012, 60:1013-1023.
93. Orellana J.A., Avendano B.C., Montero T.D. Role of connexins and pannexins in ischemic stroke. Curr Med Chem 2014, 21:2165-2182.
94. Orellana J.A., Froger N., Ezan P., Jiang J.X., Bennett M.V.L., Naus C.C., Giaume C., Sáez J.C. ATP and glutamate released via astroglial connexin 43 hemichannels mediate neuronal death through activation of pannexin 1 hemichannels. J Neurochem 2011, 118:826-840.
95. Orellana J.A., Saez P.J., Cortes-Campos C., Elizondo R.J., Shoji K.F., Contreras-Duarte S., Figueroa V., Velarde V., Jiang J.X., Nualart F., Saez J.C., Garcia M.A. Glucose increases intracellular free Ca(2+) in tanycytes via ATP released through connexin 43 hemichannels. Glia 2012, 60:53-68.
96. Orellana J.A., Sáez P.J., Cortés-campos C., Elizondo R.J., Shoji K.F., Contreras-Duarte S., Figueroa V., Velarde V., Jiang J.X., Nualart F., Sáez J.C., García M.A. Glucose increases intracellular free Ca(2+) in tanycytes via ATP released through connexin 43 hemichannels. Glia 2012, 60:53-68.
97. Orellana J.A., Saez P.J., Shoji K.F., Schalper K.A., Palacios-Prado N., Velarde V., Giaume C., Bennett M.V., Saez J.C. Modulation of brain hemichannels and gap junction channels by pro-inflammatory agents and their possible role in neurodegeneration. Antioxid Redox Signal 2009, 11:369-399.
98. Orellana J.A., Shoji K.F., Abudara V., Ezan P., Amigou E., Sáez P.J., Jiang J.X., Naus C.C., Sáez J.C., Giaume C. Amyloid β-induced death in neurons involves glial and neuronal hemichannels. J Neurosci 2011, 31:4962-4977.
99. Orellana J.A., von Bernhardi R., Giaume C., Saez J.C. Glial hemichannels and their involvement in aging and neurodegenerative diseases. Rev Neurosci 2012, 23:163-177.
100. Panchin Y., Kelmanson I., Matz M., Lukyanov K., Usman N., Lukyanov S. A ubiquitous family of putative gap junction molecules. Curr Biol 2000, 10:R473-R474.
101. Pannasch U., Freche D., Dallerac G., Ghezali G., Escartin C., Ezan P., Cohen-Salmon M., Benchenane K., Abudara V., Dufour A., Lubke J.H., Deglon N., Knott G., Holcman D., Rouach N. Connexin 30 sets synaptic strength by controlling astroglial synapse invasion. Nat Neurosci 2014, 17:549-558.
102. Pannasch U., Rouach N. Emerging role for astroglial networks in information processing: from synapse to behavior. Trends Neurosci 2013, 36:405-417.
103. Pannasch U., Vargova L., Reingruber J., Ezan P., Holcman D., Giaume C., Sykova E., Rouach N. Astroglial networks scale synaptic activity and plasticity. Proc Natl Acad Sci USA 2011, 108:8467-8472.
104. Parihar M.S., Hemnani T. Alzheimer's disease pathogenesis and therapeutic interventions. J Clin Neurosci 2004, 11:456-467.
105. Paul D.L., Ebihara L., Takemoto L.J., Swenson K.I., Goodenough D.A. Connexin46, a novel lens gap junction protein, induces voltage-gated currents in nonjunctional plasma membrane of Xenopus oocytes. J Cell Biol 1991, 115:1077-1089.
106. Perea G., Araque A. GLIA modulates synaptic transmission. Brain Res Rev 2010, 63:93-102.
107. Perea G., Navarrete M., Araque A. Tripartite synapses: astrocytes process and control synaptic information. Trends Neurosci 2009, 32:421-431.
108. Pike C.J., Walencewicz-Wasserman A.J., Kosmoski J., Cribbs D.H., Glabe C.G., Cotman C.W. Structure-activity analyses of beta-amyloid peptides: contributions of the beta 25-35 region to aggregation and neurotoxicity. J Neurochem 1995, 64:253-265.
109. 2+ mobilization and cell proliferation. J Biol Chem 2013, 288:27571-27583.
