Altered mRNA editing and expression of ionotropic glutamate receptors after Kainic Acid exposure in cyclooxygenase-2 deficient mice

PLoS ONE

Volumn 6, Issue 5, 2011, Pages

  Caracciolo, Luca ^a,b   Barbon, Alessandro ^b   Palumbo, Sara ^a   Mora, Cristina ^b   Toscano, Christopher D ^a   Bosetti, Francesca ^a,c   Barlati, Sergio ^b  

^a NATIONAL INSTITUTE ON AGING   (United States)

^b UNIVERSITY OF BRESCIA   (Italy)

^c NATIONAL INSTITUTE OF NEUROLOGICAL DISORDERS AND STROKE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD11B ANTIGEN; CELECOXIB; CYCLOOXYGENASE 2; GLIAL FIBRILLARY ACIDIC PROTEIN; GLUTAMATE RECEPTOR; GLUTAMATE RECEPTOR 2; GLUTAMATE RECEPTOR 3; GLUTAMATE RECEPTOR 4; GLUTAMATE RECEPTOR 6; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 1BETA; INTERLEUKIN 6; IONOTROPIC RECEPTOR; KAINIC ACID; MESSENGER RNA; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; CONTROLLED STUDY; CYTOKINE PRODUCTION; GENE DELETION; GENE EXPRESSION REGULATION; HIPPOCAMPUS; INFLAMMATION; LONG TERM EXPOSURE; MALE; MOUSE; NERVE EXCITABILITY; NONHUMAN; OXIDATIVE STRESS; PROTEIN EXPRESSION; PROTEIN FUNCTION; RNA EDITING; ANIMAL; C57BL MOUSE; GENETICS;

MUS;

ANIMALS; CYCLOOXYGENASE 2; KAINIC ACID; MALE; MICE; MICE, INBRED C57BL; RECEPTORS, IONOTROPIC GLUTAMATE; RNA EDITING; RNA, MESSENGER;

EID: 79955934440     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0019398     Document Type: Article

References (66)

