Astrocyte cultures exhibit P2X7 receptor channel opening in the absence of exogenous ligands

GLIA

Volumn 57, Issue 6, 2009, Pages 622-633

  Nagasawa, Kazuki ^a,b   Escartin, Carole ^a,c,d   Swanson, Raymond A ^a  

^a VETERANS AFFAIRS MEDICAL CENTER   (United States)

^b KYOTO PHARMACEUTICAL UNIVERSITY   (Japan)

^c INSTITUT DE RADIOPROTECTION ET DE SÛRETÉ NUCLÉAIRE   (France)

^d SERVICE HOSPITALIER FRÉDÉRIC JOLIOT   (France)

Author keywords

Astrocyte; ATP; Hemichannel; P2X7 receptor; Propidium iodide; YO PRO 1

Indexed keywords

1 [N,O BIS(5 ISOQUINOLINESULFONYL) N METHYLTYROSYL] 4 PHENYLPIPERAZINE; 18ALPHA GLYCYRRHETINIC ACID; ADENOSINE TRIPHOSPHATE; APYRASE; BETA,GAMMA DIBROMOMETHYLENE 6 N,N DIETHYLADENOSINE TRIPHOSPHATE; BRILLIANT BLUE; BRILLIANT BLUE G; CONNEXIN 43; DYE; FLUFENAMIC ACID; LIGAND; PHENOLSULFONPHTHALEIN; PROPIDIUM IODIDE; PURINERGIC P2X7 RECEPTOR; PYRIDOXAL PHOSPHATE 6 AZOPHENYL 2',4' DISULFONIC ACID; SMALL INTERFERING RNA; SURAMIN; UNCLASSIFIED DRUG; YO PRO 1 IODIDE; 1 (5 ISOQUINOLINESULFONYL) 2 METHYLPIPERAZINE; 6 N,N DIETHYL BETA,GAMMA DIBROMOMETHYLENE D ATP; 6-N,N-DIETHYL-BETA,GAMMA-DIBROMOMETHYLENE-D-ATP; BENZENESULFONIC ACID DERIVATIVE; BENZOXAZOLE DERIVATIVE; DRUG DERIVATIVE; PURINERGIC P2 RECEPTOR; QUINOLINE DERIVATIVE; YO PRO 1; YO-PRO 1;

ANIMAL CELL; ARTICLE; ASTROCYTE; CHANNEL GATING; CONCENTRATION RESPONSE; CONTROLLED STUDY; CULTURE MEDIUM; EXTRACELLULAR SPACE; HUMAN; HUMAN CELL; INTRACELLULAR SPACE; MICROGLIA; MOUSE; NERVE CELL CULTURE; NERVE CELL NECROSIS; NEUROTRANSMITTER UPTAKE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; RNA INTERFERENCE; SPECIES DIFFERENCE; ANIMAL; CELL CULTURE; CELL LINE; DRUG ANTAGONISM; GENE SILENCING; GENETICS; METABOLISM; WISTAR RAT;

1-(5-ISOQUINOLINESULFONYL)-2-METHYLPIPERAZINE; ADENOSINE TRIPHOSPHATE; ANIMALS; APYRASE; ASTROCYTES; BENZENESULFONATES; BENZOXAZOLES; CELL LINE; CELLS, CULTURED; GENE KNOCKDOWN TECHNIQUES; HUMANS; LIGANDS; MICE; PHENOLSULFONPHTHALEIN; PROPIDIUM; QUINOLINIUM COMPOUNDS; RATS; RATS, WISTAR; RECEPTORS, PURINERGIC P2; RNA, SMALL INTERFERING; SURAMIN;

EID: 65549156198     PISSN: 08941491     EISSN: 10981136     Source Type: Journal    
DOI: 10.1002/glia.20791     Document Type: Article

References (60)

