Home LiteratureArticle Details
PMID: 11087875 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Remodeling of alpha-amino-3-hydroxy-5-methyl-4-isoxazole-propionic acid receptor subunit composition in hippocampal neurons after global ischemia.

Opitz T, Grooms SY, Bennett MV, Zukin RS, Optiz T

Abstract

Transient global ischemia induces selective delayed cell death, primarily of principal neurons in the hippocampal CA1. However, the molecular mechanisms underlying ischemia-induced cell death are as yet unclear. The present study shows that global ischemia triggers a pronounced and cell-specific reduction in GluR2 [the subunit that limits Ca(2+) permeability of alpha-amino-3-hydroxy-5-methyl-4-isoxazole-propionic acid (AMPA) receptors] in vulnerable CA1 neurons, as evidenced by immunofluorescence of brain sections and Western blot analysis of microdissected hippocampal subfields. At 72 h after ischemia (a time before cell death), virtually all CA1 pyramidal neurons exhibited greatly reduced GluR2 immunolabeling throughout their somata and dendritic processes. GluR2 immunolabeling was unchanged in pyramidal cells of the CA3 and granule cells of the dentate gyrus, regions resistant to ischemia-induced damage. Immunolabeling of the AMPA receptor subunit GluR1 was unchanged in CA1, CA3, and dentate gyrus. Western analysis indicated that GluR2 subunit abundance was markedly reduced in CA1 at 60 and 72 h after the ischemic insult; GluR1 abundance was unchanged in all subfields at all times examined. These findings, together with the previous observation of enhanced AMPA-elicited Ca(2+) influx in postischemic CA1 neurons, show that functional GluR2-lacking, Ca(2+)-permeable AMPA receptors are expressed in vulnerable neurons before cell death. Thus, the present study provides an important link in the postulated causal chain between global ischemia and delayed death of CA1 pyramidal neurons.

MeSH Terms
Animals Blotting, Western Dentate Gyrus/metabolism,pathology Gene Expression Regulation Gerbillinae Hippocampus/metabolism,pathology Immunohistochemistry Ischemic Attack, Transient/metabolism,pathology Male Neurons/metabolism,pathology Receptors, AMPA/analysis,genetics,metabolism Time Factors Transcription, Genetic
Chemicals
Receptors, AMPA glutamate receptor ionotropic, AMPA 2 glutamate receptor ionotropic, AMPA 1
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Opitz T
Otto-von-Guericke University, Institute for Physiology, Magdeburg, D-39120 Germany.
Grooms S Y
Bennett M V
Zukin R S
Optiz T
References (60)
60 references, click to expand
  1. Knockdown of AMPA receptor GluR2 expression causes delayed neurodegeneration and increases damage by sublethal ischemia in hippocampal CA1 and CA3 neurons.
    J Neurosci. 1999 Nov 1;19(21):9218-27 PMID: 10531425
  2. The pharmacology of AMPA receptors and their antagonists.
    Stroke. 1993 Dec;24(12 Suppl):I146-7; discussion I153-4 PMID: 7504337
  3. Driving AMPA receptors into synapses by LTP and CaMKII: requirement for GluR1 and PDZ domain interaction.
    Science. 2000 Mar 24;287(5461):2262-7 PMID: 10731148
  4. Status epilepticus decreases glutamate receptor 2 mRNA and protein expression in hippocampal pyramidal cells before neuronal death.
    Proc Natl Acad Sci U S A. 2000 Mar 28;97(7):3631-6 PMID: 10725374
  5. GluR2 protein synthesis and metabolism in rat hippocampus following transient ischemia and ischemic tolerance induction.
    Neurochem Int. 2000 Jul;37(1):7-15 PMID: 10781841
  6. Delayed neuronal death in the gerbil hippocampus following ischemia.
    Brain Res. 1982 May 6;239(1):57-69 PMID: 7093691
  7. Temporal profile of neuronal damage in a model of transient forebrain ischemia.
    Ann Neurol. 1982 May;11(5):491-8 PMID: 7103425
  8. Pentameric structure and subunit stoichiometry of a neuronal nicotinic acetylcholine receptor.
    Nature. 1991 Mar 21;350(6315):235-8 PMID: 2005979
  9. Ca2+ permeability of KA-AMPA--gated glutamate receptor channels depends on subunit composition.
    Science. 1991 May 10;252(5007):851-3 PMID: 1709304
  10. Differential expression of three glutamate receptor genes in developing rat brain: an in situ hybridization study.
    Proc Natl Acad Sci U S A. 1991 May 15;88(10):4157-61 PMID: 1851996
  11. Structural determinants of ion flow through recombinant glutamate receptor channels.
    Science. 1991 Jun 21;252(5013):1715-8 PMID: 1710829
  12. The characterization and localization of the glutamate receptor subunit GluR1 in the rat brain.
    J Neurosci. 1991 Sep;11(9):2713-24 PMID: 1652625
  13. Immunochemical characterization of the non-NMDA glutamate receptor using subunit-specific antibodies. Evidence for a hetero-oligomeric structure in rat brain.
