Brief, repeated, oxygen-glucose deprivation episodes protect neurotransmission from a longer ischemic episode in the in vitro hippocampus: Role of adenosine receptors

British Journal of Pharmacology

Volumn 140, Issue 2, 2003, Pages 305-314

  Pugliese, Anna Maria ^a   Latini, Serena ^a   Corradetti, Renato ^a   Pedata, Felicita ^a  

^a UNIVERSITY OF FLORENCE   (Italy)

Author keywords

Adenosine; Cerebral ischemia; Field epsp; Hippocampal slices; Ischemic tolerance; Synaptic potential

Indexed keywords

3 PROPYL 6 ETHYL 5 [ETHYL(THIO)CARBONYL] 2 PHENYL 4 PROPYL 3 PYRIDINECARBOXYLATE; 4 [2 [7 AMINO 2 (2 FURYL) 1,2,4 TRIAZOLO[2,3 A][1,3,5]TRIAZIN 5 YLAMINO]ETHYL]PHENOL; 6 ETHYL 4 PROPYL 2 PHENYL 3 PYRIDINECARBOXYLIC ACID 5 THIOCARBOXYLIC ACID 5 ETHYL 3 PROPYL ESTER; 8 CYCLOPENTYLTHEOPHYLLINE; ADENOSINE A1 RECEPTOR; ADENOSINE A1 RECEPTOR ANTAGONIST; ADENOSINE A2A RECEPTOR; ADENOSINE A2A RECEPTOR ANTAGONIST; ADENOSINE A3 RECEPTOR; ADENOSINE A3 RECEPTOR ANTAGONIST; GLUCOSE; OXYGEN; UNCLASSIFIED DRUG;

ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN ISCHEMIA; BRAIN SLICE; CLINICAL PROTOCOL; CONTROLLED STUDY; EXCITATORY POSTSYNAPTIC POTENTIAL; HEART INFARCTION PREVENTION; HIPPOCAMPUS; IN VITRO STUDY; MALE; NEUROTRANSMISSION; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; RAT; SYNAPTIC POTENTIAL; SYNAPTIC TRANSMISSION;

ANIMALS; ANOXIA; BRAIN ISCHEMIA; ELECTRIC STIMULATION; EXCITATORY POSTSYNAPTIC POTENTIALS; GLUCOSE; HIPPOCAMPUS; ISCHEMIC PRECONDITIONING; MALE; OXYGEN; PYRIDINES; RATS; RATS, WISTAR; RECEPTOR, ADENOSINE A1; RECEPTOR, ADENOSINE A2A; RECEPTOR, ADENOSINE A3; RECEPTORS, PURINERGIC P1; SYNAPTIC TRANSMISSION; TIME FACTORS; TRIAZINES; TRIAZOLES; XANTHINES;

EID: 0141992197     PISSN: 00071188     EISSN: None     Source Type: Journal    
DOI: 10.1038/sj.bjp.0705442     Document Type: Article

References (56)

