NMDA preconditioning protects against quinolinic acid-induced seizures via PKA, PI3K and MAPK/ERK signaling pathways

Behavioural Brain Research

Volumn 219, Issue 1, 2011, Pages 92-97

  de Araújo Herculano, Bruno ^a   Vandresen Filho, Samuel ^a   Martins, Wagner Carbolin ^a   Boeck, Carina Rodrigues ^b   Tasca, Carla Inês ^a  

^a FEDERAL UNIVERSITY OF SANTA CATARINA   (Brazil)

^b UNIVERSIDADE DO EXTREMO SUL CATARINENSE   (Brazil)

Author keywords

Neuroprotection; NMDA preconditioning; PI3K; PKA; Quinolinic acid; Signaling pathways

Indexed keywords

1 [N,O BIS(5 ISOQUINOLINESULFONYL) N METHYLTYROSYL] 4 PHENYLPIPERAZINE; 2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; CHELERYTHRINE; CYCLIC AMP DEPENDENT PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE; N [2 (4 BROMOCINNAMYLAMINO)ETHYL] 5 ISOQUINOLINESULFONAMIDE; N METHYL DEXTRO ASPARTIC ACID; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE C; QUINOLINIC ACID; WORTMANNIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; ENZYME INHIBITION; MALE; MORTALITY; MOUSE; NERVE CELL NECROSIS; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; SEIZURE; SIGNAL TRANSDUCTION;

1-(5-ISOQUINOLINESULFONYL)-2-METHYLPIPERAZINE; ANDROSTADIENES; ANIMALS; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASE TYPE 2; CONDITIONING (PSYCHOLOGY); CYCLIC AMP-DEPENDENT PROTEIN KINASES; ENZYME INHIBITORS; EXCITATORY AMINO ACID AGONISTS; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FLAVONOIDS; INJECTIONS, INTRAVENTRICULAR; ISOQUINOLINES; MALE; MICE; MITOGEN-ACTIVATED PROTEIN KINASES; N-METHYLASPARTATE; PHOSPHATIDYLINOSITOL 3-KINASES; PROTEIN KINASE INHIBITORS; QUINOLINIC ACID; RECEPTORS, N-METHYL-D-ASPARTATE; SEIZURES; SIGNAL TRANSDUCTION; SULFONAMIDES;

EID: 78651390307     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2010.12.025     Document Type: Article

References (48)