1. Adriouch S, Bannas P, Schwarz N, Fliegert R, Guse AH, Seman M, Haag F, Koch-Nolte F. 2008. ADP-ribosylation at R125 gates the P2X7 ion channel by presenting a covalent ligand to its nucleotide binding site. Faseb J 22:861-869.
2. Anderson CM, Bergher JP, Swanson RA. 2004. ATP-induced ATP release from astrocytes. J Neurochem 88:246-256.
3. Anderson CM, Nedergaard M. 2006. Emerging challenges of assigning P2X7 receptor function and immunoreactivity in neurons. Trends Neurosci 29:257-262.
4. Aoyama K, Burns DM, Suh SW, Garnier P, Matsumori Y, Shiina H, Swanson RA. 2005. Acidosis causes endoplasmic reticulum stress and caspase-12-mediated astrocyte death. J Cereb Blood Flow Metab 25:358-370.
5. Bowser DN, Khakh BS. 2007. Vesicular ATP is the predominant cause of intercellular calcium waves in astrocytes. J Gen Physiol 129:485-491.
6. Bradford MM. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248-254.
7. Brandle U, Kohler K, Wheeler-Schilling TH. 1998. Expression of the P2X7-receptor subunit in neurons of the rat retina. Brain Res Mol Brain Res 62:106-109.
8. Chen Y, Vartiainen NE, Ying W, Chan PH, Koistinaho J, Swanson RA. 2001. Astrocytes protect neurons from nitric oxide toxicity by a glutathione-dependent mechanism. J Neurochem 77:1601-1610.
9. Chessell IP, Michel AD, Humphrey PP. 1998a. Effects of antagonists at the human recombinant P2X7 receptor. Br J Pharmacol 124:1314-1320.
10. Chessell IP, Simon J, Hibell AD, Michel AD, Barnard EA, Humphrey PP. 1998b. Cloning and functional characterization of the mouse P2X7 receptor. FEBS Lett 439(1-2):26-30.
11. Colomar A, Amedee T. 2001. ATP stimulation of P2X(7) receptors activates three different ionic conductances on cultured mouse Schwann cells. Eur J Neurosci 14:927-936.
12. Contreras JE, Sanchez HA, Eugenin EA, Speidel D, Theis M, Willecke K, Bukauskas FF, Bennett MV, Saez JC. 2002. Metabolic inhibition induces opening of unapposed connexin 43 gap junction hemichannels and reduces gap junctional communication in cortical astrocytes in culture. Proc Natl Acad Sci USA 99:495-500.
13. Crack BE, Pollard CE, Beukers MW, Roberts SM, Hunt SF, Ingall AH, McKechnie KC, AP IJ, Leff P. 1995. Pharmacological and biochemical analysis of FPL 67156, a novel, selective inhibitor of ecto-ATPase. Br J Pharmacol 114:475-481.
14. Deuchars SA, Atkinson L, Brooke RE, Musa H, Milligan CJ, Batten TF, Buckley NJ, Parson SH, Deuchars J. 2001. Neuronal P2X7 receptors are targeted to presynaptic terminals in the central and peripheral nervous systems. J Neurosci 21:7143-7152.
15. Di Virgilio F, Sanz JM, Chiozzi P, Falzoni S. 1999. The P2Z/P2X7 receptor of microglial cells: A novel immunomodulatory receptor. Prog Brain Res 120:355-368.
16. Duan S, Anderson CM, Keung EC, Chen Y, Chen Y, Swanson RA. 2003. P2X7 receptor-mediated release of excitatory amino acids from astrocytes. J Neurosci 23:1320-1328.
17. Faria RX, Defarias FP, Alves LA. 2005. Are second messengers crucial for opening the pore associated with P2X7 receptor? Am J Physiol Cell Physiol 288:C260-C271.
18. Ferrari D, Stroh C, Schulze-Osthoff K. 1999. P2X7/P2Z purinoreceptor-mediated activation of transcription factor NFAT in microglial cells. J Biol Chem 274:13205-13210.
19. Franke H, Grosche J, Schadlich H, Krugel U, Allgaier C, Illes P. 2001. P2X receptor expression on astrocytes in the nucleus accumbens of rats. Neuroscience 108:421-429.
20. Franke H, Gunther A, Grosche J, Schmidt R, Rossner S, Reinhardt R, Faber-Zuschratter H, Schneider D, Illes P. 2004. P2X7 receptor expression after ischemia in the cerebral cortex of rats. J Neuropathol Exp Neurol 63:686-699.