1. Minghetti L, (2007) Role of COX-2 in inflammatory and degenerative brain diseases. Subcell Biochem 42: 127-141.
2. 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.
3. Katori M, Majima M, (2000) Cyclooxygenase-2: its rich diversity of roles and possible application of its selective inhibitors. Inflamm Res 49: 367-392.
4. Kaufmann WE, Andreasson KI, Isakson PC, Worley PF, (1997) Cyclooxygenases and the central nervous system. Prostaglandins 54: 601-624.
5. Breder CD, Dewitt D, Kraig RP, (1995) Characterization of inducible cyclooxygenase in rat brain. J Comp Neurol 355: 296-315.
6. Toscano CD, Ueda Y, Tomita YA, Vicini S, Bosetti F, (2008) Altered GABAergic neurotransmission is associated with increased kainate-induced seizure in prostaglandin-endoperoxide synthase-2 deficient mice. Brain Res Bull 75: 598-609.
7. Bleakman D, Lodge D, (1998) Neuropharmacology of AMPA and kainate receptors. Neuropharmacology 37: 1187-1204.
8. Borbely S, Dobo E, Czege D, Molnar E, Bakos M, et al. (2009) Modification of ionotropic glutamate receptor-mediated processes in the rat hippocampus following repeated, brief seizures. Neuroscience 159: 358-368.
9. Fujikawa DG, (2005) Prolonged seizures and cellular injury: understanding the connection. Epilepsy Behav 7 (Suppl 3): S3-11.
10. Hou ST, MacManus JP, (2002) Molecular mechanisms of cerebral ischemia-induced neuronal death. Int Rev Cytol 221: 93-148.
11. Molinuevo JL, Llado A, Rami L, (2005) Memantine: targeting glutamate excitotoxicity in Alzheimer's disease and other dementias. Am J Alzheimers Dis Other Demen 20: 77-85.
12. Rapoport SI, Bosetti F, (2002) Do lithium and anticonvulsants target the brain arachidonic acid cascade in bipolar disorder? Arch Gen Psychiatry 59: 592-596.
13. Rothstein JD, (1995) Excitotoxicity and neurodegeneration in amyotrophic lateral sclerosis. Clin Neurosci 3: 348-359.
14. Wang Q, Yu S, Simonyi A, Sun GY, Sun AY, (2005) Kainic acid-mediated excitotoxicity as a model for neurodegeneration. Mol Neurobiol 31: 3-16.
15. Zeron MM, Hansson O, Chen N, Wellington CL, Leavitt BR, et al. (2002) Increased sensitivity to N-methyl-D-aspartate receptor-mediated excitotoxicity in a mouse model of Huntington's disease. Neuron 33: 849-860.
16. Sun AY, Cheng Y, Sun GY, (1992) Kainic acid-induced excitotoxicity in neurons and glial cells. Prog Brain Res 94: 271-280.
17. Cheng Y, Sun AY, (1994) Oxidative mechanisms involved in kainate-induced cytotoxicity in cortical neurons. Neurochem Res 19: 1557-1564.
18. Gluck MR, Jayatilleke E, Shaw S, Rowan AJ, Haroutunian V, (2000) CNS oxidative stress associated with the kainic acid rodent model of experimental epilepsy. Epilepsy Res 39: 63-71.
19. Milatovic D, Gupta RC, Dettbarn WD, (2002) Involvement of nitric oxide in kainic acid-induced excitotoxicity in rat brain. Brain Res 957: 330-337.
20. Candelario-Jalil E, Al-Dalain SM, Castillo R, Martinez G, Fernandez OS, (2001) Selective vulnerability to kainate-induced oxidative damage in different rat brain regions. J Appl Toxicol 21: 403-407.
21. Sun AY, Chen YM, (1998) Oxidative stress and neurodegenerative disorders. J Biomed Sci 5: 401-414.
22. Dingledine R, Borges K, Bowie D, Traynelis SF, (1999) The glutamate receptor ion channels. Pharmacol Rev 51: 7-61.
23. Seeburg PH, (2002) A-to-I editing: new and old sites, functions and speculations. Neuron 35: 17-20.
24. Lomeli H, Mosbacher J, Melcher T, Hoger T, Geiger JR, et al. (1994) Control of kinetic properties of AMPA receptor channels by nuclear RNA editing. Science 266: 1709-1713.
25. Kohler M, Burnashev N, Sakmann B, Seeburg PH, (1993) Determinants of Ca2+ permeability in both TM1 and TM2 of high affinity kainate receptor channels: diversity by RNA editing. Neuron 10: 491-500.
26. Egebjerg J, Heinemann SF, (1993) Ca2+ permeability of unedited and edited versions of the kainate selective glutamate receptor GluR6. Proc Natl Acad Sci U S A 90: 755-759.
27. Swanson GT, Feldmeyer D, Kaneda M, Cull-Candy SG, (1996) Effect of RNA editing and subunit co-assembly single-channel properties of recombinant kainate receptors. J Physiol 492 (Pt 1): 129-142.
28. Greger IH, Khatri L, Ziff EB, (2002) RNA editing at arg607 controls AMPA receptor exit from the endoplasmic reticulum. Neuron 34: 759-772.
29. Greger IH, Khatri L, Kong X, Ziff EB, (2003) AMPA receptor tetramerization is mediated by Q/R editing. Neuron 40: 763-774.
30. Krampfl K, Schlesinger F, Zorner A, Kappler M, Dengler R, et al. (2002) Control of kinetic properties of GluR2 flop AMPA-type channels: impact of R/G nuclear editing. Eur J Neurosci 15: 51-62.
31. Bernard A, Khrestchatisky M, (1994) Assessing the extent of RNA editing in the TMII regions of GluR5 and GluR6 kainate receptors during rat brain development. J Neurochem 62: 2057-2060.
32. Bernard A, Ferhat L, Dessi F, Charton G, Represa A, et al. (1999) Q/R editing of the rat GluR5 and GluR6 kainate receptors in vivo and in vitro: evidence for independent developmental, pathological and cellular regulation. Eur J Neurosci 11: 604-616.
33. Barbon A, Vallini I, La Via L, Marchina E, Barlati S, (2003) Glutamate receptor RNA editing: a molecular analysis of GluR2, GluR5 and GluR6 in human brain tissues and in NT2 cells following in vitro neural differentiation. Brain Res Mol Brain Res 117: 168-178.
34. Ozawa S, Kamiya H, Tsuzuki K, (1998) Glutamate receptors in the mammalian central nervous system. Prog Neurobiol 54: 581-618.
35. Doble A, (1999) The role of excitotoxicity in neurodegenerative disease: implications for therapy. Pharmacol Ther 81: 163-221.