1. ABBRACCHIO, M.P. & CATTABENI, F. (1999). Brain adenosine receptors as targets for therapeutic intervention in neurodegenerative diseases. Ann. N. Y. Acad. Sci., 890, 79-92.
2. AKETA, S., NAKASE, H., KAMADA, Y., HIRAMATSU, K. & SAKAKI, T. (2000). Chemical preconditioning with 3-nitropropionic acid in gerbil hippocampal slices: therapeutic window and the participation of adenosine receptor. Exp. Neural., 166, 385-391.
3. ALICI, K., WEBER-LUXENBURGER, G. & HEINEMANN, U. (1998). Effects of glucose deprivation in area CA1 of hippocampal slices from adult and juvenile rats. Brain Res. Dev. Brain Res., 107, 71-80.
4. BLONDEAU, N., PLAMONDON, H., RICHELME, C., HEURTEAUX, C. & LAZDUNSKI, M. (2000). K(ATP) channel openers, adenosine agonists and epileptic preconditioning are stress signals inducing hippocampal neuroprotection. Neuroscience, 100, 465-474.
5. BRAND, A., VISSIENNON, Z., ESCHKE, D. & NIEBER, K. (2001). Adenosine A(1) and A(3) receptors mediate inhibition of synaptic transmission in rat cortical neurons. Neuropharmacology, 40, 85-95.
6. CALABRESI, P., CENTONE, D., PISANI, A. & BERNARDI, G. (1997). Endogenous adenosine mediates the presynaptic inhibition induced by aglycemia at corticostriatal synapses. J. Neurosci., 17, 4509-4516.
7. CORRADETTI, R., MORONI, F., PASSANI, M.B. & PEPEU, G. (1984). 8-Phenyltheophylline potentiates the electrical activity evoked in hippocampal slices. Eur. J. Pharmacol., 103, 177-180.
8. DAWSON, V.L. & DAWSON, T.M. (2000). Neuronal ischaemic preconditioning. Trends Pharmacol. Sci., 21, 423-424.
9. DIRNAGL, U., IADECOLA, C. & MOSKOWITZ, M.A. (1999). Pathobiology of ischaemic stroke: an integrated view. Trends Neurosci., 22, 391-397.
10. DOOLETTE, D.J. & KERR, D.I. (1995). Hyperexcitability in CA1 of the rat hippocampal slice following hypoxia or adenosine. Brain Res., 677, 127-137.
11. DUNWIDDIE, T.V. & DIAO, L. (1994). Extracellular adenosine concentrations in hippocampal brain slices and the tonic inhibitory modulation of evoked excitatory responses. J. Pharmacol. Exp. Ther., 268, 537-545.
12. DUNWIDDIE, T.V., DIAO, L., KIM, H.O., JIANG, J.L. & JACOBSON, K.A. (1997). Activation of hippocampal adenosine A3 receptors produces a desensitization of A1 receptor-mediated responses in rat hippocampus. J. Neurosci., 17, 607-614.
13. FOWLER, J.C. (1990). Adenosine antagonists alter the synaptic response to in vitro ischemia in the rat hippocampus. Brain Res., 509, 331-334.
14. FOWLER, J.C. (1992). Escape from inhibition of synaptic transmission during in vitro hypoxia and hypoglycemia in the hippocampus. Brain Res., 573, 169-173.
15. FOWLER, J.C. (1994). Glucose deprivation results in a lactate preventable increase in adenosine and depression of synaptic transmission in rat hippocampal slices. J. Neurochem., 60, 572-576.
16. FURLING, D., GHRIBI, O., LAHSAINI, A., MIRAULT, M.E. & MASSICOTTE, G. (2000). Impairment of synaptic transmission by transient hypoxia in hippocampal slices: improved recovery in glutathione peroxidase transgenic mice. Proc. Natl. Acad. Sci. U.S.A., 97, 4351-4356.
17. 2+/calmodulin-dependent protein kinase II in long-term potentiation. Neuroscience, 21, 7053-7062.
18. GRIBKOFF, V.K., BAUMAN, L.A. & VANDERMAELEN, C.P. (1990). The adenosine antagonist 8-cyclopentyltheophylline reduces the depression of hippocampal neuronal responses during hypoxia. Brain Res., 512, 353-357.
19. 1 receptors, and ATP-sensitive K+ channels in cerebral ischemic preconditioning. Proc. Natl. Acad. Sci. U.S.A., 92, 4666-4670.