21. Guo C, Masin M, Qureshi OS, Murrell-Lagnado RD. 2007. Evidence for functional P2X4/P2X7 heteromeric receptors. Mol Pharmacol 72: 1447-1456.
22. Humphreys BD, Virginio C, Surprenant A, Rice J, Dubyak GR. 1998. Isoquinolines as antagonists of the P2X7 nucleotide receptor: High selectivity for the human versus rat receptor homologues. Mol Pharmacol 54:22-32.
23. Iglesias R, Locovei S, Roque AP, Alberto AP, Dahl G, Spray DC, Scemes E. 2008. P2X7 receptor-Pannexin1 complex: Pharmacology and signaling. Am J Physiol Cell Physiol 295:C752-C760.
24. 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.
25. Jiang LH, Mackenzie AB, North RA, Surprenant A. 2000. Brilliant blue G selectively blocks ATP-gated rat P2X(7) receptors. Mol Pharmacol 58:82-88.
26. Joseph SM, Buchakjian MR, Dubyak GR. 2003. Colocalization of ATP release sites and ecto-ATPase activity at the extracellular surface of human astrocytes. J Biol Chem 278:23331-23342.
27. Kim M, Spelta V, Sim J, North RA, Surprenant A. 2001. Differential assembly of rat purinergic P2X7 receptor in immune cells of the brain and periphery. J Biol Chem 276:23262-23267.
28. King BF, Liu M, Townsend-Nicholson A, Pfister J, Padilla F, Ford AP, Gever JR, Oglesby IB, Schorge S, Burnstock G. 2005. Antagonism of ATP responses at P2X receptor subtypes by the pH indicator dye, phenol red. Br J Pharmacol 145:313-322.
29. Kukley M, Barden JA, Steinhauser C, Jabs R. 2001. Distribution of P2X receptors on astrocytes in juvenile rat hippocampus. Glia 36:11-21.
30. Liu HT, Sabirov RZ, Okada Y. 2007. Oxygen-glucose deprivation induces ATP release via maxi-anion channels in astrocytes. Purinergic Signal 4:147-154.
31. Liu HT, Toychiev AH, Takahashi N, Sabirov RZ, Okada Y. 2008. Maxi-anion channel as a candidate pathway for osmosensitive ATP release from mouse astrocytes in primary culture. Cell Res 18:558-565.
32. Locovei S, Scemes E, Qiu F, Spray DC, Dahl G. 2007. Pannexin1 is part of the pore forming unit of the P2X(7) receptor death complex. FEBS Lett 581:483-488.
33. Lovatt D, Sonnewald U, Waagepetersen HS, Schousboe A, He W, Lin JH, Han X, Takano T, Wang S, Sim FJ, others. 2007. The transcriptome and metabolic gene signature of protoplasmic astrocytes in the adult murine cortex. J Neurosci 27:12255-12266.
34. Murgia M, Hanau S, Pizzo P, Rippa M, Di Virgilio F. 1993. Oxidized ATP. An irreversible inhibitor of the macrophage purinergic P2Z receptor. J Biol Chem 268:8199-8203.
35. Nagai K, Nagasawa K, Fujimoto S. 2005. Transport mechanisms for adenosine and uridine in primary-cultured rat cortical neurons and astrocytes. Biochem Biophys Res Commun 334:1343-1350.
36. Nagasawa K, Kawasaki F, Tanaka A, Nagai K, Fujimoto S. 2007. Characterization of guanine and guanosine transport in primary cultured rat cortical astrocytes and neurons. Glia 55:1397-1404.
37. Nagasawa K, Natazuka T, Chihara K, Kitazawa F, Tsumura A, Takara K, Nomiyama M, Ohnishi N, Yokoyama T. 1996. Transport mechanism of anthracycline derivatives in human leukemia cell lines: Uptake and efflux of pirarubicin in HL60 and pirarubicin-resistant HL60 cells. Cancer Chemother Pharmacol 37:297-304.
38. North RA. 2002. Molecular physiology of P2X receptors. Physiol Rev 82:1013-1067.
39. North RA, Surprenant A. 2000. Pharmacology of cloned P2X receptors. Annu Rev Pharmacol Toxicol 40:563-580.
40. Panenka W, Jijon H, Herx LM, Armstrong JN, Feighan D, Wei T, Yong VW, Ransohoff RM, MacVicar BA. 2001. P2X7-like receptor activation in astrocytes increases chemokine monocyte chemoattractant protein-1 expression via mitogen-activated protein kinase. J Neurosci 21: 7135-7142.