110. Ponsaerts R., De Vuyst E., Retamal M., D'Hondt C., Vermeire D., Wang N., De Smedt H., Zimmermann P., Himpens B., Vereecke J., Leybaert L., Bultynck G. Intramolecular loop/tail interactions are essential for connexin 43-hemichannel activity. FASEB J 2010, 24:4378-4395.
111. Prochnow N., Abdulazim A., Kurtenbach S., Wildforster V., Dvoriantchikova G., Hanske J., Petrasch-Parwez E., Shestopalov V.I., Dermietzel R., Manahan-Vaughan D., Zoidl G. Pannexin1 stabilizes synaptic plasticity and is needed for learning. PLoS One 2012, 7:e51767.
112. Quist A.P., Rhee S.K., Lin H., Lal R. Physiological role of gap-junctional hemichannels. Extracellular calcium-dependent isosmotic volume regulation. J Cell Biol 2000, 148:1063-1074.
113. Retamal M.A., Froger N., Palacios-Prado N., Ezan P., Saez P.J., Saez J.C., Giaume C. Cx43 hemichannels and gap junction channels in astrocytes are regulated oppositely by proinflammatory cytokines released from activated microglia. J Neurosci 2007, 27:13781-13792.
114. Riquelme M.A., Cea L.A., Vega J.L., Boric M.P., Monyer H., Bennett M.V., Frank M., Willecke K., Saez J.C. The ATP required for potentiation of skeletal muscle contraction is released via pannexin hemichannels. Neuropharmacology 2013, 75:594-603.
115. Rodriguez E.M., Blazquez J.L., Pastor F.E., Pelaez B., Pena P., Peruzzo B., Amat P. Hypothalamic tanycytes: a key component of brain-endocrine interaction. Int Rev Cytol 2005, 247:89-164.
116. Romanov R.A., Bystrova M.F., Rogachevskaya O.A., Sadovnikov V.B., Shestopalov V.I., Kolesnikov S.S. The ATP permeability of pannexin 1 channels in a heterologous system and in mammalian taste cells is dispensable. J Cell Sci 2012, 125(Pt 22):5514-5523.
117. Rossi D.J., Oshima T., Attwell D. Glutamate release in severe brain ischaemia is mainly by reversed uptake. Nature 2000, 403:316-321.
118. Routh V.H. Glucosensing neurons in the ventromedial hypothalamic nucleus (VMN) and hypoglycemia-associated autonomic failure (HAAF). Diabetes Metab Res Rev 2003, 19:348-356.
119. Rudkouskaya A., Chernoguz A., Haskew-Layton R.E., Mongin A.A. Two conventional protein kinase C isoforms, alpha and beta I, are involved in the ATP-induced activation of volume-regulated anion channel and glutamate release in cultured astrocytes. J Neurochem 2008, 105:2260-2270.
120. Saez J.C., Berthoud V.M., Branes M.C., Martinez A.D., Beyer E.C. Plasma membrane channels formed by connexins: their regulation and functions. Physiol Rev 2003, 83:1359-1400.
121. Saez J.C., Leybaert L. Hunting for connexin hemichannels. FEBS Lett 2014, 588:1205-1211.
122. Saez J.C., Retamal M.A., Basilio D., Bukauskas F.F., Bennett M.V. Connexin-based gap junction hemichannels: gating mechanisms. Biochim Biophys Acta 2005, 1711:215-224.
123. Sahu G., Sukumaran S., Bera A.K. Pannexins form gap junctions with electrophysiological and pharmacological properties distinct from connexins. Sci Rep 2014, 4:4955.
124. Salameh A., Blanke K., Dhein S. Mind the gap! Connexins and pannexins in physiology, pharmacology and disease. Front Pharmacol 2013, 4:144.
125. Sangaletti R., Dahl G., Bianchi L. Mechanosensitive unpaired innexin channels in C. elegans touch neurons. Am J Physiol Cell Physiol 2014, 307(10):C966-C977.
126. Santiago M.F., Veliskova J., Patel N.K., Lutz S.E., Caille D., Charollais A., Meda P., Scemes E. Targeting pannexin1 improves seizure outcome. PLoS One 2011, 6:e25178.
