The pannexins: Past and present

Frontiers in Physiology

Volumn 5 FEB, Issue , 2014, Pages

  Bond, Stephen R ^a,b   Naus, Christian C ^b  

^a NATIONAL HUMAN GENOME RESEARCH INSTITUTE   (United States)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Biochemistry; Distribution; Gating; Pannexin; Panx1; Panx2; Panx3; Structure

Indexed keywords

GAP JUNCTION PROTEIN; INNEXIN; PANNEXIN; PANNEXIN 1; PANNEXIN 2; PANNEXIN 3; PURINERGIC P2X RECEPTOR; PURINERGIC P2X3 RECEPTOR; PURINERGIC P2X4 RECEPTOR; PURINERGIC P2X7 RECEPTOR; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; BLADDER; BLOOD VESSEL TONE; BONE; BRAIN; CALCIUM SIGNALING; CARBOXY TERMINAL SEQUENCE; CARDIOVASCULAR SYSTEM; CELL CYCLE; CELL MOTILITY; CELL STRUCTURE; CHANNEL GATING; EAR; ELECTRON MICROSCOPY; EYE; GASTROINTESTINAL GLAND; GENITAL SYSTEM; HEART MUSCLE; HYDROSTATIC PRESSURE; IMMUNE SYSTEM; IMMUNITY; IMMUNOPRECIPITATION; INFLAMMATION; INNATE IMMUNITY; ISCHEMIA; KIDNEY; LUNG; NEOPLASM; NONHUMAN; OLIGOMERIZATION; PROTEIN ANALYSIS; PROTEIN CLEAVAGE; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN MODIFICATION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; PROTEIN SECONDARY STRUCTURE; PROTEIN STRUCTURE; PROTEIN TRANSPORT; REVIEW; SEIZURE; SIGNAL TRANSDUCTION; SKELETAL MUSCLE; SKIN; TONGUE; VISION;

EID: 84895452535     PISSN: None     EISSN: 1664042X     Source Type: Journal    
DOI: 10.3389/fphys.2014.00058     Document Type: Review

References (264)

1. Abascal, F., and Zardoya, R. (2012). LRRC8 proteins share a common ancestor with pannexins, and may form hexameric channels involved in cell-cell communication. Bioessays 37, 551-560. doi: 10.1002/bies.201100173.
2. Abascal, F., and Zardoya, R. (2013). Evolutionary analyses of gap junction protein families. Biochim. Biophys. Acta 1828, 4-14. doi: 10.1016/j.bbamem.2012.02.007.
3. Adamczak, S. E., de Rivero Vaccari, J. P., Dale, G., Brand Iii, F. J., Nonner, D., Bullock, M., et al. (2014). Pyroptotic neuronal cell death mediated by the AIM2 inflammasome. J. Cereb. Blood Flow Metab. doi: 10.1038/jcbfm.2013.236. [Epub ahead of print].
4. Alberto, A. V. P., Faria, R. X., Couto, C. G. C., Ferreira, L. G. B., Souza, C. A. M., Teixeira, P. C. N., et al. (2013). Is pannexin the pore associated with the P2X7 receptor? Naunyn Schmiedebergs Arch. Pharmacol. 386, 775-787. doi: 10.1007/s00210-013-0868-x.
5. Altun, Z. F., Chen, B., Wang, Z. W., and Hall, D. H. (2009). High resolution map of Caenorhabditis elegans gap junction proteins. Dev. Dyn. 238, 1936-1950. doi: 10.1002/dvdy.22025.
6. Ambrosi, C., Gassmann, O., Pranskevich, J. N., Boassa, D., Smock, A., Wang, J., et al. (2010). Pannexin1 and Pannexin2 channels show quaternary similarities to connexons and different oligomerization numbers from each other. J. Biol. Chem. 285, 24420-24431. doi: 10.1074/jbc.M110.115444.
7. Anselmi, F., Hernandez, V. H., Crispino, G., Seydel, A., Ortolano, S., Roper, S. D., et al. (2008). 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. 105, 18770-18775. doi: 10.1073/pnas.0800793105.
8. Bao, B. A., Lai, C. P., Naus, C. C., and Morgan, J. R. (2012). Pannexin1 drives multicellular aggregate compaction via a signaling cascade that remodels the actin cytoskeleton. J. Biol. Chem. 287, 8407-8416. doi: 10.1074/jbc.M111.306522.
9. Bao, L., Locovei, S., and Dahl, G. (2004). Pannexin membrane channels are mechanosensitive conduits for ATP. FEBS Lett. 572, 65-68. doi: 10.1016/j.febslet.2004.07.009.
10. Bao, L., Samuels, S., Locovei, S., Macagno, E. R., Muller, K. J., and Dahl, G. (2007). Innexins form two types of channels. FEBS Lett. 581, 5703-5708. doi: 10.1016/j.febslet.2007.11.030.
11. Bao, Y., Chen, Y., Ledderose, C., Li, L., and Junger, W. G. (2013). 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. 288, 22650-22657. doi: 10.1074/jbc.M113.476283.
12. Baranova, A., Ivanov, D., Petrash, N., Pestova, A., Skoblov, M., Kelmanson, I., et al. (2004). The mammalian pannexin family is homologous to the invertebrate innexin gap junction proteins. Genomics 83, 706-716. doi: 10.1016/j.ygeno.2003.09.025.
13. Barbe, M. T., Monyer, H., and Bruzzone, R. (2006). Cell-cell communication beyond connexins: the pannexin channels. Physiology (Bethesda) 21, 103-114. doi: 10.1152/physiol.00048.2005.
14. Bargiotas, P., Krenz, A., Hormuzdi, S. G., Ridder, D. A., Herb, A., Barakat, W., et al. (2011). Pannexins in ischemia-induced neurodegeneration. Proc. Natl. Acad. Sci. U.S.A. 108, 20772-20777. doi: 10.1073/pnas.1018262108.
15. Bargiotas, P., Krenz, A., Monyer, H., and Schwaninger, M. (2012). Functional outcome of pannexin-deficient mice after cerebral ischemia. Channels (Austin) 6, 453-456. doi: 10.4161/chan.22315.
16. Barnes, T. M. (1994). OPUS: a growing family of gap junction proteins? Trends Genet. 10, 303-305. doi: 10.1016/0168-9525(94)90023-X.
17. Barnes, T. M., and Hekimi, S. (1997). The Caenorhabditis elegans avermectin resistance and anesthetic response gene unc-9 encodes a member of a protein family implicated in electrical coupling of excitable cells. J. Neurochem. 69, 2251-2260. doi: 10.1046/j.1471-4159.1997.69062251.x.
18. Bauer, R., Löer, B., Ostrowski, K., Martini, J., Weimbs, A., Lechner, H., et al. (2005). Intercellular communication: the Drosophila innexin multiprotein family of gap junction proteins. Chem. Biol. 12, 515-526. doi: 10.1016/j.chembiol.2005.02.013.
19. Bennett, M. V., Aljure, E., Nakajima, Y., and Pappas, G. D. (1963). Electrotonic junctions between teleost spinal neurons: electrophysiology and ultrastructure. Science 141, 262-264. doi: 10.1126/science.141.3577.262.
20. Bhalla-Gehi, R., Penuela, S., Churko, J. M., Shao, Q., and Laird, D. W. (2010). Pannexin1 and pannexin3 delivery, cell surface dynamics, and cytoskeletal interactions. J. Biol. Chem. 285, 9147-9160. doi: 10.1074/jbc.M109.082008.
21. Billaud, M., Lohman, A. W., Straub, A. C., Looft-Wilson, R., Johnstone, S. R., Araj, C. A., et al. (2011). Pannexin1 regulates alpha1-adrenergic receptor-mediated vasoconstriction. Circ. Res. 109, 80-85. doi: 10.1161/CIRCRESAHA.110.237594.
22. Boassa, D., Ambrosi, C., Qiu, F., Dahl, G., Gaietta, G., and Sosinsky, G. (2007). Pannexin1 channels contain a glycosylation site that targets the hexamer to the plasma membrane. J. Biol. Chem. 282, 31733-31743. doi: 10.1074/jbc.M702422200.
23. Boassa, D., Qiu, F., Dahl, G., and Sosinsky, G. (2008). Trafficking dynamics of glycosylated pannexin 1 proteins. Cell Commun. Adhes. 15, 119-132. doi: 10.1080/15419060802013885.
24. Bond, S. R. (2012). Functional Analysis of Pannexin 3 During Mammalian and Avian Osteogenesis, and the Physiology of Pannexin 1 Ohnologs in Teleost Fish. Doctoral dissertation, University of British Columbia. Vancouver, BC. Available online at: http://hdl.handle.net/2429/43759.
25. Bond, S. R., Lau, A., Penuela, S., Sampaio, A. V., Underhill, T. M., Laird, D. W., et al. (2011). Pannexin 3 is a novel target for Runx2, expressed by osteoblasts and mature growth plate chondrocytes. J. Bone Miner. Res. 26, 2911-2922. doi: 10.1002/jbmr.509.
26. Bond, S. R., Wang, N., Leybaert, L., and Naus, C. C. (2012). Pannexin 1 ohnologs in the teleost lineage. J. Membr. Biol. 245, 483-493. doi: 10.1007/s00232-012-9497-4.
27. Brough, D., Pelegrin, P., and Rothwell, N. J. (2009). Pannexin-1-dependent caspase-1 activation and secretion of IL-1beta is regulated by zinc. Eur. J. Immunol. 39, 352-358. doi: 10.1002/eji.200838843.
28. Bruzzone, R., Barbe, M. T., Jakob, N. J., and Monyer, H. (2005). Pharmacological properties of homomeric and heteromeric pannexin hemichannels expressed in Xenopus oocytes. J. Neurochem. 92, 1033-1043. doi: 10.1111/j.1471-4159.2004.02947.x.
