Knockdown of AMPA receptor GluR2 expression causes delayed neurodegeneration and increases damage by sublethal ischemia in hippocampal CA1 and CA3 neurons

Journal of Neuroscience

Volumn 19, Issue 21, 1999, Pages 9218-9227

  Oguro, Keiji ^a   Oguro, Noriko ^a   Kojima, Takashi ^a   Grooms, Sonja Y ^a   Calderone, Agata ^a   Zheng, Xin ^a   Bennett, Michael V L ^a   Zukin, R Suzanne ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

AMPA receptors; Antisense oligonucleotides; Cerebral ischemia; Excitotoxicity; Gene expression; Hippocampus; Neurodegeneration; Status epilepticus

Indexed keywords

AMPA RECEPTOR; ANTISENSE OLIGONUCLEOTIDE;

ACTION POTENTIAL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN ISCHEMIA; CALCIUM CELL LEVEL; CELL DEATH; CONTROLLED STUDY; EPILEPTIC STATE; GENE EXPRESSION REGULATION; MEDIATOR RELEASE; NERVE DEGENERATION; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; RECEPTOR DOWN REGULATION;

EID: 0033232945     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.19-21-09218.1999     Document Type: Article

References (52)

1. Agrawal S (1996) Antisense oligonucleotides: towards clinical trials. Trends Biotechnol 14:376-387.
2. Ben-Ari Y (1985) Limbic seizure and brain damage produced by kainic acid: mechanisms and relevance to human temporal lobe epilepsy. Neuroscience 14:375-403.
3. Bennett MV, Pellegrini-Giampietro DE, Gorter JA, Aronica E, Connor JA, Zukin RS (1996) The GluR2 hypothesis: Ca(++)-permeable AMPA receptors in delayed neurodegeneration. Cold Spring Harb Symp Quant Biol 61:373-384.
4. Bochet P, Audinat E, Lambolez B, Crepel F, Rossier J, Iino M, Tsuzuki K, Ozawa S (1994) Subunit composition at the single-cell level explains functional properties of a glutamate-gated channel. Neuron 12:383-388.
5. Bowie D, Mayer ML (1995) Inward rectification of both AMPA and kainate subtype glutamate receptors generated by polyamine-mediated ion channel block. Neuron 15:453-462.
6. Brusa R, Zimmermann F, Koh DS, Feldmeyer D, Gass P, Seeburg PH, Sprengel R (1995) Early-onset epilepsy and postnatal lethality associated with an editing-deficient GluR-B allele in mice. Science 270:1677-1680.
7. Burnashev N, Monyer H, Seeburg PH, Sakmann B (1992) Divalent ion permeability of AMPA receptor channels is dominated by the edited form of a single subunit. Neuron 8:189-198.
8. Campbell JM, Bacon TA, Wickstrom E (1990) Oligodeoxynucleoside phosphorothioate stability in subcellular extracts, culture media, sera and cerebrospinal fluid. J Biochem Biophys Methods 20:259-267.
9. Chen J, Nagayama T, Jin K, Stetler RA, Zhu RL, Graham SH, Simon RP (1998) Induction of caspase-3-like protease may mediate delayed neuronal death in the hippocampus after transient cerebral ischemia. J Neurosci 18:4914-4928.
10. Choi DW (1995) Calcium: still center-stage in hypoxic-ischemic neuronal death. Trends Neurosci 18:58-60.
11. Colbourne F, Sutherland GR, Auer RN (1999) Electron microscopic evidence against apoptosis as the mechanism of neuronal death in global ischemia. J Neurosci 19:4200-4210.
12. Feldmeyer D, Kask K, Brusa R, Kornau HC, Kolhekar R, Rozov A, Burnashev N, Jensen V, Hvalby O, Sprengel R, Seeburg PH (1999) Neurological dysfunctions in mice expressing different levels of the Q/R site-unedited AMPAR subunit GluR-B. Nat Neurosci 2:57-64.
13. Freund TF, Buzsaki G, Leon A, Baimbridge KG, Somogyi P (1990) Relationship of neuronal vulnerability and calcium binding protein immunoreactivity in ischemia. Exp Brain Res 83:55-66.
