Pannexin1 channels act downstream of P2X7 receptors in ATP-induced murine T-cell death

Channels

Volumn 8, Issue 2, 2014, Pages 142-156

  Shoji, Kenji F ^a   Sáez, Pablo J ^a   Harcha, Paloma A ^a   Aguila, Hector L ^b   Sáez, Juan C ^a,c  

^a PONTIFICIA UNIVERSIDAD CATÓLICA DE CHILE   (Chile)

^b UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

^c Centro Interdisciplinario de Neurociencias de Valparaíso   (Chile)

Author keywords

Dye uptake; Membrane permeability; Necrosis; Pannexons

Indexed keywords

4BR A23187; ADENOSINE TRIPHOSPHATE; CALCIUM IONOPHORE; MEMBRANE PROTEIN; PANNEXIN 1 PROTEIN; PANNEXIN 2 PROTEIN; PANNEXIN 3 PROTEIN; PURINERGIC P2X RECEPTOR; UNCLASSIFIED DRUG; CALCIMYCIN; GAP JUNCTION PROTEIN; NERVE PROTEIN; PANX1 PROTEIN, MOUSE; PANX2 PROTEIN, MOUSE; PURINERGIC P2X7 RECEPTOR;

ANIMAL CELL; ANIMAL CELL CULTURE; ANIMAL EXPERIMENT; ARTICLE; CD4+ T LYMPHOCYTE; CELL DEATH; CELLULAR DISTRIBUTION; CYTOTOXIC T LYMPHOCYTE; ELECTROPHYSIOLOGICAL PROCEDURES; MALE; MEMBRANE CHANNEL; MOUSE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; T LYMPHOCYTE; TRANSGENIC MOUSE; ANIMAL; ANTAGONISTS AND INHIBITORS; APOPTOSIS; BAGG ALBINO MOUSE; C57BL MOUSE; CALCIUM SIGNALING; CELL CULTURE; CELL MEMBRANE PERMEABILITY; CYTOLOGY; DRUG EFFECTS; GENETICS; HUMAN; JURKAT CELL LINE; KNOCKOUT MOUSE; METABOLISM; PHYSIOLOGY; TIME LAPSE IMAGING;

ADENOSINE TRIPHOSPHATE; ANIMALS; APOPTOSIS; CALCIMYCIN; CALCIUM SIGNALING; CD4-POSITIVE T-LYMPHOCYTES; CELL MEMBRANE PERMEABILITY; CELLS, CULTURED; CONNEXINS; HUMANS; JURKAT CELLS; MALE; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, KNOCKOUT; NERVE TISSUE PROTEINS; RECEPTORS, PURINERGIC P2X7; T-LYMPHOCYTES; TIME-LAPSE IMAGING;

EID: 84901473725     PISSN: 19336950     EISSN: 19336969     Source Type: Journal    
DOI: 10.4161/chan.28122     Document Type: Article

References (82)

