Emerging functions of pannexin 1 in the eye

Frontiers in Cellular Neuroscience

Volumn 8, Issue , 2014, Pages

  Kurtenbach, Sarah ^a   Kurtenbach, Stefan ^a   Zoidl, Georg ^a  

^a YORK UNIVERSITY   (Canada)

Author keywords

ATP; Cornea; Eye; Feedback mechanism; Lens; Pannexin 1 (Panx1); Purinergic receptor signaling; Retina

Indexed keywords

3 [[5 (2, 3 DICHLOROPHENYL) 1H TETRAZOL 1 YL] METHYL] PYRIDINE; ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM); ADENOSINE TRIPHOSPHATE; AMPA RECEPTOR; CARBENOXOLONE; CONNEXIN 43; GAP JUNCTION PROTEIN; KAINIC ACID RECEPTOR; PANNEXIN 1; PANNEXIN 2; PANNEXIN 3; PROBENECID; PURINERGIC P2X RECEPTOR ANTAGONIST; PURINERGIC P2X7 RECEPTOR; UNCLASSIFIED DRUG; VANILLOID RECEPTOR 4; ZINC;

AQUEOUS HUMOR OUTFLOW; CELL INTERACTION; CORNEA; EYE; FEEDBACK SYSTEM; FISH; GLAUCOMA; HUMAN; HYPOOSMOTIC STRESS; IMMUNOCOMPETENT CELL; LENS; MICROGLIA; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; RETINA GANGLION CELL; RETINA ISCHEMIA; RETINA NERVE CELL; REVIEW; SIGNAL TRANSDUCTION; VISION; WOUND HEALING;

EID: 84907189217     PISSN: 16625102     EISSN: None     Source Type: Journal    
DOI: 10.3389/fncel.2014.00263     Document Type: Review

References (160)

1. Adamson, S. E., and Leitinger, N. (2014). The role of pannexin1 in the induction and resolution of inflammation.FEBS Lett. 588, 1416-1422. doi: 10.1016/j.febslet.2014.03.009
2. Aga, M., Bradley, J. M., Keller, K. E., Kelley, M. J., and Acott, T. S. (2008). Specialized podosome- or invadopodia-like structures (PILS) for focal trabecular meshwork extracellular matrix turnover. Invest. Ophthalmol. Vis. Sci.49, 5353-5365. doi: 10.1167/iovs.07-1666
3. Avila, M. Y., Stone, R. A., and Civan, M. M. (2001). A(1)-, A(2A)- and A(3)-subtype adenosine receptors modulate intraocular pressure in the mouse. Br. J. Pharmacol. 134, 241-245. doi: 10.1038/sj.bjp.0704267
4. 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
5. Bao, L., Locovei, S., and Dahl, G. (2004a). Pannexin membrane channels are mechanosensitive conduits for ATP.FEBS Lett. 572, 65-68. doi: 10.1016/j.febslet.2004.07.009
6. Bao, L., Sachs, F., and Dahl, G. (2004b). Connexins are mechanosensitive. Am. J. Physiol. Cell Physiol. 287, C1389-C1395. doi: 10.1152/ajpcell.00220.2004