127. Samuels S.E., Lipitz J.B., Dahl G., Muller K.J. Neuroglial ATP release through innexin channels controls microglial cell movement to a nerve injury. J Gen Physiol 2010, 136:425-442.
128. Samuels S.E., Lipitz J.B., Wang J., Dahl G., Muller K.J. Arachidonic acid closes innexin/pannexin channels and thereby inhibits microglia cell movement to a nerve injury. Dev Neurobiol 2013, 73:621-631.
129. Schafer D.P., Lehrman E.K., Stevens B. The 'quad-partite' synapse: microglia-synapse interactions in the developing and mature CNS. Glia 2013, 61:24-36.
130. Schock S.C., Leblanc D., Hakim A.M., Thompson C.S. ATP release by way of connexin 36 hemichannels mediates ischemic tolerance in vitro. Biochem Biophys Res Commun 2008, 368:138-144.
131. Shestopalov V.I., Panchin Y. Pannexins and gap junction protein diversity. Cell Mol Life Sci 2008, 65:376-394.
132. Shestopalov V.I., Slepak V.Z. Molecular pathways of pannexin1-mediated neurotoxicity. Front Physiol 2014, 5:23.
133. Sipos A., Vargas S.L., Toma I., Hanner F., Willecke K., Peti-Peterdi J. Connexin 30 deficiency impairs renal tubular ATP release and pressure natriuresis. J Am Soc Nephrol 2009, 20:1724-1732.
134. Solomon I.C., Halat T.J., El-Maghrabi M.R., O'Neal M.H. Localization of connexin26 and connexin32 in putative CO(2)-chemosensitive brainstem regions in rat. Respir Physiol 2001, 129:101-121.
135. Song Z., Routh V.H. Differential effects of glucose and lactate on glucosensing neurons in the ventromedial hypothalamic nucleus. Diabetes 2005, 54:15-22.
136. Sosinsky G.E., Boassa D., Dermietzel R., Duffy H.S., Laird D.W., MacVicar B., Naus C.C., Penuela S., Scemes E., Spray D.C., Thompson R.J., Zhao H.B., Dahl G. Pannexin channels are not gap junction hemichannels. Channels (Austin) 2011, 5:193-197.
137. Stehberg J., Moraga-Amaro R., Salazar C., Becerra A., Echeverria C., Orellana J.A., Bultynck G., Ponsaerts R., Leybaert L., Simon F., Saez J.C., Retamal M.A. Release of gliotransmitters through astroglial connexin 43 hemichannels is necessary for fear memory consolidation in the basolateral amygdala. FASEB J 2012, 26:3649-3657.
138. Stout C.E., Costantin J.L., Naus C.C.G., Charles A.C. Intercellular calcium signaling in astrocytes via ATP release through connexin hemichannels. J Biol Chem 2002, 277:10482-10488.
139. Stridh M.H., Tranberg M., Weber S.G., Blomstrand F., Sandberg M. Stimulated efflux of amino acids and glutathione from cultured hippocampal slices by omission of extracellular calcium: likely involvement of connexin hemichannels. J Biol Chem 2008, 283:10347-10356.
140. 2+ signaling. J Neurosci 2006, 26:1378-1385.
141. Svenningsen P., Burford J.L., Peti-Peterdi J. ATP releasing connexin 30 hemichannels mediate flow-induced calcium signaling in the collecting duct. Front Physiol 2013, 4:292.
142. Takagi N., Cheung H.H., Bissoon N., Teves L., Wallace M.C., Gurd J.W. The effect of transient global ischemia on the interaction of Src and Fyn with the N-methyl-d-aspartate receptor and postsynaptic densities: possible involvement of Src homology 2 domains. J Cereb Blood Flow Metab 1999, 19:880-888.
143. Takano T., Kang J., Jaiswal J.K., Simon S.M., Lin J.H., Yu Y., Li Y., Yang J., Dienel G., Zielke H.R., Nedergaard M. Receptor-mediated glutamate release from volume sensitive channels in astrocytes. Proc Natl Acad Sci USA 2005, 102:16466-16471.
144. Takeuchi H., Jin S., Wang J., Zhang G., Kawanokuchi J., Kuno R., Sonobe Y., Mizuno T., Suzumura A. Tumor necrosis factor-alpha induces neurotoxicity via glutamate release from hemichannels of activated microglia in an autocrine manner. J Biol Chem 2006, 281:21362-21368.