20. HIRAIDE, T., KATSURA, K., MURAMATSU, H., ASANO, G. & KATAYAMA, Y. (2001). Adenosine receptor antagonists cancelled the ischemic tolerance phenomenon in gerbil. Brain Res., 910, 94-98.
21. ISHIDA, T., YARIMIZU, K., GUTE, D.C. & KORTHUIS, R.J. (1997). Mechanisms of ischemic preconditioning. Shock, 8, 86-94.
22. KATO, H., LIU, Y., ARAKI, T. & KOGURE, K. (1991). Temporal profile of the effects of pretreatment with brief cerebral ischemia on the neuronal damage following secondary ischemic insult in the gerbil: cumulative damage and protective effects. Brain Res., 553, 238-242.
23. KHASPEKOV, L., SHAMLOO, M., VICTOROV, I. & WIELOCH, T. (1998). Sublethal in vitro glucose-oxygen deprivation protects cultured hippocampal neurons against a subsequent severe insult. Neuroreport, 9, 1273-1276.
24. KIRINO, T., TSUJITA, Y. & TAMURA, A. (1991). Induced tolerance to ischemia in gerbil hippocampal neurons. J. Cereb. Blood Flow Metab., 11, 299-307.
25. KITAGAWA, K., MATSUMOTO, M., TAGAYA, M., HATA, R., UEDA, H., NIINOBE, M., HANDA, N., FUKUNAGA, R., KIMURA, K. & MIKOSHlBA, K. (1990). Ischemic tolerance phenomenon found in the brain. Brain Res., 528, 21-24.
26. KLONER, R.A. & JENNINGS, R.B. (2001). Consequences of brief ischemia: stunning, preconditioning, and their clinical implications: part 2. Circulation, 104, 3158-3167.
27. LATINI, S., BORDONI, F., CORRADETTI, R., PEPEU, G. & PEDATA, F. (1998). Temporal correlation between adenosine outflow and synaptic potential inhibition in rat hippocampal slices during ischemia-like conditions. Brain Res., 794, 325-328.
28. LATINI, S., BORDONI, F., PEDATA, F. & CORRADETTI, R. (1999a). Extracellular adenosine concentrations during in vitro ischaemia in rat hippocampal slices. Br. J. Pharmacol., 127, 729-739.
29. 2A adenosine receptor stimulation and antagonism on synaptic depression induced by in vitro ischaemia in rat hippocampal slices. Br. J. Pharmacol., 128, 1035-1044.
30. LATINI, S., PUGLIESE, A.M., CORRADETTI, R. & PEDATA, F. (2001). A model of in 'vitro' preconditioning in the rat hippocampus. Soc. Neurosci. Abstr., 208, 16.
31. LI, A.H., MORO, S., MELMAN, N., JI, X.D. & JACOBSON, K.A. (1998). Structure-activity relationships and molecular modeling of 3,5-diacyl-2,4-dialkylpyridine derivatives as selective A3 adenosine receptor antagonists. J. Med. Chem., 41, 3186-3201.
32. LIU, Y., KATO, H., NAKATA, N. & KOGURE, K. (1992). Protection of rat hippocampus against ischemic neuronal damage by pretreatment with sublethal ischemia. Brain Res., 586, 121-124.
33. LUHMANN, H.J. & HEINEMANN, U. (1992). Hypoxia-induced functional alterations in adult rat neocortex. J. Neurophysiol., 67, 798-811.
34. MELANI, A., PANTONI, L., BORDONI, F., GIANFRIDDO, M., BIANCHI, L., VANNUCCHI, M.G., BERTORELLI, R., MONOPOLI, A. & PEDATA, F. (2003). The selective A2A receptor antagonist SCH 58261 reduces striatal transmitter outflow, turning behavior and ischemic brain damage induced by permanent focal ischemia in the rat. Brain Res., 959, 243-250.
35. MILLER, B.A., PEREZ, R.S., SHAH, A.R., GONZALES, E.R., PARK, T.S. & GIDDAY, J.M. (2001). Cerebral protection by hypoxic preconditioning in a murine model of focal ischemia-reperfusion. Neuroreport, 2, 1663-1669.
36. MUSLEH, W., BRUCE, A., MALFROY, B. & BAUDRY, M. (1994). Effects of EUK-8, a synthetic catalytic superoxide scavenger, on hypoxia- and acidosis-induced damage in hippocampal slices. Neuropharmacology, 33, 929-934.
37. MURRY, C.E., JENNINGS, R.B. & REIMER, K.A. (1986). Preconditioning with ischemia: a delay of lethal cell injury in ischemic myocardium. Circulation, 74, 1124-1136.