29. Bruzzone, R., Hormuzdi, S. G., Barbe, M. T., Herb, A., and Monyer, H. (2003). Pannexins, a family of gap junction proteins expressed in brain. Proc. Natl. Acad. Sci. U.S.A. 100, 13644-13649. doi: 10.1073/pnas.2233464100.
30. Bunse, S., Haghika, A., Zoidl, G., and Dermietzel, R. (2005). Identification of a potential regulator of the gap junction protein pannexin1. Cell Commun. Adhes. 12, 231-236. doi: 10.1080/15419060500511834.
31. Bunse, S., Locovei, S., Schmidt, M., Qiu, F., Zoidl, G., Dahl, G., et al. (2009). The potassium channel subunit Kvbeta3 interacts with pannexin 1 and attenuates its sensitivity to changes in redox potentials. FEBS J. 276, 6258-6270. doi: 10.1111/j.1742-4658.2009.07334.x.
32. Bunse, S., Schmidt, M., Hoffmann, S., Engelhardt, K., Zoidl, G., and Dermietzel, R. (2011). Single cysteines in the extracellular and transmembrane regions modulate pannexin 1 channel function. J. Membr. Biol. 244, 21-33. doi: 10.1007/s00232-011-9393-3.
33. Bunse, S., Schmidt, M., Prochnow, N., Zoidl, G., and Dermietzel, R. (2010). Intracellular cysteine 346 is essentially involved in regulating Panx1 channel activity. J. Biol. Chem. 285, 38444-38452. doi: 10.1074/jbc.M110.101014.
34. Burns, A. R., Phillips, S. C., and Sokoya, E. M. (2012). Pannexin protein expression in the rat middle cerebral artery. J. Vasc. Res. 49, 101-110. doi: 10.1159/000332329.
35. Burnstock, G. (2010). Control of vascular tone by purines and pyrimidines. Br. J. Pharmacol. 161, 527-529. doi: 10.1111/j.1476-5381.2010.00937.x.
36. Buvinic, S., Almarza, G., Bustamante, M., Casas, M., Lopez, J., Riquelme, M., et al. (2009). ATP released by electrical stimuli elicits calcium transients and gene expression in skeletal muscle. J. Biol. Chem. 284, 34490-34505. doi: 10.1074/jbc.M109.057315.
37. Campanucci, V. A., Dookhoo, L., Vollmer, C., and Nurse, C. A. (2012). Modulation of the carotid body sensory discharge by NO: an up-dated hypothesis. Respir. Physiol. Neurobiol. 184, 149-157. doi: 10.1016/j.resp.2012.04.005.
38. Cea, L. A., Cisterna, B. A., Puebla, C., Frank, M., Figueroa, X. F., Cardozo, C., et al. (2013). De novo expression of connexin hemichannels in denervated fast skeletal muscles leads to atrophy. Proc. Natl. Acad. Sci. U.S.A. 110, 16229-16234. doi: 10.1073/pnas.1312331110.
39. Cea, L. A., Riquelme, M. A., Cisterna, B. A., Puebla, C., Vega, J. L., Rovegno, M., et al. (2012). Connexin-and pannexin-based channels in normal skeletal muscles and their possible role in muscle atrophy. J. Membr. Biol. 245, 423-436. doi: 10.1007/s00232-012-9485-8.
40. Celetti, S. J., Cowan, K. N., Penuela, S., Shao, Q., Churko, J., and Laird, D. W. (2010). Implications of pannexin 1 and pannexin 3 for keratinocyte differentiation. J. Cell Sci. 123, 1363-1372. doi: 10.1242/jcs.056093.
41. Chekeni, F. B., Elliott, M. R., Sandilos, J. K., Walk, S. F., Kinchen, J. M., Lazarowski, E. R., et al. (2010). Pannexin 1 channels mediate "find-me" signal release and membrane permeability during apoptosis. Nature 467, 863-867. doi: 10.1038/nature09413.
42. Chen, V. C., Kristensen, A. R., Foster, L. J., and Naus, C. C. (2012). Association of connexin43 with E3 ubiquitin ligase TRIM21 reveals a mechanism for gap junction phosphodegron control. J. Proteome Res. 11, 6134-6146. doi: 10.1021/pr300790h.
43. Chen, Y., Yao, Y., Sumi, Y., Li, A., To, U. K., Elkhal, A., et al. (2010). Purinergic signaling: a fundamental mechanism in neutrophil activation. Sci. Signal. 3, ra45. doi: 10.1126/scisignal.2000549.
44. Cone, A. C., Ambrosi, C., Scemes, E., Martone, M. E., and Sosinsky, G. E. (2013). A comparative antibody analysis of pannexin1 expression in four rat brain regions reveals varying subcellular localizations. Front. Pharmacol. 4:6. doi: 10.3389/fphar.2013.00006.
45. Cornell-Bell, A. H., Finkbeiner, S. M., Cooper, M. S., and Smith, S. J. (1990). Glutamate induces calcium waves in cultured astrocytes: long-range glial signaling. Science 247, 470-473. doi: 10.1126/science.1967852.
46. Cowan, K. N., Langlois, S., Penuela, S., Cowan, B. J., and Laird, D. W. (2012). Pannexin1 and Pannexin3 exhibit distinct localization patterns in human skin appendages and are regulated during keratinocyte differentiation and carcinogenesis. Cell Commun. Adhes. 19, 45-53. doi: 10.3109/15419061.2012.712575.
47. Cruikshank, S. J., Hopperstad, M., Younger, M., Connors, B. W., Spray, D. C., and Srinivas, M. (2004). Potent block of Cx36 and Cx50 gap junction channels by mefloquine. Proc. Natl. Acad. Sci. U.S.A. 101, 12364-12369. doi: 10.1073/pnas.0402044101.
48. Csak, T., Ganz, M., Pespisa, J., Kodys, K., Dolganiuc, A., and Szabo, G. (2011). Fatty acid and endotoxin activate inflammasomes in mouse hepatocytes that release danger signals to stimulate immune cells. Hepatology 54, 133-144. doi: 10.1002/hep.24341.
49. Dahl, G. (2007). Gap junction-mimetic peptides do work, but in unexpected ways. Cell Commun. Adhes. 14, 259-264. doi: 10.1080/15419060801891018.
50. Dahl, G., and Harris, A. L. (2009). "Pannexins or Connexins?," in Connexins: A Guide, ed A. L. Harris and D. Locke (New York, NY: Humana Press), 287-301. doi: 10.1007/978-1-59745-489-6_12.
51. Dahl, G., and Locovei, S. (2006). Pannexin: to gap or not to gap, is that a question? IUBMB Life 58, 409-419. doi: 10.1080/15216540600794526.
52. Dahl, G., Qiu, F., and Wang, J. (2013). The bizarre pharmacology of the ATP release channel pannexin1. Neuropharmacology 75, 583-593. doi: 10.1016/j.neuropharm.2013.02.019.
53. Dale, H. H., Feldberg, W., and Vogt, M. (1936). Release of acetylcholine at voluntary motor nerve endings. J. Physiol. 86, 353-380.
54. Dando, R., and Roper, S. D. (2009). Cell-to-cell communication in intact taste buds through ATP signalling from pannexin 1 gap junction hemichannels. J. Physiol. 587, 5899-5906. doi: 10.1113/jphysiol.2009.180083.
55. Davidson, J. S., Baumgarten, I. M., and Harley, E. H. (1986). Reversible inhibition of intercellular junctional communication by glycyrrhetinic acid. Biochem. Biophys. Res. Commun. 134, 29-36. doi: 10.1016/0006-291X(86)90522-X.
56. de Rivero Vaccari, J. P., Lotocki, G., Alonso, O. F., Bramlett, H. M., Dietrich, W. D., and Keane, R. W. (2009). Therapeutic neutralization of the NLRP1 inflammasome reduces the innate immune response and improves histopathology after traumatic brain injury. J. Cereb. Blood Flow Metab. 29, 1251-1261. doi: 10.1038/jcbfm.2009.46.
57. DePriest, A., Phelan, P., and Martha Skerrett, I. (2011). Tryptophan scanning mutagenesis of the first transmembrane domain of the innexin Shaking-B(Lethal). Biophys. J. 101, 2408-2416. doi: 10.1016/j.bpj.2011.10.004.
58. Diezmos, E. F., Sandow, S. L., Markus, I., Shevy Perera, D., Lubowski, D. Z., King, D. W., et al. (2013). Expression and localization of pannexin-1 hemichannels in human colon in health and disease. Neurogastroenterol. Motil. 25, e395-e405. doi: 10.1111/nmo.12130.
59. Dolmatova, E., Spagnol, G., Boassa, D., Baum, J. R., Keith, K., Ambrosi, C., et al. (2012). Cardiomyocyte ATP release through pannexin 1 aids in early fibroblast activation. Am. J. Physiol. Heart Circ. Physiol. 303, H1208-H1218. doi: 10.1152/ajpheart.00251.2012.
60. Domercq, M., Perez-Samartin, A., Aparicio, D., Alberdi, E., Pampliega, O., and Matute, C. (2010). P2X7 receptors mediate ischemic damage to oligodendrocytes. Glia 58, 730-740. doi: 10.1002/glia.20958.
61. Donnelly-Roberts, D. L., Namovic, M. T., Han, P., and Jarvis, M. F. (2009). Mammalian P2X7 receptor pharmacology: comparison of recombinant mouse, rat and human P2X7 receptors. Br. J. Pharmacol. 157, 1203-1214. doi: 10.1111/j.1476-5381.2009.00233.x.
62. Dvoriantchikova, G., Ivanov, D., Barakat, D., Grinberg, A., Wen, R., Slepak, V. Z., et al. (2012). Genetic ablation of Pannexin1 protects retinal neurons from ischemic injury. PLoS ONE 7:e31991. doi: 10.1371/journal.pone.0031991.
