P2X7 receptor blockade prevents ATP excitotoxicity in neurons and reduces brain damage after ischemia

Neurobiology of Disease

Volumn 45, Issue 3, 2012, Pages 954-961

  Arbeloa, Joana ^a   Pérez Samartín, Alberto ^a   Gottlieb, Miroslav ^b   Matute, Carlos ^a  

^a UNIVERSITY OF THE BASQUE COUNTRY UPV EHU   (Spain)

^b INSTITUTE OF CHEMISTRY   (Slovakia)

Author keywords

Excitotoxicity; Ischemia; Neuronal damage; P2X7

Indexed keywords

ADENOSINE TRIPHOSPHATE; BRILLIANT BLUE; BRILLIANT BLUE G; CALCIUM ION; GLUCOSE; NEUROPROTECTIVE AGENT; OXYGEN; PURINERGIC P2X RECEPTOR ANTAGONIST; PURINERGIC P2X7 RECEPTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN CELL; BRAIN DAMAGE; BRAIN ISCHEMIA; BRAIN SLICE; CALCIUM TRANSPORT; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG MECHANISM; EXCITOTOXICITY; IN VITRO STUDY; ION TRANSPORT; MIDDLE CEREBRAL ARTERY OCCLUSION; NERVE CELL CULTURE; NERVE CELL NECROSIS; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; RAT; RECEPTOR BLOCKING;

ADENOSINE TRIPHOSPHATE; ANALYSIS OF VARIANCE; ANIMALS; ANOXIA; BRAIN INJURIES; CALCIUM; CELLS, CULTURED; CEREBRAL CORTEX; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; EMBRYO, MAMMALIAN; EXCITATORY AMINO ACID AGONISTS; GLUCOSE; INFARCTION, MIDDLE CEREBRAL ARTERY; MEMBRANE POTENTIALS; N-METHYLASPARTATE; NEUROLOGIC EXAMINATION; NEURONS; ORGANIC CHEMICALS; PATCH-CLAMP TECHNIQUES; PHOSPHOPYRUVATE HYDRATASE; PURINERGIC P2X RECEPTOR ANTAGONISTS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, PURINERGIC P2X7; ROSANILINE DYES; TETRAZOLIUM SALTS;

EID: 84856585760     PISSN: 09699961     EISSN: 1095953X     Source Type: Journal    
DOI: 10.1016/j.nbd.2011.12.014     Document Type: Article

References (55)

