Adenosine receptor ligands protect against a combination of apoptotic and necrotic cell death in cerebellar granule neurons

Experimental Brain Research

Volumn 186, Issue 1, 2008, Pages 151-160

  Fatokun, Amos A ^a   Stone, Trevor W ^a   Smith, Robert A ^a  

^a UNIVERSITY OF GLASGOW   (United Kingdom)

Author keywords

Adenosine; Apoptosis; Cerebellar granule neurons; Excitotoxicity; Necrosis

Indexed keywords

2 AMINO 5 PHOSPHONOVALERIC ACID; 2 [4 (2 CARBOXYETHYL)PHENETHYLAMINO]ADENOSINE 5' (N ETHYLCARBOXAMIDE); 3,4 DIHYDRO 5 [4 (1 PIPERIDINYL)BUTOXYL] 1 (2H) ISOQUINOLINONE; 4 [2 [7 AMINO 2 (2 FURYL) 1,2,4 TRIAZOLO[2,3 A][1,3,5]TRIAZIN 5 YLAMINO]ETHYL]PHENOL; 6 N CYCLOPENTYLADENOSINE; 8 CYCLOPENTYL 1,3 DIPROPYLXANTHINE; ADENOSINE RECEPTOR; BENZYLOXYCARBONYLASPARTYLGLUTAMYLVALYLASPARTYL FLUOROMETHYL KETONE; CASPASE 3 INHIBITOR; CYCLOSPORIN A; DIZOCILPINE; GLUTAMIC ACID; ISOQUINOLINE DERIVATIVE; KYNURENIC ACID; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR BLOCKING AGENT; N METHYL DEXTRO ASPARTIC ACID RECEPTOR STIMULATING AGENT; NICOTINAMIDE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; ATTENUATION; CELL CULTURE; CELL DEATH; CEREBELLUM; CONCENTRATION RESPONSE; DRUG MECHANISM; MEMBRANE PERMEABILITY; NERVE CELL; NEUROPROTECTION; NEUROTOXICITY; NONHUMAN; PRIORITY JOURNAL; RAT;

EID: 40149089270     PISSN: 00144819     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00221-007-1218-3     Document Type: Article

References (73)

1. MP Abbracchio F Cattabeni 1999 Brain adenosine receptors as targets for therapeutic intervention in neurodegenerative disease Ann N Y Acad Sci 890 79 92 10668415 10.1111/j.1749-6632.1999.tb07983.x 1:CAS:528:DC%2BD3cXnsVGjsA%3D%3D Abbracchio MP, Cattabeni F (1999) Brain adenosine receptors as targets for therapeutic intervention in neurodegenerative disease. Ann N Y Acad Sci 890:79–92
2. PD Alfinito SP Wang L Manzino S Rijhsinghani GD Zeevalk PK Sonsalla 2003 Adenosinergic protection of dopaminergic and GABAergic neurons against mitochondrial inhibition through receptors located in the substantia nigra and striatum, respectively J Neurosci 23 10982 10987 14645494 1:CAS:528:DC%2BD3sXpslemsrc%3D Alfinito PD, Wang SP, Manzino L, Rijhsinghani S, Zeevalk GD, Sonsalla PK (2003) Adenosinergic protection of dopaminergic and GABAergic neurons against mitochondrial inhibition through receptors located in the substantia nigra and striatum, respectively. J Neurosci 23:10982–10987
3. CG Almeida A Mendonca de RA Cunha JA Ribeiro 2003 Adenosine promotes neuronal recovery from reactive oxygen species induced lesion in rat hippocampal slices Neurosci Lett 339 127 130 12614911 10.1016/S0304-3940(02)01478-7 1:CAS:528:DC%2BD3sXhsVCktr4%3D Almeida CG, de Mendonca A, Cunha RA, Ribeiro JA (2003) Adenosine promotes neuronal recovery from reactive oxygen species induced lesion in rat hippocampal slices. Neurosci Lett 339:127–130
4. M Ankarcrona JM Dypbukt E Bonfoco B Zhivotovsky S Orrenius SA Lipton P Nicotera 1995 Glutamate-induced neuronal death: a succession of necrosis or apoptosis depending on mitochondrial function Neuron 15 961 973 7576644 10.1016/0896-6273(95)90186-8 1:CAS:528:DyaK2MXptV2gsLc%3D Ankarcrona M, Dypbukt JM, Bonfoco E, Zhivotovsky B, Orrenius S, Lipton SA, Nicotera P (1995) Glutamate-induced neuronal death: a succession of necrosis or apoptosis depending on mitochondrial function. Neuron 15:961–973
5. P Ascher L Nowak 1998 The role of divalent cations in the NMDA responses of mouse central neurones in culture J Physiol (London) 399 247 266 Ascher P, Nowak L (1998) The role of divalent cations in the NMDA responses of mouse central neurones in culture. J Physiol (London) 399:247–266
6. A Atlante S Gagliardi GM Minervini E Marra S Passarella P Calissano 1996 Rapid uncoupling of oxidative phosphorylation accompanies glutamate toxicity in rat cerebellar granule cells Neuroreport 7 2519 2523 8981415 10.1097/00001756-199611040-00023 1:CAS:528:DyaK2sXhslWmtb8%3D Atlante A, Gagliardi S, Minervini GM, Marra E, Passarella S, Calissano P (1996) Rapid uncoupling of oxidative phosphorylation accompanies glutamate toxicity in rat cerebellar granule cells. Neuroreport 7:2519–2523