63. Dvoriantchikova, G., Ivanov, D., Panchin, Y., and Shestopalov, V. I. (2006a). Expression of pannexin family of proteins in the retina. FEBS Lett. 580, 2178-2182. doi: 10.1016/j.febslet.2006.03.026.
64. Dvoriantchikova, G., Ivanov, D., Pestova, A., and Shestopalov, V. (2006b). Molecular characterization of pannexins in the lens. Mol. Vis. 12, 1417-1426. Available online at: http://www.molvis.org/molvis/v12/a160/.
65. Dykes, I. M., Freeman, F. M., Bacon, J. P., and Davies, J. A. (2004). Molecular basis of gap junctional communication in the CNS of the leech Hirudo medicinalis. J. Neurosci. 24, 886-894. doi: 10.1523/JNEUROSCI.3676-03.2004.
66. Eckert, R. (1963). Electrical Interaction of Paired Ganglion Cells in the Leech. J. Gen. Physiol. 46, 573-587. doi: 10.1085/jgp.46.3.573.
67. Finger, T. E., Danilova, V., Barrows, J., Bartel, D. L., Vigers, A. J., Stone, L., et al. (2005). ATP signaling is crucial for communication from taste buds to gustatory nerves. Science 310, 1495-1499. doi: 10.1126/science.1118435.
68. Forsyth, A. M., Wan, J., Owrutsky, P. D., Abkarian, M., and Stone, H. A. (2011). Multiscale approach to link red blood cell dynamics, shear viscosity, and ATP release. Proc. Natl. Acad. Sci. U.S.A. 108, 10986-10991. doi: 10.1073/pnas.1101315108.
69. Fröhlich, F., Bazhenov, M., Iragui-Madoz, V., and Sejnowski, T. J. (2008). Potassium dynamics in the epileptic cortex: new insights on an old topic. Neuroscientist 14, 422-433. doi: 10.1177/1073858408317955.
70. Fukushi, Y. (1999). Heterologous desensitization of muscarinic receptors by P2Z purinoceptors in rat parotid acinar cells. Eur. J. Pharmacol. 364, 55-64. doi: 10.1016/S0014-2999(98)00824-3.
71. Furshpan, E. J., and Potter, D. D. (1959). Transmission at the giant motor synapses of the crayfish. J. Physiol. 145, 289-325.
72. Fushiki, D., Hamada, Y., Yoshimura, R., and Endo, Y. (2010). Phylogenetic and bioinformatic analysis of gap junction-related proteins, innexins, pannexins and connexins. Biomed. Res. 31, 133-142. doi: 10.2220/biomedres.31.133.
73. Ganz, M., Csak, T., Nath, B., and Szabo, G. (2011). Lipopolysaccharide induces and activates the Nalp3 inflammasome in the liver. World J. Gastroenterol. 17, 4772-4778. doi: 10.3748/wjg.v17.i43.4772.
74. Gehi, R., Shao, Q., and Laird, D. W. (2011). Pathways regulating the trafficking and turnover of pannexin1 protein and the role of the C-terminal domain. J. Biol. Chem. 286, 27639-27653. doi: 10.1074/jbc.M111.260711.
75. Godecke, S., Roderigo, C., Rose, C. R., Rauch, B. H., Godecke, A., and Schrader, J. (2012). Thrombin-induced ATP release from human umbilical vein endothelial cells. Am. J. Physiol. Cell Physiol. 302, C915-C923. doi: 10.1152/ajpcell.00283.2010.
76. González, D., Gómez-Hernández, J. M., and Barrio, L. C. (2007). Molecular basis of voltage dependence of connexin channels: an integrative appraisal. Prog. Biophys. Mol. Biol. 94, 66-106. doi: 10.1016/j.pbiomolbio.2007.03.007.
77. Grundken, C., Hanske, J., Wengel, S., Reuter, W., Abdulazim, A., Shestopalov, V. I., et al. (2011). Unified patch clamp protocol for the characterization of Pannexin 1 channels in isolated cells and acute brain slices. J. Neurosci. Methods 199, 15-25. doi: 10.1016/j.jneumeth.2011.04.016.
78. Gulbransen, B. D., Bashashati, M., Hirota, S. A., Gui, X., Roberts, J. A., MacDonald, J. A., et al. (2012). Activation of neuronal P2X7 receptor-pannexin-1 mediates death of enteric neurons during colitis. Nat. Med. 18, 600-604. doi: 10.1038/nm.2679.
79. Guthrie, P. B., Knappenberger, J., Segal, M., Bennett, M. V., Charles, A. C., and Kater, S. B. (1999). ATP released from astrocytes mediates glial calcium waves. J. Neurosci. 19, 520-528.
80. Hanley, P. J., Kronlage, M., Kirschning, C., Del Rey, A., Di Virgilio, F., Leipziger, J., et al. (2012). Transient P2X7 receptor activation triggers macrophage death independent of toll-like receptors 2 and 4, Caspase-1, and Pannexin-1 Proteins. J. Biol. Chem. 287, 10650-10663. doi: 10.1074/jbc.M111.332676.
81. Hanner, F., Lam, L., Nguyen, M. T. X., Yu, A., and Peti-Peterdi, J. (2012). Intrarenal localization of the plasma membrane ATP channel pannexin1. Am. J. Physiol. Renal Physiol. 303, F1454-F1459. doi: 10.1152/ajprenal.00206.2011.
82. Hanstein, R., Negoro, H., Patel, N. K., Charollais, A., Meda, P., Spray, D. C., et al. (2013). Promises and pitfalls of a Pannexin1 transgenic mouse line. Front. Pharmacol. 4:61. doi: 10.3389/fphar.2013.00061.
83. Harris, A. L., and Locke, D. (2008). Connexins: A Guide. 1st Edn. New York, NY: Humana.
84. Hassinger, T. D., Guthrie, P. B., Atkinson, P. B., Bennett, M. V., and Kater, S. B. (1996). An extracellular signaling component in propagation of astrocytic calcium waves. Proc. Natl. Acad. Sci. U.S.A. 93, 13268-13273. doi: 10.1073/pnas.93.23.13268.
85. Hua, V. B., Chang, A. B., Tchieu, J. H., Kumar, N. M., Nielsen, P. A., and Saier, M. H. (2003). Sequence and phylogenetic analyses of 4 TMS junctional proteins of animals: connexins, innexins, claudins and occludins. J. Memb. Biol. 194, 59-76. doi: 10.1007/s00232-003-2026-8.
86. Huang, Y. J., Maruyama, Y., Dvoryanchikov, G., Pereira, E., Chaudhari, N., and Roper, S. D. (2007). The role of pannexin 1 hemichannels in ATP release and cell-cell communication in mouse taste buds. Proc. Natl. Acad. Sci. U.S.A. 104, 6436-6441. doi: 10.1073/pnas.0611280104.
87. Hung, S.-C., Choi, C. H., Said-Sadier, N., Johnson, L., Atanasova, K. R., Sellami, H., et al. (2013). P2X4 Assembles with P2X7 and Pannexin-1 in gingival epithelial cells and modulates ATP-induced reactive oxygen species production and inflammasome activation. PLoS ONE 8:e70210. doi: 10.1371/journal.pone.0070210.
88. Iglesias, R., Dahl, G., Qiu, F., Spray, D. C., and Scemes, E. (2009). Pannexin 1: the molecular substrate of astrocyte "hemichannels." J. Neurosci. 29, 7092-7097. doi: 10.1523/JNEUROSCI.6062-08.2009.
89. Iglesias, R., Locovei, S., Roque, A., Alberto, A. P., Dahl, G., Spray, D. C., et al. (2008). P2X7 receptor-Pannexin1 complex: pharmacology and signaling. Am. J. Physiol. Cell Physiol. 295, C752-C760. doi: 10.1152/ajpcell.00228.2008.
90. Iglesias, R., Spray, D. C., and Scemes, E. (2010). Mefloquine blockade of pannexin1 currents: resolution of a conflict. Cell Commun. Adhes. 16, 131-137. doi: 10.3109/15419061003642618.
91. Iglesias, R. M., and Spray, D. C. (2012). Pannexin1-mediated ATP release provides signal transmission between Neuro2A cells. Neurochem. Res. 37, 1355-1363. doi: 10.1007/s11064-012-0720-6.
92. Ishikawa, M., Iwamoto, T., Nakamura, T., Doyle, A., Fukumoto, S., and Yamada, Y. (2011). Pannexin 3 functions as an ER Ca2+ channel, hemichannel, and gap junction to promote osteoblast differentiation. J. Cell Biol. 193, 1257-1274. doi: 10.1083/jcb.201101050.
93. Islam, M. R., Uramoto, H., Okada, T., Sabirov, R. Z., and Okada, Y. (2012). Maxi-anion channel and pannexin 1 hemichannel constitute separate pathways for swelling-induced ATP release in murine L929 fibrosarcoma cells. Am. J. Physiol. Cell Physiol. 303, C924-C935. doi: 10.1152/ajpcell.00459.2011.
94. Iwabuchi, S., and Kawahara, K. (2011). Functional significance of the negative-feedback regulation of ATP release via pannexin-1 hemichannels under ischemic stress in astrocytes. Neurochem. Int. 58, 376-384. doi: 10.1016/j.neuint.2010.12.013.
95. Iwamoto, T., Nakamura, T., Doyle, A., Ishikawa, M., de Vega, S., Fukumoto, S., et al. (2010). Pannexin 3 regulates intracellular ATP/cAMP levels and promotes chondrocyte differentiation. J. Biol. Chem. 285, 18948-18958. doi: 10.1074/jbc.M110.127027.
96. Jiang, H., Zhu, A. G., Mamczur, M., Falck, J. R., Lerea, K. M., and McGiff, J. C. (2007). Stimulation of rat erythrocyte P2X7 receptor induces the release of epoxyeicosatrienoic acids. Br. J. Pharmacol. 151, 1033-1040. doi: 10.1038/sj.bjp.0707311.