    J Biol Chem. 1992 Jan 5;267(1):501-7 PMID: 1309749
  14. Biochemical characterization and localization of a non-N-methyl-D-aspartate glutamate receptor in rat brain.
    J Neurochem. 1992 Mar;58(3):1118-26 PMID: 1371146
  15. Assembly of the inhibitory glycine receptor: identification of amino acid sequence motifs governing subunit stoichiometry.
    Neuron. 1993 Dec;11(6):1049-56 PMID: 8274276
  16. Alterations of the GluR-B AMPA receptor subunit flip/flop expression in kainate-induced epilepsy and ischemia.
    Neuroscience. 1993 Dec;57(3):545-54 PMID: 8309523
  17. Subunit composition at the single-cell level explains functional properties of a glutamate-gated channel.
    Neuron. 1994 Feb;12(2):383-8 PMID: 7509161
  18. Kainate-induced status epilepticus alters glutamate and GABAA receptor gene expression in adult rat hippocampus: an in situ hybridization study.
    J Neurosci. 1994 May;14(5 Pt 1):2697-707 PMID: 8182436
  19. Differences in Ca2+ permeability of AMPA-type glutamate receptor channels in neocortical neurons caused by differential GluR-B subunit expression.
    Neuron. 1994 Jun;12(6):1281-9 PMID: 8011338
  20. The N-ethylmaleimide-sensitive fusion protein (NSF) is preferentially expressed in the nervous system.
    FEBS Lett. 1994 Jun 20;347(1):55-8 PMID: 8013662
  21. Association of N-ethylmaleimide-sensitive factor with synaptic vesicles.
    FEBS Lett. 1994 Aug 22;350(2-3):253-7 PMID: 8070574
  22. Down-regulation of AMPA receptor subunit GluR2 in amygdaloid kindling.
    J Neurochem. 1995 Jan;64(1):462-5 PMID: 7798948
  23. Model of local connectivity patterns in CA3 and CA1 areas of the hippocampus.
    Hippocampus. 1994 Oct;4(5):497-529 PMID: 7889123
  24. Regulation of cortical and subcortical glutamate receptor subunit expression by antipsychotic drugs.
    J Neurosci. 1995 Mar;15(3 Pt 2):2453-61 PMID: 7891180
  25. Calcium: still center-stage in hypoxic-ischemic neuronal death.
    Trends Neurosci. 1995 Feb;18(2):58-60 PMID: 7537408
  26. Relative abundance of subunit mRNAs determines gating and Ca2+ permeability of AMPA receptors in principal neurons and interneurons in rat CNS.
    Neuron. 1995 Jul;15(1):193-204 PMID: 7619522
  27. Inward rectification of both AMPA and kainate subtype glutamate receptors generated by polyamine-mediated ion channel block.
    Neuron. 1995 Aug;15(2):453-62 PMID: 7646897
  28. Intracellular polyamines mediate inward rectification of Ca(2+)-permeable alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid receptors.
    Proc Natl Acad Sci U S A. 1995 Sep 26;92(20):9298-302 PMID: 7568121
  29. Drugs of abuse and stress increase the expression of GluR1 and NMDAR1 glutamate receptor subunits in the rat ventral tegmental area: common adaptations among cross-sensitizing agents.
    J Neurosci. 1996 Jan;16(1):274-82 PMID: 8613793
  30. Evidence for multiple AMPA receptor complexes in hippocampal CA1/CA2 neurons.
    J Neurosci. 1996 Mar 15;16(6):1982-9 PMID: 8604042
  31. Biochemical adaptations in the mesolimbic dopamine system in response to repeated stress.
    Neuropsychopharmacology. 1996 Jun;14(6):443-52 PMID: 8726755
  32. Localization of the glutamate receptor subunit GluR1 on the surface of living and within cultured hippocampal neurons.
    Neuroscience. 1996 Nov;75(1):69-82 PMID: 8923524
  33. 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. 1996 Dec;142(2):296-312 PMID: 8934561
  34. Enhanced LTP in mice deficient in the AMPA receptor GluR2.
    Neuron. 1996 Nov;17(5):945-56 PMID: 8938126
  35. Single-channel properties of recombinant AMPA receptors depend on RNA editing, splice variation, and subunit composition.
    J Neurosci. 1997 Jan 1;17(1):58-69 PMID: 8987736
  36. Characterization of calpain-mediated proteolysis of GluR1 subunits of alpha-amino-3-hydroxy-5-methylisoxazole-4-propionate receptors in rat brain.
    J Neurochem. 1997 Apr;68(4):1484-94 PMID: 9084418
  37. Stoichiometry and assembly of a recombinant GABAA receptor subtype.
    J Neurosci. 1997 Apr 15;17(8):2728-37 PMID: 9092594
  38. The postsynaptic density: constituent and associated proteins characterized by electrophoresis, immunoblotting, and peptide sequencing.