41. Pangrsic T, Potokar M, Stenovec M, Kreft M, Fabbretti E, Nistri A, Pryazhnikov E, Khiroug L, Giniatullin R, Zorec R. 2007. Exocytotic release of ATP from cultured astrocytes. J Biol Chem 282:28749-28758.
42. Pankratov Y, Lalo U, Verkhratsky A, North RA. 2006. Vesicular release of ATP at central synapses. Pflugers Arch 452:589-597.
43. Pankratov YV, Krishtal OA. 2003. Distinct quantal features of AMPA and NMDA synaptic currents in hippocampal neurons: Implication of glutamate spillover and receptor saturation. Biophys J 85:3375-3387.
44. Pannicke T, Fischer W, Biedermann B, Schadlich H, Grosche J, Faude F, Wiedemann P, Allgaier C, Illes P, Burnstock G, others. 2000. P2X7 receptors in Muller glial cells from the human retina. J Neurosci 20:5965-5972.
45. Parvathenani LK, Tertyshnikova S, Greco CR, Roberts SB, Robertson B, Posmantur R. 2003. P2X7 mediates superoxide production in primary microglia and is up-regulated in a transgenic mouse model of Alzheimer's disease. J Biol Chem 278:13309-13317.
46. Pelegrin P, Surprenant A. 2006. Pannexin-1 mediates large pore formation and interleukin-1beta release by the ATP-gated P2X7 receptor. Embo J 25:5071-5082.
47. Rusakov DA, Kullmann DM. 1998. Extrasynaptic glutamate diffusion in the hippocampus: Ultrastructural constraints, uptake, and receptor activation. J Neurosci 18:3158-3170.
48. Seman M, Adriouch S, Scheuplein F, Krebs C, Freese D, Glowacki G, Deterre P, Haag F, Koch-Nolte F. 2003. NAD-induced T cell death: ADP-Ribosylation of cell surface proteins by ART2 activates the cytolytic P2X7 purinoceptor. Immunity 19:571-582.
49. Sim JA, Young MT, Sung HY, North RA, Surprenant A. 2004. Reanalysis of P2X7 receptor expression in rodent brain. J Neurosci 24:6307-6314.
50. Sperlagh B, Kofalvi A, Deuchars J, Atkinson L, Milligan CJ, Buckley NJ, Vizi ES. 2002. Involvement of P2X7 receptors in the regulation of neurotransmitter release in the rat hippocampus. J Neurochem 81: 1196-1211.
51. Stout CE, Costantin JL, Naus CC, Charles AC. 2002. Intercellular calcium signaling in astrocytes via ATP release through connexin hemichannels. J Biol Chem 277:10482-10488.
52. 2+ signaling. J Neurosci 26:1378-1385.
53. Surprenant A, Rassendren F, Kawashima E, North RA, Buell G. 1996. The cytolytic P2Z receptor for extracellular ATP identified as a P2X receptor (P2X7). Science 272:735-738.
54. Swanson RA, Farrell K, Stein BA. 1997. Astrocyte energetics, function, and death under conditions of incomplete ischemia: A mechanism of glial death in the penumbra. Glia 21:142-153.
55. Virginio C, Church D, North RA, Surprenant A. 1997. Effects of divalent cations, protons and calmidazolium at the rat P2X7 receptor. Neuropharmacology 36:1285-1294.
56. --dependent mechanism. Glia 37:8-18.
57. Westfall TD, Kennedy C, Sneddon P. 1996. Enhancement of sympathetic purinergic neurotransmission in the guinea-pig isolated vas deferens by the novel ecto-ATPase inhibitor ARL 67156. Br J Pharmacol 117:867-872.
58. Yamaoka K, Tanigawara Y, Nakagawa T, Uno T. 1981. A pharmacokinetic analysis program (multi) for microcomputer. J Pharmacobiodyn 4:879-885.
59. Ye ZC, Wyeth MS, Baltan-Tekkok S, Ransom BR. 2003. Functional hemichannels in astrocytes: A novel mechanism of glutamate release. J Neurosci 23:3588-3596.
60. Ying W, Chen Y, Alano CC, Swanson RA. 2002. Tricarboxylic acid cycle substrates prevent PARP-mediated death of neurons and astrocytes. J Cereb Blood Flow Metab 22:774-779.