7. EBE Becker A Bonni 2004 Cell cycle regulation of neuronal apoptosis in development and disease Prog Neurobiol 72 1 25 15019174 10.1016/j.pneurobio.2003.12.005 1:CAS:528:DC%2BD2cXhs12js7k%3D Becker EBE, Bonni A (2004) Cell cycle regulation of neuronal apoptosis in development and disease. Prog Neurobiol 72:1–25
8. WMH Behan TW Stone 2000 Role of kynurenines in the neurotoxic actions of kainic acid Br J Pharmacol 129 1764 1770 10780984 10.1038/sj.bjp.0703250 1:CAS:528:DC%2BD3cXjtV2qsrs%3D Behan WMH, Stone TW (2000) Role of kynurenines in the neurotoxic actions of kainic acid. Br J Pharmacol 129:1764–1770
9. PJ Birch CJ Grossman AG Hayes 1988 Kynurenic acid antagonises responses to NMDA via an action at the strychnine-insensitive glycine receptor Eur J Pharmacol 154 85 87 2846328 10.1016/0014-2999(88)90367-6 1:CAS:528:DyaL1cXls1entrg%3D Birch PJ, Grossman CJ, Hayes AG (1988) Kynurenic acid antagonises responses to NMDA via an action at the strychnine-insensitive glycine receptor. Eur J Pharmacol 154:85–87
10. MJL Bours ELR Swennen F Di Virgilio BN Cronstein 2006 Adenosine 5 ‘-triphosphate and adenosine as endogenous signaling molecules in immunity and inflammation Pharmacol Therap 112 358 404 10.1016/j.pharmthera.2005.04.013 1:CAS:528:DC%2BD28XhtVGjt7vF Bours MJL, Swennen ELR, Di Virgilio F, Cronstein BN (2006) Adenosine 5 ‘-triphosphate and adenosine as endogenous signaling molecules in immunity and inflammation. Pharmacol Therap 112:358–404
11. R Carpenedo E Meli F Peruginelli DE Pellegrini-Giampietro F Moroni 2002 Kynurenine 3-mono-oxygenase inhibitors attenuate post-ischemic neuronal death in organotypic hippocampal slice cultures J Neurochem 82 1465 1471 12354294 10.1046/j.1471-4159.2002.01090.x 1:CAS:528:DC%2BD38XnsV2hs7o%3D Carpenedo R, Meli E, Peruginelli F, Pellegrini-Giampietro DE, Moroni F (2002) Kynurenine 3-mono-oxygenase inhibitors attenuate post-ischemic neuronal death in organotypic hippocampal slice cultures. J Neurochem 82:1465–1471
12. G Cebers B Zhivotovsky M Ankarcrona S Liljuquist 1997 AMPA neurotoxicity in cultured cerebellar granule neurons: mode of cell death Brain Res Bull 43 393 403 9241442 10.1016/S0361-9230(97)00025-7 1:CAS:528:DyaK2sXkvFymsbo%3D Cebers G, Zhivotovsky B, Ankarcrona M, Liljuquist S (1997) AMPA neurotoxicity in cultured cerebellar granule neurons: mode of cell death. Brain Res Bull 43:393–403
13. JF Chen ZH Huang JY Ma JM Zhu R Moratalla D Standaert MA Moskowitz JS Fink MA Schwarzschild 1999 A2A adenosine receptor deficiency attenuates brain injury induced by transient focal ischemia in mice J Neurosci 19 9192 9200 10531422 1:CAS:528:DyaK1MXnslyisLc%3D Chen JF, Huang ZH, Ma JY, Zhu JM, Moratalla R, Standaert D, Moskowitz MA, Fink JS, Schwarzschild MA (1999) A2A adenosine receptor deficiency attenuates brain injury induced by transient focal ischemia in mice. J Neurosci 19:9192–9200
14. DW Choi M Maulucci-Gedde AR Kriedstein 1987 Glutamate neurotoxicity in cortical cell culture J Neurosci 7 357 368 2880937 1:CAS:528:DyaL2sXhtFCisbw%3D Choi DW, Maulucci-Gedde M, Kriedstein AR (1987) Glutamate neurotoxicity in cortical cell culture. J Neurosci 7:357–368
15. JH Connick TW Stone 1989 Quinolinic acid neurotoxicity: protection by intracerebral phenylisopropyl adenosine (PIA) and potentiation by hypotension Neurosci Lett 101 191 196 2771165 10.1016/0304-3940(89)90529-6 1:CAS:528:DyaL1MXksFWqtrk%3D Connick JH, Stone TW (1989) Quinolinic acid neurotoxicity: protection by intracerebral phenylisopropyl adenosine (PIA) and potentiation by hypotension. Neurosci Lett 101:191–196
16. JH Connick GC Heywood GJ Sills GG Thompson MJ Brodie TW Stone 1992 Nicotinylalanine increases cerebral kynurenic acid content and has anticonvulsant activity Gen Pharmacol 23 235 239 1639238 1:CAS:528:DyaK38Xit1yjtL8%3D Connick JH, Heywood GC, Sills GJ, Thompson GG, Brodie MJ, Stone TW (1992) Nicotinylalanine increases cerebral kynurenic acid content and has anticonvulsant activity. Gen Pharmacol 23:235–239