1. Trautmann A. Extracellular ATP in the immune system: more than just a "danger signal". Sci Signal 2009; 2:pe6; PMID:19193605; http://dx.doi.org/10.1126/scisignal.256pe6
2. Gu B, Bendall LJ, Wiley JS. Adenosine triphosphate-induced shedding of CD23 and L-selectin (CD62L) from lymphocytes is mediated by the same receptor but different metalloproteases. Blood 1998; 92:946-51; PMID:9680363
3. 7 receptor-dependent ATP-induced shedding of CD27 in mouse lymphocytes. Immunol Lett 2006; 102:98-105; PMID:16207496; http://dx.doi.org/10.1016/j.imlet.2005.08.004
4. Langston HP, Ke Y, Gewirtz AT, Dombrowski KE, Kapp JA. Secretion of IL-2 and IFN-gamma, but not IL-4, by antigen-specific T cells requires extracellular ATP. J Immunol 2003; 170:2962-70; PMID:12626548
5. Baricordi OR, Melchiorri L, Adinolfi E, Falzoni S, Chiozzi P, Buell G, Di Virgilio F. Increased proliferation rate of lymphoid cells transfected with the P2X(7) ATP receptor. J Biol Chem 1999; 274:33206-8; PMID:10559192; http://dx.doi.org/10.1074/jbc.274.47.33206
6. Chen L, Brosnan CF. Exacerbation of experimental autoimmune encephalomyelitis in P2X7R-/- mice: evidence for loss of apoptotic activity in lymphocytes. J Immunol 2006; 176:3115-26; PMID:16493071
7. Woehrle T, Yip L, Elkhal A, Sumi Y, Chen Y, Yao Y, Insel PA, Junger WG. Pannexin-1 hemichannel-mediated ATP release together with P2X1 and P2X4 receptors regulate T-cell activation at the immune synapse. Blood 2010; 116:3475-84; PMID:20660288; http://dx.doi.org/10.1182/blood-2010-04-277707
8. Di Virgilio F, Chiozzi P, Ferrari D, Falzoni S, Sanz JM, Morelli A, Torboli M, Bolognesi G, Baricordi OR. Nucleotide receptors: an emerging family of regulatory molecules in blood cells. Blood 2001; 97:587-600; PMID:11157473; http://dx.doi.org/10.1182/blood.V97.3.587
9. 7 receptor signalling complex. EMBO J 2001; 20:6347-58; PMID:11707406; http://dx.doi.org/10.1093/emboj/20.22.6347
10. Adinolfi E, Pizzirani C, Idzko M, Panther E, Norgauer J, Di Virgilio F, Ferrari D. P2X(7) receptor: Death or life? Purinergic Signal 2005; 1:219-27; PMID:18404507; http://dx.doi.org/10.1007/s11302-005-6322-x
11. 7 receptor expression levels determine lethal effects of a purine based danger signal in T lymphocytes. Cell Immunol 2006; 243:58-65; PMID:17286969; http://dx.doi.org/10.1016/j.cellimm.2006.12.003
12. 7 receptor-dependent and -independent T cell death is induced by nicotinamide adenine dinucleotide. J Immunol 2005; 174:1971-9; PMID:15699125
13. Locovei S, Scemes E, Qiu F, Spray DC, Dahl G. Pannexin1 is part of the pore forming unit of the P2X(7) receptor death complex. FEBS Lett 2007; 581:483-8; PMID:17240370; http://dx.doi.org/10.1016/j.febslet.2006.12.056
14. 7 receptor. EMBO J 2006; 25:5071-82; PMID:17036048; http://dx.doi.org/10.1038/sj.emboj.7601378
15. Bruzzone R, Hormuzdi SG, Barbe MT, Herb A, Monyer H. Pannexins, a family of gap junction proteins expressed in brain. Proc Natl Acad Sci U S A 2003; 100:13644-9; PMID:14597722; http://dx.doi.org/10.1073/pnas.2233464100
16. Locovei S, Bao L, Dahl G. Pannexin 1 in erythrocytes: function without a gap. Proc Natl Acad Sci U S A 2006; 103:7655-9; PMID:16682648; http://dx.doi.org/10.1073/pnas.0601037103
