COX-2, but not COX-1, activity is necessary for the induction of perforant path long-term potentiation and spatial learning in vivo

European Journal of Neuroscience

Volumn 27, Issue 11, 2008, Pages 2999-3008

  Cowley, T R ^a   Fahey, B ^a   O'Mara, S M ^a  

^a TRINITY COLLEGE DUBLIN   (Ireland)

Author keywords

c FOS; ERK; Hippocampus; Rat; Synaptic plasticity

Indexed keywords

CELECOXIB; CYCLOOXYGENASE 1 INHIBITOR; CYCLOOXYGENASE 2; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 3; PROSTAGLANDIN E2; SC 58560;

ANIMAL EXPERIMENT; ARTICLE; BEHAVIOR; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; GENE EXPRESSION; HIPPOCAMPUS; LEARNING; LONG TERM MEMORY; LONG TERM POTENTIATION; MALE; MAZE TEST; MEMORY; MEMORY CONSOLIDATION; NERVE CELL PLASTICITY; NONHUMAN; ONCOGENE C FOS; PERFORANT NERVE TRACT; PHOSPHORYLATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SIGNAL TRANSDUCTION; SYNAPTIC TRANSMISSION; WESTERN BLOTTING;

ANIMALS; CYCLOOXYGENASE 1; CYCLOOXYGENASE 2; DINOPROSTONE; ENZYME INHIBITORS; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; HIPPOCAMPUS; LEARNING; LONG-TERM POTENTIATION; MALE; MAZE LEARNING; MEMBRANE PROTEINS; MEMORY DISORDERS; NEURONAL PLASTICITY; PERFORANT PATHWAY; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-FOS; RATS; RATS, WISTAR; SPACE PERCEPTION; SYNAPSES; SYNAPTIC TRANSMISSION;

EID: 45149104720     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2008.06251.x     Document Type: Article

References (47)

