P2X receptors as targets for the treatment of status epilepticus

Frontiers in Cellular Neuroscience

Volumn 7, Issue NOV, 2013, Pages

  Henshall, David C ^a   Diaz Hernandez, Miguel ^b,c   Miras Portugal, M Teresa ^b,c   Engel, Tobias ^a  

^a ROYAL COLLEGE OF SURGEONS IN IRELAND   (Ireland)

^b UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

^c HOSPITAL CLÍNICO SAN CARLOS   (Spain)

Author keywords

Anticonvulsant; ATP; Epilepsy; Hippocampus; Interleukin 1 ; Microglia; Neuroprotection

Indexed keywords

3 [[5 (2, 3 DICHLOROPHENYL) 1H TETRAZOL 1 YL] METHYL] PYRIDINE; ADENOSINE TRIPHOSPHATE; KAINIC ACID; LORAZEPAM; PHENYTOIN; PILOCARPINE; PURINERGIC P2X RECEPTOR; PURINERGIC P2X RECEPTOR ANTAGONIST; PURINERGIC P2X1 RECEPTOR; PURINERGIC P2X2 RECEPTOR; PURINERGIC P2X3 RECEPTOR; PURINERGIC P2X4 RECEPTOR; PURINERGIC P2X5 RECEPTOR; PURINERGIC P2X6 RECEPTOR; PURINERGIC P2X7 RECEPTOR; UNCLASSIFIED DRUG;

ARTICLE; ASTROCYTE; CELL DEATH; DISEASE SEVERITY; DOWN REGULATION; EPILEPTIC STATE; EXCITABILITY; EXCITOTOXICITY; EXOCYTOSIS; HIPPOCAMPUS; HUMAN; IMMUNOREACTIVITY; INCIDENCE; INFLAMMATION; MICROGLIA; MORTALITY; NEUROPATHIC PAIN; NONHUMAN; PROTEIN EXPRESSION; SEIZURE;

EID: 84888401362     PISSN: 16625102     EISSN: None     Source Type: Journal    
DOI: 10.3389/fncel.2013.00237     Document Type: Article

References (107)

1. Abbracchio, M. P., Burnstock, G., Verkhratsky, A., and Zimmermann, H. (2009). Purinergic signalling in the nervous system: an overview. Trends Neurosci. 32, 19-29. doi: 10.1016/j.tins.2008.10.001.
2. Alves, L. A., Bezerra, R. J., Faria, R. X., Ferreira, L. G., and Da Silva Frutuoso, V. (2013). Physiological roles and potential therapeutic applications of the P2X7 receptor in inflammation and pain. Molecules 18, 10953-10972. doi: 10.3390/molecules180910953.
3. Anderson, C. M., and Nedergaard, M. (2006). Emerging challenges of assigning P2X7 receptor function and immunoreactivity in neurons. Trends Neurosci. 29, 257-262. doi: 10.1016/j.tins.2006.03.003.
4. Arbeloa, J., Perez-Samartin, A., Gottlieb, M., and Matute, C. (2012). P2X7 receptor blockade prevents ATP excitotoxicity in neurons and reduces brain damage after ischemia. Neurobiol. Dis. 45, 954-961. doi: 10.1016/j.nbd.2011.12.014.
5. Armstrong, J. N., Brust, T. B., Lewis, R. G., and Macvicar, B. A. (2002). Activation of presynaptic P2X7-like receptors depresses mossy fiber-CA3 synaptic transmission through p38 mitogen-activated protein kinase. J. Neurosci. 22, 5938-5945.
6. Avignone, E., Ulmann, L., Levavasseur, F., Rassendren, F., and Audinat, E. (2008). Status epilepticus induces a particular microglial activation state characterized by enhanced purinergic signaling. J. Neurosci. 28, 9133-9144. doi: 10.1523/JNEUROSCI.1820-08.2008.