1. Abbracchio M.P., Burnstock G., Verkhratsky A., Ziermann H. Purinergic signalling in the nervous system: an overview. Trends Neurosci. 2009, 32:19-29.
2. Amadio S., D'Ambrosi N., Cavaliere F., Murra B., Sancesario G., Bernardi G., Burnstock G., Volonte C. P2 receptor modulation and cytotoxic function in cultured CNS neurons. Neuropharmacology 2002, 42:489-501.
3. Anderson C.M., Nedergaard M. Emerging challenges of assigning P2X7 receptor function and immunoreactivity in neurons. Trends Neurosci. 2006, 29:257-262.
4. Bao L., Locovei S., Dahl G. Pannexin membrane channels are mechanosensitive conduits for ATP. FEBS Lett. 2004, 572:65-68.
5. Bederson J.B., Pitts L.H., Tsuji M., Nishimura M.C., Davis R.L., Bartkowski H. Rat middle cerebral artery occlusion: evaluation of the model and development of a neurologic examination. Stroke 1986, 17:472-476.
6. Braun N., Zhu Y., Krieglstein J., Culmsee C., Zimmermann H. Upregulation of the enzyme chain hydrolyzing extracellular ATP after transient forebrain ischemia in the rat. J. Neurosci. 1998, 18:4891-4900.
7. Burnstock G. Historical review ATP as a neurotransmitter. Trends Pharmacol. Sci. 2006, 27:166-176.
8. Burnstock G. Physiology and pathophysiology of purinergic neurotransmission. Physiol. Rev. 2007, 87:659-797.
9. Burnstock G., Knight G.E. Cellular distribution and functions of P2 receptor subtypes in different systems. Int. Rev. Cytol. 2004, 240:31-304.
10. Callaway J.K., Knight M.J., Watkins D.J., Beart P.M., Jarrott B., Delaney P.M. A novel, rapid, computerised method for quantitation of neuronal damage in a rat model of stroke. J. Neurosci. Meth. 2000, 102:53-60.
11. Cavaliere F., Sancesario G., Bernardi G., Volonte C. Extracellular ATP and nerve growth factor intensify hypoglycemia-induced cell death in primary neurons: role of P2 and NGFRp75 receptors. J. Neurochem. 2002, 83:1129-1138.
12. Cavaliere F., Amadio S., Sancesario G., Bernardi G., Volonté C. Synaptic P2X7 and oxygen/glucose deprivation in organotypic hippocampal cultures. J. Cereb. Blood Flow Metab. 2004, 24:392-398.
13. Cheung N.S., Pascoe C.J., Giardina S.F., John C.A., Beart P.M. Micromolar l-glutamate induces extensive apoptosis in an apoptotic-necrotic continuum of insult-dependent, excitotoxic injury in cultured cortical neurones. Neuropharmacology 1998, 37:1419-1429.
14. Dale N., Frenguelli B.G. Release of adenosine and ATP during ischemia and epilepsy. Curr. Neuropharmacol. 2009, 7:160-179.
15. Díaz-Hernández M., Díez-Zaera M., Sánchez-Nogueiro J., Gómez-Villafuertes R., Canals J.M., Alberch J., Miras-Portugal M.T., Lucas J.J. Altered P2X7-receptor level and function in mouse models of Huntington's disease and therapeutic efficacy of antagonist administration. FASEB J. 2009, 23:1893-1906.
16. Domercq M., Perez-Samartin A., Aparicio D., Alberdi E., Pampliega O., Matute C. P2X7 receptors mediate ischemic damage to oligodendrocytes. Glia 2010, 58:730-740.
17. Franke H., Gunther A., Grosche J., Schmidt R., Rossner S., Reinhardt R., Faber- Zuschratter H., Schneider D., Illes P. P2X7 receptor expression after ischemia in the cerebral cortex of rats. J. Neuropath. Exp. Neur. 2004, 63:686-699.
18. Frenguelli B.G., Wigmore G., Llaudet E., Dale N. Temporal and mechanistic dissociation of ATP, adenosine release during ischaemia in the mammalian hippocampus. J. Neurochem. 2007, 101:1400-1413.
19. Gever J.R., Cockayne D.A., Dillon M.P., Burnstock G., Ford A.P. Pharmacology of P2X channels. Pflugers Arch. 2006, 452:513-537.
20. Huang Y.J., Maruyama Y., Dvoryanchikov G., Pereira E., Chaudhari N., Roper S.D. The role of pannexin 1 hemichannels in ATP release and cell-cell communication in mouse taste buds. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:6436-6441.
21. Jiang L.H., Mackenzie A.B., North R.A., Surprenant A. Brilliant blue G selectively blocks ATP-gated rat P2X(7) receptors. Mol. Pharmacol. 2000, 58:82-88.
22. 3H]purine outflow evoked by short-term hypoxia and hypoglycemia in rat hippocampal slices. Brain Res. 1999, 823:183-190.
23. Kang J., Kang N., Lovatt D., Torres A., Zhao Z., Lin J., Nedergaard M. Connexin 43 hemichannels are permeable to ATP. J. Neurosci. 2008, 28:4702-4711.
24. Khakh B.S., North R.A. P2X receptors as cell surface ATP sensors in health and disease. Nature 2006, 442:527-532.
25. Kim M., Jiang L.H., Wilson H.L., North R.A., Surprenant A. Proteomic and functional evidence for a P2X7 receptor signalling complex. EMBO J. 2001, 20:6347-6358.
26. Larm J.A., Cheung N.S., Beart P.M. (S)-5-Fluorowillardiine-mediated neurotoxicity in cultured murine cortical neurones occurs via AMPA and kainate receptors. Eur. J. Pharmacol. 1996, 314:249-254.
27. Le Feuvre R., Brough D., Rothwell N. Extracellular ATP and P2X7 receptors in neurodegeneration. Eur. J. Pharmacol. 2002, 447:261-269.
28. Lipton S.A. Pathologically activated therapeutics for neuroprotection. Nat. Rev. Neurosci. 2007, 8:803-808.
