Synaptic and extrasynaptic nmda receptors differentially modulate neuronal cyclooxygenase-2 function, lipid peroxidation, and neuroprotection

Journal of Neuroscience

Volumn 31, Issue 39, 2011, Pages 13710-13721

  Stark, David T ^a   Bazan, Nicolas G ^a  

^a LOUISIANA STATE UNIVERSITY HEALTH SCIENCES CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARACHIDONIC ACID; CYCLOOXYGENASE 2; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; PHOSPHOLIPASE A2; PHOSPHOLIPID;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; CONTROLLED STUDY; ELECTROSPRAY MASS SPECTROMETRY; ENZYME REGULATION; ENZYME SUBSTRATE; EXCITOTOXICITY; FEMALE; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HYDROLYSIS; IMAGE ANALYSIS; LIPID PEROXIDATION; LIPIDOMICS; MALE; MOUSE; NERVE CELL CULTURE; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; SYNAPTIC TRANSMISSION;

ANIMALS; ANIMALS, NEWBORN; CELLS, CULTURED; CYCLOOXYGENASE 2; FEMALE; LIPID PEROXIDATION; MALE; MICE; MICE, INBRED C57BL; NEURONS; NEUROPROTECTIVE AGENTS; ORGAN CULTURE TECHNIQUES; RECEPTORS, N-METHYL-D-ASPARTATE; SYNAPSES;

EID: 80053254091     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3544-11.2011     Document Type: Article

References (68)