7. Bernardino, L., Balosso, S., Ravizza, T., Marchi, N., Ku, G., Randle, J. C., et al. (2008). Inflammatory events in hippocampal slice cultures prime neuronal susceptibility to excitotoxic injury: a crucial role of P2X7 receptor-mediated IL-1beta release. J. Neurochem. 106, 271-280. doi: 10.1111/j.1471-4159.2008.05387.x.
8. Bhattacharya, A., Wang, Q., Ao, H., Shoblock, J. R., Lord, B., Aluisio, L., et al. (2013). Pharmacological characterization of a novel centrally permeable P2X7 receptor antagonist: JNJ-47965567. Br. J. Pharmacol. 170, 624-640. doi: 10.1111/bph.12314.
9. Bialer, M., and White, H. S. (2010). Key factors in the discovery and development of new antiepileptic drugs. Nat. Rev. Drug Discov. 9, 68-82. doi: 10.1038/nrd2997.
10. Boison, D. (2008). The adenosine kinase hypothesis of epileptogenesis. Prog. Neurobiol. 84, 249-262. doi: 10.1016/j.pneurobio.2007.12.002.
11. Boison, D. (2013a). Adenosine kinase: exploitation for therapeutic gain. Pharmacol. Rev. 65, 906-943. doi: 10.1124/pr.112.006361.
12. Boison, D. (2013b). Role of adenosine in status epilepticus: a potential new target?Epilepsia 54(Suppl. 6), 20-22. doi: 10.1111/epi.12268.
13. Brophy, G. M., Bell, R., Claassen, J., Alldredge, B., Bleck, T. P., Glauser, T., et al. (2012). Guidelines for the evaluation and management of status epilepticus. Neurocrit. Care 17, 3-23. doi: 10.1007/s12028-012-9695-z.
14. Burnstock, G. (2007). Physiology and pathophysiology of purinergic neurotransmission. Physiol. Rev. 87, 659-797. doi: 10.1152/physrev.00043.2006.
15. Burnstock, G. (2008). Purinergic signalling and disorders of the central nervous system. Nat. Rev. Drug Discov. 7, 575-590. doi: 10.1038/nrd2605.
16. Cavaliere, F., Amadio, S., Dinkel, K., Reymann, K.G., and Volonte, C. (2007). P2 receptor antagonist trinitrophenyl-adenosine-triphosphate protects hippocampus from oxygen and glucose deprivation cell death. J. Pharmacol. Exp. Ther. 323, 70-77. doi: 10.1124/jpet.106.119024.
17. Cervetto, C., Frattaroli, D., Maura, G., and Marcoli, M. (2013). Motor neuron dysfunction in a mouse model of ALS: gender-dependent effect of P2X7 antagonism. Toxicology 311, 69-77. doi: 10.1016/j.tox.2013.04.004.
18. Chakfe, Y., Seguin, R., Antel, J. P., Morissette, C., Malo, D., Henderson, D., et al. (2002). ADP and AMP induce interleukin-1beta release from microglial cells through activation of ATP-primed P2X7 receptor channels. J. Neurosci. 22, 3061-3069.
19. Chen, J. W., and Wasterlain, C. G. (2006). Status epilepticus: pathophysiology and management in adults. Lancet Neurol. 5, 246-256. doi: 10.1016/S1474-4422(06)70374-X.
20. Chen, S., Ma, Q., Krafft, P. R., Chen, Y., Tang, J., Zhang, J., et al. (2013). P2X7 receptor antagonism inhibits p38 mitogen-activated protein kinase activation and ameliorates neuronal apoptosis after subarachnoid hemorrhage in rats. Crit. Care Med. doi: 10.1097/CCM.0b013e31829a8246. [Epub ahead of print].
21. Chessell, I. P., Simon, J., Hibell, A. D., Michel, A. D., Barnard, E. A., and Humphrey, P. P. (1998). Cloning and functional characterisation of the mouse P2X7 receptor. FEBS Lett. 439, 26-30. doi: 10.1016/S0014-5793(98)01332-5.