97. Jiang, T., Xu, R. X., Zhang, A. W., Di, W., Xiao, Z. J., Miao, J. Y., et al. (2012). Effects of transcranial direct current stimulation on hemichannel pannexin-1 and neural plasticity in rat model of cerebral infarction. Neuroscience 226, 421-426. doi: 10.1016/j.neuroscience.2012.09.035.
98. Jiang, T., Long, H., Ma, Y., Long, L., Li, Y., Li, F., et al. (2013). Altered expression of pannexin proteins in patients with temporal lobe epilepsy. Mol. Med. Rep. 8, 1801-1806. doi: 10.3892/mmr.2013.1739.
99. Jorquera, G., Altamirano, F., Contreras-Ferrat, A., Almarza, G., Buvinic, S., Jacquemond, V., et al. (2013). Cav1.1 controls frequency-dependent events regulating adult skeletal muscle plasticity. J. Cell Sci. 126, 1189-1198. doi: 10.1242/jcs.116855.
100. Kandarian, B., Sethi, J., Wu, A., Baker, M., Yazdani, N., Kym, E., et al. (2012). The medicinal leech genome encodes 21 innexin genes: different combinations are expressed by identified central neurons. Dev. Genes Evol. 222, 29-44. doi: 10.1007/s00427-011-0387-z.
101. Kanjanamekanant, K., Luckprom, P., and Pavasant, P. (2013). P2X7 receptor-Pannexin1 interaction mediates stress-induced interleukin-1 beta expression in human periodontal ligament cells. J. Periodont. Res. doi: 10.1111/jre.12139. [Epub ahead of print].
102. Kanneganti, T. D., Lamkanfi, M., Kim, Y. G., Chen, G., Park, J. H., Franchi, L., et al. (2007). Pannexin-1-mediated recognition of bacterial molecules activates the cryopyrin inflammasome independent of toll-like receptor signaling. Immunity 26, 433-443. doi: 10.1016/j.immuni.2007.03.008.
103. Karatas, H., Erdener, S. E., Gursoy-Ozdemir, Y., Lule, S., Eren-Koçak, E., Sen, Z. D., et al. (2013). Spreading depression triggers headache by activating neuronal Panx1 channels. Science 339, 1092-1095. doi: 10.1126/science.1231897.
104. Katoh, K., and Standley, D. M. (2013). MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol. Biol. Evol. 30, 772-780. doi: 10.1093/molbev/mst010.
105. Kienitz, M. C., Bender, K., Dermietzel, R., Pott, L., and Zoidl, G. (2011). Pannexin 1 constitutes the large conductance cation channel of cardiac myocytes. J. Biol. Chem. 286, 290-298. doi: 10.1074/jbc.M110.163477.
106. Kim, J. E., and Kang, T. C. (2011). The P2X7 receptor-pannexin-1 complex decreases muscarinic acetylcholine receptor-mediated seizure susceptibility in mice. J. Clin. Invest. 121, 2037-2047. doi: 10.1172/JCI44818.
107. Kranz, K., Dorgau, B., Pottek, M., Herrling, R., Schultz, K., Bolte, P., et al. (2013). Expression of Pannexin1 in the outer plexiform layer of the mouse retina and physiological impact of its knockout. J. Comp. Neurol. 521, 1119-1135. doi: 10.1002/cne.23223.
108. Kronlage, M., Song, J., Sorokin, L., Isfort, K., Schwerdtle, T., Leipziger, J., et al. (2010). Autocrine purinergic receptor signaling is essential for macrophage chemotaxis. Sci. Signal. 3, ra55. doi: 10.1126/scisignal.2000588.
109. Kügelgen, V. I. (2006). Pharmacological profiles of cloned mammalian P2Y-receptor subtypes. Pharmacol. Ther. 110, 415-432. doi: 10.1016/j.pharmthera.2005.08.014.
110. Kumar, N. M., and Gilula, N. B. (1986). Cloning and characterization of human and rat liver cDNAs coding for a gap junction protein. J. Cell Biol. 103, 767-776. doi: 10.1083/jcb.103.3.767.
111. Kurtenbach, S., Prochnow, N., Kurtenbach, S., Klooster, J., Zoidl, C., Dermietzel, R., et al. (2013). Pannexin1 channel proteins in the zebrafish retina have shared and unique properties. PLoS ONE 8:e77722. doi: 10.1371/journal.pone.0077722.
112. Lai, C. P., Bechberger, J. F., and Naus, C. C. (2009). Pannexin2 as a novel growth regulator in C6 glioma cells. Oncogene 28, 4402-4408. doi: 10.1038/onc.2009.283.
113. Lai, C. P., Bechberger, J. F., Thompson, R. J., MacVicar, B. A., Bruzzone, R., and Naus, C. C. (2007). Tumor-suppressive effects of pannexin 1 in C6 glioma cells. Cancer Res. 67, 1545-1554. doi: 10.1158/0008-5472.CAN-06-1396.
114. Lai, P. (2010). The Role of Pannexins, a Novel Gap Junction Family, in Glioma Oncogenicity and Neuronal Differentiation. Doctoral dissertation, University of British Columbia. Vancouver, BC. Available onlie at: http://hdl.handle.net/2429/23502.
115. Lamkanfi, M., Malireddi, R. K. S., and Kanneganti, T.-D. (2009). Fungal zymosan and mannan activate the cryopyrin inflammasome. J. Biol. Chem. 284, 20574-20581. doi: 10.1074/jbc.M109.023689.
116. Landesman, Y., White, T. W., Starich, T. A., Shaw, J. E., Goodenough, D. A., and Paul, D. L. (1999). Innexin-3 forms connexin-like intercellular channels. J. Cell Sci. 112(Pt 14), 2391-2396.
117. Leal Denis, M. F., Incicco, J. J., Espelt, M. V., Verstraeten, S. V., Pignataro, O. P., Lazarowski, E. R., et al. (2013). Kinetics of extracellular ATP in mastoparan 7-activated human erythrocytes. Biochim. Biophys. Acta 1830, 4692-4707. doi: 10.1016/j.bbagen.2013.05.033.
118. Lehmann, C., Lechner, H., Löer, B., Knieps, M., Herrmann, S., Famulok, M., et al. (2006). Heteromerization of innexin gap junction proteins regulates epithelial tissue organization in Drosophila. Mol. Biol. Cell 17, 1676-1685. doi: 10.1091/mbc.E05-11-1059.
119. Lemaire, I., Falzoni, S., Zhang, B., Pellegatti, P., and Di Virgilio, F. (2011). The P2X7 receptor and Pannexin-1 are both required for the promotion of multinucleated macrophages by the inflammatory cytokine GM-CSF. J. Immunol. 187, 3878-3887. doi: 10.4049/jimmunol.1002780.
120. Li, A., Leung, C. T., Peterson-Yantorno, K., Mitchell, C. H., and Civan, M. M. (2010). 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, C1308-C1317. doi: 10.1152/ajpcell.00333.2010.
121. Li, A., Leung, C. T., Peterson-Yantorno, K., Stamer, W. D., Mitchell, C. H., and Civan, M. M. (2012a). Mechanisms of ATP release by human trabecular meshwork cells, the enabling step in purinergic regulation of aqueous humor outflow. J. Cell. Physiol. 227, 172-182. doi: 10.1002/jcp.22715.
122. Li, S., Bjelobaba, I., Yan, Z., Kucka, M., Tomic, M., and Stojilkovic, S. S. (2011a). Expression and roles of pannexins in ATP release in the pituitary gland. Endocrinology 152, 2342-2352. doi: 10.1210/en.2010-1216.
123. Li, S., Tomic, M., and Stojilkovic, S. S. (2011b). Characterization of novel Pannexin 1 isoforms from rat pituitary cells and their association with ATP-gated P2X channels. Gen. Comp. Endocrinol. 174, 202-210. doi: 10.1016/j.ygcen.2011.08.019.
124. Li, Y., Du, X.-F., Liu, C.-S., Wen, Z.-L., and Du, J.-L. (2012b). Reciprocal regulation between resting microglial dynamics and neuronal activity in vivo. Dev. Cell 23, 1189-1202. doi: 10.1016/j.devcel.2012.10.027.
125. Lin, J. H.-C., Takano, T., Arcuino, G., Wang, X., Hu, F., Darzynkiewicz, Z., et al. (2007). Purinergic signaling regulates neural progenitor cell expansion and neurogenesis. Dev. Biol. 302, 356-366. doi: 10.1016/j.ydbio.2006.09.017.
126. Litvin, O., Tiunova, A., Connell-Alberts, Y., Panchin, Y., and Baranova, A. (2006). What is hidden in the pannexin treasure trove: the sneak peek and the guesswork. J. Cell. Mol. Med. 10, 613-634. doi: 10.1111/j.1582-4934.2006.tb00424.x.
127. Liu, H. T., Toychiev, A. H., Takahashi, N., Sabirov, R. Z., and Okada, Y. (2008). Maxi-anion channel as a candidate pathway for osmosensitive ATP release from mouse astrocytes in primary culture. Cell Res. 18, 558-565. doi: 10.1038/cr.2008.49.
128. Locovei, S., Bao, L., and Dahl, G. (2006a). Pannexin 1 in erythrocytes: function without a gap. Proc. Natl. Acad. Sci. U.S.A. 103, 7655-7659. doi: 10.1073/pnas.0601037103.
129. Locovei, S., Scemes, E., Qiu, F., Spray, D. C., and Dahl, G. (2007). Pannexin1 is part of the pore forming unit of the P2X(7) receptor death complex. FEBS Lett. 581, 483-488. doi: 10.1016/j.febslet.2006.12.056.
130. Locovei, S., Wang, J., and Dahl, G. (2006b). Activation of pannexin 1 channels by ATP through P2Y receptors and by cytoplasmic calcium. FEBS Lett. 580, 239-244. doi: 10.1016/j.febslet.2005.12.004.