1. Akaneya Y, Tsumoto T (2006) Bidirectional trafficking of prostaglandin E2 receptors involved in long-term potentiation in visual cortex. J Neurosci 26:10209-10221
2. Arnold FJ, Hofmann F, Bengtson CP, Wittmann M, Vanhoutte P, Bading H (2005) Microelectrode array recordings of cultured hippocampal networks reveal a simple model for transcription and protein synthesisdependent plasticity. J Physiol 564:3-19
3. Bazan NG (2003) Synaptic lipid signaling: significance of polyunsaturated fatty acids and platelet-activating factor. J Lipid Res 44:2221-2233
4. Bazan NG (2006) Cell survival matters: docosahexaenoic acid signaling, neuroprotection and photoreceptors. Trends Neurosci 29:263-271
5. Beart PM, O'Shea RD (2007) Transporters for L-glutamate: an update on their molecular pharmacology and pathological involvement. Br J Pharmacol 150:5-17
6. Bengtson CP, Dick O, Bading H (2008) A quantitative method to assess extrasynapticNMDAreceptor function in the protective effect of synaptic activity against neurotoxicity. BMC Neurosci 9:11.
7. Block ML, Zecca L, Hong JS (2007) Microglia-mediated neurotoxicity: uncovering the molecular mechanisms. Nat Rev Neurosci 8:57-69
8. Carlson NG (2003) Neuroprotection of cultured cortical neurons mediated by the cyclooxygenase-2 inhibitor APHS can be reversed by a prostanoid. J Neurosci Res 71:79-88
9. Chen C, Bazan NG (2005) Endogenous PGE2 regulates membrane excitability and synaptic transmission in hippocampal CA1 pyramidal neurons. J Neurophysiol 93:929-941
10. Chen C, Magee JC, Bazan NG (2002) Cyclooxygenase-2 regulates prostaglandin E2 signaling in hippocampal long-term synaptic plasticity. J Neurophysiol 87:2851-2857
11. Dumuis A, Sebben M, Haynes L, Pin JP, Bockaert J (1988) NMDAreceptors activate the arachidonic acid cascade system in striatal neurons. Nature 336:68-70
12. Gendron TF, Brunette E, Mealing GA, Nguyen A, Tauskela JS, Morley P (2004) Opposing effects of cyclooxygenase-2 selective inhibitors on oxygen-glucose deprivation-induced neurotoxicity. Eur J Pharmacol 493:45-55
13. Gordon GR, Choi HB, Rungta RL, Ellis-Davies GC, MacVicar BA (2008) Brain metabolism dictates the polarity of astrocyte control over arterioles. Nature 456:745-749
14. Groeger AL, Cipollina C, Cole MP, Woodcock SR, Bonacci G, Rudolph TK, Rudolph V, Freeman BA, Schopfer FJ (2010) Cyclooxygenase-2 generates anti-inflammatory mediators from omega-3 fatty acids. Nat Chem Biol 6:433-441
15. Hardingham GE, Bading H (2010) Synaptic versus extrasynaptic NMDA receptor signalling: implications for neurodegenerative disorders. Nat Rev Neurosci 11:682-696
16. Hardingham GE, Fukunaga Y, Bading H (2002) Extrasynaptic NMDARs oppose synaptic NMDARs by triggering CREB shut-off and cell death pathways. Nat Neurosci 5:405-414
17. Hewett SJ, Uliasz TF, Vidwans AS, Hewett JA (2000) Cyclooxygenase-2 contributes to N-methyl-D-aspartate-mediated neuronal cell death in primary cortical cell culture. J Pharmacol Exp Ther 293:417-425
18. Hunot S, Vila M, Teismann P, Davis RJ, Hirsch EC, Przedborski S, Rakic P, Flavell RA (2004) JNK-mediated induction of cyclooxygenase 2 is required for neurodegeneration in a mouse model of Parkinson's disease. Proc Natl Acad Sci U S A 101:665-670
19. Iadecola C, Niwa K, Nogawa S, Zhao X, Nagayama M, Araki E, Morham S, Ross ME (2001) Reduced susceptibility to ischemic brain injury and N-methylaspartate-mediated neurotoxicity in cyclooxygenase-2-deficient mice. Proc Natl Acad SciUS A98:1294-1299
20. Inoue H, Nanayama T, Hara S, Yokoyama C, Tanabe T (1994) The cyclic AMP response element plays an essential role in the expression of the human prostaglandin-endoperoxide synthase 2 gene in differentiated U937 monocytic cells. FEBS Lett 350:51-54
21. Kalgutkar AS, Crews BC, Rowlinson SW, Garner C, Seibert K, Marnett LJ (1998) Aspirin-like molecules that covalently inactivate cyclooxygenase-2. Science 280:1268-1270
22. Kaufmann WE, Worley PF, 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
23. Kawano T, Anrather J, Zhou P, Park L, Wang G, Frys KA, Kunz A, Cho S, Orio M, Iadecola C (2006) Prostaglandin E2 EP1 receptors: downstream effectors of COX-2 neurotoxicity. Nat Med 12:225-229
24. Keene CD, Chang RC, Lopez-Yglesias AH, Shalloway BR, Sokal I, Li X, Reed PJ, Keene LM, Montine KS, Breyer RM, Rockhill JK, Montine TJ (2010) Suppressed accumulation of cerebral amyloid beta peptides in aged transgenic Alzheimer's disease mice by transplantation with wild-type or prostaglandin E-2 receptor subtype 2-null bone marrow. Am J Pathol 177:346-354