7. 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
8. Barishak, Y. R. (1992). Embryology of the eye and its adnexae. Dev. Ophthalmol. 24, 1-142.
9. Beckel, J. M., Argall, A. J., Lim, J. C., Xia, J., Lu, W., Coffey, E. E., et al. (2014). Mechanosensitive release of adenosine 5′-triphosphate through pannexin channels and mechanosensitive upregulation of pannexin channels in optic nerve head astrocytes: a mechanism for purinergic involvement in chronic strain. Glia 62, 1486-1501. doi: 10.1002/glia.22695
10. Berthoud, V. M., Minogue, P. J., Osmolak, P., Snabb, J. I., and Beyer, E. C. (2014). Roles and regulation of lens epithelial cell connexins. FEBS Lett. 588, 1297-1303. doi: 10.1016/j.febslet.2013.12.024
11. Beyer, E. C., and Berthoud, V. M. (2014). Connexin hemichannels in the lens. Front. Physiol. 5:20. doi: 10.3389/fphys.2014.00020
12. Bloomfield, S. A., Xin, D., and Persky, S. E. (1995). A comparison of receptive field and tracer coupling size of horizontal cells in the rabbit retina. Vis. Neurosci. 12, 985-999. doi: 10.1017/s0952523800009524
13. 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
14. Bond, S. R., and Naus, C. C. (2014). The pannexins: past and present. Front. Physiol. 5:58. doi: 10.3389/fphys.2014.00058
15. 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
16. Boyce, A. K., Wicki-Stordeur, L. E., and Swayne, L. A. (2014). Powerful partnership: crosstalk between pannexin 1 and the cytoskeleton. Front. Physiol. 5:27. doi: 10.3389/fphys.2014.00027
17. 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
18. 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
19. Burkhardt, D. A., and Fahey, P. K. (1998). Contrast enhancement and distributed encoding by bipolar cells in the retina. J. Neurophysiol. 80, 1070-1081.
20. 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
21. Conway, B. R. (2007). Color vision: mice see hue too. Curr. Biol. 17, R457-R460. doi: 10.1016/j.cub.2007.04.017
22. Cuthbert, A. W. (2001). Assessment of CFTR chloride channel openers in intact normal and cystic fibrosis murine epithelia. Br. J. Pharmacol. 132, 659-668. doi: 10.1038/sj.bjp.0703859
23. 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
24. 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
25. Davalos, D., Grutzendler, J., Yang, G., Kim, J. V., Zuo, Y., Jung, S., et al. (2005). ATP mediates rapid microglial response to local brain injury in vivo. Nat. Neurosci. 8, 752-758. doi: 10.1038/nn1472
26. Delamere, N. A., and Tamiya, S. (2009). Lens ion transport: from basic concepts to regulation of Na,K-ATPase activity. Exp. Eye Res. 88, 140-143. doi: 10.1016/j.exer.2008.05.005
27. de Rivero Vaccari, J. P., Lotocki, G., Alonso, O. F., Bramlett, H. M., Dietrich, W. D., Keane, R. W., et al. (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
28. De Vuyst, E., Decrock, E., Cabooter, L., Dubyak, G. R., Naus, C. C., Evans, W. H., et al. (2006). Intracellular calcium changes trigger connexin 32 hemichannel opening. EMBO J. 25, 34-44. doi: 10.1038/sj.emboj.7600908
29. D'hondt, C., Iyyathurai, J., Vinken, M., Rogiers, V., Leybaert, L., Himpens, B., et al. (2013). Regulation of connexin- and pannexin-based channels by post-translational modifications. Biol. Cell 105, 373-398. doi: 10.1111/boc.201200096
30. Domercq, M., Vazquez-Villoldo, N., and Matute, C. (2013). Neurotransmitter signaling in the pathophysiology of microglia. Front. Cell. Neurosci. 7:49. doi: 10.3389/fncel.2013.00049
31. 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
32. 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
33. Dvoriantchikova, G., Ivanov, D., Pestova, A., and Shestopalov, V. (2006b). Molecular characterization of pannexins in the lens. Mol. Vis. 12, 1417-1426.
34. Fahrenfort, I., Steijaert, M., Sjoerdsma, T., Vickers, E., Ripps, H., van Asselt, J., et al. (2009). Hemichannel-mediated and pH-based feedback from horizontal cells to cones in the vertebrate retina. PLoS One 4:e6090. doi: 10.1371/journal.pone.0006090
35. Fontainhas, A. M., Wang, M., Liang, K. J., Chen, S., Mettu, P., Damani, M., et al. (2011). Microglial morphology and dynamic behavior is regulated by ionotropic glutamatergic and GABAergic neurotransmission. PLoS One6:e15973. doi: 10.1371/journal.pone.0015973
36. Francis, B. A., and Alvarado, J. (1997). The cellular basis of aqueous outflow regulation. Curr. Opin. Ophthalmol. 8, 19-27. doi: 10.1097/00055735-199704000-00005
37. Furukawa, T., Ogura, T., Katayama, Y., and Hiraoka, M. (1998). Characteristics of rabbit ClC-2 current expressed in Xenopus oocytes and its contribution to volume regulation. Am. J. Physiol. 274, C500-C512.