1. Dirnagl U., Simon R.P., Hallenbeck J.M. Ischemic tolerance and endogenous neuroprotection. Trends Neurosci 2003, 26:248-254.
2. Boeck C.R., Kroth E.H., Bronzatto M.J., Vendite D. Adenosine receptors co-operate with NMDA preconditioning to protect cerebellar granule cells against glutamate neurotoxicity. Neuropharmacology 2005, 49:17-24.
3. Boeck C.R., Ganzella M., Lottermann A., Vendite D. NMDA preconditioning protects against seizures and hippocampal neurotoxicity induced by quinolinic acid in mice. Epilepsia 2004, 45:745-750.
4. Vandresen-Filho S., De Araújo Herculano B., Franco J.L., Boeck C.R., Dafré A.L., Tasca C.I. Evaluation of glutathione metabolism in NMDA preconditioning against quinolinic acid-induced seizures in mice cerebral cortex and hippocampus. Brain Res 2007, 1184:38-45.
5. Chuang D.M., Gao X.M., Paul S.M. N-methyl-d-aspartate exposure blocks glutamate toxicity in cultured cerebellar granule cells. Mol Pharmacol 1992, 42:210-216.
6. Dickie B.G.M., Holmes C., Greenfield S.A. Neurotoxic and neurotrophic effects of chronic N-methyl-d-aspartate exposure upon mesencephalic dopaminergic neurons in organotypic culture. Neuroscience 1996, 72:731-741.
7. Pringle A.K., Thomas S.J., Signorelli F., Iannotti F. Ischaemic pre-conditioning in organotypic hippocampal slice cultures is inversely correlated to the induction of the 72kDa heat shock protein (HSP72). Brain Res 1999, 845:152-164.
8. Valentim L.M., Rodnight R., Geyer A.B., Horn A.P., Tavares A., Cimarosti H., et al. Changes in heat shock protein 27 phosphorylation and immunocontent in response to preconditioning to oxygen and glucose deprivation in organotypic hippocampal cultures. Neuroscience 2003, 118:379-386.
9. Ogita K., Okuda H., Yamamoto Y., Nishiyama N., Yoneda Y. In vivo neuroprotective role of NMDA receptors against kainate-induced excitotoxicity in murine hippocampal pyramidal neurons. J Neurochem 2003, 85:1336-1346.
10. Miao B., Yin X.H., Pei D.S., Zhang Q.G., Zhang G.Y. Neuroprotective effects of preconditioning ischemia on ischemic brain injury through down-regulating activation of JNK1/2 via N-methyl-d-aspartate receptor-mediated Akt1 activation. J Biol Chem 2005, 280(23):21693-21699.
11. Gidday J.M. Cerebral preconditioning and ischaemic tolerance. Nat Rev Neurosci 2006, 7:437-448.
12. Jia J., Wang X., Li H., Han S., Zu P., Li J. Activations of nPKCe{open} and ERK1/2 were involved in oxygen-glucose deprivation-induced neuroprotection via NMDA receptors in hippocampal slices of mice. J Neurosurg Anesthesiol 2007, 19:18-24.
13. Marais E., Genade S., Lochner A. CREB activation and ischaemic preconditioning. Cardiovasc Drugs Ther 2008, 22(1):3-17.
14. Redel A., Lange M., Jazbutyte V., Lotz C., Smul T.M., Roewer N., et al. Activation of mitochondrial large-conductance calcium-activated K+ channels via protein kinase a mediates desflurane-induced preconditioning. Anesth Analg 2008, 106:384-391.
15. Van Rensburg R., Errington D.R., Ennaceur A., Lees G., Obrenovitch T.P., Chazot P.L. A new model for the study of high-K+-induced preconditioning in cultured neurones: role of N-methyl-d-aspartate and α7-nicotinic acetylcholine receptors. J Neurosci Methods 2009, 177(2):311-316.
16. Miyawaki T., Mashiko T., Ofengeim D., Flannery R.J., Noh K.M., Fujisawa S., et al. Ischemic preconditioning blocks BAD translocation, Bcl-xL cleavage, and large channel activity in mitochondria of postischemic hippocampal neurons. PNAS 2008, 105(12):4892-4897.
17. Stone T.W., Behan W.M., MacDonald M., Darlington L.G. Possible mediation of quinolinic acid-induced hippocampal damage by reactive oxygen species. Amino Acids 2000, 19:275-281.
18. Naredo I.V., Poeggeler B., Sanches V.S., Caballero B., Zapico C.T., Garcia O.A., et al. Melatonin neutralizes neurotoxicity induced by quinolinic acid in brain tissue culture. J Pineal Res 2005, 39:266-275.
19. Stone T.W. Kynurenines in the CNS: from endogenous obscurity to therapeutic importance. Prog Neurobiol 2001, 64:185-218.
20. Heyes M.P., Wyler A.R., Devinsky J.A. Quinolinic acid concentrations in brain and cerebrospinal fluid of patients with intractable complex partial seizures. Epilepsia 1990, 31:172-177.
21. Tavares R.G., Santos C.I., Alves C.E., Porciuncula L.B., Emanuelli L.O., Souza T. Quinolinic acid stimulates synaptosomal glutamate release and inhibits glutamate uptake into astrocytes. Neurochem Int 2002, 40:621-627.
22. Tavares R.G., Tasca C.I., Santos C., Souza M., Dutra-Filho D.O. Quinolinic acid inhibits glutamate uptake into synaptic vesicles from rat brain. Neuroreport 2000, 11:249-253.
23. Schmidt A.P., Lara D.R., Marahin J.F., Perla A.S., Souza D.O. Guanosine and GMP prevent seizures induced by quinolinic acid in mice. Brain Res 2000, 864:40-43.
24. Ganzella M., Jardim F.M., Boeck C.R., Vendite D. Time course of oxidative events in the hippocampus following intracerebroventricular infusion of quinolinic acid in mice. Neurosci Res 2006, 55:397-402.