22. Choi, H. K., Ryu, H. J., Kim, J. E., Jo, S. M., Choi, H. C., Song, H. K., et al. (2012). The roles of P2X7 receptor in regional-specific microglial responses in the rat brain following status epilepticus. Neurol. Sci. 33, 515-525. doi: 10.1007/s10072-011-0740-z.
23. Collo, G., Neidhart, S., Kawashima, E., Kosco-Vilbois, M., North, R. A., and Buell, G. (1997). Tissue distribution of the P2X7 receptor. Neuropharmacology 36, 1277-1283. doi: 10.1016/S0028-3908(97)00140-8.
24. Collo, G., North, R. A., Kawashima, E., Merlo-Pich, E., Neidhart, S., Surprenant, A., et al. (1996). Cloning of P2X5 and P2X6 receptors and the distribution and properties of an extended family of ATP-gated ion channels. J. Neurosci. 16, 2495-2507.
25. Craigie, E., Birch, R. E., Unwin, R. J., and Wildman, S. S. (2013). The relationship between P2X4 and P2X7: a physiologically important interaction? Front. Physiol. 4:216. doi: 10.3389/fphys.2013.00216.
26. Curia, G., Longo, D., Biagini, G., Jones, R. S., and Avoli, M. (2008). The pilocarpine model of temporal lobe epilepsy. J. Neurosci. Methods 172, 143-157. doi: 10.1016/j.jneumeth.2008.04.019.
27. Dale, N., and Frenguelli, B. G. (2009). Release of adenosine and ATP during ischemia and epilepsy. Curr. Neuropharmacol. 7, 160-179. doi: 10.2174/157015909789152146.
28. Deuchars, S. A., Atkinson, L., Brooke, R. E., Musa, H., Milligan, C. J., Batten, T. F., et al. (2001). Neuronal P2X7 receptors are targeted to presynaptic terminals in the central and peripheral nervous systems. J. Neurosci. 21, 7143-7152.
29. Devinsky, O., Vezzani, A., Najjar, S., De Lanerolle, N. C., and Rogawski, M. A. (2013). Glia and epilepsy: excitability and inflammation. Trends Neurosci. 36, 174-184. doi: 10.1016/j.tins.2012.11.008.
30. Diaz-Hernandez, J. I., Gomez-Villafuertes, R., Leon-Otegui, M., Hontecillas-Prieto, L., Del Puerto, A., Trejo, J. L., et al. (2012). In vivo P2X7 inhibition reduces amyloid plaques in Alzheimer's disease through GSK3beta and secretases. Neurobiol. Aging33, 1816-1828. doi: 10.1016/j.neurobiolaging.2011.09.040.
31. Diaz-Hernandez, M., Del Puerto, A., Diaz-Hernandez, J. I., Diez-Zaera, M., Lucas, J. J., Garrido, J. J., et al. (2008). Inhibition of the ATP-gated P2X7 receptor promotes axonal growth and branching in cultured hippocampal neurons. J. Cell. Sci. 121, 3717-3728. doi: 10.1242/jcs.034082.
32. Diaz-Hernandez, M., Diez-Zaera, M., Sanchez-Nogueiro, J., Gomez-Villafuertes, R., Canals, J. M., Alberch, J., et al. (2009). Altered P2X7-receptor level and function in mouse models of Huntington's disease and therapeutic efficacy of antagonist administration. FASEB J. 23, 1893-1906. doi: 10.1096/fj.08-122275.
33. Di Virgilio, F., Chiozzi, P., Falzoni, S., Ferrari, D., Sanz, J. M., Venketaraman, V., et al. (1998). Cytolytic P2X purinoceptors. Cell Death Differ. 5, 191-199. doi: 10.1038/sj.cdd.4400341.
34. Dona, F., Ulrich, H., Persike, D. S., Conceicao, I. M., Blini, J. P., Cavalheiro, E. A., et al. (2009). Alteration of purinergic P2X4 and P2X7 receptor expression in rats with temporal-lobe epilepsy induced by pilocarpine. Epilepsy Res. 83, 157-167. doi: 10.1016/j.eplepsyres.2008.10.008.