36. Meldrum BS, (2000) Glutamate as a neurotransmitter in the brain: review of physiology and pathology. J Nutr 130: 1007S-1015S.
37. Langenbach R, Morham SG, Tiano HF, Loftin CD, Ghanayem BI, et al. (1995) Prostaglandin synthase 1 gene disruption in mice reduces arachidonic acid-induced inflammation and indomethacin-induced gastric ulceration. Cell 83: 483-492.
38. Morham SG, Langenbach R, Loftin CD, Tiano HF, Vouloumanos N, et al. (1995) Prostaglandin synthase 2 gene disruption causes severe renal pathology in the mouse. Cell 83: 473-482.
39. Barbon A, Fumagalli F, La Via L, Caracciolo L, Racagni G, et al. (2007) Chronic phencyclidine administration reduces the expression and editing of specific glutamate receptors in rat prefrontal cortex. Exp Neurol 208: 54-62.
40. Livak KJ, Schmittgen TD, (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25: 402-408.
41. Toscano CD, Prabhu VV, Langenbach R, Becker KG, Bosetti F, (2007) Differential gene expression patterns in cyclooxygenase-1 and cyclooxygenase-2 deficient mouse brain. Genome Biol 8: R14.
42. Aid S, Langenbach R, Bosetti F, (2008) Neuroinflammatory response to lipopolysaccharide is exacerbated in mice genetically deficient in cyclooxygenase-2. J Neuroinflammation 5: 17.
43. Barbon A, Fumagalli F, Caracciolo L, Madaschi L, Lesma E, et al. (2010) Acute spinal cord injury persistently reduces R/G RNA editing of AMPA receptors. J Neurochem 114: 397-407.
44. Marsicano G, Goodenough S, Monory K, Hermann H, Eder M, et al. (2003) CB1 cannabinoid receptors and on-demand defense against excitotoxicity. Science 302: 84-88.
45. Ishii T, Moriyoshi K, Sugihara H, Sakurada K, Kadotani H, et al. (1993) Molecular characterization of the family of the N-methyl-D-aspartate receptor subunits. J Biol Chem 268: 2836-2843.
46. Rumbaugh G, Vicini S, (1999) Distinct synaptic and extrasynaptic NMDA receptors in developing cerebellar granule neurons. J Neurosci 19: 10603-10610.
47. 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.
48. Gascon S, Sobrado M, Roda JM, Rodriguez-Pena A, Diaz-Guerra M, (2008) Excitotoxicity and focal cerebral ischemia induce truncation of the NR2A and NR2B subunits of the NMDA receptor and cleavage of the scaffolding protein PSD-95. Mol Psychiatry 13: 99-114.
49. Gascon S, Deogracias R, Sobrado M, Roda JM, Renart J, et al. (2005) Transcription of the NR1 subunit of the N-methyl-D-aspartate receptor is down-regulated by excitotoxic stimulation and cerebral ischemia. J Biol Chem 280: 35018-35027.
50. Grooms SY, Opitz T, Bennett MV, Zukin RS, (2000) Status epilepticus decreases glutamate receptor 2 mRNA and protein expression in hippocampal pyramidal cells before neuronal death. Proc Natl Acad Sci U S A 97: 3631-3636.
51. Ohno K, Okada M, Tsutsumi R, Kohara A, Yamaguchi T, (1997) Kainate excitotoxicity is mediated by AMPA- but not kainate-preferring receptors in embryonic rat hippocampal cultures. Neurochem Int 31: 715-722.
52. Choi DW, (1988) Calcium-mediated neurotoxicity: relationship to specific channel types and role in ischemic damage. Trends Neurosci 11: 465-469.
53. Choi DW, (1988) Glutamate neurotoxicity and diseases of the nervous system. Neuron 1: 623-634.
54. Weiss JH, Choi DW, (1991) Differential vulnerability to excitatory amino acid-induced toxicity and selective neuronal loss in neurodegenerative diseases. Can J Neurol Sci 18: 394-397.
55. Beal MF, (1994) Huntington's disease, energy, and excitotoxicity. Neurobiol Aging 15: 275-276.
56. Choi DW, (1989) Non-NMDA receptor-mediated neuronal injury in Alzheimer's disease? Neurobiol Aging 10: 605-606; discussion 618-620.
57. Greenamyre JT, Young AB, (1989) Excitatory amino acids and Alzheimer's disease. Neurobiol Aging 10: 593-602.
58. Korczak B, Nutt SL, Fletcher EJ, Hoo KH, Elliott CE, et al. (1995) cDNA cloning and functional properties of human glutamate receptor EAA3 (GluR5) in homomeric and heteromeric configuration. Receptors Channels 3: 41-49.
59. Grigorenko EV, Bell WL, Glazier S, Pons T, Deadwyler S, (1998) Editing status at the Q/R site of the GluR2 and GluR6 glutamate receptor subunits in the surgically excised hippocampus of patients with refractory epilepsy. Neuroreport 9: 2219-2224.
60. Kortenbruck G, Berger E, Speckmann EJ, Musshoff U, (2001) RNA editing at the Q/R site for the glutamate receptor subunits GLUR2, GLUR5, and GLUR6 in hippocampus and temporal cortex from epileptic patients. Neurobiol Dis 8: 459-468.
61. Vollmar W, Gloger J, Berger E, Kortenbruck G, Kohling R, et al. (2004) RNA editing (R/G site) and flip-flop splicing of the AMPA receptor subunit GluR2 in nervous tissue of epilepsy patients. Neurobiol Dis 15: 371-379.
62. Kawahara Y, Ito K, Sun H, Aizawa H, Kanazawa I, et al. (2004) Glutamate receptors: RNA editing and death of motor neurons. Nature 427: 801.
63. Kwak S, Kawahara Y, (2005) Deficient RNA editing of GluR2 and neuronal death in amyotropic lateral sclerosis. J Mol Med 83: 110-120.
64. Maas S, Patt S, Schrey M, Rich A, (2001) Underediting of glutamate receptor GluR-B mRNA in malignant gliomas. Proc Natl Acad Sci U S A 98: 14687-14692.
65. Harada A, Teng J, Takei Y, Oguchi K, Hirokawa N, (2002) MAP2 is required for dendrite elongation, PKA anchoring in dendrites, and proper PKA signal transduction. J Cell Biol 158: 541-549.
66. Pereno GL, Beltramino CA, (2010) Timed changes of synaptic zinc, synaptophysin and MAP2 in medial extended amygdala of epileptic animals are suggestive of reactive neuroplasticity. Brain Res 1328: 130-138.