17. Junger WG. Immune cell regulation by autocrine purinergic signalling. Nat Rev Immunol 2011; 11:201-12; PMID:21331080; http://dx.doi.org/10.1038/nri2938
18. MacVicar BA, Thompson RJ. Non-junction functions of pannexin-1 channels. Trends Neurosci 2010; 33:93-102; PMID:20022389; http://dx.doi.org/10.1016/j. tins.2009.11.007
19. Ma W, Hui H, Pelegrin P, Surprenant A. Pharmacological characterization of pannexin-1 currents expressed in mammalian cells. J Pharmacol Exp Ther 2009; 328:409-18; PMID:19023039; http://dx.doi.org/10.1124/jpet.108.146365
20. Qiu F, Dahl G. A permeant regulating its permeation pore: inhibition of pannexin 1 channels by ATP. Am J Physiol Cell Physiol 2009; 296:C250-5; PMID:18945939; http://dx.doi.org/10.1152/ajpcell.00433.2008
21. Chekeni FB, Elliott MR, Sandilos JK, Walk SF, Kinchen JM, Lazarowski ER, Armstrong AJ, Penuela S, Laird DW, Salvesen GS, et al. Pannexin 1 channels mediate 'find-me' signal release and membrane permeability during apoptosis. Nature 2010; 467:863-7; PMID:20944749; http://dx.doi.org/10.1038/nature09413
22. 7 receptor and Pannexin-1 are both required for the promotion of multinucleated macrophages by the inflammatory cytokine GM-CSF. J Immunol 2011; 187:3878-87; PMID:21865551; http://dx.doi.org/10.4049/jimmunol.1002780
23. Sáez PJ, Shoji KF, Retamal MA, Harcha PA, Ramírez G, Jiang JX, von Bernhardi R, Sáez JC. ATP is required and advances cytokine-induced gap junction formation in microglia in vitro. Mediators Inflamm 2013; 2013:216402; PMID:23737642; http://dx.doi.org/10.1155/2013/216402
24. Schenk U, Westendorf AM, Radaelli E, Casati A, Ferro M, Fumagalli M, Verderio C, Buer J, Scanziani E, Grassi F. Purinergic control of T cell activation by ATP released through pannexin-1 hemichannels. Sci Signal 2008; 1:ra6; PMID:18827222; http://dx.doi.org/10.1126/scisignal.1160583
25. Brough D, Pelegrin P, Rothwell NJ. Pannexin- 1-dependent caspase-1 activation and secretion of IL-1beta is regulated by zinc. Eur J Immunol 2009; 39:352-8; PMID:19130485; http://dx.doi.org/10.1002/eji.200838843
26. Kanneganti TD, Lamkanfi M, Kim YG, Chen G, Park JH, Franchi L, Vandenabeele P, Núñez G. Pannexin-1-mediated recognition of bacterial molecules activates the cryopyrin inflammasome independent of Toll-like receptor signaling. Immunity 2007; 26:433-43; PMID:17433728; http://dx.doi.org/10.1016/j.immuni.2007.03.008
27. Marina-García N, Franchi L, Kim YG, Miller D, McDonald C, Boons GJ, Núñez G. Pannexin-1-mediated intracellular delivery of muramyl dipeptide induces caspase-1 activation via cryopyrin/NLRP3 independently of Nod2. J Immunol 2008; 180:4050-7; PMID:18322214
28. Pelegrin P, Surprenant A. Pannexin-1 couples to maitotoxin- and nigericin-induced interleukin-1beta release through a dye uptake-independent pathway. J Biol Chem 2007; 282:2386-94; PMID:17121814; http://dx.doi.org/10. 1074/jbc.M610351200
29. Qu Y, Misaghi S, Newton K, Gilmour LL, Louie S, Cupp JE, Dubyak GR, Hackos D, Dixit VM. Pannexin-1 is required for ATP release during apoptosis but not for inflammasome activation. J Immunol 2011; 186:6553-61; PMID:21508259; http://dx.doi.org/10.4049/jimmunol.1100478