35. Duan, S., Anderson, C. M., Keung, E. C., Chen, Y., and Swanson, R. A. (2003). P2X7 receptor-mediated release of excitatory amino acids from astrocytes. J. Neurosci. 23, 1320-1328.
36. Engel, T., Gomez-Villafuertes, R., Tanaka, K., Mesuret, G., Sanz-Rodriguez, A., Garcia-Huerta, P., et al. (2012a). Seizure suppression and neuroprotection by targeting the purinergic P2X7 receptor during status epilepticus in mice. FASEB J. 26, 1616-1628. doi: 10.1096/fj.11-196089.
37. Engel, T., Jimenez-Pacheco, A., Miras-Portugal, M. T., Diaz-Hernandez, M., and Henshall, D. C. (2012b). P2X7 receptor in epilepsy; role in pathophysiology and potential targeting for seizure control. Int. J. Physiol. Pathophysiol. Pharmacol. 4, 174-187.
38. Fabene, P. F., Merigo, F., Galie, M., Benati, D., Bernardi, P., Farace, P., et al. (2007). Pilocarpine-induced status epilepticus in rats involves ischemic and excitotoxic mechanisms. PLoS ONE 2:e1105. doi: 10.1371/journal.pone.0001105.
39. Ferrari, D., Villalba, M., Chiozzi, P., Falzoni, S., Ricciardi-Castagnoli, P., and Di Virgilio, F. (1996). Mouse microglial cells express a plasma membrane pore gated by extracellular ATP. J. Immunol. 156, 1531-1539.
40. Gever, J. R., Cockayne, D. A., Dillon, M. P., Burnstock, G., and Ford, A. P. (2006). Pharmacology of P2X channels. Pflugers Arch. 452, 513-537. doi: 10.1007/s00424-006-0070-9.
41. Guo, W., Xu, X., Gao, X., Burnstock, G., He, C., and Xiang, Z. (2008). Expression of P2X5 receptors in the mouse CNS. Neuroscience 156, 673-692. doi: 10.1016/j.neuroscience.2008.07.062.
42. Houser, C. R., Zhang, N., Peng, Z., Huang, C. S., and Cetina, Y. (2012). Neuroanatomical clues to altered neuronal activity in epilepsy: from ultrastructure to signaling pathways of dentate granule cells. Epilepsia 53(Suppl. 1), 67-77. doi: 10.1111/j.1528-1167.2012.03477.x.
43. 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.
44. Jimenez-Pacheco, A., Mesuret, G., Sanz-Rodriguez, A., Tanaka, K., Mooney, C., Conroy, R., et al. (2013). Increased neocortical expression of the P2X7 receptor after status epilepticus and anticonvulsant effect of P2X7 receptor antagonist A-438079. Epilepsia 54, 1551-1561. doi: 10.1111/epi.12257.
45. Kang, T. C., An, S. J., Park, S. K., Hwang, I. K., and Won, M. H. (2003). P2X2 and P2X4 receptor expression is regulated by a GABA(A) receptor-mediated mechanism in the gerbil hippocampus. Brain Res. Mol. Brain Res. 116, 168-175. doi: 10.1016/S0169-328X(03)00260-2.
46. Kanjhan, R., Housley, G. D., Burton, L. D., Christie, D. L., Kippenberger, A., Thorne, P. R., et al. (1999). Distribution of the P2X2 receptor subunit of the ATP-gated ion channels in the rat central nervous system. J. Comp. Neurol. 407, 11-32. doi: 10.1002/(SICI)1096-9861(19990428)407:1<11::AID-CNE2>3.0.CO;2-R.
47. Khakh, B. S. (2001). Molecular physiology of P2X receptors and ATP signalling at synapses. Nat. Rev. Neurosci. 2, 165-174. doi: 10.1038/35058521.
48. Khakh, B. S., Gittermann, D., Cockayne, D. A., and Jones, A. (2003). ATP modulation of excitatory synapses onto interneurons. J. Neurosci. 23, 7426-7437.