38. Goel, M., Picciani, R. G., Lee, R. K., and Bhattacharya, S. K. (2010). Aqueous humor dynamics: a review. Open Ophthalmol. J. 4, 52-59. doi: 10.2174/1874364101004010052
39. Goldsmith, P., and Harris, W. A. (2003). The zebrafish as a tool for understanding the biology of visual disorders.Semin. Cell Dev. Biol. 14, 11-18. doi: 10.1016/s1084-9521(02)00167-2
40. Gong, H., Tripathi, R. C., and Tripathi, B. J. (1996). Morphology of the aqueous outflow pathway. Microsc. Res. Tech. 33, 336-367. doi: 10.1002/(sici)1097-0029(19960301)33:4<336::aid-jemt4>3.0.co;2-n
41. Grek, C. L., Rhett, J. M., and Ghatnekar, G. S. (2014). Cardiac to cancer: connecting connexins to clinical opportunity. FEBS Lett. 588, 1349-1364. doi: 10.1016/j.febslet.2014.02.047
42. Hagins, W. A., Penn, R. D., and Yoshikami, S. (1970). Dark current and photocurrent in retinal rods. Biophys. J. 10, 380-412. doi: 10.1016/s0006-3495(70)86308-1
43. Hanner, F., Lam, L., Nguyen, M. T., 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
44. Hirasawa, H., Yamada, M., and Kaneko, A. (2012). Acidification of the synaptic cleft of cone photoreceptor terminal controls the amount of transmitter release, thereby forming the receptive field surround in the vertebrate retina. J. Physiol. Sci. 62, 359-375. doi: 10.1007/s12576-012-0220-0
45. Huang, Y., Grinspan, J. B., Abrams, C. K., and Scherer, S. S. (2007a). Pannexin1 is expressed by neurons and glia but does not form functional gap junctions. Glia 55, 46-56. doi: 10.1002/glia.20435
46. Huang, Y. J., Maruyama, Y., Dvoryanchikov, G., Pereira, E., Chaudhari, N., and Roper, S. D. (2007b). 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
47. Husain, S., Shearer, T. W., and Crosson, C. E. (2007). Mechanisms linking adenosine A1 receptors and extracellular signal-regulated kinase 1/2 activation in human trabecular meshwork cells. J. Pharmacol. Exp. Ther. 320, 258-265. doi: 10.1124/jpet.106.110981
48. Iglesias, R., Dahl, G., Qiu, F., Spray, D. C., and Scemes, E. (2009a). Pannexin 1: the molecular substrate of astrocyte "hemichannels". J. Neurosci. 29, 7092-7097. doi: 10.1523/jneurosci.6062-08.2009
49. Iglesias, R., Spray, D. C., and Scemes, E. (2009b). Mefloquine blockade of Pannexin1 currents: resolution of a conflict. Cell Commun. Adhes. 16, 131-137. doi: 10.3109/15419061003642618
50. Isakson, B. E., and Thompson, R. J. (2014). Pannexin-1 as a potentiator of ligand-gated receptor signaling. Channels (Austin) 8, 118-123. doi: 10.4161/chan.27978
51. Jackman, S. L., Babai, N., Chambers, J. J., Thoreson, W. B., and Kramer, R. H. (2011). A positive feedback synapse from retinal horizontal cells to cone photoreceptors. PLoS Biol. 9:e1001057. doi: 10.1371/journal.pbio.1001057
52. Jackson, D. G., Wang, J., Keane, R. W., Scemes, E., and Dahl, G. (2014). ATP and potassium ions: a deadly combination for astrocytes. Sci. Rep. 4:4576. doi: 10.1038/srep04576
53. Jaillon, O., Aury, J. M., Brunet, F., Petit, J. L., Stange-Thomann, N., Mauceli, E., et al. (2004). Genome duplication in the teleost fish Tetraodon nigroviridis reveals the early vertebrate proto-karyotype. Nature 431, 946-957. doi: 10.1038/nature03025
54. Johnstone, S. R., Billaud, M., Lohman, A. W., Taddeo, E. P., and Isakson, B. E. (2012). Posttranslational modifications in connexins and pannexins. J. Membr. Biol. 245, 319-332. doi: 10.1007/s00232-012-9453-3
55. Kamermans, M., and Fahrenfort, I. (2004). Ephaptic interactions within a chemical synapse: hemichannel-mediated ephaptic inhibition in the retina. Curr. Opin. Neurobiol. 14, 531-541. doi: 10.1016/j.conb.2004.08.016