17. C Cosi H Suzuki D Milani L Facci M Menegazzi G Vantini Y Kanai SD Skaper 1994 Poly(ADP-ribose) polymerase—early involvement in glutamate-induced neurotoxicity in cultured cerebellar granule cells J Neurosci Res 39 38 46 7807591 10.1002/jnr.490390106 1:CAS:528:DyaK2cXlvFKmu7w%3D Cosi C, Suzuki H, Milani D, Facci L, Menegazzi M, Vantini G, Kanai Y, Skaper SD (1994) Poly(ADP-ribose) polymerase—early involvement in glutamate-induced neurotoxicity in cultured cerebellar granule cells. J Neurosci Res 39:38–46
18. JT Coyle P Puttfarcken 1993 Oxidative stress, glutamate, and neurodegenerative disorders Science 262 689 695 7901908 10.1126/science.7901908 1:CAS:528:DyaK2cXlvVek Coyle JT, Puttfarcken P (1993) Oxidative stress, glutamate, and neurodegenerative disorders. Science 262:689–695
19. JT Coyle 2006 Glial metabolites of tryptophan and excitotoxicity: coming unglued Exp Neurol 197 4 7 16300760 1:CAS:528:DC%2BD2MXhtlGitrzE 10.1016/j.expneurol.2005.10.021 Coyle JT (2006) Glial metabolites of tryptophan and excitotoxicity: coming unglued. Exp Neurol 197:4–7
20. A Cozzi R Carpenedo F Moroni 1999 Kynurenine hydroxylase inhibitors reduce ischemic brain damage: studies with (m-nitrobenzoyl)-alanine (mNBA) and 3,4-dimethoxy-[-N-4-(nitrophenyl)thiazol-2YL]-benzenesulfonamide (Ro 61–8048) in models of focal or global brain ischemia J Cereb Blood Flow Metab 19 771 777 10413032 10.1097/00004647-199907000-00007 1:CAS:528:DC%2BD3cXksVCqsbk%3D Cozzi A, Carpenedo R, Moroni F (1999) Kynurenine hydroxylase inhibitors reduce ischemic brain damage: studies with (m-nitrobenzoyl)-alanine (mNBA) and 3,4-dimethoxy-[-N-4-(nitrophenyl)thiazol-2YL]-benzenesulfonamide (Ro 61–8048) in models of focal or global brain ischemia. J Cereb Blood Flow Metab 19:771–777
21. I D’Alimonte P Ballerini E Nargi S Buccella P Giuliani P Di Iorio F Caciagli R Ciccarelli 2007 Staurosporine-induced apoptosis in astrocytes is prevented by A(1) adenosine receptor activation Neurosci Lett 418 66 71 17400382 10.1016/j.neulet.2007.02.061 1:CAS:528:DC%2BD2sXkslWqurk%3D D’Alimonte I, Ballerini P, Nargi E, Buccella S, Giuliani P, Di Iorio P, Caciagli F, Ciccarelli R (2007) Staurosporine-induced apoptosis in astrocytes is prevented by A(1) adenosine receptor activation. Neurosci Lett 418:66–71
22. OP Dall’lgna LO Porciuncula DO Souza RA Cunha DR Lara 2003 Neuroprotection by caffeine and adenosine A(2A) receptor blockade of beta-amyloid neurotoxicity Br J Pharmacol 138 1207 1209 12711619 10.1038/sj.bjp.0705185 1:CAS:528:DC%2BD3sXjsFGitbY%3D Dall’lgna OP, Porciuncula LO, Souza DO, Cunha RA, Lara DR (2003) Neuroprotection by caffeine and adenosine A(2A) receptor blockade of beta-amyloid neurotoxicity. Br J Pharmacol 138:1207–1209
23. VL Dawson TM Dawson 2004 Deadly conversations: nuclear-mitochondrial cross-talk J Bioenerg Biomembr 36 287 294 15377859 10.1023/B:JOBB.0000041755.22613.8d 1:CAS:528:DC%2BD2cXnsFyis78%3D Dawson VL, Dawson TM (2004) Deadly conversations: nuclear-mitochondrial cross-talk. J Bioenerg Biomembr 36:287–294
24. A Mendonca de AM Sebastiao JA Ribeiro 1995 Inhibition of NMDA receptor-mediated currents in isolated rat hippocampal neurones by adenosine A1 receptor activation Neuroreport 6 1097 1100 7662885 10.1097/00001756-199505300-00006 de Mendonca A, Sebastiao AM, Ribeiro JA (1995) Inhibition of NMDA receptor-mediated currents in isolated rat hippocampal neurones by adenosine A1 receptor activation. Neuroreport 6:1097–1100
25. F Dessi C Charriaut-Mariangue M Khrestchatisky Y Ben-Ari 1993 Glutamate-induced neuronal death is not a programmed cell death in cerebellar culture J Neurochem 60 1953 1955 8097239 10.1111/j.1471-4159.1993.tb13427.x 1:CAS:528:DyaK3sXktVWmsbg%3D Dessi F, Charriaut-Mariangue C, Khrestchatisky M, Ben-Ari Y (1993) Glutamate-induced neuronal death is not a programmed cell death in cerebellar culture. J Neurochem 60:1953–1955