49. Khakh, B. S., and North, R. A. (2006). P2X receptors as cell-surface ATP sensors in health and disease. Nature 442, 527-532. doi: 10.1038/nature04886.
50. 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.
51. Kim, J. E., Kwak, S. E., Jo, S. M., and Kang, T. C. (2009). Blockade of P2X receptor prevents astroglial death in the dentate gyrus following pilocarpine-induced status epilepticus. Neurol. Res. 31, 982-988. doi: 10.1179/174313209X389811.
52. Kim, J. E., Ryu, H. J., Yeo, S. I., and Kang, T. C. (2011a). P2X7 receptor differentially modulates astroglial apoptosis and clasmatodendrosis in the rat brain following status epilepticus. Hippocampus 21, 1318-1333. doi: 10.1002/hipo.20850.
53. Kim, J. E., Ryu, H. J., and Kang, T. C. (2011b). P2X7 receptor activation ameliorates CA3 neuronal damage via a tumor necrosis factor-alpha-mediated pathway in the rat hippocampus following status epilepticus. J. Neuroinflammation 8:62. doi: 10.1186/1742-2094-8-62.
54. Kim, M., Jiang, L. H., Wilson, H. L., North, R. A., and Surprenant, A. (2001). Proteomic and functional evidence for a P2X7 receptor signalling complex. EMBO J. 20, 6347-6358. doi: 10.1093/emboj/20.22.6347.
55. Klaft, Z. J., Schulz, S. B., Maslarova, A., Gabriel, S., Heinemann, U., and Gerevich, Z. (2012). Extracellular ATP differentially affects epileptiform activity via purinergic P2X7 and adenosine A1 receptors in naive and chronic epileptic rats. Epilepsia 53, 1978-1986. doi: 10.1111/j.1528-1167.2012.03724.x.
56. Lalo, U., Pankratov, Y., Wichert, S. P., Rossner, M. J., North, R. A., Kirchhoff, F., et al. (2008). P2X1 and P2X5 subunits form the functional P2X receptor in mouse cortical astrocytes. J. Neurosci. 28, 5473-5480. doi: 10.1523/JNEUROSCI.1149-08.2008.
57. Lazarowski, E. R., Boucher, R. C., and Harden, T. K. (2003). Mechanisms of release of nucleotides and integration of their action as P2X-and P2Y-receptor activating molecules. Mol. Pharmacol. 64, 785-795. doi: 10.1124/mol.64.4.785.
58. Le Feuvre, R. A., Brough, D., Touzani, O., and Rothwell, N. J. (2003). Role of P2X7 receptors in ischemic and excitotoxic brain injury in vivo. J. Cereb. Blood Flow Metab. 23, 381-384. doi: 10.1097/00004647-200303000-00013.
59. Le, K. T., Villeneuve, P., Ramjaun, A. R., Mcpherson, P. S., Beaudet, A., and Seguela, P. (1998). Sensory presynaptic and widespread somatodendritic immunolocalization of central ionotropic P2X ATP receptors. Neuroscience 83, 177-190. doi: 10.1016/80306-4522(97)00365-5.
60. Li, T., Ren, G., Lusardi, T., Wilz, A., Lan, J. Q., Iwasato, T., et al. (2008). Adenosine kinase is a target for the prediction and prevention of epileptogenesis in mice. J. Clin. Invest. 118, 571-582. doi: 10.1172/JCI33737.
61. Liu, G., Gu, B., He, X. P., Joshi, R. B., Wackerle, H. D., Rodriguiz, R. M., et al. (2013). Transient inhibition of TrkB kinase after status epilepticus prevents development of temporal lobe epilepsy. Neuron 79, 31-38. doi: 10.1016/j.neuron.2013.04.027.
62. Lopatar, J., Dale, N., and Frenguelli, B. G. (2011). Minor contribution of ATP P2 receptors to electrically-evoked electrographic seizure activity in hippocampal slices: evidence from purine biosensors and P2 receptor agonists and antagonists. Neuropharmacology 61, 25-34. doi: 10.1016/j.neuropharm.2011.02.011.