56. Kamermans, M., Fahrenfort, I., Schultz, K., Janssen-Bienhold, U., Sjoerdsma, T., and Weiler, R. (2001). Hemichannel-mediated inhibition in the outer retina. Science 292, 1178-1180. doi: 10.1126/science.1060101
57. 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
58. 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
59. 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
60. 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
61. 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
62. Klaassen, L. J., Fahrenfort, I., and Kamermans, M. (2012). Connexin hemichannel mediated ephaptic inhibition in the retina. Brain Res. 1487, 25-38. doi: 10.1016/j.brainres.2012.04.059
63. Klaassen, L. J., Sun, Z., Steijaert, M. N., Bolte, P., Fahrenfort, I., Sjoerdsma, T., et al. (2011). Synaptic transmission from horizontal cells to cones is impaired by loss of connexin hemichannels. PLoS Biol. 9:e1001107. doi: 10.1371/journal.pbio.1001107
64. 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
65. Krizaj, D., Ryskamp, D. A., Tian, N., Tezel, G., Mitchell, C. H., Slepak, V. Z., et al. (2014). From mechanosensitivity to inflammatory responses: new players in the pathology of glaucoma. Curr. Eye Res. 39, 105-119. doi: 10.3109/02713683.2013.836541
66. 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
67. 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
68. 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
69. Lamkanfi, M., Malireddi, R. K., 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
70. Lee, J. E., Liang, K. J., Fariss, R. N., and Wong, W. T. (2008). Ex vivo dynamic imaging of retinal microglia using time-lapse confocal microscopy. Invest. Ophthalmol. Vis. Sci. 49, 4169-4176. doi: 10.1167/iovs.08-2076
71. 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
72. 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
73. Li, A., Zhang, X., Zheng, D., Ge, J., Laties, A. M., and Mitchell, C. H. (2011). Sustained elevation of extracellular ATP in aqueous humor from humans with primary chronic angle-closure glaucoma. Exp. Eye Res. 93, 528-533. doi: 10.1016/j.exer.2011.06.020
74. Liang, J., Takeuchi, H., Jin, S., Noda, M., Li, H., Doi, Y., et al. (2010). Glutamate induces neurotrophic factor production from microglia via protein kinase C pathway. Brain Res. 1322, 8-23. doi: 10.1016/j.brainres.2010.01.083
75. Liu, H., Chen, Y., Niu, Y., Zhang, K., Kang, Y., Ge, W., et al. (2014a). TALEN-mediated gene mutagenesis in rhesus and cynomolgus monkeys. Cell Stem Cell 14, 323-328. doi: 10.1016/j.stem.2014.01.018
76. Liu, Z., Zhou, X., Zhu, Y., Chen, Z. F., Yu, B., Wang, Y., et al. (2014b). Generation of a monkey with MECP2 mutations by TALEN-based gene targeting. Neurosci. Bull. 30, 381-386. doi: 10.1007/s12264-014-1434-8
77. 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
78. 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
79. Lohman, A. W., Billaud, M., and Isakson, B. E. (2012a). Mechanisms of ATP release and signalling in the blood vessel wall. Cardiovasc. Res. 95, 269-280. doi: 10.1093/cvr/cvs187
80. Lohman, A. W., and Isakson, B. E. (2014). Differentiating connexin hemichannels and pannexin channels in cellular ATP release. FEBS Lett. 588, 1379-1388. doi: 10.1016/j.febslet.2014.02.004
81. 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
82. MacVicar, B. A., and Thompson, R. J. (2010). Non-junction functions of pannexin-1 channels. Trends Neurosci. 33, 93-102. doi: 10.1016/j.tins.2009.11.007