26. MR Domenici A Scotti Carolis de A Sagratella 1996 Block by N6-L-phenylisopropyladenosine of the electrophysiological and morphological correlates of hippocampal ischaemic injury in the gerbil Br J Pharmacol 118 1551 1557 8832085 1:CAS:528:DyaK28XkvVWktL8%3D Domenici MR, Scotti de Carolis A, Sagratella A (1996) Block by N6-L-phenylisopropyladenosine of the electrophysiological and morphological correlates of hippocampal ischaemic injury in the gerbil. Br J Pharmacol 118:1551–1557
27. YS Du KR Bales RC Dodel E Hamilton-Byrd JW Horn DL Czilli LK Simmons BH Ni SM Paul 1997 Activation of a caspase 3-related cysteine protease is required for glutamate-mediated apoptosis of cultured cerebellar granule neurons Proc Natl Acad Sci USA 94 11657 11662 9326666 10.1073/pnas.94.21.11657 1:CAS:528:DyaK2sXmslejt7w%3D Du YS, Bales KR, Dodel RC, Hamilton-Byrd E, Horn JW, Czilli DL, Simmons LK, Ni BH, Paul SM (1997) Activation of a caspase 3-related cysteine protease is required for glutamate-mediated apoptosis of cultured cerebellar granule neurons. Proc Natl Acad Sci USA 94:11657–11662
28. D Eschke A Brand P Scheibler S Hess K Eger C Allgaier K Nieber 2001 Effect of an adenosine A(1) receptor agonist and a novel pyrimidoindole on membrane properties and neurotransmitter release in rat cortical and hippocampal neurons Neurochem Int 38 391 398 11222919 10.1016/S0197-0186(00)00113-3 1:CAS:528:DC%2BD3MXit1artrw%3D Eschke D, Brand A, Scheibler P, Hess S, Eger K, Allgaier C, Nieber K (2001) Effect of an adenosine A(1) receptor agonist and a novel pyrimidoindole on membrane properties and neurotransmitter release in rat cortical and hippocampal neurons. Neurochem Int 38:391–398
29. AA Fatokun TW Stone RA Smith 2006 Hydrogen peroxide-induced oxidative stress in MC3T3-E1 cells: the effects of glutamate and protection by purines Bone 39 542 551 16616712 10.1016/j.bone.2006.02.062 1:CAS:528:DC%2BD28XotFyksbg%3D Fatokun AA, Stone TW, Smith RA (2006) Hydrogen peroxide-induced oxidative stress in MC3T3-E1 cells: the effects of glutamate and protection by purines. Bone 39:542–551
30. AA Fatokun TW Stone RA Smith 2007 Cell death in rat cerebellar granule neurones induced by hydrogen peroxide in vitro: mechanisms and protection by adenosine receptor ligands Brain Res 1132 193 202 17188658 10.1016/j.brainres.2006.11.008 1:CAS:528:DC%2BD2sXntlKktw%3D%3D Fatokun AA, Stone TW, Smith RA (2007) Cell death in rat cerebellar granule neurones induced by hydrogen peroxide in vitro: mechanisms and protection by adenosine receptor ligands. Brain Res 1132:193–202
31. S Fossati G Cipriani F Moroni A Chiarugi 2007 Neither energy collapse nor transcription underlie in vitro neurotoxicity of poly(ADP-ribose) polymerase hyper-activation Neurochem Int 50 203 210 17052800 10.1016/j.neuint.2006.08.009 1:CAS:528:DC%2BD28Xht12msrbM Fossati S, Cipriani G, Moroni F, Chiarugi A (2007) Neither energy collapse nor transcription underlie in vitro neurotoxicity of poly(ADP-ribose) polymerase hyper-activation. Neurochem Int 50:203–210
32. R Franco S Ferre M Torvinen S Gines J Hilion F Ciruela EI Canela J Mallol V Casado C Lluis K Fuxe 2001 Adenosine/dopamine receptor-receptor interactions in the central nervous system Drug Devel Res 52 296 302 10.1002/ddr.1127 1:CAS:528:DC%2BD3MXjsVajtrY%3D Franco R, Ferre S, Torvinen M, Gines S, Hilion J, Ciruela F, Canela EI, Mallol J, Casado V, Lluis C, Fuxe K (2001) Adenosine/dopamine receptor-receptor interactions in the central nervous system. Drug Devel Res 52:296–302
33. Y Gao JW Phillis 1994 CGS 15943, an adenosine A2 receptor antagonist, reduces cerebral ischemic injury in the mongolian gerbil Life Sci 55 PL61 PL65 8007757 10.1016/0024-3205(94)00889-2 1:CAS:528:DyaK2cXksV2qt7g%3D Gao Y, Phillis JW (1994) CGS 15943, an adenosine A2 receptor antagonist, reduces cerebral ischemic injury in the mongolian gerbil. Life Sci 55:PL61–PL65
34. MP Goldberg H Monyer JH Weiss DW Choi 1988 Adenosine reduces cortical neuronal injury induced by oxygen or glucose deprivation in vitro Neurosci Lett 89 323 327 3419631 10.1016/0304-3940(88)90547-2 1:CAS:528:DyaL1cXksV2js7k%3D Goldberg MP, Monyer H, Weiss JH, Choi DW (1988) Adenosine reduces cortical neuronal injury induced by oxygen or glucose deprivation in vitro. Neurosci Lett 89:323–327