25. Kim E, Raval AP, Defazio RA, Perez-Pinzon MA (2007) Ischemic preconditioning via epsilon protein kinase C activation requires cyclooxygenase-2 activation in vitro. Neuroscience 145:931-941
26. Koch H, Huh SE, Elsen FP, Carroll MS, Hodge RD, Bedogni F, Turner MS, Hevner RF, Ramirez JM (2010) Prostaglandin E2-induced synaptic plasticity in neocortical networks of organotypic slice cultures. J Neurosci 30:11678-11687
27. Kotilinek LA, Westerman MA, Wang Q, Panizzon K, Lim GP, Simonyi A, Lesne S, Falinska A, Younkin LH, Younkin SG, Rowan M, Cleary J, Wallis RA, Sun GY, Cole G, Frautschy S, Anwyl R, Ashe KH (2008) Cyclooxygenase-2 inhibition improves amyloid-beta-mediated suppression of memory and synaptic plasticity. Brain 131:651-664
28. Le TD, Shirai Y, Okamoto T, Tatsukawa T, Nagao S, Shimizu T, Ito M (2010) Lipid signaling in cytosolic phospholipase A2alpha-cyclooxygenase-2 cascade mediates cerebellar long-term depression and motor learning. Proc Natl Acad Sci U S A 107:3198-3203
29. Lee B, Dziema H, Lee KH, Choi YS, Obrietan K (2007) CRE-mediated transcription and COX-2 expression in the pilocarpine model of status epilepticus. Neurobiol Dis 25:80-91
30. Léveillé F, El GF, Gouix E, Lecocq M, Lobner D, Nicole O, Buisson A (2008) Neuronal viability is controlled by a functional relation between synaptic and extrasynaptic NMDA receptors. FASEB J 22:4258-4271
31. Léveillé F, Papadia S, Fricker M, Bell KF, Soriano FX, Martel MA, Puddifoot C, Habel M, Wyllie DJ, Ikonomidou C, Tolkovsky AM, Hardingham GE (2010) Suppression of the intrinsic apoptosis pathway by synaptic activity. J Neurosci 30:2623-2635
32. Liang X, Wang Q, Hand T, Wu L, Breyer RM, Montine TJ, Andreasson K (2005) Deletion of the prostaglandin E2 EP2 receptor reduces oxidative damage and amyloid burden in a model of Alzheimer's disease. J Neurosci 25:10180-10187
33. Manabe Y, Anrather J, Kawano T, Niwa K, Zhou P, Ross ME, Iadecola C (2004) Prostanoids, not reactive oxygen species, mediate COX-2-dependent neurotoxicity. Ann Neurol 55:668-675
34. Marcheselli VL, Hong S, Lukiw WJ, Tian XH, Gronert K, Musto A, Hardy M, Gimenez JM, Chiang N, Serhan CN, Bazan NG (2003) Novel docosanoids inhibit brain ischemia-reperfusion-mediated leukocyte infiltration and proinflammatory gene expression. J Biol Chem 278:43807-43817
35. Marszalek JR, Lodish HF (2005) Docosahexaenoic acid, fatty acidinteracting proteins, and neuronal function: breastmilk and fish are good for you. Annu Rev Cell Dev Biol 21:633-657
36. McCullough L, Wu L, Haughey N, Liang X, Hand T, Wang Q, Breyer RM, Andreasson K (2004) Neuroprotective function of the PGE2 EP2 receptor in cerebral ischemia. J Neurosci 24:257-268
37. Nakayama M, Uchimura K, Zhu RL, Nagayama T, Rose ME, Stetler RA, Isakson PC, Chen J, Graham SH (1998) Cyclooxygenase-2 inhibition prevents delayed death of CA1 hippocampal neurons following global ischemia. Proc Natl Acad Sci U S A 95:10954-10959
38. Niwa K, Araki E, Morham SG, Ross ME, Iadecola C (2000) Cyclooxygenase-2 contributes to functional hyperemia in whisker-barrel cortex. J Neurosci 20:763-770
39. Nogawa S, Zhang F, Ross ME, Iadecola C (1997) Cyclo-oxygenase-2 gene expression in neurons contributes to ischemic brain damage. J Neurosci 17:2746-2755
40. Okamoto S, Pouladi MA, Talantova M, Yao D, Xia P, Ehrnhoefer DE, Zaidi R, Clemente A, Kaul M, Graham RK, Zhang D, Vincent Chen HS, Tong G, Hayden MR, Lipton SA (2009) Balance between synaptic versus extrasynapticNMDAreceptor activity influences inclusions and neurotoxicity of mutant huntingtin. Nat Med 15:1407-1413
41. Okubo Y, IinoM (2011) Visualization of glutamate as a volume transmitter. J Physiol 589:481-488
42. Okubo Y, Sekiya H, Namiki S, Sakamoto H, Iinuma S, Yamasaki M, Watanabe M, Hirose K, Iino M (2010) Imaging extrasynaptic glutamate dynamics in the brain. Proc Natl Acad Sci U S A 107:6526-6531
43. Palop JJ, Chin J, Mucke L (2006) A network dysfunction perspective on neurodegenerative diseases. Nature 443:768-773
44. Palop JJ, Chin J, Roberson ED, Wang J, Thwin MT, Bien-Ly N, Yoo J, Ho KO, Yu GQ, Kreitzer A, Finkbeiner S, Noebels JL, Mucke L (2007) Aberrant excitatory neuronal activity and compensatory remodeling of inhibitory hippocampal circuits in mouse models of Alzheimer's disease. Neuron 55:697-711
45. 2+ and the cAMP response element-binding protein family mediate a late phase of activity-dependent neuroprotection. J Neurosci 25:4279-4287
46. Papadia S, Soriano FX, Léveillé F, Martel MA, Dakin KA, Hansen HH, Kaindl A, Sifringer M, Fowler J, Stefovska V, McKenzie G, Craigon M, Corriveau R, Ghazal P, Horsburgh K, Yankner BA, Wyllie DJ, Ikonomidou C, Hardingham GE (2008) Synaptic NMDA receptor activity boosts intrinsic antioxidant defenses. Nat Neurosci 11:476-487