83. Madry, C., Haglerod, C., and Attwell, D. (2010). The role of pannexin hemichannels in the anoxic depolarization of hippocampal pyramidal cells. Brain 133, 3755-3763. doi: 10.1093/brain/awq284
84. Mali, P., Esvelt, K. M., and Church, G. M. (2013a). Cas9 as a versatile tool for engineering biology. Nat. Methods 10, 957-963. doi: 10.1038/nmeth.2649
85. Mali, P., Yang, L., Esvelt, K. M., Aach, J., Guell, M., Dicarlo, J. E., et al. (2013b). RNA-guided human genome engineering via Cas9. Science 339, 823-826. doi: 10.1126/science.1232033
86. Mayo, C., Ren, R., Rich, C., Stepp, M. A., and Trinkaus-Randall, V. (2008). Regulation by P2X7: epithelial migration and stromal organization in the cornea. Invest. Ophthalmol. Vis. Sci. 49, 4384-4391. doi: 10.1167/iovs.08-1688
87. Mertsch, K., Hanisch, U. K., Kettenmann, H., and Schnitzer, J. (2001). Characterization of microglial cells and their response to stimulation in an organotypic retinal culture system. J. Comp. Neurol. 431, 217-227. doi: 10.1002/1096-9861(20010305)431:2<217::aid-cne1066>3.3.co;2-k
88. 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
89. Mitchell, C. H., Peterson-Yantorno, K., Carre, D. A., Mcglinn, A. M., Coca-Prados, M., Stone, R. A., et al. (1999). A3 adenosine receptors regulate Cl- channels of nonpigmented ciliary epithelial cells. Am. J. Physiol. 276, C659-C666.
90. Monaco, E. A. 3rd, and Friedlander, R. M. (2012). A novel target for ischemic stroke therapy: pannexins.Neurosurgery 70, N13-N14. doi: 10.1227/01.neu.0000413220.21264.df
91. 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
92. Nimmerjahn, A., Kirchhoff, F., and Helmchen, F. (2005). Resting microglial cells are highly dynamic surveillants of brain parenchyma in vivo. Science 308, 1314-1318. doi: 10.1126/science.1110647
93. Niu, Y., Shen, B., Cui, Y., Chen, Y., Wang, J., Wang, L., et al. (2014). Generation of gene-modified cynomolgus monkey via Cas9/RNA-mediated gene targeting in one-cell embryos. Cell 156, 836-843. doi: 10.1016/j.cell.2014.01.027
94. Orellana, J. A., Velasquez, S., Williams, D. W., Saez, J. C., Berman, J. W., and Eugenin, E. A. (2013). Pannexin1 hemichannels are critical for HIV infection of human primary CD4+ T lymphocytes. J. Leukoc. Biol. 94, 399-407. doi: 10.1189/jlb.0512249
95. 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
96. Pau, H. (2008). Retinopathy of prematurity: clinic and pathogenesis. Disproportion between apoptosis of vitreal and proliferation of retinal vascularization. Ophthalmologica 222, 220-224. doi: 10.1159/000130069
97. Peichl, L., and Gonzalez-Soriano, J. (1993). Unexpected presence of neurofilaments in axon-bearing horizontal cells of the mammalian retina. J. Neurosci. 13, 4091-4100. doi: 10.1098/rspb.1993.0051
98. 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
99. Penn, R. D., and Hagins, W. A. (1969). Signal transmission along retinal rods and the origin of the electroretinographic a-wave. Nature 223, 201-204. doi: 10.1038/223201a0
100. 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
101. 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
102. Penuela, S., Kelly, J. J., Churko, J. M., Barr, K. J., Berger, A. C., and Laird, D. W. (2014a). Panx1 regulates cellular properties of keratinocytes and dermal fibroblasts in skin development and wound healing. J. Invest. Dermatol.134, 2026-2035. doi: 10.1038/jid.2014.86
103. Penuela, S., Simek, J., and Thompson, R. J. (2014b). Regulation of pannexin channels by post-translational modifications. FEBS Lett. 588, 1411-1415. doi: 10.1016/j.febslet.2014.01.028
