P2X7 receptor activation regulates microglial cell death during oxygen-glucose deprivation

Neuropharmacology

Volumn 73, Issue , 2013, Pages 311-319

  Eyo, Ukpong B ^a   Miner, Sam A ^a   Ahlers, Katelin E ^a   Wu, Long Jun ^b   Dailey, Michael E ^a  

^a UNIVERSITY OF IOWA   (United States)

^b RUTGERS UNIVERSITY   (United States)

Author keywords

ATP; Cell death; Microglia; OGD; P2X7; Stroke

Indexed keywords

APYRASE; BRILLIANT BLUE; CALCIUM ION; GLUCOSE; OXYGEN; PURINERGIC P2X7 RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN CELL; BRAIN ISCHEMIA; CELL DEATH; CELL FUNCTION; CELL SURVIVAL; CONTROLLED STUDY; EXTRACELLULAR CALCIUM; FEMALE; HIPPOCAMPUS; IN VITRO STUDY; MALE; MICROGLIA; MOUSE; NONHUMAN; PRIORITY JOURNAL; REGULATORY MECHANISM; TIME LAPSE IMAGING; TISSUE SECTION;

ATP; CELL DEATH; MICROGLIA; OGD; P2X7; STROKE;

ANIMALS; ANOXIA; APYRASE; CALCIUM; CELL DEATH; CELLS, CULTURED; EXTRACELLULAR SPACE; FEMALE; GLUCOSE; HIPPOCAMPUS; ISCHEMIA; MALE; MEMBRANE POTENTIALS; MICE; MICE, KNOCKOUT; MICROGLIA; PURINERGIC P2X RECEPTOR ANTAGONISTS; RECEPTORS, PURINERGIC P2X7; ROSANILINE DYES;

EID: 84885129284     PISSN: 00283908     EISSN: 18737064     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2013.05.032     Document Type: Article

References (61)