131. Lohman, A. W., Billaud, M., Straub, A. C., Johnstone, S. R., Best, A. K., Lee, M., et al. (2012a). Expression of pannexin isoforms in the systemic murine arterial network. J. Vasc. Res. 49, 405-416. doi: 10.1159/000338758.
132. Lohman, A. W., Weaver, J. L., Billaud, M., Sandilos, J. K., Griffiths, R., Straub, A. C., et al. (2012b). S-nitrosylation inhibits pannexin 1 channel function. J. Biol. Chem. 287, 39602-39612. doi: 10.1074/jbc.M112.397976.
133. Lutz, S. E., González-Fernández, E., Ventura, J. C. C., Perez-Samartin, A., Tarassishin, L., Negoro, H., et al. (2013). Contribution of pannexin1 to experimental autoimmune encephalomyelitis. PLoS ONE 8:e66657. doi: 10.1371/journal.pone.0066657.
134. Ma, W., Compan, V., Zheng, W., Martin, E., North, R. A., Verkhratsky, A., et al. (2012). Pannexin 1 forms an anion-selective channel. Pflugers Arch. 463, 585-592. doi: 10.1007/s00424-012-1077-z.
135. Ma, W., Hui, H., Pelegrin, P., and Surprenant, A. (2009). Pharmacological characterization of pannexin-1 currents expressed in mammalian cells. J. Pharmacol. Exp. Ther. 328, 409-418. doi: 10.1124/jpet.108.146365.
136. Magie, C. R., and Martindale, M. Q. (2008). Cell-cell adhesion in the cnidaria: insights into the evolution of tissue morphogenesis. Biol. Bull. 214, 218-232. doi: 10.2307/25470665.
137. Marina-Garcia, N., Franchi, L., Kim, Y. G., Miller, D., McDonald, C., Boons, G. J., et al. (2008). Pannexin-1-mediated intracellular delivery of muramyl dipeptide induces caspase-1 activation via Cryopyrin/NLRP3 independently of Nod2. J. Immunol. 180, 4050-4057. Available online at: http://www.jimmunol.org/content/180/6/4050.
138. Martins, I., Wang, Y., Michaud, M., Ma, Y., Sukkurwala, A. Q., Shen, S., et al. (2014). Molecular mechanisms of ATP secretion during immunogenic cell death. Cell Death Differ. 21, 79-91. doi: 10.1038/cdd.2013.75.
139. McKuen, M. J., Dahl, G., and Fields, K. A. (2013). Assessing a potential role of host Pannexin 1 during Chlamydia trachomatis infection. PLoS ONE 8:e63732. doi: 10.1371/journal.pone.0063732.
140. Melhorn, M. I., Brodsky, A. S., Estanislau, J., Khoory, J. A., Illigens, B., Hamachi, I., et al. (2013). CR1-mediated ATP release by human red blood cells promotes CR1 clustering and modulates the immune transfer process. J. Biol. Chem. 288, 31139-31153. doi: 10.1074/jbc.M113.486035.
141. Meng, X.-F., Wang, X.-L., Tian, X.-J., Yang, Z.-H., Chu, G.-P., Zhang, J., et al. (2013). Nod-like receptor protein 1 inflammasome mediates neuron injury under high glucose. Mol. Neurobiol. doi: 10.1007/s12035-013-8551-2. [Epub ahead of print].
142. Minkiewicz, J., de Rivero Vaccari, J. P., and Keane, R. W. (2013). Human astrocytes express a novel NLRP2 inflammasome. Glia 61, 1113-1121. doi: 10.1002/glia.22499.
143. Montalbetti, N., Leal Denis, M. F., Pignataro, O. P., Kobatake, E., Lazarowski, E. R., and Schwarzbaum, P. J. (2011). Homeostasis of extracellular ATP in human erythrocytes. J. Biol. Chem. 286, 38397-38407. doi: 10.1074/jbc.M111.221713.
144. Murata, Y., Yasuo, T., Yoshida, R., Obata, K., Yanagawa, Y., Margolskee, R. F., et al. (2010). Action potential-enhanced ATP release from taste cells through hemichannels. J. Neurophysiol. 104, 896-901. doi: 10.1152/jn.00414.2010.
145. Mylvaganam, S., Zhang, L., Wu, C., Zhang, Z. J., Samoilova, M., Eubanks, J., et al. (2010). Hippocampal seizures alter the expression of the pannexin and connexin transcriptome. J. Neurochem. 112, 92-102. doi: 10.1111/j.1471-4159.2009.06431.x.
146. Nash, M. S., Willets, J. M., Billups, B., John Challiss, R. A., and Nahorski, S. R. (2004). Synaptic activity augments muscarinic acetylcholine receptor-stimulated inositol 1,4,5-trisphosphate production to facilitate Ca2+ release in hippocampal neurons. J. Biol. Chem. 279, 49036-49044. doi: 10.1074/jbc.M407277200.
147. Negoro, H., Lutz, S. E., Liou, L. S., Kanematsu, A., Ogawa, O., Scemes, E., et al. (2013). Pannexin 1 involvement in bladder dysfunction in a multiple sclerosis model. Sci. Rep. 3, 2152. doi: 10.1038/srep02152.
148. Oishi, S., Sasano, T., Tateishi, Y., Tamura, N., Isobe, M., and Furukawa, T. (2012). Stretch of atrial myocytes stimulates recruitment of macrophages via ATP released through gap-junction channels. J. Pharmacol. Sci. 120, 296-304. doi: 10.1254/jphs.12202FP.
149. Orellana, J. A., Froger, N., Ezan, P., Jiang, J. X., Bennett, M. V., Naus, C. C., et al. (2011). ATP and glutamate released via astroglial connexin 43 hemichannels mediate neuronal death through activation of pannexin 1 hemichannels. J. Neurochem. 118, 826-840. doi: 10.1111/j.1471-4159.2011.07210.x.
150. Orellana, J. A., Montero, T. D., and von Bernhardi, R. (2013a). Astrocytes inhibit nitric oxide-dependent Ca(2+) dynamics in activated microglia: involvement of ATP released via pannexin 1 channels. Glia 61, 2023-2037. doi: 10.1002/glia.22573.
151. Orellana, J. A., Velasquez, S., Williams, D. W., Saez, J. C., Berman, J. W., and Eugenin, E. A. (2013b). Pannexin1 hemichannels are critical for HIV infection of human primary CD4+ T lymphocytes. J. Leukoc. Biol. 94, 399-407. doi: 10.1189/jlb.0512249.
152. Oshima, A., Matsuzawa, T., Nishikawa, K., and Fujiyoshi, Y. (2013). Oligomeric structure and functional characterization of Caenorhabditis elegans Innexin-6 gap junction protein. J. Biol. Chem. 288, 10513-10521. doi: 10.1074/jbc.M112.428383.
153. Ostrowski, K., Bauer, R., and Hoch, M. (2008). The Drosophila innexin 7 gap junction protein is required for development of the embryonic nervous system. Cell Commun. Adhes. 15, 155-167. doi: 10.1080/15419060802013976.
154. Panchin, Y., Kelmanson, I., Matz, M., Lukyanov, K., Usman, N., and Lukyanov, S. (2000). A ubiquitous family of putative gap junction molecules. Curr. Biol. 10, R473-R474. doi: 10.1016/S0960-9822(00)00576-5.
155. Panchin, Y. V. (2005). Evolution of gap junction proteins-the pannexin alternative. J. Exp. Biol. 208, 1415-1419. doi: 10.1242/jeb.01547.
156. Paoletti, A., Raza, S. Q., Voisin, L., Law, F., Caillet, M., Martins, I., et al. (2013). Editorial: pannexin-1-the hidden gatekeeper for HIV-1. J. Leukoc. Biol. 94, 390-392. doi: 10.1189/jlb.0313148.
157. Paul, D. L. (1986). Molecular cloning of cDNA for rat liver gap junction protein. J. Cell Biol. 103, 123-134. doi: 10.1083/jcb.103.1.123.
158. Pelegrin, P., Barroso-Gutierrez, C., and Surprenant, A. (2008). P2X7 receptor differentially couples to distinct release pathways for IL-1beta in mouse macrophage. J. Immunol. 180, 7147-7157. Available online at: http://www.jimmunol.org/content/180/11/7147.
159. Pelegrin, P., and Surprenant, A. (2006). Pannexin-1 mediates large pore formation and interleukin-1beta release by the ATP-gated P2X7 receptor. EMBO J. 25, 5071-5082. doi: 10.1038/sj.emboj.7601378.
160. Pelegrin, P., and Surprenant, A. (2007). Pannexin-1 couples to maitotoxin-and nigericin-induced interleukin-1beta release through a dye uptake-independent pathway. J. Biol. Chem. 282, 2386-2394. doi: 10.1074/jbc.M610351200.
161. Penn, R. D. (1966). Ionic communication between liver cells. J. Cell Biol. 29, 171-174. doi: 10.1083/jcb.29.1.171.
162. Penuela, S., Bhalla, R., Gong, X. Q., Cowan, K. N., Celetti, S. J., Cowan, B. J., et al. (2007). Pannexin 1 and pannexin 3 are glycoproteins that exhibit many distinct characteristics from the connexin family of gap junction proteins. J. Cell Sci. 120, 3772-3783. doi: 10.1242/jcs.009514.
163. Penuela, S., Bhalla, R., Nag, K., and Laird, D. W. (2009). Glycosylation regulates pannexin intermixing and cellular localization. Mol. Biol. Cell 20, 4313-4323. doi: 10.1091/mbc.E09-01-0067.
164. Penuela, S., Celetti, S. J., Bhalla, R., Shao, Q., and Laird, D. W. (2008). Diverse subcellular distribution profiles of pannexin 1 and pannexin 3. Cell Commun. Adhes. 15, 133-142. doi: 10.1080/15419060802014115.
165. Penuela, S., Gyenis, L., Ablack, A., Churko, J. M., Berger, A. C., Litchfield, D. W., et al. (2012). Loss of pannexin 1 attenuates melanoma progression by reversion to a melanocytic phenotype. J. Biol. Chem. 287, 29184-29193. doi: 10.1074/jbc.M112.377176.