30. Riquelme MA, Cea LA, Vega JL, Boric MP, Monyer H, Bennett MV, Frank M, Willecke K, Sáez JC. The ATP required for potentiation of skeletal muscle contraction is released via pannexin hemichannels. Neuropharmacology 2013; 75:594-603; PMID:23583931; http://dx.doi.org/10.1016/j.neuropharm.2013.03.022
31. Peñuela S, Bhalla R, Nag K, Laird DW. Glycosylation regulates pannexin intermixing and cellular localization. Mol Biol Cell 2009; 20:4313-23; PMID:19692571; http://dx.doi.org/10.1091/mbc.E09-01-0067
32. Li S, Tomic M, Stojilkovic SS. Characterization of novel Pannexin 1 isoforms from rat pituitary cells and their association with ATP-gated P2X channels. Gen Comp Endocrinol 2011; 174:202-10; PMID:21907716; http://dx.doi.org/10.1016/j.ygcen.2011.08.019
33. Ambrosi C, Gassmann O, Pranskevich JN, Boassa D, Smock A, Wang J, Dahl G, Steinem C, Sosinsky GE. Pannexin1 and Pannexin2 channels show quaternary similarities to connexons and different oligomerization numbers from each other. J Biol Chem 2010; 285:24420-31; PMID:20516070; http://dx.doi.org/10.1074/jbc. M110.115444
34. Swayne LA, Sorbara CD, Bennett SA. Pannexin 2 is expressed by postnatal hippocampal neural progenitors and modulates neuronal commitment. J Biol Chem 2010; 285:24977-86; PMID:20529862; http://dx.doi.org/10.1074/jbc.M110.130054
35. Schalper KA, Palacios-Prado N, Orellana JA, Sáez JC. Currently used methods for identification and characterization of hemichannels. Cell Commun Adhes 2008; 15:207-18; PMID:18649191; http://dx.doi.org/10.1080/ 15419060802014198
36. Silverman W, Locovei S, Dahl G. Probenecid, a gout remedy, inhibits pannexin 1 channels. Am J Physiol Cell Physiol 2008; 295:C761-7; PMID:18596212; http://dx.doi.org/10.1152/ajpcell.00227.2008
37. Bopp T, Becker C, Klein M, Klein-Hessling S, Palmetshofer A, Serfling E, Heib V, Becker M, Kubach J, Schmitt S, et al. Cyclic adenosine monophosphate is a key component of regulatory T cell-mediated suppression. J Exp Med 2007; 204:1303-10; PMID:17502663; http://dx.doi.org/10.1084/jem.20062129
38. Elgueta R, Tobar JA, Shoji KF, De Calisto J, Kalergis AM, Bono MR, Rosemblatt M, Sáez JC. Gap junctions at the dendritic cell-T cell interface are key elements for antigen-dependent T cell activation. J Immunol 2009; 183:277-84; PMID:19542439; http://dx.doi.org/10.4049/jimmunol.0801854
39. Oviedo-Orta E, Errington RJ, Evans WH. Gap junction intercellular communication during lymphocyte transendothelial migration. Cell Biol Int 2002; 26:253-63; PMID:11991653; http://dx.doi.org/10.1006/cbir.2001.0840
40. Bermudez-Fajardo A, Ylihärsilä M, Evans WH, Newby AC, Oviedo-Orta E. CD4+ T lymphocyte subsets express connexin 43 and establish gap junction channel communication with macrophages in vitro. J Leukoc Biol 2007; 82:608-12; PMID:17596336; http://dx.doi.org/10.1189/jlb.0307134
41. Chused TM, Apasov S, Sitkovsky M. Murine T lymphocytes modulate activity of an ATP-activated P2Z-type purinoceptor during differentiation. J Immunol 1996; 157:1371-80; PMID:8759716
42. Aswad F, Kawamura H, Dennert G. High sensitivity of CD4+CD25+ regulatory T cells to extracellular metabolites nicotinamide adenine dinucleotide and ATP: a role for P2X7 receptors. J Immunol 2005; 175:3075-83; PMID:16116196
43. Vanden Abeele F, Bidaux G, Gordienko D, Beck B, Panchin YV, Baranova AV, Ivanov DV, Skryma R, Prevarskaya N. Functional implications of calcium permeability of the channel formed by pannexin 1. J Cell Biol 2006; 174:535-46; PMID:16908669; http://dx.doi.org/10.1083/jcb.200601115