1. Alberdi, E., Sanchez-Gomez, M.V., Matute, C., 2005. Calcium and glial cell death. Cell Calcium 38, 417-425.
2. Arbeloa, J., Perez-Samartin, A., Gottlieb, M., Matute, C., 2012. P2X7 receptor blockade prevents ATP excitotoxicity in neurons and reduces brain damage after ischemia. Neurobiol. Dis. 45, 954-961.
3. Avignone, E., Ulmann, L., Levavasseur, F., Rassendren, F., Audinat, E., 2008. Status epilepticus induces a particular microglial activation state characterized by enhanced purinergic signaling. J. Neurosci. 28 (37), 9133-9144.
4. Barreto, G., White, R.E., Ouyang, Y., Xu, L., Giffard, R.G., 2011. Astrocytes: targets for neuroprotection in stroke. Cent. Nerv Syst. Agents Med. Chem. 11, 164-173.
5. Boucsein, C., Zacharias, R., Farber, K., Pavlovic, S., Hanisch, U.K., Kettenmann, H., 2003. Purinergic receptors on microglial cells: functional expression in acute brain slices and modulation of microglial activation in vitro. Eur. J. Neurosci. 17, 2267-2276.
6. Brautigam, V.M., Frasier, C., Nikodemova, M., Watters, J.J., 2005. Purinergic receptor modulation of BV-2 microglial cell activity: potential involvement of p38 MAP kinase and CREB. J. Neuroimmunol. 166, 113-125.
7. Burnstock, G., 2007. Physiology and pathophysiology of purinergic neurotransmission. Physiol. Rev. 87, 659-797.
8. Chu, K., Yin, B., Wang, J., Peng, G., Liang, H., Xu, Z., Du, Y., Fang, M., Xia, Q., Benyan, L., 2012. Inhibition of P2X7 receptor ameliorates transient global cerebral ischemia/reperfusion injury via modulating inflammatory responses in the rat hippocampus. J. Neuroinflammation 9, 69.
9. Di Virgilio, F., Sanz, J.M., Chiozzi, P., Falzoni, S., 1999. The P2Z/P2X7 receptor of microglial cells: a novel immunomodulatory receptor. Prog. Brain Res. 120, 355-368.
10. Domercq, M., Perez-Samartin, A., Aparicio, D., Alberdi, E., Pampliega, O., Matute, C., 2010. P2X7 receptors mediate ischemic damage to oligodendrocytes. Glia 58, 730-740.
11. Donnelly-Roberts, D.L., Namovic, M.T., Han, P., Jarvis, M.F., 2009. Mammalian P2X7 receptor pharmacology: comparison of recombinant mouse, rat and human P2X7 receptors. Br. J. Pharmacol. 157, 1203-1214.
12. Duan, S., Anderson, C.M., Keung, E.C., Chen, Y., Chen, Y., Swanson, R.A., 2003. P2X7 receptor-mediated release of excitatory amino acids from astrocytes. J. Neurosci. 23 (4), 1320-1328.
13. Eyo, U., Dailey, M.E., 2012. Effects of oxygen-glucose deprivation on microglial mobility and viability in developing mouse hippocampal tissues. Glia 60, 1747-1760.
14. Faustino, J.V., Wang, X., Johnson, C.E., Klibanov, A., Derugin, N., Wendland, M.F., Vexler, Z.S., 2011. Microglial cells contribute to endogenous brain defenses after acute neonatal focal stroke. J. Neurosci. 31, 12992-13001.
15. Ferrari, D., Chiozzi, P., Falzoni, S., Dal Susino, M., Collo, G., Buell, G., Di Virgilio, F., 1997. ATP-mediated cytotoxicity in microglial cells. Neuropharmacology 36, 1295-1301.
16. Ferrari, D., Los, M., Bauer, M.K., Vandenabeele, P., Wesselborg, S., Schulze-Osthoff, K., 1999. P2Z purinoreceptor ligation induces activation of caspases with distinct roles in apoptotic and necrotic alterations of cell death. FEBS Lett. 447, 71-75.
17. Ferrari, D., Villalba, M., Chiozzi, P., Falzoni, S., Ricciardi- Castagnoli, P., Di Virgilio, F., 1996. Mouse microglial cells express a plasma membrane pore gated by extracellular ATP. J. Immunol. 156, 1531-1539.
18. Frenguelli, B.G., Wigmore, G., Llaudet, E., Dale, N., 2007. Temporal and mechanistic dissociation of ATP and adenosine release during ischaemia in the mammalian hippocampus. J. Neurochem. 101, 1400-1413.
19. Friedle, S.A., Curet, M.A., Watters, J.J., 2010. Recent patents on novel P2X(7) receptor antagonists and their potential for reducing central nervous system inflammation. Recent Pat CNS Drug Discov. 5, 35-45.
20. Ginsberg, M., 2008. Neuroprotection for ischemic stroke: past, present and future. Neuropharmacology 55, 363-389.