35. JP Hannon KM Bray-French RM Phillips JR Fozard 1998 Further pharmacological characterization of the adenosine receptor subtype mediating inhibition of oxidative burst in human isolated neutrophils Drug Dev Res 43 214 224 10.1002/(SICI)1098-2299(199804)43:4<214::AID-DDR5>3.0.CO;2-L 1:CAS:528:DyaK1cXltFGhu7s%3D Hannon JP, Bray-French KM, Phillips RM, Fozard JR (1998) Further pharmacological characterization of the adenosine receptor subtype mediating inhibition of oxidative burst in human isolated neutrophils. Drug Dev Res 43:214–224
36. ST Hou JP MacManus 2002 Molecular mechanisms of cerebral ischemia-induced neuronal death Int Rev Cytol 221 93 148 12455747 1:CAS:528:DC%2BD3sXhtVyhur4%3D Hou ST, MacManus JP (2002) Molecular mechanisms of cerebral ischemia-induced neuronal death. Int Rev Cytol 221:93–148
37. ST Hou SX Jiang A Desbois D Huang J Kelly L Tessier L Karchewski J Kappler 2006 Calpain-cleaved collapsin response mediator protein-3 induces neuronal death after glutamate toxicity and cerebral ischemia J Neurosci 26 2241 2249 16495451 10.1523/JNEUROSCI.4485-05.2006 1:CAS:528:DC%2BD28XitFCms7w%3D Hou ST, Jiang SX, Desbois A, Huang D, Kelly J, Tessier L, Karchewski L, Kappler J (2006) Calpain-cleaved collapsin response mediator protein-3 induces neuronal death after glutamate toxicity and cerebral ischemia. J Neurosci 26:2241–2249
38. PA Jones RA Smith TW Stone 1998 Protection against hippocampal kainate excitotoxicity by intracerebral administration of an adenosine A 2A receptor antagonist Brain Res 800 328 335 9685693 10.1016/S0006-8993(98)00540-X 1:CAS:528:DyaK1cXks1Krtbo%3D Jones PA, Smith RA, Stone TW (1998a) Protection against hippocampal kainate excitotoxicity by intracerebral administration of an adenosine A 2A receptor antagonist. Brain Res 800:328–335
39. PA Jones RA Smith TW Stone 1998 Protection against kainate-induced excitotoxicity by adenosine A 2A receptor agonists and antagonists Neuroscience 85 229 237 9607714 10.1016/S0306-4522(97)00613-1 1:CAS:528:DyaK1cXislCgsrc%3D Jones PA, Smith RA, Stone TW (1998b) Protection against kainate-induced excitotoxicity by adenosine A 2A receptor agonists and antagonists. Neuroscience 85:229–237
40. H Kawasaki T Morooka S Shimohama J Kimura T Hirano Y Gotoh E Nishida 1997 Activation and involvement of p38 mitogen-activated protein kinase in glutamate-induced apoptosis in rat cerebellar granule cells J Biol Chem 272 18518 18521 9228012 10.1074/jbc.272.30.18518 1:CAS:528:DyaK2sXltVSgsr0%3D Kawasaki H, Morooka T, Shimohama S, Kimura J, Hirano T, Gotoh Y, Nishida E (1997) Activation and involvement of p38 mitogen-activated protein kinase in glutamate-induced apoptosis in rat cerebellar granule cells. J Biol Chem 272:18518–18521
41. M Kelly A Bailey C Ledent I Kitchen S Hourani 2004 Characterization of [H-3]ZM241385 binding in wild-type and adenosine A(2A) receptor knockout mice Eur J Pharmacol 504 55 59 15507221 10.1016/j.ejphar.2004.09.052 1:CAS:528:DC%2BD2cXovFans7c%3D Kelly M, Bailey A, Ledent C, Kitchen I, Hourani S (2004) Characterization of [H-3]ZM241385 binding in wild-type and adenosine A(2A) receptor knockout mice. Eur J Pharmacol 504:55–59
42. S Kure T Tominaga T Yoshimoto K Tada K Narisawa 1991 Glutamate triggers internucleosomal DNA cleavage in neuronal cells Biochem Biophys Res Commun 179 39 45 1679329 10.1016/0006-291X(91)91330-F 1:CAS:528:DyaK3MXlvF2gt7c%3D Kure S, Tominaga T, Yoshimoto T, Tada K, Narisawa K (1991) Glutamate triggers internucleosomal DNA cleavage in neuronal cells. Biochem Biophys Res Commun 179:39–45
43. RD Lasley G Kristo BJ Keith RM Mentzer Jr 2007 The A(2a)/A(2b) receptor antagonist ZM-241385 blocks the cardioprotective effect of adenosine agonist pretreatment in in vivo rat myocardium Amer J Physiol Heart Circ Physiol 292 H426 H431 10.1152/ajpheart.00675.2006 1:CAS:528:DC%2BD2sXisFGisL8%3D Lasley RD, Kristo G, Keith BJ, Mentzer RM Jr (2007) The A(2a)/A(2b) receptor antagonist ZM-241385 blocks the cardioprotective effect of adenosine agonist pretreatment in in vivo rat myocardium. Amer J Physiol Heart Circ Physiol 292:H426–H431