44. Schanne FA, Kane AB, Young EE, Farber JL. Calcium dependence of toxic cell death: a final common pathway. Science 1979; 206:700-2; PMID:386513; http://dx.doi.org/10.1126/science.386513
45. Peñuela S, Bhalla R, Gong XQ, Cowan KN, Celetti SJ, Cowan BJ, Bai D, Shao Q, Laird DW. Pannexin 1 and pannexin 3 are glycoproteins that exhibit many distinct characteristics from the connexin family of gap junction proteins. J Cell Sci 2007; 120:3772-83; PMID:17925379; http://dx.doi.org/10.1242/jcs. 009514
46. Peñuela S, Celetti SJ, Bhalla R, Shao Q, Laird DW. Diverse subcellular distribution profiles of pannexin 1 and pannexin 3. Cell Commun Adhes 2008; 15:133-42; PMID:18649185; http://dx.doi.org/10.1080/ 15419060802014115
47. Baranova A, Ivanov D, Petrash N, Pestova A, Skoblov M, Kelmanson I, Shagin D, Nazarenko S, Geraymovych E, Litvin O, et al. The mammalian pannexin family is homologous to the invertebrate innexin gap junction proteins. Genomics 2004; 83:706-16; PMID:15028292; http://dx.doi.org/10.1016/j.ygeno.2003.09.025
48. Buvinic S, Almarza G, Bustamante M, Casas M, López J, Riquelme M, Sáez JC, Huidobro-Toro JP, Jaimovich E. ATP released by electrical stimuli elicits calcium transients and gene expression in skeletal muscle. J Biol Chem 2009; 284:34490-505; PMID:19822518; http://dx.doi.org/10.1074/jbc. M109.057315
49. Ransford GA, Fregien N, Qiu F, Dahl G, Conner GE, Salathe M. Pannexin 1 contributes to ATP release in airway epithelia. Am J Respir Cell Mol Biol 2009; 41:525-34; PMID:19213873; http://dx.doi.org/10.1165/rcmb.2008-0367OC
50. Bao L, Locovei S, Dahl G. Pannexin membrane channels are mechanosensitive conduits for ATP. FEBS Lett 2004; 572:65-8; PMID:15304325; http://dx.doi.org/ 10.1016/j.febslet.2004.07.009
51. Locovei S, Wang J, Dahl G. Activation of pannexin 1 channels by ATP through P2Y receptors and by cytoplasmic calcium. FEBS Lett 2006; 580:239-44; PMID:16364313; http://dx.doi.org/10.1016/j.febslet.2005.12.004
52. Bennett MV, Contreras JE, Bukauskas FF, Sáez JC. New roles for astrocytes: gap junction hemichannels have something to communicate. Trends Neurosci 2003; 26:610-7; PMID:14585601; http://dx.doi.org/10.1016/j.tins.2003. 09.008
53. Thompson RJ, Macvicar BA. Connexin and pannexin hemichannels of neurons and astrocytes. Channels (Austin) 2008; 2:81-6; PMID:18849665; http://dx.doi.org/10.4161/chan.2.2.6003
54. Bunse S, Locovei S, Schmidt M, Qiu F, Zoidl G, Dahl G, Dermietzel R. The potassium channel subunit Kvbeta3 interacts with pannexin 1 and attenuates its sensitivity to changes in redox potentials. FEBS J 2009; 276:6258-70; PMID:19780818; http://dx.doi.org/10.1111/j.1742-4658.2009.07334.x
55. Thompson RJ, Jackson MF, Olah ME, Rungta RL, Hines DJ, Beazely MA, MacDonald JF, MacVicar BA. Activation of pannexin-1 hemichannels augments aberrant bursting in the hippocampus. Science 2008; 322:1555-9; PMID:19056988; http://dx.doi.org/10.1126/science.1165209
56. Orellana JA, Shoji KF, Abudara V, Ezan P, Amigou E, Sáez PJ, Jiang JX, Naus CC, Sáez JC, Giaume C. Amyloid β-induced death in neurons involves glial and neuronal hemichannels. J Neurosci 2011; 31:4962-77; PMID:21451035; http://dx.doi.org/10.1523/JNEUROSCI.6417-10.2011