166. Penuela, S., Lohman, A. W., Lai, W., Gyenis, L., Litchfield, D. W., Isakson, B. E., et al. (2014). Diverse post-translational modifications of the pannexin family of channel-forming proteins. Channels (Austin), 8. doi: 10.4161/chan.27422. [Epub ahead of print].
167. Phelan, P. (2005). Innexins: members of an evolutionarily conserved family of gap-junction proteins. Biochim. Biophys. Acta 1711, 225-245. doi: 10.1016/j.bbamem.2004.10.004.
168. Phelan, P., Bacon, J. P., Davies, J. A., Stebbings, L. A., Todman, M. G., Avery, L., et al. (1998a). Innexins: a family of invertebrate gap-junction proteins. Trends Genet. 14, 348-349. doi: 10.1016/S0168-9525(98)01547-9.
169. Phelan, P., Stebbings, L. A., Baines, R. A., Bacon, J. P., Davies, J. A., and Ford, C. (1998b). Drosophila Shaking-B protein forms gap junctions in paired Xenopus oocytes. Nature 391, 181-184. doi: 10.1038/34426.
170. Pinheiro, A. R., Paramos-de-Carvalho, D., Certal, M., Costa, C., Magalhaes-Cardoso, M. T., Ferreirinha, F., et al. (2013a). Bradykinin-induced Ca2+ signaling in human subcutaneous fibroblasts involves ATP release via hemichannels leading to P2Y12 receptors activation. Cell Commun. Signal 11, 70. doi: 10.1186/1478-811X-11-70.
171. Pinheiro, A. R., Paramos-de-Carvalho, D., Certal, M., Costa, M. A., Costa, C., Magalhaes-Cardoso, M. T., et al. (2013b). Histamine induces ATP release from human subcutaneous fibroblasts, via pannexin-1 hemichannels, leading to Ca2+ mobilization and cell proliferation. J. Biol. Chem. 288, 27571-27583. doi: 10.1074/jbc.M113.460865.
172. Poornima, V., Madhupriya, M., Kootar, S., Sujatha, G., Kumar, A., and Bera, A. K. (2012). P2X7 receptor-pannexin 1 hemichannel association: effect of extracellular calcium on membrane permeabilization. J. Mol. Neurosci. 46, 585-594. doi: 10.1007/s12031-011-9646-8.
173. Prochnow, N., Abdulazim, A., Kurtenbach, S., Wildförster, V., Dvoriantchikova, G., Hanske, J., et al. (2012). Pannexin1 stabilizes synaptic plasticity and is needed for learning. PLoS ONE 7:e51767. doi: 10.1371/journal.pone.0051767.
174. Prochnow, N., Hoffmann, S., Dermietzel, R., and Zoidl, G. (2009a). Replacement of a single cysteine in the fourth transmembrane region of zebrafish pannexin 1 alters hemichannel gating behavior. Exp. Brain Res. 199, 255-264. doi: 10.1007/s00221-009-1957-4.
175. Prochnow, N., Hoffmann, S., Vroman, R., Klooster, J., Bunse, S., Kamermans, M., et al. (2009b). Pannexin1 in the outer retina of the zebrafish, Danio rerio. Neuroscience 162, 1039-1054. doi: 10.1016/j.neuroscience.2009.04.064.
176. Qiao, Y., Wang, P., Qi, J., Zhang, L., and Gao, C. (2012). TLR-induced NF-κ B activation regulates NLRP3 expression in murine macrophages. FEBS Lett. 586, 1022-1026. doi: 10.1016/j.febslet.2012.02.045.
177. Qiu, F., and Dahl, G. P. (2009). A permeant regulating its permeation pore: inhibition of pannexin 1 channels by ATP. Am. J. Physiol. Cell Physiol. 296, C250-C255. doi: 10.1152/ajpcell.00433.2008.
178. Qiu, F., Wang, J., and Dahl, G. (2012). Alanine substitution scanning of pannexin1 reveals amino acid residues mediating ATP sensitivity. Purinergic Signal. 8, 81-90. doi: 10.1007/s11302-011-9263-6.
179. Qiu, F., Wang, J., Spray, D. C., Scemes, E., and Dahl, G. (2011). Two non-vesicular ATP release pathways in the mouse erythrocyte membrane. FEBS Lett. 585, 3430-3435. doi: 10.1016/j.febslet.2011.09.033.
180. Qu, Y., Misaghi, S., Newton, K., Gilmour, L. L., Louie, S., Cupp, J. E., et al. (2011). Pannexin-1 is required for ATP release during apoptosis but not for inflammasome activation. J. Immunol. 189, 6553-6561. doi: 10.4049/jimmunol.1100478.
181. Ransford, G. A., Fregien, N., Qiu, F., Dahl, G., Conner, G. E., and Salathe, M. (2009). Pannexin 1 contributes to ATP release in airway epithelia. Am. J. Respir. Cell Mol. Biol. 41, 525-534. doi: 10.1165/rcmb.2008-0367OC.
182. Ray, A., Zoidl, G., Wahle, P., and Dermietzel, R. (2006). Pannexin expression in the cerebellum. Cerebellum 5, 189-192. doi: 10.1080/14734220500530082.
183. Ray, A., Zoidl, G., Weickert, S., Wahle, P., and Dermietzel, R. (2005). Site-specific and developmental expression of pannexin1 in the mouse nervous system. Eur. J. Neurosci. 21, 3277-3290. doi: 10.1111/j.1460-9568.2005.04139.x.
184. Reigada, D., Lu, W., Zhang, M., and Mitchell, C. H. (2008). Elevated pressure triggers a physiological release of ATP from the retina: possible role for pannexin hemichannels. Neuroscience 157, 396-404. doi: 10.1016/j.neuroscience.2008.08.036.
185. Resta, V., Novelli, E., Vozzi, G., Scarpa, C., Caleo, M., Ahluwalia, A., et al. (2007). Acute retinal ganglion cell injury caused by intraocular pressure spikes is mediated by endogenous extracellular ATP. Eur. J. Neurosci. 25, 2741-2754. doi: 10.1111/j.1460-9568.2007.05528.x.
186. Reyes, J. P., Hernandez-Carballo, C. Y., Perez-Flores, G., Perez-Cornejo, P., and Arreola, J. (2009). Lack of coupling between membrane stretching and pannexin-1 hemichannels. Biochem. Biophys. Res. Commun. 380, 50-53. doi: 10.1016/j.bbrc.2009.01.021.
187. + channels in lung epithelium by ATP release through pannexin and connexin hemichannels. FASEB J. 28, 45-55. doi: 10.1096/fj.13-229252.
188. Rigato, C., Swinnen, N., Buckinx, R., Couillin, I., Mangin, J.-M., Rigo, J.-M., et al. (2012). Microglia proliferation is controlled by P2X7 receptors in a Pannexin-1-Independent manner during early embryonic spinal cord invasion. J. Neurosci. 32, 11559-11573. doi: 10.1523/JNEUROSCI.1042-12.2012.
189. Riquelme, M. A., Cea, L. A., Vega, J. L., Boric, M. P., Monyer, H., Bennett, M. V. L., et al. (2013). The ATP required for potentiation of skeletal muscle contraction is released via pannexin hemichannels. Neuropharmacology 75, 594-603. doi: 10.1016/j.neuropharm.2013.03.022.
190. Romanov, R. A., Bystrova, M. F., Rogachevskaya, O. A., and Kolesnikov, S. S. (2011). Channel activity of recombinant pannexin 1. Biochem. Moscow Suppl. A 5, 343-349. doi: 10.1134/S1990747811050126.
191. Romanov, R. A., Bystrova, M. F., Rogachevskaya, O. A., Sadovnikov, V. B., Shestopalov, V. I., and Kolesnikov, S. S. (2012). The ATP permeability of pannexin 1 channels in a heterologous system and in mammalian taste cells is dispensable. J. Cell Sci. 125, 5514-5523. doi: 10.1242/jcs.111062.
192. Romanov, R. A., Rogachevskaja, O. A., Bystrova, M. F., Jiang, P., Margolskee, R. F., and Kolesnikov, S. S. (2007). Afferent neurotransmission mediated by hemichannels in mammalian taste cells. EMBO J. 26, 657-667. doi: 10.1038/sj.emboj.7601526.
193. Romanov, R. A., Rogachevskaja, O. A., Khokhlov, A. A., and Kolesnikov, S. S. (2008). Voltage dependence of ATP secretion in mammalian taste cells. J. Gen. Physiol. 132, 731-744. doi: 10.1085/jgp.200810108.
194. Samuels, S. E., Lipitz, J. B., Wang, J., Dahl, G., and Muller, K. J. (2013). Arachidonic acid closes innexin/pannexin channels and thereby inhibits microglia cell movement to a nerve injury. Dev. Neurobiol. 73, 621-631. doi: 10.1002/dneu.22088.
195. Sandilos, J. K., Chiu, Y.-H. H., Chekeni, F. B., Armstrong, A. J., Walk, S. F., Ravichandran, K. S., et al. (2012). Pannexin 1, an ATP release channel, is activated by caspase cleavage of its pore-associated C terminal autoinhibitory region. J. Biol. Chem. 287, 11303-11311. doi: 10.1074/jbc.M111.323378.
196. Santiago, M. F., Veliskova, J., Patel, N. K., Lutz, S. E., Caille, D., Charollais, A., et al. (2011). Targeting pannexin1 improves seizure outcome. PLoS ONE 6:e25178. doi: 10.1371/journal.pone.0025178.
197. Scemes, E., and Giaume, C. (2006). Astrocyte calcium waves: what they are and what they do. Glia 54, 716-725. doi: 10.1002/glia.20374.