47. Rossi DJ, Oshima T, Attwell D (2000) Glutamate release in severe brain ischaemia is mainly by reversed uptake. Nature 403:316-321
48. Sanchez-Mejia RO, Mucke L (2010) Phospholipase A2 and arachidonic acid in Alzheimer's disease. Biochim Biophys Acta 1801:784-790
49. Sang N, Zhang J, Marcheselli V, Bazan NG, Chen C (2005) Postsynaptically synthesized prostaglandin E2 (PGE2) modulates hippocampal synaptic transmission via a presynaptic PGE2 EP2 receptor. J Neurosci 25:9858-9870
50. Savonenko A, Munoz P, Melnikova T, Wang Q, Liang X, Breyer RM, Montine TJ, Kirkwood A, Andreasson K (2009) Impaired cognition, sensorimotor gating, and hippocampal long-term depression in mice lacking the prostaglandin E2 EP2 receptor. Exp Neurol 217:63-73
51. Serhan CN, Clish CB, Brannon J, Colgan SP, Chiang N, Gronert K (2000) Novel functional sets of lipid-derived mediators with antiinflammatory actions generated from omega-3 fatty acids via cyclooxygenase 2-nonsteroidal antiinflammatory drugs and transcellular processing. J Exp Med 192:1197-1204
52. Serhan CN, Hong S, Gronert K, Colgan SP, Devchand PR, Mirick G, Moussignac RL (2002) Resolvins: a family of bioactive products of omega-3 fatty acid transformation circuits initiated by aspirin treatment that counter proinflammation signals. J Exp Med 196:1025-1037
53. Serhan CN, Chiang N, Van Dyke TE (2008) Resolving inflammation: dual antiinflammatory and pro-resolution lipid mediators. Nat Rev Immunol 8:349-361
54. Smith WL, DeWitt DL, Garavito RM (2000) Cyclooxygenases: structural, cellular, and molecular biology. Annu Rev Biochem 69:145-182
55. Soriano FX, Papadia S, Hofmann F, Hardingham NR, Bading H, Hardingham GE (2006) Preconditioning doses of NMDA promote neuroprotection by enhancing neuronal excitability. J Neurosci 26:4509-4518
56. Stella N, Pellerin L, Magistretti PJ (1995) Modulation of the glutamate-evoked release of arachidonic acid from mouse cortical neurons: involvement of a pH-sensitive membrane phospholipase A2. J Neurosci 15:3307-3317
57. Tauskela JS, Fang H, Hewitt M, Brunette E, Ahuja T, Thivierge JP, Comas T, Mealing GA (2008) Elevated synaptic activity preconditions neurons against an in vitro model of ischemia. J Biol Chem 283:34667-34676
58. Taylor AL, Bonventre JV, Uliasz TF, Hewett JA, Hewett SJ (2008) Cytosolic phospholipase A2 alpha inhibition prevents neuronal NMDA receptorstimulated arachidonic acid mobilization and prostaglandin production but not subsequent cell death. J Neurochem 106:1828-1840
59. Tian J, Kim SF, Hester L, Snyder SH (2008) S-nitrosylation/activation of COX-2 mediates NMDA neurotoxicity. Proc Natl Acad Sci U S A 105:10537-10540
60. Tu B, Bazan NG (2003) Hippocampal kindling epileptogenesis upregulates neuronal cyclooxygenase-2 expression in neocortex. Exp Neurol 179:167-175
61. Wahl AS, Buchthal B, Rode F, Bomholt SF, Freitag HE, Hardingham GE, Rønn LC, Bading H (2009) Hypoxic/ischemic conditions induce expression of the putative pro-death gene Clca1 via activation of extrasynaptic N-methyl-D-aspartate receptors. Neuroscience 158:344-352
62. Watt AJ, van Rossum MC, MacLeod KM, Nelson SB, Turrigiano GG (2000) Activity coregulates quantal AMPA and NMDA currents at neocortical synapses. Neuron 26:659-670
63. Wittmann M, Queisser G, Eder A, Wiegert JS, Bengtson CP, Hellwig A, Wittum G, Bading H (2009) Synaptic activity induces dramatic changes in the geometry of the cell nucleus: interplay between nuclear structure, histone H3 phosphorylation, and nuclear calcium signaling. J Neurosci 29:14687-14700
64. Wu L, Wang Q, Liang X, Andreasson K (2007) Divergent effects of prostaglandin receptor signaling on neuronal survival. Neurosci Lett 421:253-258
65. Xia P, Chen HS, Zhang D, Lipton SA (2010) Memantine preferentially blocks extrasynaptic over synaptic NMDA receptor currents in hippocampal autapses. J Neurosci 30:11246-11250
66. Yamagata K, Andreasson KI, Kaufmann WE, Barnes CA, Worley PF (1993) Expression of a mitogen-inducible cyclooxygenase in brain neurons: regulation by synaptic activity and glucocorticoids. Neuron 11:371-386
67. Yang H, Zhang J, Breyer RM, Chen C (2009) Altered hippocampal longterm synaptic plasticity in mice deficient in the PGE2 EP2 receptor. J Neurochem 108:295-304
68. Zhang SJ, Steijaert MN, Lau D, Schütz G, Delucinge-Vivier C, Descombes P, Bading H (2007) Decoding NMDA receptor signaling: identification of genomic programs specifying neuronal survival and death. Neuron 53: 549-562.