57. Oviedo-Orta E, Hoy T, Evans WH. Intercellular communication in the immune system: differential expression of connexin40 and 43, and perturbation of gap junction channel functions in peripheral blood and tonsil human lymphocyte subpopulations. Immunology 2000; 99:578-90; PMID:10792506; http://dx.doi.org/10. 1046/j.1365-2567.2000.00991.x
58. Sánchez HA, Orellana JA, Verselis VK, Sáez JC. Metabolic inhibition increases activity of connexin-32 hemichannels permeable to Ca2+ in transfected HeLa cells. Am J Physiol Cell Physiol 2009; 297:C665-78; PMID:19587218; http://dx.doi.org/10.1152/ajpcell.00200.2009
59. Schalper KA, Sánchez HA, Lee SC, Altenberg GA, Nathanson MH, Sáez JC. Connexin 43 hemichannels mediate the Ca2+ influx induced by extracellular alkalinization. Am J Physiol Cell Physiol 2010; 299:C1504-15; PMID:20881238; http://dx.doi.org/10.1152/ajpcell.00015.2010
60. Bianchi BR, Lynch KJ, Touma E, Niforatos W, Burgard EC, Alexander KM, Park HS, Yu H, Metzger R, Kowaluk E, et al. Pharmacological characterization of recombinant human and rat P2X receptor subtypes. Eur J Pharmacol 1999; 376:127-38; PMID:10440098; http://dx.doi.org/10.1016/S0014-2999(99)00350-7
61. De Vuyst E, Wang N, Decrock E, De Bock M, Vinken M, Van Moorhem M, Lai C, Culot M, Rogiers V, Cecchelli R, et al. Ca(2+) regulation of connexin 43 hemichannels in C6 glioma and glial cells. Cell Calcium 2009; 46:176-87; PMID:19656565; http://dx.doi.org/10.1016/j.ceca.2009.07.002
62. Ataullakhanov FI, Vitvitsky VM. What determines the intracellular ATP concentration. Biosci Rep 2002; 22:501-11; PMID:12635847; http://dx.doi.org/10. 1023/A:1022069718709
63. Cotrina ML, Lin JH, Alves-Rodrigues A, Liu S, Li J, Azmi-Ghadimi H, Kang J, Naus CC, Nedergaard M. Connexins regulate calcium signaling by controlling ATP release. Proc Natl Acad Sci U S A 1998; 95:15735-40; PMID:9861039; http://dx.doi.org/10.1073/pnas.95.26.15735
64. Corriden R, Insel PA. Basal release of ATP: an autocrine-paracrine mechanism for cell regulation. Sci Signal 2010; 3:re1; PMID:20068232; http://dx.doi.org/10.1126/scisignal.3104re1
65. Hisadome K, Koyama T, Kimura C, Droogmans G, Ito Y, Oike M. Volume-regulated anion channels serve as an auto/paracrine nucleotide release pathway in aortic endothelial cells. J Gen Physiol 2002; 119:511-20; PMID:12034759; http://dx.doi.org/10.1085/jgp.20028540
66. Sabirov RZ, Okada Y. ATP-conducting maxi-anion channel: a new player in stress-sensory transduction. Jpn J Physiol 2004; 54:7-14; PMID:15040843; http://dx.doi.org/10.2170/jjphysiol.54.7
67. Suadicani SO, Brosnan CF, Scemes E. P2X7 receptors mediate ATP release and amplification of astrocytic intercellular Ca2+ signaling. J Neurosci 2006; 26:1378-85; PMID:16452661; http://dx.doi.org/10.1523/JNEUROSCI.3902-05.2006
68. Tokunaga A, Tsukimoto M, Harada H, Moriyama Y, Kojima S. Involvement of SLC17A9-dependent vesicular exocytosis in the mechanism of ATP release during T cell activation. J Biol Chem 2010; 285:17406-16; PMID:20382737; http://dx.doi.org/10.1074/jbc.M110.112417