63. Loscher, W. (2002). Animal models of epilepsy for the development of antiepileptogenic and disease-modifying drugs. A comparison of the pharmacology of kindling and post-status epilepticus models of temporal lobe epilepsy. Epilepsy Res. 50, 105-123. doi: 10.1016/S0920-1211(02)00073-6.
64. Loscher, W. (2009). Molecular mechanisms of drug resistance in status epilepticus. Epilepsia 50(Suppl. 12), 19-21. doi: 10.1111/j.1528-1167.2009.02367.x.
65. Lowenstein, D. H. (2005). Treatment options for status epilepticus. Curr. Opin. Pharmacol. 5, 334-339. doi: 10.1016/j.coph.2005.04.003.
66. Marcellino, D., Suarez-Boomgaard, D., Sanchez-Reina, M. D., Aguirre, J. A., Yoshitake, T., Yoshitake, S., et al. (2010). On the role of P2X(7) receptors in dopamine nerve cell degeneration in a rat model of Parkinson's disease: studies with the P2X(7) receptor antagonist A-438079. J. Neural Transm. 117, 681-687. doi: 10.1007/s00702-010-0400-0.
67. Marchi, N., Fan, Q., Ghosh, C., Fazio, V., Bertolini, F., Betto, G., et al. (2009). Antagonism of peripheral inflammation reduces the severity of status epilepticus. Neurobiol. Dis. 33, 171-181. doi: 10.1016/j.nbd.2008.10.002.
68. Masin, M., Young, C., Lim, K., Barnes, S. J., Xu, X. J., Marschall, V., et al. (2012). Expression, assembly and function of novel C-terminal truncated variants of the mouse P2X7 receptor: re-evaluation of P2X7 knockouts. Br. J. Pharmacol. 165, 978-993. doi: 10.1111/j.1476-5381.2011.01624.x.
69. Matute, C., Torre, I., Perez-Cerda, F., Perez-Samartin, A., Alberdi, E., Etxebarria, E., et al. (2007). P2X(7) receptor blockade prevents ATP excitotoxicity in oligodendrocytes and ameliorates experimental autoimmune encephalomyelitis. J. Neurosci. 27, 9525-9533. doi: 10.1523/JNEUROSCI.0579-07.2007.
70. McGaraughty, S., Chu, K. L., Namovic, M. T., Donnelly-Roberts, D. L., Harris, R. R., Zhang, X. F., et al. (2007). P2X7-related modulation of pathological nociception in rats. Neuroscience 146, 1817-1828. doi: 10.1016/j.neuroscience.2007.03.035.
71. Melani, A., Amadio, S., Gianfriddo, M., Vannucchi, M. G., Volonte, C., Bernardi, G., et al. (2006). P2X7 receptor modulation on microglial cells and reduction of brain infarct caused by middle cerebral artery occlusion in rat. J. Cereb. Blood Flow Metab. 26, 974-982. doi: 10.1038/sj.jcbfm.9600250.
72. Monif, M., Reid, C. A., Powell, K. L., Smart, M. L., and Williams, D. A. (2009). The P2X7 receptor drives microglial activation and proliferation: a trophic role for P2X7R pore.J. Neurosci. 29, 3781-3791. doi: 10.1523/JNEUROSCI.5512-08.2009.
73. Mouri, G., Jimenez-Mateos, E., Engel, T., Dunleavy, M., Hatazaki, S., Paucard, A., et al. (2008). Unilateral hippocampal CA3-predominant damage and short latency epileptogenesis after intra-amygdala microinjection of kainic acid in mice. Brain Res. 1213, 140-151. doi: 10.1016/j.brainres.2008.03.061.
74. Murphy, N., Cowley, T. R., Richardson, J. C., Virley, D., Upton, N., Walter, D., et al. (2012). The neuroprotective effect of a specific P2X(7) receptor antagonist derives from its ability to inhibit assembly of the NLRP3 inflammasome in glial cells. Brain Pathol. 22, 295-306. doi: 10.1111/j.1750-3639.2011.00531.x.
