Molecular pathways of pannexin1-mediated neurotoxicity

Frontiers in Physiology

Volumn 5 FEB, Issue , 2014, Pages

  Shestopalov, Valery I ^a,b,c   Slepak, Vladlen Z ^b  

^a UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

^c VAVILOV INSTITUTE OF GENERAL GENETICS   (Russian Federation)

Author keywords

Calcium; Danger signals; Hemichannel; Inflammasome; Neuronal death; Neurotoxicity; Pannexin; Signaling

Indexed keywords

ADENOSINE TRIPHOSPHATE; CALCIUM ION; CYTOKINE; FIBROBLAST GROWTH FACTOR; GLUTAMIC ACID; INFLAMMASOME; ION; MEMBRANE PROTEIN; NUCLEOTIDE; PANNEXIN 1; POTASSIUM ION; UNCLASSIFIED DRUG; ZINC ION;

CALCIUM CELL LEVEL; CELL KILLING; CELL MEMBRANE PERMEABILITY; CENTRAL NERVOUS SYSTEM; GAP JUNCTION; HUMAN; MEMBRANE CHANNEL; NERVE CELL NECROSIS; NERVOUS SYSTEM INJURY; NEUROPROTECTION; NEUROTOXICITY; NONHUMAN; PARACRINE SIGNALING; PYRAMIDAL NERVE CELL; RETINA GANGLION CELL; REVIEW;

EID: 84895459686     PISSN: None     EISSN: 1664042X     Source Type: Journal    
DOI: 10.3389/fphys.2014.00023     Document Type: Review

References (115)