44. S Latini F Pedata 2001 Adenosine in the central nervous system: release mechanisms and extracellular concentrations J Neurochem 79 463 484 11701750 10.1046/j.1471-4159.2001.00607.x 1:CAS:528:DC%2BD3MXotlSht7Y%3D Latini S, Pedata F (2001) Adenosine in the central nervous system: release mechanisms and extracellular concentrations. J Neurochem 79:463–484
45. Y-S Lau MM Mouradian 1993 Protection against acute MPT-induced dopamine depletion in mice by adenosine J Neurochem 60 768 771 8419552 10.1111/j.1471-4159.1993.tb03215.x 1:CAS:528:DyaK3sXhtFymsrg%3D Lau Y-S, Mouradian MM (1993) Protection against acute MPT-induced dopamine depletion in mice by adenosine. J Neurochem 60:768–771
46. XH Li JC Eisenach 2005 Adenosine reduces glutamate release in rat spinal synaptosomes Anesthesiology 103 1060 1065 16249681 10.1097/00000542-200511000-00021 1:CAS:528:DC%2BD2MXhtFCru7vN Li XH, Eisenach JC (2005) Adenosine reduces glutamate release in rat spinal synaptosomes. Anesthesiology 103:1060–1065
47. YP Lin A Desbois S Jiang ST Hou 2004 Group B vitamins protect murine cerebellar granule cells from glutamate/NMDA toxicity Neuroreport 15 2241 2244 15371742 10.1097/00001756-200410050-00020 1:CAS:528:DC%2BD2cXnsFejsrw%3D Lin YP, Desbois A, Jiang S, Hou ST (2004) Group B vitamins protect murine cerebellar granule cells from glutamate/NMDA toxicity. Neuroreport 15:2241–2244
48. LV Lopes RA Cunha JA Ribeiro 1999 ZM 241385, an adenosine A(2A) receptor antagonist, inhibits hippocampal A(1) receptor responses Eur J Pharmacol 383 395 398 10594334 10.1016/S0014-2999(99)00659-7 1:CAS:528:DyaK1MXnslGqtrc%3D Lopes LV, Cunha RA, Ribeiro JA (1999) ZM 241385, an adenosine A(2A) receptor antagonist, inhibits hippocampal A(1) receptor responses. Eur J Pharmacol 383:395–398
49. LJ Martin NA Al-Abdulla AM Brambrink JR Kirsch FE Sieber C Portera-Cailliau 1998 Neurodegeneration in excitotoxicity, global cerebral ischemia, and target deprivation: a perspective on the contributions of apoptosis and necrosis Brain Res Bull 46 281 309 9671259 10.1016/S0361-9230(98)00024-0 1:STN:280:DyaK1czjsVegtg%3D%3D Martin LJ, Al-Abdulla NA, Brambrink AM, Kirsch JR, Sieber FE, Portera-Cailliau C (1998) Neurodegeneration in excitotoxicity, global cerebral ischemia, and target deprivation: a perspective on the contributions of apoptosis and necrosis. Brain Res Bull 46:281–309
50. A Monopoli G Lozza A Forloni A Mattavelli E Ongini 1998 Blockade of adenosine A 2A receptors by SCH 58261 results in neuroprotective effects in cerebral ischaemia in rats Neuroreport 9 3955 3959 9875735 10.1097/00001756-199812010-00034 1:CAS:528:DyaK1MXjtVChtg%3D%3D Monopoli A, Lozza G, Forloni A, Mattavelli A, Ongini E (1998) Blockade of adenosine A 2A receptors by SCH 58261 results in neuroprotective effects in cerebral ischaemia in rats. NeuroReport 9:3955–3959
51. F Moroni E Meli F Peruginelli A Chiarugi A Cozzi R Picca P Romagnoli R Pellicciari DE Pellegrini-Giampietro 2001 Poly(ADP-ribose) polymerase inhibitors attenuate necrotic but not apoptotic neuronal death in experimental models of cerebral ischemia Cell Death Differ 8 921 932 11526447 10.1038/sj.cdd.4400884 1:CAS:528:DC%2BD3MXmtFCjsr0%3D Moroni F, Meli E, Peruginelli F, Chiarugi A, Cozzi A, Picca R, Romagnoli P, Pellicciari R, Pellegrini-Giampietro DE (2001) Poly(ADP-ribose) polymerase inhibitors attenuate necrotic but not apoptotic neuronal death in experimental models of cerebral ischemia. Cell Death Differ 8:921–932
52. A Ogura M Miyamoto Y Kudo 1988 Neuronal death in vitro: parallelism between survivability of hippocampal neurons and sustained elevation of cytosolic Ca 2+ after exposure to glutamate receptor agonist Exp Brain Res 73 447 458 2906295 10.1007/BF00406601 1:CAS:528:DyaL1MXhsVynsLc%3D Ogura A, Miyamoto M, Kudo Y (1988) Neuronal death in vitro: parallelism between survivability of hippocampal neurons and sustained elevation of cytosolic Ca 2+ after exposure to glutamate receptor agonist. Exp Brain Res 73:447–458