38. NAKAMURA, M., NAGAKIMURA, K., MATSUMOTO, M. & SAKABE, T. (2002). Rapid tolerance to focal cerebral ischemia in rats is attenuated by adenosine A1 receptor antagonist. J. Cereb. Blood Flow Metab., 22, 161-170.
39. PASCHEN, W. & MIES, G. (1999). Effect of induced tolerance on biochemical disturbances in hippocampal slices from the gerbil during and after oxygen/glucose deprivation. Neuroreport, 10, 1417-1421.
40. PEARSON, T., NURITOVA, F., CALDWELL, D., DALE, N. & FRENGUELLI, B.G. (2001). A depletable pool of adenosine in area CA1 of the rat hippocampus. J. Neurosci., 21, 2298-2307.
41. 2A receptors in ischemia. Ann. N. Y. Acad. Sci., 939, 74-84.
42. PEDATA, F., LATINI, S., PUGLIESE, A.M. & PEPEU, G. (1993). Investigations into the adenosine outflow from hippocampal slices evoked by ischemia-like conditions. J. Neurochem., 61, 284-289.
43. PEREZ-PINZON, M.A., MUMFORD, P.L., ROSENTHAL, M. & SICK, T.J. (1996). Anoxic preconditioning in hippocampal slices: role of adenosine. Neuroscience, 75, 687-694.
44. PEREZ-PINZON, M.A. & BORN, J.G. (1999). Rapid preconditioning neuroprotection following anoxia in hippocampal slices: role of the K+ ATP channel and protein kinase C. Neuroscience, 89, 453-459.
45. PLASCHKE, K., WEIGAND, M.A., MICHEL, A., MARTIN, E. & BARDENHEUER, H.J. (2000). Permanent cerebral hypoperfusion: 'preconditioning-like' effects on rat energy metabolism towards acute systemic hypotension. Brain Res., 858, 363-370.
46. PRINGLE, A.K., THOMAS, S.J., SIGNORELLI, F. & IANNOTTI, F. (1999). Ischaemic preconditioning in organotypic hippocampal slice cultures is inversely correlated to the induction of the 72 kDa heat shock protein (HSP72). Brain Res., 845, 152-164.
47. RAVAL, A.P., DAVE, K.R., MOCHLY-ROSEN, D., SICK, T.J. & PEREZ-PINZON, M.A. (2003). Epsilon PKC is required for the induction of tolerance by ischemic and NMDA-mediated preconditioning in the organotypic hippocampal slice. J. Neurosci., 23, 384-391.
48. SCHURR, A., REID, K.H., TSENG, M.T., WEST, C. & RIGOR, B.M. (1986). Adaptation of adult brain tissue to anoxia and hypoxia in vitro. Brain Res., 374, 244-248.
49. SCHURR, A. & RIGOR, B.M. (1989). Cerebral ischemia revisited: new insights as revealed using in vitro brain slice preparations. Experientia., 45, 684-695.
50. SCHURR, A., PAYNE, R.S., MILLER, J.J. & RIGOR, B.M. (1997). Brain lactate, not glucose, fuels the recovery of synaptic function from hypoxia upon reoxygenation: an in vitro study. Brain Res., 744, 105-111.
51. SICK, T.J., SOLOW, E.L. & ROBERTS, E.L. (1987). Extracellular potassium ion activity and electrophysiology in the hippocampal slice: paradoxical recovery of synaptic transmission during anoxia. Brain Res., 418, 227-234.
52. STONE, T.W. (2000). Effects of clomethiazole on spreading depression in the rat hippocampal slice. Eur. J. Pharmacol., 399, 29-34.
53. TIAN, G.F. & BAKER, A.J. (2002). Protective effect of high glucose against ischemia-induced synaptic transmission damage in rat hippocampal slices. J. Neurophysiol., 88, 236-248.
54. TOKUNAGA, H., HIRAMATSU, K. & SAKAKI, T. (1998). Effect of preceding in vivo sublethal ischemia on the evoked potentials during secondary in vitro hypoxia evaluated with gerbil hippocampal slices. Brain Res., 784, 316-320.
55. VON LUBITZ, D.K. (1999). Adenosine and cerebral ischemia: therapeutic future or death of a brave concept? Eur. J. Pharmacol., 365, 9-25.
56. ZHU, P.J. & KRNJEVIC, K. (1999). Persistent block of CA1 synaptic function by prolonged hypoxia. Neuroscience, 90, 759-770.