1. Abulafia, D. P., de Rivero Vaccari, J. P., Lozano, J. D., Lotocki, G., Keane, R. W., and Dietrich, W. D. (2009). Inhibition of the inflammasome complex reduces the inflammatory response after thromboembolic stroke in mice. J. Cereb. Blood Flow Metab. 29, 534-544. doi: 10.1038/jcbfm.2008.143.
2. Arai, J., Katai, N., Kuida, K., Kikuchi, T., and Yoshimura, N. (2006). Decreased retinal neuronal cell death in caspase-1 knockout mice. Jpn. J. Ophthalmol. 50, 417-425. doi: 10.1007/s10384-006-0352-y.
3. Ayna, G., Krysko, D. V., Kaczmarek, A., Petrovski, G., Vandenabeele, P., and Fesus, L. (2012). ATP release from dying autophagic cells and their phagocytosis are crucial for inflammasome activation in macrophages. PLoS ONE 7:e40069. doi: 10.1371/journal.pone.0040069.
4. Bales, K. R., Du, Y., Dodel, R. C., Yan, G. M., Hamilton-Byrd, E., and Paul, S. M. (1998). The NF-kappaB/Rel family of proteins mediates Abeta-induced neurotoxicity and glial activation. Brain Res. Mol. Brain Res. 57, 63-72. doi: 10.1016/S0169-328X(98)00066-7.
5. 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.
6. 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.
7. Barakat, D. J., Dvoriantchikova, G., Ivanov, D., and Shestopalov, V. I. (2012). Astroglial NF-kappaB mediates oxidative stress by regulation of NADPH oxidase in a model of retinal ischemia reperfusion injury. J. Neurochem. 120, 586-597. doi: 10.1111/j.1471-4159.2011.07595.x.
8. 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.
9. 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.
10. Bennett, M. V., and Goodenough, D. A. (1978). Gap junctions, electrotonic coupling, and intercellular communication. Neurosci. Res. Program Bull. 16, 1-486.
11. Bennett, M. V., and Zukin, R. S. (2004). Electrical coupling and neuronal synchronization in the Mammalian brain. Neuron 41, 495-511. doi: 10.1016/S0896-6273(04)00043-1.
12. Bernier, L. P. (2012). Purinergic regulation of inflammasome activation after central nervous system injury. J. Gen. Physiol. 140, 571-575. doi: 10.1085/jgp.201210875.
13. 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.
14. Brambilla, R., Dvoriantchikova, G., Barakat, D., Ivanov, D., Bethea, J. R., and Shestopalov, V. I. (2012). Transgenic inhibition of astroglial NF-kappaB protects from optic nerve damage and retinal ganglion cell loss in experimental optic neuritis. J. Neuroinflammation 9:213. doi: 10.1186/1742-2094-9-213.
15. Brambilla, R., Persaud, T., Hu, X., Karmally, S., Shestopalov, V. I., Dvoriantchikova, G., et al. (2009). Transgenic inhibition of astroglial NF-kappa B improves functional outcome in experimental autoimmune encephalomyelitis by suppressing chronic central nervous system inflammation. J. Immunol. 182, 2628-2640. doi: 10.4049/jimmunol.0802954.
16. 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.
17. 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.
18. 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.
19. 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.
20. Choi, B. Y., Jang, B. G., Kim, J. H., Lee, B. E., Sohn, M., Song, H. K., et al. (2012) Prevention of traumatic brain injury-induced neuronal death by inhibition of NADPH oxidase activation. Brain Res. 1481, 49-58. doi: 10.1016/j.brainres.2012.08.032.
21. Dahl, G. (2007). Gap junction-mimetic peptides do work, but in unexpected ways. Cell Commun. Adhes. 14, 259-264. doi: 10.1080/15419060801891018.
22. Dahl, G., and Keane, R. W. (2012). Pannexin: from discovery to bedside in 11+/-4 years? Brain Res. 1487, 150-159. doi: 10.1016/j.brainres.2012.04.058.
23. 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.
24. de Rivero Vaccari, J. P., Bastien, D., Yurcisin, G., Pineau, I., Dietrich, W. D., De Koninck, Y., et al. (2012). P2X4 receptors influence inflammasome activation after spinal cord injury. J. Neurosci. 32, 3058-3066. doi: 10.1523/JNEUROSCI.4930-11.2012.
25. 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.