53. MN Perkins TW Stone 1982 An iontophoretic investigation of the actions of convulsant kynurenines and their interaction with the endogenous excitant quinolinic acid Brain Res 247 184 187 6215086 10.1016/0006-8993(82)91048-4 1:CAS:528:DyaL38Xls1Slsr4%3D Perkins MN, Stone TW (1982) An iontophoretic investigation of the actions of convulsant kynurenines and their interaction with the endogenous excitant quinolinic acid. Brain Res 247:184–187
54. JW Phillis 1995 The effect of selective A1 and A 2A adenosine receptor antagonists on cerebral ischemic injury in the gerbil Brain Res 705 79 84 8821736 10.1016/0006-8993(95)01153-6 1:CAS:528:DyaK28XlvVGntw%3D%3D Phillis JW (1995) The effect of selective A1 and A 2A adenosine receptor antagonists on cerebral ischemic injury in the gerbil. Brain Res 705:79–84
55. JP Pin R Duvoisin 1995 The metabotropic glutamate receptors: structure and functions Neuropharmacology 34 1 26 7623957 10.1016/0028-3908(94)00129-G 1:CAS:528:DyaK2MXktF2ns7o%3D Pin JP, Duvoisin R (1995) The metabotropic glutamate receptors: structure and functions. Neuropharmacology 34:1–26
56. SM Poucher JR Keddie P Singh SM Stoggall PWR Caulkett G Jones MG Collis 1995 The in vitro pharmacology of ZM-241385, a potent, nonxanthine, A(2a) selective adenosine receptor antagonist Br J Pharmacol 115 1096 1102 7582508 1:CAS:528:DyaK2MXnt1Gksrk%3D Poucher SM, Keddie JR, Singh P, Stoggall SM, Caulkett PWR, Jones G, Collis MG (1995) The in vitro pharmacology of ZM-241385, a potent, nonxanthine, A(2a) selective adenosine receptor antagonist. Br J Pharmacol 115:1096–1102
57. K Prass U Dirnagl 1998 Glutamate antagonists in therapy and stroke Rest Neurol Neurosci 13 3 10 1:CAS:528:DyaK1cXotFSnsrs%3D Prass K, Dirnagl U (1998) Glutamate antagonists in therapy and stroke. Rest Neurol Neurosci 13:3–10
58. N Rebola RJ Rodrigues CR Oliveira RA Cunha 2005 Different roles of adenosine A(1), A(2A) and A(3) receptors in controlling kainate-induced toxicity in cortical cultured neurons Neurochem Int 47 317 325 16011860 10.1016/j.neuint.2005.05.009 1:CAS:528:DC%2BD2MXmt1SksL8%3D Rebola N, Rodrigues RJ, Oliveira CR, Cunha RA (2005) Different roles of adenosine A(1), A(2A) and A(3) receptors in controlling kainate-induced toxicity in cortical cultured neurons. Neurochem Int 47:317–325
59. F Ruiz G Alvarez M Ramos M Hernandez E Bogonez J Satrustegui 2000 Cyclosporin A targets involved in protection against glutamate excitotoxicity Eur J Pharmacol 404 29 39 10980260 10.1016/S0014-2999(00)00584-7 1:CAS:528:DC%2BD3cXmt1aju7Y%3D Ruiz F, Alvarez G, Ramos M, Hernandez M, Bogonez E, Satrustegui J (2000) Cyclosporin A targets involved in protection against glutamate excitotoxicity. Eur J Pharmacol 404:29–39
60. JA Segal P Skolnick 2000 Spermine-induced toxicity in cerebellar granule neurons is independent of its actions at NMDA receptors J Neurochem 74 60 69 10617106 10.1046/j.1471-4159.2000.0740060.x 1:CAS:528:DC%2BD3cXlt1On Segal JA, Skolnick P (2000) Spermine-induced toxicity in cerebellar granule neurons is independent of its actions at NMDA receptors. J Neurochem 74:60–69
61. Y Sei DJKE Lubitz von MP Abbraccchio XD Ji KA Jacobson 1997 Adenosine A3 receptor agonist-induced neurotoxicity in rat cerebellar granule neurons Drug Dev Res 40 267 273 10.1002/(SICI)1098-2299(199703)40:3<267::AID-DDR7>3.0.CO;2-I 1:CAS:528:DyaK2sXltlWgs7Y%3D Sei Y, von Lubitz DJKE, Abbraccchio MP, Ji XD, Jacobson KA (1997) Adenosine A3 receptor agonist-induced neurotoxicity in rat cerebellar granule neurons. Drug Dev Res 40:267–273
62. MJ Sheardown LJS Knutsen 1996 Unexpected neuroprotection observed with the adenosine A 2A receptor agonist CGS21680 Drug Develop Res 39 108 114 10.1002/(SICI)1098-2299(19960901)39:1<108::AID-DDR8>3.0.CO;2-J 1:CAS:528:DyaK2sXhtFamtb0%3D Sheardown MJ, Knutsen LJS (1996) Unexpected neuroprotection observed with the adenosine A 2A receptor agonist CGS21680. Drug Develop Res 39:108–114