21. Gu, B.J., Saunders, B.M., Petrou, S., Wiley, J.S., 2011. P2X(7) is a scavenger receptor for apoptotic cells in the absence of its ligand, extracellular ATP. J. Immunol. 187, 2365-2375.
22. Haas, S., Brockhaus, J., Verkhratsky, A., Kettenmann, H., 1996. ATP-induced membrane currents in ameboid microglia acutely isolated from mouse brain slices. Neuroscience 75, 257-261.
23. Hanley, P.J., Kronlage, M., Kirschning, C., Del Rey, A., Di Virgilio, F., Leipziger, J., Chessell, I.P., Sargin, S., Filippov, M.A., Lindemann, O., Mohr, S., Konigs, V., Schillers, H., Bahler, M., Schwab, A., 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.
24. Hayashi, Y., Tomimatsu, Y., Suzuki, H., Yamada, J., Wu, Z., Yao, H., Kagamiishi, Y., Tateishi, N., Sawada, M., Nakanishi, H., 2006. The intra-arterial injection of microglia protects hippocampal CA1 neurons against global ischemia-induced functional deficits in rats. Neuroscience 142, 87-96.
25. Hibell, A.D., Kidd, E.J., Chessell, I.P., Humphrey, P.P., Michel, A.D., 2000. Apparent species differences in the kinetic properties of P2X(7) receptors. Br. J. Pharmacol. 130, 167-173.
26. Imai, F., Suzuki, H., Oda, J., Ninomiya, T., Ono, K., Sano, H., Sawada, M., 2007. Neuroprotective effect of exogenous microglia in global brain ischemia. J. Cereb. Blood Flow Metab. 27, 488-500.
27. Jabs, R., Matthias, K., Grote, A., Grauer, M., Seifert, G., Steinhauser, C., 2007. Lack of P2X receptor mediated currents in astrocytes and GluR type glial cells of the hippocampal CA1 region. Glia 55, 1648-1655.
28. Jeong, H.K., Ji, K.M., Kim, B., Kim, J., Jou, I., Joe, E.H., 2010. Inflammatory responses are not sufficient to cause delayed neuronal death in ATP-induced acute brain injury. PLoS One 5, e13756.
29. Jiang, L.H., Mackenzie, A.B., North, R.A., Surprenant, A., 2000. Brilliant blue G selectively blocks ATP-gated rat P2X(7) receptors. Mol. Pharmacol. 58, 82-88.
30. Jung, S., Aliberti, J., Graemmel, P., Sunshine, M.J., Kreutzberg, G.W., Sher, A., Littman, D.R., 2000. Analysis of fractalkine receptor CX(3)CR1 function by targeted deletion and green fluorescent protein reporter gene insertion. Mol. Cell Biol. 20, 4106-4114.
31. Juranyi, Z., Sperlagh, B., Vizi, E.S., 1999. Involvement of P2 purinoceptors and the nitric oxide pathway in [3H]purine outflow evoked by short-term hypoxia and hypoglycemia in rat hippocampal slices. Brain Res. 823, 183-190.
32. Kitamura, Y., Takata, K., Inden, M., Tsuchiya, D., Yanagisawa, D., Nakata, J., Taniguchi, T., 2004. Intracerebroventricular injection of microglia protects against focal brain ischemia. J. Pharmacol. Sci. 94, 203-206.
33. Kitamura, Y., Yanagisawa, D., Inden, M., Takata, K., Tsuchiya, D., Kawasaki, T., Taniguchi, T., Shimohama, S., 2005. Recovery of focal brain ischemia-induced behavioral dysfunction by intracerebroventricular injection of microglia. J. Pharmacol. Sci. 97, 289-293.
34. Lalancette-Hebert, M., Gowing, G., Simard, A., Weng, Y.C., Kriz, J., 2007. Selective ablation of proliferating microglial cells exacerbates ischemic injury in the brain. J. Neurosci. 27, 2596-2605.
35. Le Feuvre, R.A., Brough, D., Touzani, O., Rothwell, N.J., 2003. Role of P2X7 receptors in ischemic and excitotoxic brain injury in vivo. J. Cereb. Blood Flow Metab. 23, 381-384.
36. Liu, H.T., Sabirov, R.Z., Okada, Y., 2008. Oxygen-glucose deprivation induces ATP release via maxi-anion channels in astrocytes. Purinergic Signal 4, 147-154.
37. Lyons, S.A., Kettenmann, H., 1998. Oligodendrocytes and microglia are selectively vulnerable to combined hypoxia and hypoglycemia injury in vitro. J. Cereb. Blood Flow Metab. 18, 521-530.
38. Matute, C., Domercq, M., Sanchez-Gomez, M.V., 2006. Glutamate-mediated glial injury: mechanisms and clinical importance. Glia 53, 212-224.