26. de Rivero Vaccari, J. P., Lotocki, G., Marcillo, A. E., Dietrich, W. D., and Keane, R. W. (2008) A molecular platform in neurons regulates inflammation after spinal cord injury. J. Neurosci. 28, 3404-3414. doi: 10.1523/JNEUROSCI.0157-08.2008.
27. Doll, R., Hill, I. D., and Hutton, C. F. (1965). Treatment of gastric ulcer with carbenoxolone sodium and oestrogens. Gut 6, 19-24. doi: 10.1136/gut.6.1.19.
28. 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.
29. Draguhn, A., Traub, R. D., Schmitz, D., and Jefferys, J. G. (1998). Electrical coupling underlies high-frequency oscillations in the hippocampus in vitro. Nature 394, 189-192. doi: 10.1038/28184.
30. Dvoriantchikova, G., Barakat, D., Brambilla, R., Agudelo, C., Hernandez, E., Bethea, J. R., et al. (2009). Inactivation of astroglial NF-kappa B promotes survival of retinal neurons following ischemic injury. Eur. J. Neurosci. 30, 175-185. doi: 10.1111/j.1460-9568.2009.06814.x.
31. Dvoriantchikova, G., Grant, J., Santos, A. R., Hernandez, E., and Ivanov, D. (2012a). Neuronal NAD(P)H oxidases contribute to ROS production and mediate RGC death after ischemia. Invest. Ophthalmol. Vis. Sci. 53, 2823-2830. doi: 10.1167/iovs.12-9526.
32. Dvoriantchikova, G., Ivanov, D., Barakat, D., Grinberg, A., Wen, R., Slepak, V. Z., et al. (2012b). Genetic ablation of Pannexin1 protects retinal neurons from ischemic injury. PLoS ONE 7:e31991. doi: 10.1371/journal.pone.0031991.
33. Dvoriantchikova, G., Ivanov, D., Panchin, Y., and Shestopalov, V. I. (2006). Expression of pannexin family of proteins in the retina. FEBS Lett. 580, 2178-2182. doi: 10.1016/j.febslet.2006.03.026.
34. Fleshner, M. (2013). Stress-evoked sterile inflammation, danger associated molecular patterns (DAMPs), microbial associated molecular patterns (MAMPs) and the inflammasome. Brain Behav. Immun. 27, 1-7. doi: 10.1016/j.bbi.2012.08.012.
35. Franchi, L., Munoz-Planillo, R., and Nunez, G. (2012). Sensing and reacting to microbes through the inflammasomes. Nat. Immunol. 13, 325-332. doi: 10.1038/ni.2231.
36. Franke, H., Krugel, U., and Illes, P. (2006). P2 receptors and neuronal injury. Pflugers Arch. 452, 622-644. doi: 10.1007/s00424-006-0071-8.
37. Garre, J. M., Retamal, M. A., Cassina, P., Barbeito, L., Bukauskas, F. F., Saez, J. C., et al. (2010). FGF-1 induces ATP release from spinal astrocytes in culture and opens pannexin and connexin hemichannels. Proc. Natl. Acad. Sci. U.S.A. 107, 22659-22664. doi: 10.1073/pnas.1013793107.
38. 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.
39. Goodenough, D. A., Dick, J. S. 2nd., and Lyons, J. E. (1980). Lens metabolic cooperation: a study of mouse lens transport and permeability visualized with freeze-substitution autoradiography and electron microscopy. J. Cell Biol. 86, 576-589. doi: 10.1083/jcb.86.2.576.
40. Gourine, A. V., Dale, N., Llaudet, E., Poputnikov, D. M., Spyer, K. M., and Gourine, V. N. (2007). Release of ATP in the central nervous system during systemic inflammation: real-time measurement in the hypothalamus of conscious rabbits. J. Physiol. 585, 305-316. doi: 10.1113/jphysiol.2007.143933.
41. 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.
42. Hardingham, G. E. (2009). Coupling of the NMDA receptor to neuroprotective and neurodestructive events. Biochem. Soc. Trans. 37, 1147-11460. doi: 10.1042/BST0371147.
43. 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.
44. 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.
45. 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.
46. Innocenti, B., Pfeiffer, S., Zrenner, E., Kohler, K., and Guenther, E. (2004). ATP-induced non-neuronal cell permeabilization in the rat inner retina. J. Neurosci. 24, 8577-8583. doi: 10.1523/JNEUROSCI.2812-04.2004.
47. Johnson, A. D., and Owens, G. K. (1999). Differential activation of the SMalpha A promoter in smooth vs. skeletal muscle cells by bHLH factors. Am. J. Physiol. Cell Physiol. 276, C1420-C1431.
48. Jones, F. S., Kioussi, C., Copertino, D. W., Kallunki, P., Holst, B. D., and Edelman, G. M. (1997). Barx2, a new homeobox gene of the Bar class, is expressed in neural and craniofacial structures during development. Proc. Natl. Acad. Sci. U.S.A. 94, 2632-2637. doi: 10.1073/pnas.94.6.2632.