1. +-dependent phospholipase A2. J. Neurochem., 91, 1389 1397.
2. Bradford, M.M. (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.
3. Brock, T.G., McNish, R.W. Peters-Golden, M. (1999) Arachidonic acid is preferentially metabolized by cyclooxygenase-2 to prostacyclin and prostaglandin E2. J. Biol. Chem., 274, 11660 11666.
4. Chandrasekharan, N.V., Dai, H., Roos, K.L., Evanson, N.K., Tomsik, J., Elton, T.S. Simmons, D.L. (2002) COX-3, a cyclooxygenase-1 variant inhibited by acetaminophen and other analgesic/antipyretic drugs: cloning, structure, and expression. Proc. Natl Acad. Sci. U.S.A., 99, 13926 13931.
5. Chen, C. Bazan, N.G. (2005) Endogenous PGE2 regulates membrane excitability and synaptic transmission in hippocampal CA1 pyramidal neurons. J. Neurophysiol., 93, 929 941.
6. Chen, C., Magee, J.C. Bazan, N.G. (2002) Cyclooxygenase-2 regulates prostaglandin E2 signaling in hippocampal long-term synaptic plasticity. J. Neurophysiol., 87, 2851 2857.
7. Ciceri, P., Zhang, Y., Shaffer, A.F., Leahy, K.M., Woerner, M.B., Smith, W.G., Seibert, K. Isakson, P.C. (2002) Pharmacology of celecoxib in rat brain after kainate administration. J. Pharmacol. Exp. Ther., 302, 846 852.
8. Coogan, A.N., O'Leary, D.M. O'Connor, J.J. (1999) P42/44 MAP Kinase inhibitor PD98059 attenuates multiple forms of synaptic plasticity in rat dentate gyrus in vitro. J. Neurophysiol., 81, 103 110.
9. Davis, S. Laroche, S. (1998) A molecular biological approach to synaptic plasticity and learning. C. R. Acad. Sci. III, 321, 97 107.
10. English, J.D. Sweatt, J.D. (1997) A requirement for the mitogen-activated protein kinase cascade in hippocampal long term potentiation. J. Biol. Chem., 272, 19103 19106.
11. Gobbo, O.L. O'Mara, S.M. (2004) Post-treatment, but not pre-treatment, with the selective cyclooxygenase-2 inhibitor celecoxib markedly enhances functional recovery from kainic acid-induced neurodegeneration. Neuroscience, 125, 317 327.
12. Hochman, J.S. Shah, N.R. (2006) What price pain relief? Circulation, 113, 2868 2870.
13. +-ATPases: a plausible link with its anti-tumour effect and cardiovascular risks. Biochem. J., 366, 831 837.
14. Kaufmann, W.E., Worley, P.F., Pegg, J., Bremer, M. Isakson, P. (1996) COX-2, a synaptically induced enzyme, is expressed by excitatory neurons at postsynaptic sites in rat cerebral cortex. Proc. Natl Acad. Sci. U.S.A., 93, 2317 2321.
15. Kujubu, D.A., Fletcher, B.S., Varnum, B.C., Lim, R.W. Herschman, H.R. (1991) TIS10, a phorbol ester tumor promoter-inducible mRNA from Swiss 3T3 cells, encodes a novel prostaglandin synthase/cyclooxygenase homologue. J. Biol. Chem., 266, 12866 12872.
16. Laemmli, U.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature, 227, 680 685.
17. Lai, K.-C., Chu, K.-M., Hui, W.-M., Wong, B.C.-Y., Hu, W.H.-C., Wong, W.-M., Chan, A.O.-O., Wong, J. Lam, S.-K. (2005) Celecoxib compared with lansoprazole and naproxen to prevent gastrointestinal ulcer complications. Am. J. Med., 118, 1271 1278.
18. Lerea, L.S., Carlson, N.G. McNamara, J.O. (1995) N-methyl-D-aspartate receptors activate transcription of c-fos and NGFI-A by distinct phospholipase A2-requiring intracellular signaling pathways. Mol. Pharmacol., 47, 1119 1125.
19. Lerea, L.S., Carlson, N.G., Simonato, M., Morrow, J.D., Roberts, J.L. McNamara, J.O. (1997) Prostaglandin F2alpha is required for NMDA receptor-mediated induction of c-fos mRNA in dentate gyrus neurons. J. Neurosci., 17, 117 124.
20. Lømo, T. (1971) Patterns of activation in a monosynaptic cortical pathway: the perforant path input to the dentate area of the hippocampal formation. Exp. Brain Res., 12, 18 45.
21. Lynch, M.A. (2004) Long-term potentiation and memory. Physiol. Rev., 84, 87 136.
22. Marder, C.P. Buonomano, D.V. (2004) Timing and balance of inhibition enhance the effect of long-term potentiation on cell firing. J. Neurosci., 24, 8873 8884.
23. Matsumura, K., Watanabe, Y., Imai-Matsumura, K., Connolly, M., Koyama, Y., Onoe, H. Watanabe, Y. (1992) Mapping of prostaglandin E2 binding sites in rat brain using quantitative autoradiography. Brain Res., 581, 292 298.
24. Niederberger, E., Tegeder, I., Vetter, G., Schmidtko, A., Schmidt, H., Euchenhofer, C., Brautigam, L., Grosch, S. Geisslinger, G. (2001) Celecoxib loses its anti-inflammatory efficacy at high doses through activation of NF-kappaB. FASEB J., 15, 1622 1624.
25. O'Donnell, E., Vereker, E. Lynch, M.A. (2000) Age-related impairment in LTP is accompanied by enhanced activity of stress-activated protein kinases: analysis of underlying mechanisms. Eur. J. Neurosci., 12, 345 352.