198. Schenk, U., Westendorf, A. M., Radaelli, E., Casati, A., Ferro, M., Fumagalli, M., et al. (2008). Purinergic control of T cell activation by ATP released through pannexin-1 hemichannels. Sci. Signal. 1, ra6. doi: 10.1126/scisignal.1160583.
199. Schroder, K., and Tschopp, J. (2010). The inflammasomes. Cell 140, 821-832. doi: 10.1016/j.cell.2010.01.040.
200. Seminario-Vidal, L., Okada, S. F., Sesma, J. I., Kreda, S. M., van Heusden, C. A., Zhu, Y., et al. (2011). Rho signaling regulates pannexin 1-mediated ATP release from airway epithelia. J. Biol. Chem. 286, 26277-26286. doi: 10.1074/jbc.M111.260562.
201. Seror, C., Melki, M. T., Subra, F., Raza, S. Q., Bras, M., Saidi, H., et al. (2011). Extracellular ATP acts on P2Y2 purinergic receptors to facilitate HIV-1 infection. J. Exp. Med. 208, 1823-1834. doi: 10.1084/jem.20101805.
202. Shahidullah, M., Mandal, A., Beimgraben, C., and Delamere, N. A. (2012). Hyposmotic stress causes ATP release and stimulates Na,K-ATPase activity in porcine lens. J. Cell. Physiol. 227, 1428-1437. doi: 10.1002/jcp.22858.
203. Siebert, A. P., Ma, Z., Grevet, J. D., Demuro, A., Parker, I., and Foskett, J. K. (2013). Structural and functional similarities of calcium homeostasis modulator 1 (CALHM1) ion channel with connexins, pannexins, and innexins. J. Biol. Chem. 288, 6140-6153. doi: 10.1074/jbc.M112.409789.
204. Silverman, W., Locovei, S., and Dahl, G. (2008). Probenecid, a gout remedy, inhibits pannexin 1 channels. Am. J. Physiol. Cell Physiol. 295, C761-C767. doi: 10.1152/ajpcell.00227.2008.
205. Silverman, W. R., de Rivero Vaccari, J. P., Locovei, S., Qiu, F., Carlsson, S. K., Scemes, E., et al. (2009). The pannexin 1 channel activates the inflammasome in neurons and astrocytes. J. Biol. Chem. 284, 18143-18151. doi: 10.1074/jbc.M109.004804.
206. Skals, M., Jorgensen, N. R., Leipziger, J., and Praetorius, H. A. (2009). Alpha-hemolysin from Escherichia coli uses endogenous amplification through P2X receptor activation to induce hemolysis. Proc. Natl. Acad. Sci. U.S.A. 106, 4030-4035. doi: 10.1073/pnas.0807044106.
207. Skals, M., Leipziger, J., and Praetorius, H. A. (2011). Haemolysis induced by alpha-toxin from Staphylococcus aureus requires P2X receptor activation. Pflugers Arch. 462, 669-679. doi: 10.1007/s00424-011-1010-x.
208. Solan, J. L., and Lampe, P. D. (2009). Connexin43 phosphorylation: structural changes and biological effects. Biochem. J. 419, 261-272. doi: 10.1042/BJ20082319.
209. Solle, M., Labasi, J., Perregaux, D. G., Stam, E., Petrushova, N., Koller, B. H., et al. (2001). Altered cytokine production in mice lacking P2X(7) receptors. J. Biol. Chem. 276, 125-132. doi: 10.1074/jbc.M006781200.
210. Sorge, R. E., Trang, T., Dorfman, R., Smith, S. B., Beggs, S., Ritchie, J., et al. (2012). Genetically determined P2X7 receptor pore formation regulates variability in chronic pain sensitivity. Nat. Med. 18, 595-599. doi: 10.1038/nm.2710.
211. Sosinsky, G. E., Boassa, D., Dermietzel, R., Duffy, H. S., Laird, D. W., Macvicar, B., et al. (2011). Pannexin channels are not gap junction hemichannels. Channels (Austin). 5, 193-197. doi: 10.4161/chan.5.3.15765.
212. Sridharan, M., Adderley, S. P., Bowles, E. A., Egan, T. M., Stephenson, A. H., Ellsworth, M. L., et al. (2010). Pannexin 1 is the conduit for low oxygen tension-induced ATP release from human erythrocytes. Am. J. Physiol. Heart Circ. Physiol. 299, H1146-H1152. doi: 10.1152/ajpheart.00301.2010.
213. Sridharan, M., Bowles, E. A., Richards, J. P., Krantic, M., Davis, K. L., Dietrich, K. A., et al. (2012). Prostacyclin receptor-mediated ATP release from erythrocytes requires the voltage-dependent anion channel. Am. J. Physiol. Heart Circ. Physiol. 302, H553-H559. doi: 10.1152/ajpheart.00998.2011.
214. Starich, T. A., Herman, R. K., and Shaw, J. E. (1993). Molecular and genetic analysis of unc-7, a Caenorhabditis elegans gene required for coordinated locomotion. Genetics 133, 527-541.
215. Starich, T. A., Lee, R. Y., Panzarella, C., Avery, L., and Shaw, J. E. (1996). eat-5 and unc-7 represent a multigene family in Caenorhabditis elegans involved in cell-cell coupling. J. Cell Biol. 134, 537-548. doi: 10.1083/jcb.134.2.537.
216. Stebbings, L. A., Todman, M. G., Phelan, P., Bacon, J. P., and Davies, J. A. (2000). Two Drosophila innexins are expressed in overlapping domains and cooperate to form gap-junction channels. Mol. Biol. Cell 11, 2459-2470. doi: 10.1091/mbc.11.7.2459.
217. Stebbings, L. A., Todman, M. G., Phillips, R., Greer, C. E., Tam, J., Phelan, P., et al. (2002). Gap junctions in Drosophila: developmental expression of the entire innexin gene family. Mech. Dev. 113, 197-205. doi: 10.1016/S0925-4773(02)00025-4.
218. Suadicani, S. O., Iglesias, R., Wang, J., Dahl, G., Spray, D. C., and Scemes, E. (2012). ATP signaling is deficient in cultured pannexin1-null mouse astrocytes. Glia 60, 1106-1116. doi: 10.1002/glia.22338.
219. Sumi, Y., Woehrle, T., Chen, Y., Yao, Y., Li, A., and Junger, W. G. (2010). Adrenergic receptor activation involves ATP release and feedback through purinergic receptors. Am. J. Physiol. Cell Physiol. 299, C1118-C1126. doi: 10.1152/ajpcell.00122.2010.
220. Swayne, L. A., Sorbara, C. D., and Bennett, S. A. (2010). Pannexin 2 is expressed by postnatal hippocampal neural progenitors and modulates neuronal commitment. J. Biol. Chem. 285, 24977-24986. doi: 10.1074/jbc.M110.130054.
221. Takeuchi, O., and Akira, S. (2010). Pattern recognition receptors and inflammation. Cell 140, 805-820. doi: 10.1016/j.cell.2010.01.022.
222. Tang, W., Ahmad, S., Shestopalov, V. I., and Lin, X. (2008). Pannexins are new molecular candidates for assembling gap junctions in the cochlea. Neuroreport 19, 1253-1257. doi: 10.1097/WNR.0b013e32830891f5.
223. Taruno, A., Matsumoto, I., Ma, Z., Marambaud, P., and Foskett, J. K. (2013). How do taste cells lacking synapses mediate neurotransmission? CALHM1, a voltage-gated ATP channel. Bioessays 35, 1111-1118. doi: 10.1002/bies.201300077.
224. Tazuke, S. I., Schulz, C., Gilboa, L., Fogarty, M., Mahowald, A. P., Guichet, A., et al. (2002). A germline-specific gap junction protein required for survival of differentiating early germ cells. Development 129, 2529-2539. Available online at: http://dev.biologists.org/content/129/10/2529.long.
225. Thompson, R. J., Jackson, M. F., Olah, M. E., Rungta, R. L., Hines, D. J., Beazely, M. A., et al. (2008). Activation of pannexin-1 hemichannels augments aberrant bursting in the hippocampus. Science 322, 1555-1559. doi: 10.1126/science.1165209.
226. Thompson, R. J., Zhou, N., and MacVicar, B. A. (2006). Ischemia opens neuronal gap junction hemichannels. Science 312, 924-927. doi: 10.1126/science.1126241.
227. Timóteo, M. A., Carneiro, I., Silva, I., Noronha-Matos, J. B., Ferreirinha, F., Silva-Ramos, M., et al. (2013). ATP released via pannexin-1 hemichannels mediates bladder overactivity triggered by urothelial P2Y6 receptors. Biochem. Pharmacol. 87, 371-379. doi: 10.1016/j.bcp.2013.11.007.
228. Turmel, P., Dufresne, J., Hermo, L., Smith, C. E., Penuela, S., Laird, D. W., et al. (2011). Characterization of pannexin1 and pannexin3 and their regulation by androgens in the male reproductive tract of the adult rat. Mol. Reprod. Dev. 78, 124-138. doi: 10.1002/mrd.21280.
229. Valladares, D., Almarza, G., Contreras, A., Pavez, M., Buvinic, S., Jaimovich, E., et al. (2013). Electrical stimuli are anti-apoptotic in skeletal muscle via extracellular ATP. Alteration of this signal in mdx mice is a likely cause of dystrophy. PLoS ONE 8:e75340. doi: 10.1371/journal.pone.0075340.
230. Vanden Abeele, F., Bidaux, G., Gordienko, D., Beck, B., Panchin, Y. V., Baranova, A. V., et al. (2006). Functional implications of calcium permeability of the channel formed by pannexin 1. J. Cell Biol. 174, 535-546. doi: 10.1083/jcb.200601115.
231. Vessey, D. A., Li, L., and Kelley, M. (2010). Pannexin-I/P2X 7 purinergic receptor channels mediate the release of cardioprotectants induced by ischemic pre-and postconditioning. J. Cardiovasc. Pharmacol. Ther. 15, 190-195. doi: 10.1177/1074248409360356.