75. Nicke, A., Kuan, Y. H., Masin, M., Rettinger, J., Marquez-Klaka, B., Bender, O., et al. (2009). A functional P2X7 splice variant with an alternative transmembrane domain 1 escapes gene inactivation in P2X7 knock-out mice. J. Biol. Chem. 284, 25813-25822. doi: 10.1074/jbc.M109.033134.
76. Norenberg, W., and Illes, P. (2000). Neuronal P2X receptors: localisation and functional properties. Naunyn Schmiedebergs Arch. Pharmacol. 362, 324-339. doi: 10.1007/s002100000311.
77. North, R. A. (2002). Molecular physiology of P2X receptors. Physiol. Rev. 82, 1013-1067.
78. North, R. A., and Jarvis, M. F. (2013). P2X receptors as drug targets. Mol. Pharmacol. 83, 759-769. doi: 10.1124/mol.112.083758.
79. North, R. A., and Surprenant, A. (2000). Pharmacology of cloned P2X receptors. Annu. Rev. Pharmacol. Toxicol. 40, 563-580. doi: 10.1146/annurev.pharmtox.40.1.563.
80. Pankratov, Y. V., Lalo, U. V., and Krishtal, O. A. (2002). Role for P2X receptors in long-term potentiation. J. Neurosci. 22, 8363-8369.
81. Papp, L., Balazsa, T., Kofalvi, A., Erdelyi, F., Szabo, G., Vizi, E. S., et al. (2004). P2X receptor activation elicits transporter-mediated noradrenaline release from rat hippocampal slices. J. Pharmacol. Exp. Ther. 310, 973-980. doi: 10.1124/jpet.104.066712.
82. 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.
83. Peng, W., Cotrina, M. L., Han, X., Yu, H., Bekar, L., Blum, L., et al. (2009). Systemic administration of an antagonist of the ATP-sensitive receptor P2X7 improves recovery after spinal cord injury. Proc. Natl. Acad. Sci. U.S.A. 106, 12489-12493. doi: 10.1073/pnas.0902531106.
84. Rappold, P. M., Lynd-Balta, E., and Joseph, S. A. (2006). P2X7 receptor immunoreactive profile confined to resting and activated microglia in the epileptic brain. Brain Res. 1089, 171-178. doi: 10.1016/j.brainres.2006.03.040.
85. Ross, F. M., Brodie, M. J., and Stone, T. W. (1998). Modulation by adenine nucleotides of epileptiform activity in the CA3 region of rat hippocampal slices. Br. J. Pharmacol. 123, 71-80. doi: 10.1038/sj.bjp.0701586.
86. Rubio, M. E., and Soto, F. (2001). Distinct Localization of P2X receptors at excitatory postsynaptic specializations. J. Neurosci. 21, 641-653.
87. Seguela, P., Haghighi, A., Soghomonian, J. J., and Cooper, E. (1996). A novel neuronal P2x ATP receptor ion channel with widespread distribution in the brain. J. Neurosci. 16, 448-455.
88. Shorvon, S. (2011). The treatment of status epilepticus. Curr. Opin. Neurol. 24, 165-170. doi: 10.1097/WCO.0b013e3283446f31.
89. Sim, J. A., Young, M. T., Sung, H. Y., North, R. A., and Surprenant, A. (2004). Reanalysis of P2X7 receptor expression in rodent brain. J. Neurosci. 24, 6307-6314. doi: 10.1523/JNEUROSCI.1469-04.2004.
90. Skaper, S. D., Debetto, P., and Giusti, P. (2010). The P2X7 purinergic receptor: from physiology to neurological disorders. FASEB J. 24, 337-345. doi: 10.1096/fj.09-138883.
91. Slaughter, L. A., Patel, A. D., and Slaughter, J. L. (2013). Pharmacological treatment of neonatal seizures: a systematic review. J. Child Neurol. 28, 351-364. doi: 10.1177/0883073812470734.
92. 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.