26. Paulson, S.K., Zhang, J.Y., Breau, A.P., Hribar, J.D., Liu, N.W., Jessen, S.M., Lawal, Y.M., Cogburn, J.N., Gresk, C.J., Markos, C.S., Maziasz, T.J., Schoenhard, G.L. Burton, E.G. (2000) Pharmacokinetics, tissue distribution, metabolism, and excretion of celecoxib in rats. Drug Metab. Dispos., 28, 514 521.
27. Paxinos, G. Watson, C. (1997) The Rat Brain in Stereotaxic Coordinates. Academic Press, London.
28. Platenik, J., Kuramoto, N. Yoneda, Y. (2000) Molecular mechanisms associated with long-term consolidation of the NMDA signals. Life Sci., 67, 335 364.
29. Rall, J.M., Mach, S.A. Dash, P.K. (2003) Intrahippocampal infusion of a cyclooxygenase-2 inhibitor attenuates memory acquisition in rats. Brain Res., 968, 273 276.
30. Roberson, E.D., English, J.D., Adams, J.P., Selcher, J.C., Kondratick, C. Sweatt, J.D. (1999) The mitogen-activated protein kinase cascade couples PKA and PKC to cAMP response element binding protein phosphorylation in area CA1 of hippocampus. J. Neurosci., 19, 4337 4348.
31. Sang, N., Zhang, J., Marcheselli, V., Bazan, N.G. Chen, C. (2005) Postsynaptically synthesized prostaglandin E2 (PGE2) modulates hippocampal synaptic transmission via a presynaptic PGE2 EP2 receptor. J. Neurosci., 25, 9858 9870.
32. Schwieler, L., Erhardt, S., Nilsson, L., Linderholm, K. Engberg, G. (2006) Effects of COX-1 and COX-2 inhibitors on the firing of rat midbrain dopaminergic neurons - possible involvement of endogenous kynurenic acid. Synapse, 59, 290 298.
33. Sekiyama, N., Mizuta, S., Hori, A. Kobayashi, S. (1995) Prostaglandin E2 facilitates excitatory synaptic transmission in the nucleus tractus solitarii of rats. Neurosci. Lett., 188, 101 104.
34. Shaw, K.N., Commins, S. O'Mara, S.M. (2003) Deficits in spatial learning and synaptic plasticity induced by the rapid and competitive broad-spectrum cyclooxygenase inhibitor ibuprofen are reversed by increasing endogenous brain-derived neurotrophic factor. Eur. J. Neurosci., 17, 2438 2446.
35. Shimizu, T. Wolfe, L.S. (1990) Arachidonic acid cascade and signal transduction. J. Neurochem., 55, 1 15.
36. Smith, C.J., Zhang, Y., Koboldt, C.M., Muhammad, J., Zweifel, B.S., Shaffer, A., Talley, J.J., Masferrer, J.L., Seibert, K. Isakson, P.C. (1998) Pharmacological analysis of cyclooxygenase-1 in inflammation. Proc. Natl Acad. Sci. U.S.A., 95, 13313 13318.
37. Solomon, D.H., Avorn, J., Stürmer, T., Glynn, R.J., Mogun, H. Schneeweiss, S. (2006) Cardiovascular outcomes in new users of coxibs and nonsteroidal antiinflammatory drugs: high-risk subgroups and time course of risk. Arthritis Rheum., 54, 1378 1389.
38. Swinney, D.C., Mak, A.Y., Barnett, J. Ramesha, C.S. (1997) Differential allosteric regulation of prostaglandin H synthase 1 and 2 by arachidonic acid. J. Biol. Chem., 272, 12393 12398.
39. Teather, L.A., Packard, M.G. Bazan, N.G. (2002) Post-training cyclooxygenase-2 (COX-2) inhibition impairs memory consolidation. Learn Mem., 9, 41 47.
40. Teng, X.W., Abu-Mellal, A.K. Davies, N.M. (2003) Formulation dependent pharmacokinetics, bioavailability and renal toxicity of a selective cyclooxygenase-1 inhibitor SC-560 in the rat. J. Pharm. Pharm. Sci., 6, 205 210.
41. Vane, J.R., Bakhle, Y.S. Botting, R.M. (1998) Cyclooxygenase 1 and 2. Annu. Rev. Pharmacol. Toxicol., 38, 97 120.
42. Warner, T.D., Giuliano, F., Vojnovic, I., Bukasa, A., Mitchell, J.A. Vane, J.R. (1999) Nonsteroid drug selectivities for cyclo-oxygenase-1 rather than cyclo-oxygenase-2 are associated with human gastrointestinal toxicity: a full in vitro analysis. Proc. Natl Acad. Sci. U.S.A., 96, 7563 7568.
43. Williams, J.H., Errington, M.L., Lynch, M.A. Bliss, T.V. (1989) Arachidonic acid induces a long-term activity-dependent enhancement of synaptic transmission in the hippocampus. Nature, 341, 739 742.
44. Xia, Z., Dudek, H., Miranti, C.K. Greenberg, M.E. (1996) Calcium influx via the NMDA receptor induces immediate early gene transcription by a MAP kinase/ERK-dependent mechanism. J. Neurosci., 16, 5425 5436.
45. Xie, W.L., Chipman, J.G., Robertson, D.L., Erikson, R.L. Simmons, D.L. (1991) Expression of a mitogen-responsive gene encoding prostaglandin synthase is regulated by mRNA splicing. Proc. Natl Acad. Sci. U.S.A., 88, 2692 2696.
46. Yamagata, K., Andreasson, K.I., Kaufmann, W.E., Barnes, C.A. Worley, P.F. (1993) Expression of a mitogen-inducible cyclooxygenase in brain neurons: regulation by synaptic activity and glucocorticoids. Neuron, 11, 371 386.
47. Zhang, J., Goorha, S., Raghow, R. Ballou, L.R. (2002) The tissue-specific, compensatory expression of cyclooxygenase-1 and -2 in transgenic mice. Prostaglandins Other Lipid mediat., 67, 121 135.