232. Vessey, D. A., Li, L., and Kelley, M. (2011a). Ischemic preconditioning requires opening of pannexin-1/P2X(7) channels not only during preconditioning but again after index ischemia at full reperfusion. Mol. Cell. Biochem. 351, 77-84. doi: 10.1007/s11010-011-0713-9.
233. Vessey, D. A., Li, L., and Kelley, M. (2011b). P2X7 receptor agonists pre-and postcondition the heart against ischemia-reperfusion injury by opening pannexin-1/P2X channels. Am. J. Physiol. Heart Circ. Physiol. 301, H881-H887. doi: 10.1152/ajpheart.00305.2011.
234. Viklund, H., and Elofsson, A. (2008). OCTOPUS: improving topology prediction by two-track ANN-based preference scores and an extended topological grammar. Bioinformatics 24, 1662-1668. doi: 10.1093/bioinformatics/btn221.
235. Vogt, A., Hormuzdi, S. G., and Monyer, H. (2005). Pannexin1 and Pannexin2 expression in the developing and mature rat brain. Brain Res. Mol. Brain Res. 141, 113-120. doi: 10.1016/j.molbrainres.2005.08.002.
236. Wang, H., Xing, Y., Mao, L., Luo, Y., Kang, L., and Meng, G. (2013a). Pannexin-1 influences peritoneal cavity cell population but is not involved in NLRP3 inflammasome activation. Protein Cell 4, 259-265. doi: 10.1007/s13238-013-2114-1.
237. Wang, J., and Dahl, G. (2010). SCAM analysis of Panx1 suggests a peculiar pore structure. J. Gen. Physiol. 136, 515-527. doi: 10.1085/jgp.201010440.
238. Wang, J., Jackson, D. G., and Dahl, G. (2013b). The food dye FD&C Blue No. 1 is a selective inhibitor of the ATP release channel Panx1. J. Gen. Physiol. 141, 649-656. doi: 10.1085/jgp.201310966.
239. Wang, J., Ma, M., Locovei, S., Keane, R. W., and Dahl, G. (2007). Modulation of membrane channel currents by gap junction protein mimetic peptides: size matters. Am. J. Physiol. Cell Physiol. 293, C1112-C1119. doi: 10.1152/ajpcell.00097.2007.
240. Wang, X. H., Streeter, M., Liu, Y. P., and Zhao, H. B. (2009). Identification and characterization of pannexin expression in the mammalian cochlea. J. Comp. Neurol. 512, 336-346. doi: 10.1002/cne.21898.
241. Wang, Y., Martins, I., Ma, Y., Kepp, O., Galluzzi, L., and Kroemer, G. (2013c). Autophagy-dependent ATP release from dying cells via lysosomal exocytosis. Autophagy 9, 1624-1625. doi: 10.4161/auto.25873.
242. Weickert, S., Ray, A., Zoidl, G., and Dermietzel, R. (2005). Expression of neural connexins and pannexin1 in the hippocampus and inferior olive: a quantitative approach. Brain Res. Mol. Brain Res. 133, 102-109. doi: 10.1016/j.molbrainres.2004.09.026.
243. Weilinger, N. L., Tang, P. L., and Thompson, R. J. (2012). Anoxia-induced NMDA receptor activation opens pannexin channels via Src family kinases. J. Neurosci. 32, 12579-12588. doi: 10.1523/JNEUROSCI.1267-12.2012.
244. Whittington, M. A., Traub, R. D., and Jefferys, J. G. (1995). Erosion of inhibition contributes to the progression of low magnesium bursts in rat hippocampal slices. J. Physiol. 486(Pt 3), 723-734.
245. Wicki-Stordeur, L. E., Boyce, A. K. J., and Swayne, L. A. (2013). Analysis of a pannexin 2-pannexin 1 chimeric protein supports divergent roles for pannexin C-termini in cellular localization. Cell Commun. Adhes. 20, 73-79. doi: 10.3109/15419061.2013.791681.
246. Wicki-Stordeur, L. E., Dzugalo, A. D., Swansburg, R. M., Suits, J. M., and Swayne, L. A. (2012). Pannexin 1 regulates postnatal neural stem and progenitor cell proliferation. Neural Dev. 7, 11. doi: 10.1186/1749-8104-7-11.
247. Wicki-Stordeur, L. E., and Swayne, L. A. (2012). Large pore ion and metabolite-permeable channel regulation of postnatal ventricular zone neural stem and progenitor cells: interplay between aquaporins, connexins, and pannexins? Stem Cells Int. 2012, 454180. doi: 10.1155/2012/454180.
248. Wicki-Stordeur, L. E., and Swayne, L. A. (2013). Panx1 regulates neural stem and progenitor cell behaviours associated with cytoskeletal dynamics and interacts with multiple cytoskeletal elements. Cell Commun. Signal. 11, 62. doi: 10.1186/1478-811X-11-62.
249. Wilson, D. M. (1961). The connections between the lateral giant fibers of earthworms. Comp. Biochem. Physiol. 3, 274-284. doi: 10.1016/0010-406X(61)90014-7.
250. Woehrle, T., Yip, L., Elkhal, A., Sumi, Y., Chen, Y., Yao, Y., et al. (2010a). Pannexin-1 hemichannel-mediated ATP release together with P2X1 and P2X4 receptors regulate T-cell activation at the immune synapse. Blood 116, 3475-3484. doi: 10.1182/blood-2010-04-277707.
251. Woehrle, T., Yip, L., Manohar, M., Sumi, Y., Yao, Y., Chen, Y., et al. (2010b). Hypertonic stress regulates T cell function via pannexin-1 hemichannels and P2X receptors. J. Leukoc. Biol. 88, 1181-1189. doi: 10.1189/jlb.0410211.
252. Wu, C.-L., Shih, M.-F. M., Lai, J. S.-Y., Yang, H.-T., Turner, G. C., Chen, L., et al. (2011). Heterotypic gap junctions between two neurons in the drosophila brain are critical for memory. Curr. Biol. 21, 848-854. doi: 10.1016/j.cub.2011.02.041.
253. Xia, J., Lim, J. C., Lu, W., Beckel, J. M., Macarak, E. J., Laties, A. M., et al. (2012). Neurons respond directly to mechanical deformation with pannexin-mediated ATP release and autostimulation of P2X7 receptors. J. Physiol. 590, 2285-2304. doi: 10.1113/jphysiol.2012.227983.
254. Xiao, F., Waldrop, S. L., Khimji, A.-K., and Kilic, G. (2012). Pannexin1 contributes to pathophysiological ATP release in lipoapoptosis induced by saturated free fatty acids in liver cells. Am. J. Physiol. Cell Physiol. 303, C1034-C1044. doi: 10.1152/ajpcell.00175.2012.
255. Xiong, X.-X., Gu, L.-J., Shen, J., Kang, X.-H., Zheng, Y.-Y., Yue, S.-B., et al. (2014). Probenecid protects against transient focal cerebral ischemic injury by inhibiting HMGB1 release and attenuating AQP4 expression in mice. Neurochem. Res. 39, 216-224. doi: 10.1007/s11064-013-1212-z.
256. Xu, X. J., Boumechache, M., Robinson, L. E., Marschall, V., Gorecki, D. C., Masin, M., et al. (2012). Splice variants of the P2X7 receptor reveal differential agonist dependence and functional coupling with pannexin-1. J. Cell Sci. 125, 3776-3789. doi: 10.1242/jcs.099374.
257. Yen, M. R., and Saier, M. H. J. (2007). Gap junctional proteins of animals: the innexin/pannexin superfamily. Prog. Biophys. Mol. Biol. 94, 5-14. doi: 10.1016/j.pbiomolbio.2007.03.006.
258. Zappalà, A., Cicero, D., Serapide, M. F., Paz, C., Catania, M. V., Falchi, M., et al. (2006). Expression of pannexin1 in the CNS of adult mouse: cellular localization and effect of 4-aminopyridine-induced seizures. Neuroscience 141, 167-178. doi: 10.1016/j.neuroscience.2006.03.053.
259. Zappalà, A., Li Volti, G., Serapide, M. F., Pellitteri, R., Falchi, M., La Delia, F., et al. (2007). Expression of pannexin2 protein in healthy and ischemized brain of adult rats. Neuroscience 148, 653-667. doi: 10.1016/j.neuroscience.2007.06.028.
260. Zhan, H., Moore, C. S., Chen, B., Zhou, X., Ma, X.-M., Ijichi, K., et al. (2012). Stomatin inhibits pannexin-1-mediated whole-cell currents by interacting with its carboxyl terminal. PLoS ONE 7:e39489. doi: 10.1371/journal.pone.0039489.
261. Zhang, H., Chen, Y., and Zhang, C. (2012a). Patterns of heterogeneous expression of pannexin 1 and pannexin 2 transcripts in the olfactory epithelium and olfactory bulb. J. Mol. Histol. 43, 651-660. doi: 10.1007/s10735-012-9443-x.
262. Zhang, M., Piskuric, N. A., Vollmer, C., and Nurse, C. A. (2012b). P2Y2 receptor activation opens pannexin-1 channels in rat carotid body type II cells: potential role in amplifying the neurotransmitter ATP. J. Physiol. 590, 4335-4350. doi: 10.1113/jphysiol.2012.236265.
263. Zoidl, G., Kremer, M., Zoidl, C., Bunse, S., and Dermietzel, R. (2008). Molecular diversity of connexin and pannexin genes in the retina of the zebrafish Danio rerio. Cell Commun. Adhes. 15, 169-183. doi: 10.1080/15419060802014081.
264. Zoidl, G., Petrasch-Parwez, E., Ray, A., Meier, C., Bunse, S., Habbes, H. W., et al. (2007). Localization of the pannexin1 protein at postsynaptic sites in the cerebral cortex and hippocampus. Neuroscience 146, 9-16. doi: 10.1016/j.neuroscience.2007.01.061.