49. 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.
50. Karatas, H., Erdener, S. E., Gursoy-Ozdemir, Y., Lule, S., Eren-Kocak, 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.
51. Kawamura, M. Jr., Ruskin, D. N., and Masino, S. A. (2010). Metabolic autocrine regulation of neurons involves cooperation among pannexin hemichannels, adenosine receptors, and KATP channels. J. Neurosci. 30, 3886-3895. doi: 10.1523/JNEUROSCI.0055-10.2010.
52. Kim, C. H., Neiswender, H., Baik, E. J., Xiong, W. C., and Mei, L. (2008). Beta-catenin interacts with MyoD and regulates its transcription activity. Mol. Cell. Biol. 28, 2941-2951. doi: 10.1128/MCB.01682-07.
53. Krizaj, D., Ryskamp, D. A., Tian, N., Tezel, G., Mitchell, C. H., Slepak, V. Z., et al. (2013). From mechanosensitivity to inflammatory responses: new players in the pathology of glaucoma. Curr. Eye Res. 39, 105-119. doi: 10.3109/02713683.2013.836541.
54. Kumar, A., Velloso, C. P., Imokawa, Y., and Brockes, J. P. (2004). The regenerative plasticity of isolated urodele myofibers and its dependence on MSX1. PLoS Biol. 2:E218. doi: 10.1371/journal.pbio.0020218.
55. Lamkanfi, M. (2011). Emerging inflammasome effector mechanisms. Nat. Rev. Immunol. 11, 213-20. doi: 10.1038/nri2936.
56. Lamkanfi, M., Sarkar, A., Vande Walle, L., Vitari, A. C., Amer, A. O., Wewers, M. D., et al. (2010). Inflammasome-dependent release of the alarmin HMGB1 in endotoxemia. J. Immunol. 185, 4385-4392. doi: 10.4049/jimmunol.1000803.
57. Lazarewicz, J. W., Wroblewski, J. T., and Costa, E. (1990). N-methyl-D-aspartate-sensitive glutamate receptors induce calcium-mediated arachidonic acid release in primary cultures of cerebellar granule cells. J. Neurochem. 55, 1875-1881. doi: 10.1111/j.1471-4159.1990.tb05771.x.
58. Li, A., Leung, C. T., Peterson-Yantorno, K., Stamer, W. D., Mitchell, C. H., and Civan, M. M. (2012). 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.
59. Li, S., Tomic, M., and Stojilkovic, S. S. (2011). 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.
60. Li, W., Li, J., Sama, A. E., and Wang, H. (2013). Carbenoxolone blocks endotoxin-induced PKR activation and HMGB1 release. Mol Med. 19, 203-211. doi: 10.2119/molmed.2013.00064.
61. Lobner, D., and Lipton, P. (1993). Intracellular calcium levels and calcium fluxes in the CA1 region of the rat hippocampal slice during in vitro ischemia: relationship to electrophysiological cell damage. J. Neurosci. 13, 4861-4871.
62. 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.
63. 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.
64. 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.
65. Maher, J. J. (2009). DAMPs ramp up drug toxicity. J. Clin. Invest. 119, 246-249. doi: 10.1172/JCI38178.
66. Matute, C., and Cavaliere, F. (2011). Neuroglial interactions mediated by purinergic signalling in the pathophysiology of CNS disorders. Semin. Cell Dev. Biol. 22, 252-259. doi: 10.1016/j.semcdb.2011.02.011.
67. Meloni, B. P., Meade, A. J., Kitikomolsuk, D., and Knuckey, N. W. (2011). Characterisation of neuronal cell death in acute and delayed in vitro ischemia (oxygen-glucose deprivation) models. J. Neurosci. Methods 195, 67-74. doi: 10.1016/j.jneumeth.2010.11.023.
68. Melov, S., Tarnopolsky, M. A., Beckman, K., Felkey, K., and Hubbard, A. (2007). Resistance exercise reverses aging in human skeletal muscle. PLoS ONE 2:e465. doi: 10.1371/journal.pone.0000465.
69. Mochizuki, T., Sokabe, T., Araki, I., Fujishita, K., Shibasaki, K., Uchida, K., et al. (2009). The TRPV4 cation channel mediates stretch-evoked Ca2+ influx and ATP release in primary urothelial cell cultures. J. Biol. Chem. 284, 21257-21264. doi: 10.1074/jbc.M109.020206.
70. Nowak, K. J., and Davies, K. E. (2004). Duchenne muscular dystrophy and dystrophin: pathogenesis and opportunities for treatment. EMBO Rep. 5, 872-876. doi: 10.1038/sj.embor.7400221.
71. 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 connexin43 hemichannels mediate neuronal death through activation of pannexin 1 hemichannels. J. Neurochem. 118, 826-840. doi: 10.1111/j.1471-4159.2011.07210.x.