104. Postlethwait, J. H. (2007). The zebrafish genome in context: ohnologs gone missing. J. Exp. Zool. B Mol. Dev. Evol.308, 563-577. doi: 10.1002/jez.b.21137
105. Pottek, M., Hoppenstedt, W., Janssen-Bienhold, U., Schultz, K., Perlman, I., and Weiler, R. (2003). Contribution of connexin26 to electrical feedback inhibition in the turtle retina. J. Comp. Neurol. 466, 468-477. doi: 10.1002/cne.10897
106. 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
107. Prochnow, N., Hoffmann, S., Vroman, R., Klooster, J., Bunse, S., Kamermans, M., et al. (2009). Pannexin1 in the outer retina of the zebrafish, Danio rerio. Neuroscience 162, 1039-1054. doi: 10.1016/j.neuroscience.2009.04.064
108. Puthussery, T., Yee, P., Vingrys, A. J., and Fletcher, E. L. (2006). Evidence for the involvement of purinergic P2X receptors in outer retinal processing. Eur. J. Neurosci. 24, 7-19. doi: 10.1111/j.1460-9568.2006.04895.x
109. Qiu, F., and Dahl, G. (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
110. 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
111. Ravi, V., and Venkatesh, B. (2008). Rapidly evolving fish genomes and teleost diversity. Curr. Opin. Genet. Dev. 18, 544-550. doi: 10.1016/j.gde.2008.11.001
112. Ray, A., Zoidl, G., Wahle, P., and Dermietzel, R. (2006). Pannexin expression in the cerebellum. Cerebellum 5, 189-192. doi: 10.1080/14734220500530082
113. 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
114. 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
115. 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
116. Retamal, M. A. (2014). Connexin and Pannexin hemichannels are regulated by redox potential. Front. Physiol.5:80. doi: 10.3389/fphys.2014.00080
117. Retamal, M. A., Schalper, K. A., Shoji, K. F., Bennett, M. V., and Saez, J. C. (2007). Opening of connexin 43 hemichannels is increased by lowering intracellular redox potential. Proc. Natl. Acad. Sci. U S A 104, 8322-8327. doi: 10.1073/pnas.0702456104
118. 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
119. Sabirov, R. Z., Dutta, A. K., and Okada, Y. (2001). Volume-dependent ATP-conductive large-conductance anion channel as a pathway for swelling-induced ATP release. J. Gen. Physiol. 118, 251-266. doi: 10.1085/jgp.118.3.251
120. Saez, J. C., and Leybaert, L. (2014). Hunting for connexin hemichannels. FEBS Lett. 588, 1205-1211. doi: 10.1016/j.febslet.2014.03.004
121. 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
122. Schalper, K. A., Orellana, J. A., Berthoud, V. M., and Saez, J. C. (2009). Dysfunctions of the diffusional membrane pathways mediated by hemichannels in inherited and acquired human diseases. Curr. Vasc. Pharmacol. 7, 486-505. doi: 10.2174/157016109789043937
123. 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: 10.3410/f.1123131.580258
124. Seminario-Vidal, L., Kreda, S., Jones, L., O'Neal, W., Trejo, J., Boucher, R. C., et al. (2009). Thrombin promotes release of ATP from lung epithelial cells through coordinated activation of rho- and Ca2+-dependent signaling pathways. J. Biol. Chem. 284, 20638-20648. doi: 10.1074/jbc.M109.004762
125. 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
126. Séror, 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
127. 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
128. Shearer, T. W., and Crosson, C. E. (2002). Adenosine A1 receptor modulation of MMP-2 secretion by trabecular meshwork cells. Invest. Ophthalmol. Vis. Sci. 43, 3016-3020.