145. Takeuchi H., Mizoguchi H., Doi Y., Jin S., Noda M., Liang J., Li H., Zhou Y., Mori R., Yasuoka S., Li E., Parajuli B., Kawanokuchi J., Sonobe Y., Sato J., Yamanaka K., Sobue G., Mizuno T., Suzumura A. Blockade of gap junction hemichannel suppresses disease progression in mouse models of amyotrophic lateral sclerosis and Alzheimer's disease. PLoS One 2011, 6:e21108.
146. Thompson R.J., Macvicar B.A. Connexin and pannexin hemichannels of neurons and astrocytes. Channels (Austin) 2008, 2:81-86.
147. 2+ acts as a mediator of communication from neurons to glia. Sci Signal 2012, 5:ra8.
148. Tremblay M.E., Lowery R.L., Majewska A.K. Microglial interactions with synapses are modulated by visual experience. PLoS Biol 2010, 8:e1000527.
149. Trexler E.B., Bennett M.V., Bargiello T.A., Verselis V.K. Voltage gating and permeation in a gap junction hemichannel. Proc Natl Acad Sci USA 1996, 93:5836-5841.
150. Valiunas V., Weingart R. Electrical properties of gap junction hemichannels identified in transfected HeLa cells. Pflugers Arch 2000, 440:366-379.
151. Vanden Abeele F., Bidaux G., Gordienko D., Beck B., Panchin Y.V., Baranova A.V., Ivanov D.V., Skryma R., Prevarskaya N. Functional implications of calcium permeability of the channel formed by pannexin 1. J Cell Biol 2006, 174:535-546.
152. 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 2003, 196:173-184.
153. Wake H., Moorhouse A.J., Miyamoto A., Nabekura J. Microglia: actively surveying and shaping neuronal circuit structure and function. Trends Neurosci 2013, 36:209-217.
154. Wang N., De Bock M., Decrock E., Bol M., Gadicherla A., Vinken M., Rogiers V., Bukauskas F.F., Bultynck G., Leybaert L. Paracrine signaling through plasma membrane hemichannels. Biochim Biophys Acta 2013, 1828(1):35-50.
155. Wang Y., Belousov A.B. Deletion of neuronal gap junction protein connexin 36 impairs hippocampal LTP. Neurosci Lett 2011, 502:30-32.
156. Weilinger N.L., Tang P.L., Thompson R.J. Anoxia-induced NMDA receptor activation opens pannexin channels via Src family kinases. J Neurosci 2012, 32:12579-12588.
157. +-sensitive neurons by purinergic signalling. J Physiol 2012, 590:2137-2150.
158. Williams J.A., Imamura M., Fregni F. Updates on the use of non-invasive brain stimulation in physical and rehabilitation medicine. J Rehabil Med 2009, 41:305-311.
159. Williams R.H., Alexopoulos H., Jensen L.T., Fugger L., Burdakov D. Adaptive sugar sensors in hypothalamic feeding circuits. Proc Natl Acad Sci USA 2008, 105:11975-11980.
160. Xu Z., Chen R.Q., Gu Q.H., Yan J.Z., Wang S.H., Liu S.Y., Lu W. Metaplastic regulation of long-term potentiation/long-term depression threshold by activity-dependent changes of NR2A/NR2B ratio. J Neurosci 2009, 29:8764-8773.
161. Ye Z.-C., Wyeth M.S., Baltan-Tekkok S., Ransom B.R. Functional hemichannels in astrocytes: a novel mechanism of glutamate release. J Neurosci 2003, 23:3588-3596.
162. Yuan D., Wang Q., Wu D., Yu M., Zhang S., Li L., Tao L., Harris A.L. Monocyte-endothelial adhesion is modulated by Cx43-stimulated ATP release from monocytes. Biochem Biophys Res Commun 2012, 420:536-541.
163. Zanotti S., Charles A. Extracellular calcium sensing by glial cells: low extracellular calcium induces intracellular calcium release and intercellular signaling. J Neurochem 1997, 69:594-602.
164. Zhang Q., Fukuda M., Van Bockstaele E., Pascual O., Haydon P.G. Synaptotagmin IV regulates glial glutamate release. Proc Natl Acad Sci USA 2004, 101:9441-9446.