25. Piermartiri T.C.B., Vandresen-Filho S., Herculano B.A., Martins W.C., Dal'agnolo D., Stroeh E., et al. Atorvastatin prevents hippocampal cell death due to quinolinic acid-induced seizures in mice by increasing Akt phosphorylation and glutamate uptake. Neurotox Res 2009, 16(2):106-115.
26. Almeida R.C., Souza D.G., Soletti R.C., López M.G., Rodrigues A.L.S., Gabilan N.H. Involvement of PKA, MAPK/ERK and CaMKII, but not PKC in the acute antidepressant-like effect of memantine in mice. Neurosci Lett 2005, 395:93-97.
27. Ozaita A., Puighermanal E., Maldonado R. Regulation of PI3K/Akt/GSK-3 pathway by cannabinoids in the brain. J Neurochem 2007, 102:1105-1114.
28. Stone T.W., Darlington L.G. Endogenous Kynurenines as targets for drug discovery and development. Nat Rev Drug Discov 2002, 1:609-620.
29. Chou W.H., Messing R.O. Protein kinase C isozymes in stroke. Trends Cardiovasc Med 2005, 15:47-51.
30. Barnett M.E., Magdwick D.K., Takemoto D.J. Protein kinase C as a stress sensor. Cell Signal 2007, 19:1820-1829.
31. Jung M., Watson D.G., Simpkins J.W. Suppression of protein kinase Ce{open} mediates 17b-estradiol-induced neuroprotection in an immortalized hippocampal cell line. J Neurochem 2005, 95:745-755.
32. Hayashi S., Ueyama T., Kajimoto T., Yagi K., Kohmura E., Saito N. Involvement of γ Protein kinase C in estrogen-induced neuroprotection against focal brain ischemia through G protein-coupled estrogen receptor. J Neurochem 2005, 93:883-891.
33. Raval A.P., Dave K.R., Mochly-Rosen D., Sick T.J., Pérez-Pinzón M.A. e{open}PKC is required for the induction of tolerance by Ischemic and NMDA-Mediated Preconditioning in the organotypic hippocampal slice. J Neurosci 2003, 23:384-391.
34. Carter D.S., Naqeeb Haider S., Blair R.E., Deshpande L.S., Sombati S., Delorenzo R.J. Altered calcium/calmodulin kinase II activity changes calcium homeostasis that underlies epileptiform activity in hippocampal neurons in culture. J Pharmacol Exp Ther 2006, 319:1021-1031.
35. Suh H.W., Lee H.K., Seo Y.J., Kwon M.S., Shim E.J., Lee J.Y., et al. Kainic acid (KA)-induced Ca2+/Calmodulin-dependent protein kinase II (CaMK II) expression in the neurons, astrocytes and microglia of the mouse hippocampal CA3 region, and the phosphorylated CaMK II only in the hippocampal neurons. Neurosci Lett 2005, 381:223-227.
36. Tauskela J.S., Brunette E., Monette R., Comas T., Morley P. Preconditioning of cortical neurons by oxygen-glucose deprivation: tolerance induction through abbreviated neurotoxic signaling. Am J Physiol Cell Physiol 2003, 285:899-911.
37. Giordano G., Sánchez-Pérez A.M., Montoliu C., Berezney R., Malyavantham K., Costa L.G., et al. Activation of NMDA receptors induces protein kinase A-mediated phosphorylation and degradation of matrin 3. Blocking these effects prevents NMDA-induced neuronal death. J Neurochem 2005, 94:808-818.
38. Skeberdis V.A., Chevaleyre V., Lau C.G., Goldberg J.H., Pettit D.L., Suadicani S.O., et al. Protein Kinase A regulates calcium permeability of NMDA receptors. Nat Neurosci 2006, 9:501-510.
39. Man H.Y., Sekine-Aizawa Y., Huganir R.L. Regulation of α-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid receptor trafficking through PKA phosphorylation of the Glu receptor 1 subunit. PNAS 2006, 109:3579-3584.
40. Yang Y., Wang X.B., Frerking M., Zhou Q. Delivery of AMPA receptors to perisynaptic sites precedes the full expression of long-term potentiation. PNAS 2008, 105:11388-11393.
41. Yano S., Morioka M., Fukunaga K., Kawano T., Hara T., Kai Y., et al. Activation of Akt/protein kinase B contributes to induction of ischemic tolerance in the CA1 subfield of gerbil hippocampus. J Cereb Blood Flow Metab 2001, 21:351-360.
42. Yano S., Tokumitsu H., Soderling T.R. Calcium promotes cell survival through CaM-K kinase activation of the protein-kinase B pathway. Nature 1998, 396:584-587.
43. Soriano F.X., Papadia S., Hofmann F., Hardingham N.R., Bading H., Hardingham G.E. Preconditioning doses of NMDA promote neuroprotection by enhancing neuronal excitability. J Neurosci 2006, 26(17):4509-4518.
44. Toyoda H., Zhao M.G., Xu H., Wu L.J., Ren M., Zhuo M. Requirement of extracellular signal-regulated kinase/mitogen-activated protein kinase for long-term potentiation in adult mouse anterior cingulate cortex. Mol Pain 2007, 3:36.
45. Gao X., Zhang H., Takahashi T., Hsieh J., Liao J., Steinberg G.K., et al. The Akt signaling pathway contributes to postconditioning's protection against stroke; the protection is associated with the MAPK and PKC pathways. J Neurochem 2008, 105:943-955.
46. Youssef F., Stone T.W., Addae J.I. Interactions of glutamate receptor agonists with long-term potentiation in the rat hippocampal slice. Eur J Pharmacol 2000, 398(2000):349-359.
47. Youssef F., Addae J.I., Stone T.W. NMDA-induced preconditioning attenuates synaptic plasticity in the rat hippocampus. Brain Res 2006, 1073-1074(2006):183-189.
48. Tang B., Ji Y., Traub R.J. Estrogen alters spinal NMDA receptor activity via a PKA signaling pathway in a visceral pain model in the rat. Pain 2008, 137(3):540-549.