29. Lo E.H. A new penumbra: transitioning from injury into repair after stroke. Nat. Med. 2008, 14:497-500.
30. Locovei S., Bao L., Dahl G. Pannexin 1 in erythrocytes: function without a gap. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:7655-7659.
31. Longa E.Z., Weinstein P.R., Carlson S., Cummins R. Reversible middle cerebral artery occlusion without craniectomy in rats. Stroke 1989, 20:84-91.
32. Lutz P.L., Kabler S. Release of adenosine and ATP in the brain of the freshwater turtle (Trachemys scripta) during long-term anoxia. Brain Res. 1997, 769:281-286.
33. Matute C., Torre I., Pérez-Cerdá F., Pérez-Samartín A., Alberdi E., Etxebarria E., Arranz A.M., Ravid R., Rodriguez-Antigüedad A., Sánchez-Gómez M.V., Domercq M. P2X7 receptor blockade prevents ATP excitotoxicity in oligodendrocytes and ameliorates experimental autoimmune encephalomyelitis. J. Neurosci. 2007, 27:9525-9533.
34. Melani A., Turchi D., Vannucchi M.G., Cipriani S., Gianfriddo M., Pedata F. ATP extracellular concentrations are increased in the rat striatum during in vivo ischemia. Neurochem. Int. 2005, 47:442-448.
35. Melani A., Amadio S., Gianfriddo M., Vannucchi M.G., Volontè C., Bernardi G., Pedata F., Sancesario G. P2X7 receptor modulation on microglial cells and reduction of brain infarct caused by middle cerebral artery occlusion in rat. J. Cereb. Blood Flow Metab. 2006, 26:974-982.
36. Milius D., Sperlagh B., Illes P. Up-regulation of P2X7 receptor-immunoreactivity by in vitro ischemia on the plasma membrane of cultures rat cortical neurons. Neurosci. Lett. 2008, 446:45-50.
37. Moatassim C., Dubyak G.R. A novel pathway for the activation of phospholipase D by P2z purinergic receptors in BAC1.2F5 macrophages. J. Biol. Chem. 1992, 267:23664-23673.
38. North R.A. Molecular physiology of P2X receptors. Physiol. Rev. 2002, 82:1013-1067.
39. Pankratov Y., Lalo U., Verkhratsky A., North R.A. Quantal release of ATP in mouse cortex. J. Gen. Physiol. 2007, 129:257-265.
40. Pellegatti P., Falzoni S., Pinton P., Rizzuto R., Di Virgilio F. A novel recombinant plasma membrane-targeted luciferase reveals a new pathway for ATP secretion. Mol. Biol. Cell 2005, 16:3659-3665.
41. Peng W., Cotrina M.L., Han X., Yu H., Bekar L., Blum L., Takano T., Tian G.F., Goldman S.A., Nedergaard M. Systemic administration of an antagonist of the ATP-sensitive receptor P2X7 improves recovery after spinal cord injury. Proc. Natl. Acad. Sci. U. S. A. 2009, 106. 12489-1243.
42. Petruzzi E., Orlando C., Pinzani P., Sestini R., Del Rosso A., Dini G., Tanganelli E., Buggiani A., Pazzagli M. Adenosine triphosphate release by osmotic shock and hemoglobin A1C in diabetic subjects erythrocytes. Metabolism 1994, 43:435-440.
43. Pubill D., Dayanithi G., Siatka C., Andres M., Dufour M.N., Guillon G., Mendre C. ATP induces intracellular calcium increases and actin cytoskeleton disaggregation via P2X receptors. Cell Calcium 2001, 29:299-309.
44. Ralevic V., Burnstock G. Receptors for purines and pirimidines. Pharmacol. Rev. 1998, 50:413-492.
45. Reigada D., Lu W., Zhang M., Mitchell C.H. Elevated pressure triggers a physiological release of ATP from the retina: possible role for pannexin hemichannels. Neuroscience 2008, 157:396-404.
46. Rossi D.J., Brady J.D., Mohr C. Astrocyte metabolism and signaling during brain ischemia. Nat. Neurosci. 2007, 10:1377-1386.
47. Schmued L.C., Stowers C.C., Scallet A.C., Xu L. Fluoro-Jade C results in ultra high resolution and contrast labeling of degenerating neurons. Brain Res. 2005, 1035:24-31.
48. Sperlágh B., Vizi S., Wirkner K., Illes P. P2X7 receptors in the nervous system. Prog. Neurobiol. 2006, 78:327-346.
49. Surprenant A., Rassendren F., Kawashima E., North R.A., Buell G. The cytolytic P2Z receptor for extracellular ATP identified as a P2X receptor (P2X7). Science 1996, 272:735-738.
50. Thompson R.J., Zhou N., MacVicar B.A. Ischemia opens neuronal gap junction hemichannels. Science 2006, 312:924-927.
51. Wang X., Arcuino G., Takano T., Lin J., Peng W.G., Wan P., Li P., Xu Q., Liu Q.S., Goldman S.A., Nedergaard M. P2X7 receptor inhibition improves recovery after spinal cord injury. Nat. Med. 2004, 10:821-827.
52. Wieraszko A., Goldsmith G., Seyfried T.N. Stimulation dependent release of adenosine triphosphate from hippocampal slices. Brain Res. 1989, 485:244-250.
53. Wirkner K., Köfalvi A., Fischer W., Günther A., Franke H., Gröger-Arndt H., Nörenberg W., Madarász E., Vizi E.S., Schneider D., Sperlágh B., Illes P. Supersensitivity of P2X receptors in cerebrocortical cell cultures after in vitro ischemia. J. Neurochem. 2005, 95:1421-1437.
54. Yenari M.A., Kauppinen T.M., Swanson R.A. Microglial activation in stroke: therapeutic targets. Neurotherapeutics 2010, 7:378-391.
55. Yu Y., Ugawa S., Ueda T., Ishida Y., Inoue K., Kyaw Nyunt A., Umemura A., Mase M., Yamada K., Shimada S. Cellular localization of P2X7 receptor mRNA in the rat brain. Brain Res. 2008, 1194:45-55.