129. 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
130. 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
131. Skapinker, R., and Rothberg, A. D. (1987). Postnatal regression of the tunica vasculosa lentis. J. Perinatol. 7, 279-281.
132. 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
133. 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
134. 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
135. Sun, Z., Risner, M. L., van Asselt, J. B., Zhang, D. Q., Kamermans, M., and McMahon, D. G. (2012). Physiological and molecular characterization of connexin hemichannels in zebrafish retinal horizontal cells. J. Neurophysiol. 107, 2624-2632. doi: 10.1152/jn.01126.2011
136. 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
137. 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
138. Toris, C. B., Gabelt, B. T., and Kaufman, P. L. (2008). Update on the mechanism of action of topical prostaglandins for intraocular pressure reduction. Surv. Ophthalmol. 53(Suppl. 1), S107-S120. doi: 10.1016/j.survophthal.2008.08.010
139. Ueda, T., Shikano, M., Kamiya, T., Joh, T., and Ugawa, S. (2011). The TRPV4 channel is a novel regulator of intracellular Ca2+ in human esophageal epithelial cells. Am. J. Physiol. Gastrointest. Liver Physiol. 301, G138-G147. doi: 10.1152/ajpgi.00511.2010
140. 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
141. 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
142. Volgyi, B., Kovacs-Oller, T., Atlasz, T., Wilhelm, M., and Gabriel, R. (2013). Gap junctional coupling in the vertebrate retina: variations on one theme? Prog. Retin. Eye Res. 34, 1-18. doi: 10.1016/j.preteyeres.2012.12.002
143. Vroman, R., Klaassen, L. J., Howlett, M. H., Cenedese, V., Klooster, J., Sjoerdsma, T., et al. (2014). Extracellular ATP hydrolysis inhibits synaptic transmission by increasing ph buffering in the synaptic cleft. PLoS Biol.12:e1001864. doi: 10.1371/journal.pbio.1001864
144. Vroman, R., Klaassen, L. J., and Kamermans, M. (2013). Ephaptic communication in the vertebrate retina. Front. Hum. Neurosci. 7:612. doi: 10.3389/fnhum.2013.00612
145. Wang, J., Jackson, D. G., and Dahl, G. (2013). 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
146. 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
147. 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
148. Woehrle, T., Yip, L., Elkhal, A., Sumi, Y., Chen, Y., Yao, Y., et al. (2010). 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
149. Wong, W. T., Wang, M., and Li, W. (2011). Regulation of microglia by ionotropic glutamatergic and GABAergic neurotransmission. Neuron Glia Biol. 7, 41-46. doi: 10.1017/S1740925x11000123
150. 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
151. Xiang, Z., Chen, M., Ping, J., Dunn, P., Lv, J., Jiao, B., et al. (2006). Microglial morphology and its transformation after challenge by extracellular ATP in vitro. J. Neurosci. Res. 83, 91-101. doi: 10.1002/jnr.20709
152. Xin, D., and Bloomfield, S. A. (1999). Dark- and light-induced changes in coupling between horizontal cells in mammalian retina. J. Comp. Neurol. 405, 75-87. doi: 10.1002/(sici)1096-9861(19990301)405:1<75::aid-cne6>3.0.co;2-d
153. Yang, L., Mali, P., Kim-Kiselak, C., and Church, G. (2014). CRISPR-Cas-mediated targeted genome editing in human cells. Methods Mol. Biol. 1114, 245-267. doi: 10.1007/978-1-62703-761-7_16
154. 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
155. 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
156. Zhang, H., Chen, Y., and Zhang, C. (2012). 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
157. Zhang, X., Li, A., Ge, J., Reigada, D., Laties, A. M., and Mitchell, C. H. (2007). Acute increase of intraocular pressure releases ATP into the anterior chamber. Exp. Eye Res. 85, 637-643. doi: 10.1016/j.exer.2007.07.016
158. Zhang, J., Peng, S., Lin, M., and Du, C. (2005). [Clinical study of twenty-four-hour pattern of intraocular pressure in normal person and patient with primary open-angle glaucoma]. Yan Ke Xue Bao 21, 127-130.
159. 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
160. 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