72. Orellana, J. A., Hernandez, D. E., Ezan, P., Velarde, V., Bennett, M. V., Giaume, C., et al. (2010). Hypoxia in high glucose followed by reoxygenation in normal glucose reduces the viability of cortical astrocytes through increased permeability of connexin 43 hemichannels. Glia 58, 329-343. doi: 10.1002/glia.20926.
73. Orellana, J. A., Saez, P. J., Shoji, K. F., Schalper, K. A., Palacios-Prado, N., Velarde, V., et al. (2009). Modulation of brain hemichannels and gap junction channels by pro-inflammatory agents and their possible role in neurodegeneration. Antioxid. Redox Signal. 11, 369-399. doi: 10.1089/ars.2008.2130.
74. Paramo, B., Montiel, T., Hernandez-Espinosa, D. R., Rivera-Martinez, M., Moran, J., and Massieu, L. (2013). Calpain activation induced by glucose deprivation is mediated by oxidative stress and contributes to neuronal damage. Int. J. Biochem. Cell Biol. 45, 2596-2604. doi: 10.1016/j.biocel.2013.08.013.
75. Pelegrin, P. (2008). Targeting interleukin-1 signaling in chronic inflammation: focus on P2X(7) receptor and Pannexin-1. Drug News Perspect. 21, 424-433. doi: 10.1358/dnp.2008.21.8.1265800.
76. 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.
77. 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.
78. 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.
79. Pelegrin, P., and Surprenant, A. (2009). The P2X(7) receptor-pannexin connection to dye uptake and IL-1beta release. Purinergic Signal. 5, 129-137. doi: 10.1007/s11302-009-9141-7.
80. Prochnow, N., Abdulazim, A., Kurtenbach, S., Wildforster, 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.
81. 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. 186, 6553-6561. doi: 10.4049/jimmunol.1100478.
82. 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.
83. Reuss, B., Hertel, M., Werner, S., and Unsicker, K. (2000). Fibroblast growth factors-5 and-9 distinctly regulate expression and function of the gap junction protein connexin43 in cultured astroglial cells from different brain regions. Glia 30, 231-241. doi: 10.1002/(SICI)1098-1136(200005)30:3<231::AID-GLIA3>3.0.CO;2-1.
84. Riteau, N., Baron, L., Villeret, B., Guillou, N., Savigny, F., Ryffel, B., et al. (2012). ATP release and purinergic signaling: a common pathway for particle-mediated inflammasome activation. Cell Death Dis. 3:e403. doi: 10.1038/cddis.2012.144.
85. Rosenbaum, D. M., Degterev, A., David, J., Rosenbaum, P. S., Roth, S., Grotta, J. C., et al. (2010). Necroptosis, a novel form of caspase-independent cell death, contributes to neuronal damage in a retinal ischemia-reperfusion injury model. J. Neurosci. Res. 88, 1569-1576. doi: 10.1002/jnr.22314.
86. Ryskamp, D. A., Witkovsky, P., Barabas, P., Huang, W., Koehler, C., Akimov, N. P., et al. (2011). The polymodal ion channel transient receptor potential vanilloid 4 modulates calcium flux, spiking rate, and apoptosis of mouse retinal ganglion cells. J. Neurosci. 31, 7089-7101. doi: 10.1523/JNEUROSCI.0359-11.2011.
87. Saez, J. C., Schalper, K. A., Retamal, M. A., Orellana, J. A., Shoji, K. F., and Bennett, M. V. (2010). Cell membrane permeabilization via connexin hemichannels in living and dying cells. Exp. Cell Res. 316, 2377-2389. doi: 10.1016/j.yexcr.2010.05.026.
88. Sandilos, J. K., Chiu, Y. 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.
89. Seil, M., Fontanils, U., Etxebarria, I. G., Pochet, S., Garcia-Marcos, M., Marino, A., et al. (2008). Pharmacological evidence for the stimulation of NADPH oxidase by P2X(7) receptors in mouse submandibular glands. Purinergic Signal. 4, 347-355. doi: 10.1007/s11302-008-9118-y.
90. 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.
91. Shahidullah, M., Mandal, A., and Delamere, N. A. (2012). TRPV4 in porcine lens epithelium regulates hemichannel-mediated ATP release and Na-K-ATPase activity. Am. J. Physiol. Cell Physiol. 302, C1751-C1761. doi: 10.1152/ajpcell.00010.2012.