14. Friedman LK, Pellegrini-Giampietro DE, Sperber EF, Bennett MV, Moshe SL, Zukin RS (1994) Kainate-induced status epilepticus alters glutamate and GABAA receptor gene expression in adult rat hippocampus: an in situ hybridization study. J Neurosci 14:2697-2707.
15. Friedman LK, Sperber EF, Moshe SL, Bennett MV, Zukin RS (1997) Developmental regulation of glutamate and GABA(A) receptor gene expression in rat hippocampus following kainate-induced status epilepticus. Dev Neurosci 19:529-542.
16. Geiger JR, Melcher T, Koh DS, Sakmann B, Seeburg PH, Jonas P, Monyer H (1995) Relative abundance of subunit mRNAs determines gating and Ca2+ permeability of AMPA receptors in principal neurons and interneurons in rat CNS. Neuron 15:193-204.
17. Gorter JA, Petrozzino JJ, Aronica EM, Rosenbaum DM, Opitz T, Bennett MV, Connor JA, Zukin RS (1997) Global ischemia induces downregulation of GluR2 mRNA and increases AMPA receptor-mediated Ca2+ influx in hippocampal CA1 neurons of gerbil. J Neurosci 17:6179-6188.
18. Gyurko R, Tran D, Phillips MI (1997) Time course of inhibition of hypertension by antisense oligonucleotides targeted to AT1 angiotensin receptor mRNA in spontaneously hypertensive rats. Am J Hypertens 10:56S-62S.
19. Heurteaux C, Lauritzen I, Widmann C, Lazdunski M (1995) Essential role of adenosine, adenosine A1 receptors, and ATP-sensitive K+ channels in cerebral ischemic preconditioning. Proc Natl Acad Sci USA 92:4666-4670.
20. Hollmann M, Hartley M, Heinemann S (1991) Ca2+ permeability of KA-AMPA-gated glutamate receptor channels depends on subunit composition. Science 252:851-853.
21. Hsu M, Buzsaki G (1993) Vulnerability of mossy fiber targets in the rat hippocampus to forebrain ischemia. J Neurosci 13:3964-3979.
22. Jia Z, Agopyan N, Miu P, Xiong Z, Henderson J, Gerlai R, Taverna FA, Velumian A, MacDonald J, Carlen P, Abramow-Newerly W, Roder J (1996) Enhanced LTP in mice deficient in the AMPA receptor GluR2. Neuron 17:945-956.
23. Jonas P, Racca C, Sakmann B, Seeburg PH, Monyer H (1994) Differences in Ca2+ permeability of AMPA-type glutamate receptor channels in neocortical neurons caused by differential GluR-B subunit expression. Neuron 12:1281-1289.
24. Kirino T (1982) Delayed neuronal death in the gerbil hippocampus following ischemia. Brain Res 239:57-69.
25. Koh JY, Suh SW, Gwag BJ, He YY, Hsu CY, Choi DW (1996) The role of zinc in selective neuronal death after transient global cerebral ischemia. Science 272:1013-1016.
26. Koike M, Iino M, Ozawa S (1997) Blocking effect of 1-naphthyl acetyl spermine on Ca(2+)-permeable AMPA receptors in cultured rat hippocampal neurons. Neurosci Res 29:27-36.
27. Nadler JV (1981) Minireview. Kainic acid as a tool for the study of temporal lobe epilepsy. Life Sci 29:2031-2042.
28. Nurse S, Corbett D (1996) Neuroprotection after several days of mild, drug-induced hypothermia. J Cereb Blood Flow Metab 16:474-480.
29. Oguro K, Nakamura M, Masuzawa T (1995) Histochemical study of Ca(2+)-ATPase activity in ischemic CA1 pyramidal neurons in the gerbil hippocampus. Acta Neuropathol (Berl) 90:448-453.
30. Pellegrini-Giampietro DE, Zukin RS, Bennett MV, Cho S, Pulsinelli WA (1992a) Switch in glutamate receptor subunit gene expression in CA1 subfield of hippocampus following global ischemia in rats. Proc Natl Acad Sci USA [Erratum (1993) 90:780] 89:10499-10503.
31. Pellegrini-Giampietro DE, Bennett MV, Zukin RS (1992b) Are Ca(2+)-permeable kainate/AMPA receptors more abundant in immature brain? Neurosci Lett 144:65-69.
32. Pellegrini-Giampietro DE, Gorter JA, Bennett MV, Zukin RS (1997) The GluR2 (GluR-B) hypothesis: Ca(2+)-permeable AMPA receptors in neurological disorders. Trends Neurosci 20:464-470.