69. Taruno A, Vingtdeux V, Ohmoto M, Ma Z, Dvoryanchikov G, Li A, Adrien L, Zhao H, Leung S, Abernethy M, et al. CALHM1 ion channel mediates purinergic neurotransmission of sweet, bitter and umami tastes. Nature 2013; 495:223-6; PMID:23467090; http://dx.doi.org/10.1038/nature11906
70. 7 receptor expression in evolutive and indolent forms of chronic B lymphocytic leukemia. Blood 2002; 99:706-8; PMID:11781259; http://dx.doi.org/10.1182/blood.V99.2.706
71. Wiley JS, Dao-Ung LP, Gu BJ, Sluyter R, Shemon AN, Li C, Taper J, Gallo J, Manoharan A. A loss-of-function polymorphic mutation in the cytolytic P2X7 receptor gene and chronic lymphocytic leukaemia: a molecular study. Lancet 2002; 359:1114-9; PMID:11943260; http://dx.doi.org/10.1016/S0140-6736(02)08156-4
72. Paneesha S, Starczynski J, Pepper C, Delgado J, Hooper L, Fegan C, Pratt G. The P2X7 receptor gene polymorphism 1513 A - >C has no effect on clinical prognostic markers and survival in multiple myeloma. Leuk Lymphoma 2006; 47:281-4; PMID:16321858; http://dx.doi.org/10.1080/10428190500305901
73. 7 polymorphism and chronic lymphocytic leukaemia: lack of correlation with incidence, survival and abnormalities of chromosome 12. Leukemia 2003; 17:2097-100; PMID:12931211; http://dx.doi.org/10. 1038/sj.leu.2403125
74. Persechini PM, Bisaggio RC, Alves-Neto JL, Coutinho-Silva R. Extracellular ATP in the lymphohematopoietic system: P2Z purinoceptors off membrane permeabilization. Braz J Med Biol Res 1998; 31:25-34; PMID:9686176; http://dx.doi.org/10.1590/S0100-879X1998000100004
75. Taylor SR, Alexander DR, Cooper JC, Higgins CF, Elliott JI. Regulatory T cells are resistant to apoptosis via TCR but not P2X7. J Immunol 2007; 178:3474-82; PMID:17339442
76. Tsukimoto M, Maehata M, Harada H, Ikari A, Takagi K, Degawa M. P2X7 receptor-dependent cell death is modulated during murine T cell maturation and mediated by dual signaling pathways. J Immunol 2006; 177:2842-50; PMID:16920919
77. Strasser A, Pellegrini M. T-lymphocyte death during shutdown of an immune response. Trends Immunol 2004; 25:610-5; PMID:15489190; http://dx.doi.org/10. 1016/j.it.2004.08.012
78. Brañes MC, Contreras JE, Sáez JC. Activation of human polymorphonuclear cells induces formation of functional gap junctions and expression of connexins. Med Sci Monit 2002; 8:BR313-23; PMID:12165735
79. Yaffe D, Saxel O. A myogenic cell line with altered serum requirements for differentiation. Differentiation 1977; 7:159-66; PMID:558123; http://dx.doi.org/10.1111/j.1432-0436.1977.tb01507.x
80. Wang XH, Streeter M, Liu YP, Zhao HB. 4 Identification and characterization of pannexin expression in the mammalian cochlea. J Comp Neurol 2009; 512:336-46; PMID:19009624; http://dx.doi.org/10.1002/cne.21898
81. Anselmi F, Hernandez VH, Crispino G, Seydel A, Ortolano S, Roper SD, Kessaris N, Richardson W, Rickheit G, Filippov MA, et al. ATP release through connexin hemichannels and gap junction transfer of second messengers propagate Ca2+ signals across the inner ear. Proc Natl Acad Sci U S A 2008; 105:18770-5; PMID:19047635; http://dx.doi.org/10.1073/pnas.0800793105
82. Bargiotas P, Krenz A, Hormuzdi SG, Ridder DA, Herb A, Barakat W, Peñuela S, von Engelhardt J, Monyer H, Schwaninger M. Pannexins in ischemia-induced neurodegeneration. Proc Natl Acad Sci U S A 2011; 108:20772-7; PMID:22147915; http://dx.doi.org/10.1073/pnas.1018262108