92. Shiose, S., Chen, Y., Okano, K., Roy, S., Kohno, H., Tang, J., et al. (2011). Toll-like receptor 3 is required for development of retinopathy caused by impaired all-trans-retinal clearance in mice. J. Biol. Chem. 286, 15543-15555. doi: 10.1074/jbc.M111.228551.
93. 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.
94. 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.
95. Striedinger, K., Petrasch-Parwez, E., Zoidl, G., Napirei, M., Meier, C., Eysel, U. T., et al. (2005). Loss of connexin36 increases retinal cell vulnerability to secondary cell loss. Eur. J. Neurosci. 22, 605-616. doi: 10.1111/j.1460-9568.2005.04228.x.
96. Strowig, T., Henao-Mejia, J., Elinav, E., and Flavell, R. (2012). Inflammasomes in health and disease. Nature 481, 278-286. doi: 10.1038/nature10759.
97. 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.
98. Sucher, N. J., Lipton, S. A., and Dreyer, E. B. (1997). Molecular basis of glutamate toxicity in retinal ganglion cells. Vision Res. 37, 3483-3493. doi: 10.1016/S0042-6989(97)00047-3.
99. 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.
100. 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.
101. Trenholme, C. M., Williams, R. L., Desjardins, R. E., Frischer, H., Carson, P. E., Rieckmann, K. H., et al. (1975). Mefloquine (WR 142,490) in the treatment of human malaria. Science 190, 792-794. doi: 10.1126/science.1105787.
102. 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.
103. Weilinger, N. L., Maslieieva, V., Bialecki, J., Sridharan, S. S., Tang, P. L., and Thompson, R. J. (2013). Ionotropic receptors and ion channels in ischemic neuronal death and dysfunction. Acta Pharmacol. Sin. 34, 39-48. doi: 10.1038/aps.2012.95.
104. 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.
105. 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.
106. Willingham, S. B., Allen, I. C., Bergstralh, D. T., Brickey, W. J., Huang, M. T., Taxman, D. J., et al. (2009). NLRP3 (NALP3, Cryopyrin) facilitates in vivo caspase-1 activation, necrosis, and HMGB1 release via inflammasome-dependent and-independent pathways. J. Immunol. 183, 2008-2015. doi: 10.4049/jimmunol.0900138.
107. Wurm, A., Lipp, S., Pannicke, T., Linnertz, R., Krugel, U., Schulz, A., et al. (2010). Endogenous purinergic signaling is required for osmotic volume regulation of retinal glial cells. J. Neurochem. 112, 1261-1272. doi: 10.1111/j.1471-4159.2009.06541.x.
108. Wurm, A., Pannicke, T., Wiedemann, P., Reichenbach, A., and Bringmann, A. (2008). Glial cell-derived glutamate mediates autocrine cell volume regulation in the retina: activation by VEGF. J. Neurochem. 104, 386-399. doi: 10.1111/j.1471-4159.2007.04992.x.
109. 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(Pt 10), 2285-2304. doi: 10.1113/jphysiol.2012.227983.
110. Yang, H., Hreggvidsdottir, H. S., Palmblad, K., Wang, H., Ochani, M., Li, J., et al. (2010). A critical cysteine is required for HMGB1 binding to Toll-like receptor 4 and activation of macrophage cytokine release. Proc. Natl. Acad. Sci. U.S.A. 107, 11942-11947. doi: 10.1073/pnas.1003893107.
111. Zhang, L., Deng, T., Sun, Y., Liu, K., Yang, Y., and Zheng, X. (2008). Role for nitric oxide in permeability of hippocampal neuronal hemichannels during oxygen glucose deprivation. J. Neurosci. Res. 86, 2281-2291. doi: 10.1002/jnr.21675.
112. Zhang, M., Piskuric, N. A., Vollmer, C., and Nurse, C. A. (2012). P2Y2 receptor activation opens pannexin-1 channels in rat carotid body type II cells: potential role in amplifying the neurotransmitter ATP. J. Physiol. 590(Pt 17), 4335-4350. doi: 10.1113/jphysiol.2012.236265.
113. Zhang, X., Zhang, M., Laties, A. M., and Mitchell, C. H. (2005a). Stimulation of P2X7 receptors elevates Ca2+ and kills retinal ganglion cells. Invest. Ophthalmol. Vis. Sci. 46, 2183-2191. doi: 10.1167/iovs.05-0052.
114. Zhang, Z., Trautmann, K., and Schluesener, H. J. (2005b). Microglia activation in rat spinal cord by systemic injection of TLR3 and TLR7/8 agonists. J. Neuroimmunol. 164, 154-160. doi: 10.1016/j.jneuroim.2005.03.014.
115. 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.