93. Sperk, G. (1994). Kainic acid seizures in the rat. Prog. Neurobiol. 42, 1-32. doi: 10.1016/0301-0082(94)90019-1.
94. Sperlagh, B., Heinrich, A., and Csolle, C. (2007). P2 receptor-mediated modulation of neurotransmitter release-an update. Purinergic Signal. 3, 269-284. doi: 10.1007/s11302-007-9080-0.
95. Surprenant, A., Rassendren, F., Kawashima, E., North, R. A., and Buell, G. (1996). The cytolytic P2Z receptor for extracellular ATP identified as a P2X receptor (P2X7). Science 272, 735-738. doi: 10.1126/science.272.5262.735.
96. Synowiec, A. S., Singh, D. S., Yenugadhati, V., Valeriano, J. P., Schramke, C. J., and Kelly, K. M. (2013). Ketamine use in the treatment of refractory status epilepticus. Epilepsy Res. 105, 183-188. doi: 10.1016/j.eplepsyres.2013.01.007.
97. Trang, T., Beggs, S., and Salter, M. W. (2012). ATP receptors gate microglia signaling in neuropathic pain. Exp. Neurol. 234, 354-361. doi: 10.1016/j.expneurol.2011.11.012.
98. Ulmann, L., Levavasseur, F., Avignone, E., Peyroutou, R., Hirbec, H., Audinat, E., et al. (2013). Involvement of P2X4 receptors in hippocampal microglial activation after status epilepticus. Glia 61, 1306-1319. doi: 10.1002/glia.22516.
99. Vessey, D. A., Li, L., and Kelley, M. (2011). 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.
100. Vezzani, A., Balosso, S., Maroso, M., Zardoni, D., Noe, F., and Ravizza, T. (2010). ICE/caspase 1 inhibitors and IL-1beta receptor antagonists as potential therapeutics in epilepsy. Curr. Opin. Investig. Drugs 11, 43-50.
101. Virginio, C., Mackenzie, A., Rassendren, F. A., North, R. A., and Surprenant, A. (1999). Pore dilation of neuronal P2X receptor channels. Nat. Neurosci. 2, 315-321. doi: 10.1038/7225.
102. Wasterlain, C. G., and Chen, J. W. (2006). "Definition and classification of status epilepticus, " in Status Epilepticus: Mechanisms and Management, eds C. G. Wasterlain and D. M. Treiman. (Cambridge, MA: MIT Press), 11-16.
103. Wieraszko, A., and Seyfried, T. N. (1989). Increased amount of extracellular ATP in stimulated hippocampal slices of seizure prone mice. Neurosci. Lett. 106, 287-293. doi: 10.1016/0304-3940(89)90178-X.
104. Yanagisawa, D., Kitamura, Y., Takata, K., Hide, I., Nakata, Y., and Taniguchi, T. (2008). Possible involvement of P2X7 receptor activation in microglial neuroprotection against focal cerebral ischemia in rats. Biol. Pharm. Bull. 31, 1121-1130. doi: 10.1248/bpb.31.1121.
105. Yu, Q., Guo, Z., Liu, X., Ouyang, Q., He, C., Burnstock, G., et al. (2013). Block of P2X7 receptors could partly reverse the delayed neuronal death in area CA1 of the hippocampus after transient global cerebral ischemia. Purinergic Signal. doi: 10.1007/s11302-013-9379-y. [Epub ahead of print].
106. Yu, Y., Ugawa, S., Ueda, T., Ishida, Y., Inoue, K., Kyaw Nyunt, A., et al. (2008). Cellular localization of P2X7 receptor mRNA in the rat brain. Brain Res. 1194, 45-55. doi: 10.1016/j.brainres.2007.11.064.
107. Ziemann, A. E., Schnizler, M. K., Albert, G. W., Severson, M. A., Howard, M. A. 3rd., Welsh, M. J., et al. (2008). Seizure termination by acidosis depends on ASIC1a. Nat. Neurosci. 11, 816-822. doi: 10.1038/nn.2132.