63. HH Slagsvold OJ Marvik G Eidem N Kristoffersen RE Paulsen 2000 Detection of high molecular weight DNA fragments characteristic of early stage apoptosis in cerebellar granule cells exposed to glutamate Exp Brain Res 135 173 178 11131501 10.1007/s002210000521 1:CAS:528:DC%2BD3cXotFWhtrY%3D Slagsvold HH, Marvik OJ, Eidem G, Kristoffersen N, Paulsen RE (2000) Detection of high molecular weight DNA fragments characteristic of early stage apoptosis in cerebellar granule cells exposed to glutamate. Exp Brain Res 135:173–178
64. AJ Smith TW Stone RA Smith 2007 Neurotoxicity of tryptophan metabolites Biochem Soc Trans 35 1287 1289 17956331 10.1042/BST0350535 1:CAS:528:DC%2BD2sXht1eru7bI Smith AJ, Stone TW, Smith RA (2007) Neurotoxicity of tryptophan metabolites. Biochem Soc Trans 35:1287–1289
65. RA Smith T Walker X Xie ST Hou 2003 Involvement of the transcription factor E2F1/Rb in kainic acid-induced death of murine cerebellar granule cells Mol Brain Res 116 70 79 12941462 10.1016/S0169-328X(03)00253-5 1:CAS:528:DC%2BD3sXms1ylsbY%3D Smith RA, Walker T, Xie X, Hou ST (2003) Involvement of the transcription factor E2F1/Rb in kainic acid-induced death of murine cerebellar granule cells. Mol Brain Res 116:70–79
66. TW Stone WM Behan 2007 Interleukin-1beta but not tumor necrosis factor-alpha potentiates neuronal damage by quinolinic acid: protection by an adenosine A(2A) receptor antagonist J Neurosci Res 85 1077 1085 17304576 10.1002/jnr.21212 1:CAS:528:DC%2BD2sXks1Ohtrk%3D Stone TW, Behan WM (2007) Interleukin-1beta but not tumor necrosis factor-alpha potentiates neuronal damage by quinolinic acid: protection by an adenosine A(2A) receptor antagonist. J Neurosci Res 85:1077–1085
67. TW Stone LG Darlington 2002 Endogenous kynurenines as targets for drug discovery and development Nat Rev Drug Discov 1 609 620 12402501 10.1038/nrd870 1:CAS:528:DC%2BD38XlslGqtr4%3D Stone TW, Darlington LG (2002) Endogenous kynurenines as targets for drug discovery and development. Nat Rev Drug Discov 1:609–620
68. TW Stone 2002 Purines and neuroprotection Adv Exp Med Biol 513 249 280 12575824 1:CAS:528:DC%2BD3sXotlymsL8%3D Stone TW (2002) Purines and neuroprotection. Adv Exp Med Biol 513:249–280
69. TW Stone 2005 Adenosine, neurodegeneration and neuroprotection Neurol Res 27 161 168 15829179 10.1179/016164105X21896 1:CAS:528:DC%2BD2MXjt1ajs70%3D Stone TW (2005) Adenosine, neurodegeneration and neuroprotection. Neurol Res 27:161–168
70. Z Vissiennon K Sichardt U Koetter A Brattström K Nieber 2006 Valerian extract Ze 911 inhibits postsynaptic potentials by activation of adenosine A1 receptors in rat cortical neurons Planta Med 72 579 583 16673319 10.1055/s-2006-931561 1:CAS:528:DC%2BD28Xotlyms7o%3D Vissiennon Z, Sichardt K, Koetter U, Brattström A, Nieber K (2006) Valerian extract Ze 911 inhibits postsynaptic potentials by activation of adenosine A1 receptors in rat cortical neurons. Planta Med 72:579–583
71. K Wirkner Z Gerevich T Krause A Gunther L Koles D Schneider W Norenberg P Illes 2004 Adenosine A(2A) receptor-induced inhibition of NMDA and GABA(A) receptor-mediated synaptic currents in a subpopulation of rat striatal neurons Neuropharmacology 46 994 1007 15081796 10.1016/j.neuropharm.2004.01.008 1:CAS:528:DC%2BD2cXjtVOitrg%3D Wirkner K, Gerevich Z, Krause T, Gunther A, Koles L, Schneider D, Norenberg W, Illes P (2004) Adenosine A(2A) receptor-induced inhibition of NMDA and GABA(A) receptor-mediated synaptic currents in a subpopulation of rat striatal neurons. Neuropharmacology 46:994–1007
72. LG Wu P Saggau 1994 Adenosine inhibits evoked synaptic transmission primarily by reducing presynaptic calcium influx in area CA1 of hippocampus Neuron 12 1139 1148 8185949 10.1016/0896-6273(94)90321-2 1:CAS:528:DyaK2cXkslCnsrw%3D Wu LG, Saggau P (1994) Adenosine inhibits evoked synaptic transmission primarily by reducing presynaptic calcium influx in area CA1 of hippocampus. Neuron 12:1139–1148
73. GM Yan BH Ni M Weller KA Wood SM Paul 1994 Depolarization or glutamate-receptor activation blocks apoptotic cell-death of cultured CGNs Brain Res 656 43 51 7804844 10.1016/0006-8993(94)91364-1 1:CAS:528:DyaK2cXlslWis78%3D Yan GM, Ni BH, Weller M, Wood KA, Paul SM (1994) Depolarization or glutamate-receptor activation blocks apoptotic cell-death of cultured CGNs. Brain Res 656:43–51