39. Melani, A., Corti, F., Stephan, H., Muller, C.E., Donati, C., Bruni, P., Vannucchi, M.G., Pedata, F., 2012. Ecto-ATPase inhibition: ATP and adenosine release under physiological and ischemic in vivo conditions in the rat striatum. Exp. Neurol. 233, 193-204.
40. Melani, A., Turchi, D., Vannucchi, M.G., Cipriani, S., Gianfriddo, M., Pedata, F., 2005. ATP extracellular concentrations are increased in the rat striatum during in vivo ischemia. Neurochem. Int. 47, 442-448.
41. Narantuya, D., Nagai, A., Sheikh, A.M., Masuda, J., Kobayashi, S., Yamaguchi, S., Kim, S.U., 2010. Human microglia transplanted in rat focal ischemia brain induce neuroprotection and behavioral improvement. PLoS One 5, e11746.
42. Nedergaard, M., Dirnagl, U., 2005. Role of glial cells in cerebral ischemia. Glia 50, 281-286.
43. Nelson, K.B., 2007. Perinatal ischemic stroke. Stroke 38, 742-745.
44. Neumann, J., Gunzer, M., Gutzeit, H.O., Ullrich, O., Reymann, K.G., Dinkel, K., 2006. Microglia provide neuroprotection after ischemia. FASEB J. 20, 714-716.
45. Nörenberg, W., Schunk, J., Fischer, W., Sobottka, H., Riedel, T., Oliveira, J.F., Franke, H., Illes, P., 2010. Electrophysiological classification of P2X7 receptors in rat cultured neocortical astroglia. Br. J. Pharmacol. 160 (8), 1941-1952. Aug.
46. North, R.A., 2002. Molecular physiology of P2X receptors. Physiol. Rev. 82, 1013-1067.
47. Oliveira, J.F., Riedel, T., Leichsenring, A., Heine, C., Franke, H., Krügel, U., Nörenberg, W., Illes, P., 2011. Rodent cortical astroglia express in situ functional P2X7 receptors sensing pathologically high ATP concentrations. Cereb. Cortex 21 (4), 806-820. Apr.
48. Pelegrín, P., 2011. Many ways to dilate the P2X7 receptor pore. Br. J. Pharm. 163, 908-911.
49. Raouf, R., Chabot-Dore, A.J., Ase, A.R., Blais, D., Seguela, P., 2007. Differential regulation of microglial P2X4 and P2X7 ATP receptors following LPS-induced activation. Neuropharmacology 53, 496-504.
50. Rigato, C., Swinnen, N., Buckinx, R., Couillin, I., Mangin, J.M., Rigo, J.M., Legendre, P., Le Corronc, H., 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.
51. Ryu, J.K., Kim, J., Choi, S.H., Oh, Y.J., Lee, Y.B., Kim, S.U., Jin, B.K., 2002. ATP-induced in vivo neurotoxicity in the rat striatum via P2 receptors. Neuroreport 13, 1611-1615.
52. Skaper, S.D., 2011. Ion channels on microglia: therapeutic targets for neuroprotection. CNS Neurol. Disord. Drug Targets 10, 44-56.
53. Solle, M., Labasi, J., Perregaux, D.G., Stam, E., Petrushova, N., Koller, B.H., Griffiths, R.J., Gabel, C.A., 2001. Altered cytokine production in mice lacking P2X(7) receptors. J. Biol. Chem. 276, 125-132.
54. Szydlowska, K., Tymianski, M., 2010. Calcium, ischemia and excitotoxicity. Cell Calcium 47, 122-129.
55. Takano, T., Oberheim, N., Cotrina, M.L., Nedergaard, M., 2009. Astrocytes and ischemic injury. Stroke 40, S8-S12.
56. Weinstein, J.R., Koerner, I.P., Moller, T., 2010. Microglia in ischemic brain injury. Future Neurol. 5 (2), 227-246.
57. Wu, L.J., Vadakkan, K.I., Zhuo, M., 2007. ATP-induced chemotaxis of microglial processes requires P2Y receptor-activated initiation of outward potassium currents. Glia 55, 810-821.
58. Wu, L.J., Wu, G., Sharif, M.R.A., Baker, A., Jia, Y., Fahey, F.H., Luo, H.R., Feener, E.P., Clapham, D.E., 2012. The voltage-gated proton channel Hv1 enhances brain damage from ischemic stroke. Nat. Neurosci. 15, 565-573.
59. Yanagisawa, D., Kitamura, Y., Takata, K., Hide, I., Nakata, Y., Taniguchi, T., 2008. Possible involvement of P2X7 receptor activation in microglial neuroprotection against focal cerebral ischemia in rats. Biol. Pharm. Bull 31 (6), 1121-1130.
60. Yenari, M.A., Giffard, R.G., 2001. Ischemic vulnerability of primary murine microglial cultures. Neurosci. Lett. 298, 5-8.
61. Yrjanheikki, J., Keinanen, R., Pellikka, M., Hokfelt, T., Koistinaho, J., 1998. Tetracyclines inhibit microglial activation and are neuroprotective in global brain ischemia. Proc. Natl. Acad. Sci. USA 95, 15769-15774.