    J Neurochem. 1992 Aug;59(2):667-78 PMID: 1629737
  39. Switch in glutamate receptor subunit gene expression in CA1 subfield of hippocampus following global ischemia in rats.
    Proc Natl Acad Sci U S A. 1992 Nov 1;89(21):10499-503 PMID: 1438239
  40. Genetic determinants of susceptibility to excitotoxic cell death: implications for gene targeting approaches.
    Proc Natl Acad Sci U S A. 1997 Apr 15;94(8):4103-8 PMID: 9108112
  41. Global ischemia induces downregulation of Glur2 mRNA and increases AMPA receptor-mediated Ca2+ influx in hippocampal CA1 neurons of gerbil.
    J Neurosci. 1997 Aug 15;17(16):6179-88 PMID: 9236229
  42. Differential localization of delta glutamate receptors in the rat cerebellum: coexpression with AMPA receptors in parallel fiber-spine synapses and absence from climbing fiber-spine synapses.
    J Neurosci. 1997 Jan 15;17(2):834-42 PMID: 8987804
  43. Differential dependence on GluR2 expression of three characteristic features of AMPA receptors.
    J Neurosci. 1997 Dec 15;17(24):9393-406 PMID: 9390995
  44. Phosphorylation of the alpha-amino-3-hydroxy-5-methylisoxazole4-propionic acid receptor GluR1 subunit by calcium/calmodulin-dependent kinase II.
    J Biol Chem. 1997 Dec 19;272(51):32528-33 PMID: 9405465
  45. Assembly of proteins to postsynaptic densities after transient cerebral ischemia.
    J Neurosci. 1998 Jan 15;18(2):625-33 PMID: 9425004
  46. Neuronal expression of zinc finger transcription factor REST/NRSF/XBR gene.
    J Neurosci. 1998 Feb 15;18(4):1280-96 PMID: 9454838
  47. Corticosteroid regulation of ion channel conductances and mRNA levels in individual hippocampal CA1 neurons.
    J Neurosci. 1998 Apr 1;18(7):2685-96 PMID: 9502826
  48. NSF binding to GluR2 regulates synaptic transmission.
    Neuron. 1998 Jul;21(1):87-97 PMID: 9697854
  49. The AMPA receptor GluR2 C terminus can mediate a reversible, ATP-dependent interaction with NSF and alpha- and beta-SNAPs.
    Neuron. 1998 Jul;21(1):99-110 PMID: 9697855
  50. Transcriptional regulation of the GluR2 gene: neural-specific expression, multiple promoters, and regulatory elements.
    J Neurosci. 1998 Sep 1;18(17):6723-39 PMID: 9712644
  51. Interaction of the N-ethylmaleimide-sensitive factor with AMPA receptors.
    Neuron. 1998 Aug;21(2):393-400 PMID: 9728920
  52. Turnover analysis of glutamate receptors identifies a rapidly degraded pool of the N-methyl-D-aspartate receptor subunit, NR1, in cultured cerebellar granule cells.
    J Biol Chem. 1999 Jan 1;274(1):151-7 PMID: 9867823
  53. Genetic regulation of glutamate receptor ion channels.
    Annu Rev Pharmacol Toxicol. 1999;39:221-41 PMID: 10331083
  54. Rapid spine delivery and redistribution of AMPA receptors after synaptic NMDA receptor activation.
    Science. 1999 Jun 11;284(5421):1811-6 PMID: 10364548
  55. Differential distribution of intracellular glutamate receptors in dendrites.
    J Neurosci. 1999 Jul 1;19(13):5549-62 PMID: 10377362
  56. AMPA receptor protein expression and function in astrocytes cultured from hippocampus.
    J Neurosci Res. 1999 Aug 15;57(4):557-71 PMID: 10440906
  57. Transcriptional repression by REST: recruitment of Sin3A and histone deacetylase to neuronal genes.
    Nat Neurosci. 1999 Oct;2(10):867-72 PMID: 10491605
  58. Ischemic cell death in brain neurons.
    Physiol Rev. 1999 Oct;79(4):1431-568 PMID: 10508238
  59. Antagonism of the NMDA and non-NMDA receptors in global versus focal brain ischemia.
    Prog Brain Res. 1993;96:125-35 PMID: 8392737
  60. The TINS/TiPS Lecture. The molecular biology of mammalian glutamate receptor channels.
    Trends Neurosci. 1993 Sep;16(9):359-65 PMID: 7694406
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
0027-8424
Published
2000-11-21
Pages
13360-5
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC27229
Subset
IM
Grants
NINDS NIH HHS · NS 07512 · United States
NINDS NIH HHS · NS 20752 · United States
NINDS NIH HHS · NS 31282 · United States
Corrections
ErratumIn
-
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]