33. Pulsinelli W, Sarokin A, Buchan A (1993) Antagonism of the NMDA and non-NMDA receptors in global versus focal brain ischemia. Prog Brain Res 96:125-135.
34. Pulsinelli WA, Brierley JB, Plum F (1982) Temporal profile of neuronal damage in a model of transient forebrain ischemia. Ann Neurol 11:491-498.
35. Schmidt-Kastner R, Freund TF (1991) Selective vulnerability of the hippocampus in brain ischemia. Neuroscience 40:599-636.
36. Sheardown MJ, Suzdak PD, Nordholm L (1993) AMPA, but not NMDA, receptor antagonism is neuroprotective in gerbil global ischaemia, even when delayed 24 h. Eur J Pharmacol 236:347-353.
37. Sheng M, Pak DT (1999) Glutamate receptor anchoring proteins and the molecular organization of excitatory synapses. Ann NY Acad Sci 868:483-493.
38. 2+] and [H+] in the hippocampus during recovery from short-term, transient ischemia. J Cereb Blood Flow Metab 12:759-772.
39. Song I, Kamboj S, Xia J, Dong H, Liao D, Huganir RL (1998) Interaction of the N-ethylmaleimide-sensitive factor with AMPA receptors. Neuron 21:393-400.
40. Takei N, Endo Y (1994) Ca2+ ionophore-induced apoptosis on cultured embryonic rat cortical neurons. Brain Res 652:65-70.
41. Tsubokawa H, Oguro K, Masuzawa T, Kawai N (1994) Ca(2+)-dependent non-NMDA receptor-mediated synaptic currents in ischemic CA1 hippocampal neurons. J Neurophysiol 71:1190-1196.
42. Tsubokawa H, Oguro K, Masuzawa T, Nakaima T, Kawai N (1995) Effects of a spider toxin and its analogue on glutamate-activated currents in the hippocampal CA1 neuron after ischemia. J Neurophysiol 74:218-225.
43. Tsuda M, Imaizumi K, Katayama T, Kitagawa K, Wanaka A, Tohyama M, Takagi T (1997) Expression of zinc transporter gene, ZnT-1, is induced after transient forebrain ischemia in the gerbil. J Neurosci 17:6678-6684.
44. Verdoorn TA, Burnashev N, Monyer H, Seeburg PH, Sakmann B (1991) Structural determinants of ion flow through recombinant glutamate receptor channels. Science 252:1715-1718.
45. Vissavajjhala P, Janssen WG, Hu Y, Gazzaley AH, Moran T, Hof PR, Morrison JH (1996) Synaptic distribution of the AMPA-GluR2 subunit and its colocalization with calcium-binding proteins in rat cerebral cortex: an immunohistochemical study using a GluR2-specific monoclonal antibody. Exp Neurol 142:296-312.
46. Wahlestedt C (1994) Antisense oligonucleotide strategies in neuropharmacology. Trends Pharmacol Sci 15:42-46.
47. Wahlestedt C, Golanov E, Yamamoto S, Yee F, Ericson H, Yoo H, Inturrisi CE, Reis DJ (1993) Antisense oligodeoxynucleotides to NMDA-R1 receptor channel protect cortical neurons from excitotoxicity and reduce focal ischaemic infarctions. Nature 363:260-263.
48. Washburn MS, Numberger M, Zhang S, Dingledine R (1997) Differential dependence on GluR2 expression of three characteristic features of AMPA receptors. J Neurosci 17:9393-9406.
49. Weiss B, Zhou LW, Zhang SP, Qin ZH (1993) Antisense oligode-oxynucleotide inhibits D2 dopamine receptor-mediated behavior and D2 messenger RNA. Neuroscience 55:607-612.
50. Weiss B, Davidkova G, Zhang SP (1997) Antisense strategies in neuro-biology. Neurochem Int 31:321-348.
51. Wenthold RJ, Yokotani N, Doi K, Wada K (1992) Immunochemical characterization of the non-NMDA glutamate receptor using subunit-specific antibodies. Evidence for a hetero-oligomeric structure in rat brain. J Biol Chem 267:501-507.
52. Yaida Y, Nowak Jr TS (1995) Distribution of phosphodiester and phosphorothioate oligonucleotides in rat brain after intraventricular and intrahippocampal administration determined by in situ hybridization. Regul Pept 59:193-199.