Home LiteratureArticle Details
PMID: 15456836 Published · ppublish English Journal Article Research Support, U.S. Gov't, Non-P.H.S. Research Support, U.S. Gov't, P.H.S.

Altered expression of the delta subunit of the GABAA receptor in a mouse model of temporal lobe epilepsy.

Peng Z, Huang CS, Stell BM, Mody I, Houser CR

Abstract

delta Subunit-containing GABA(A) receptors are located predominantly at nonsynaptic sites in the dentate gyrus where they may play important roles in controlling neuronal excitability through tonic inhibition and responses to GABA spillover. Immunohistochemical methods were used to determine whether delta subunit expression was altered after pilocarpine-induced status epilepticus in C57BL/6 mice in ways that could increase excitability of the dentate gyrus. In pilocarpine-treated animals, the normal diffuse labeling of the delta subunit in the dentate molecular layer was decreased by 4 d after status epilepticus (latent period) and remained low throughout the period of chronic seizures. In contrast, diffuse labeling of alpha4 and gamma2 subunits, potentially interrelated GABA(A) receptor subunits, was increased during the chronic period. Interestingly, delta subunit labeling of many interneurons progressively increased after pilocarpine treatment. Consistent with the observed changes in delta subunit labeling, physiological studies revealed increased excitability in the dentate gyrus of slices obtained from the pilocarpine-treated mice and demonstrated that physiological concentrations of the neurosteroid tetrahydrodeoxycorticosterone were less effective in reducing excitability in the pilocarpine-treated animals than in controls. The findings support the idea that alterations in nonsynaptic delta subunit-containing GABA(A) receptors in both principal cells and interneurons could contribute to increased seizure susceptibility in the hippocampal formation in a temporal lobe epilepsy model.

MeSH Terms
Animals Brain/metabolism Densitometry Dentate Gyrus/metabolism,physiopathology Desoxycorticosterone/analogs & derivatives,pharmacology Disease Models, Animal Epilepsy, Temporal Lobe/chemically induced,metabolism,pathology,physiopathology Hippocampus/pathology Immunohistochemistry Interneurons/metabolism Male Mice Mice, Inbred C57BL Muscarinic Agonists Neurons/pathology Pilocarpine Receptors, GABA-A/biosynthesis
Chemicals
Muscarinic Agonists Receptors, GABA-A Pilocarpine Desoxycorticosterone tetrahydrodeoxycorticosterone
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Peng Zechun
Department of Neurobiology, David Geffen School of Medicine at University of California, Los Angeles, Los Angeles, California 90095-1763, USA.
Huang Christine S
Stell Brandon M
Mody Istvan
Houser Carolyn R
References (56)
56 references, click to expand
  1. Pharmacological characterization of a novel cell line expressing human alpha(4)beta(3)delta GABA(A) receptors.
    Br J Pharmacol. 2002 Aug;136(7):965-74 PMID: 12145096
  2. GABA(A) receptor subunits in the rat hippocampus I: immunocytochemical distribution of 13 subunits.
    Neuroscience. 1997 Oct;80(4):987-1000 PMID: 9284055
  3. A simple and sensitive antigen retrieval method for free-floating and slide-mounted tissue sections.
    J Neurosci Methods. 1999 Nov 15;93(2):149-62 PMID: 10634500
  4. Overlapping microarray profiles of dentate gyrus gene expression during development- and epilepsy-associated neurogenesis and axon outgrowth.
    J Neurosci. 2003 Mar 15;23(6):2218-27 PMID: 12657681
  5. Alteration in the sensitivity of GABA(A) receptors to allosteric modulatory drugs in rat hippocampus after chronic intermittent ethanol treatment.
    Alcohol Clin Exp Res. 1998 Dec;22(9):2165-73 PMID: 9884165
  6. Selective alterations in GABAA receptor subtypes in human temporal lobe epilepsy.
    J Neurosci. 2000 Jul 15;20(14):5401-19 PMID: 10884325
  7. alpha4beta3delta GABA(A) receptors characterized by fluorescence resonance energy transfer-derived measurements of membrane potential.
    J Biol Chem. 2001 Oct 19;276(42):38934-9 PMID: 11495904
  8. Altered expression of the delta subunit of the GABAA receptor in a mouse model of temporal lobe epilepsy.
    J Neurosci. 2004 Sep 29;24(39):8629-39 PMID: 15456836
  9. Up-regulation of GAD65 and GAD67 in remaining hippocampal GABA neurons in a model of temporal lobe epilepsy.
    J Comp Neurol. 1999 Sep 27;412(3):488-505 PMID: 10441235
  10. Subdivisions in the multiple GABAergic innervation of granule cells in the dentate gyrus of the rat hippocampus.
    Eur J Neurosci. 1993 May 1;5(5):411-29 PMID: 8261118
  11. Subunit composition and quantitative importance of hetero-oligomeric receptors: GABAA receptors containing alpha6 subunits.
    J Neurosci. 1998 Apr 1;18(7):2449-57 PMID: 9502805
  12. GABA uptake regulates cortical excitability via cell type-specific tonic inhibition.
    Nat Neurosci. 2003 May;6(5):484-90 PMID: 12679782
  13. 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
  14. Altered pharmacology of synaptic and extrasynaptic GABAA receptors on CA1 hippocampal neurons is consistent with subunit changes in a model of alcohol withdrawal and dependence.
    J Pharmacol Exp Ther. 2004 Sep;310(3):1234-45 PMID: 15126642
  15. Tonically active GABA A receptors: modulating gain and maintaining the tone.
    Trends Neurosci. 2004 May;27(5):262-9 PMID: 15111008
  16. Characterisation of delta-subunit containing GABAA receptors from rat brain.
    Eur J Pharmacol. 1995 Aug 15;290(3):175-81 PMID: 7589211
  17. GABA(A) receptor subunits in the rat hippocampus II: altered distribution in kainic acid-induced temporal lobe epilepsy.
    Neuroscience. 1997 Oct;80(4):1001-17 PMID: 9284056
  18. The kindling model of alcohol dependence: similar persistent reduction in seizure threshold to pentylenetetrazol in animals receiving chronic ethanol or chronic pentylenetetrazol.
    Alcohol Clin Exp Res. 1993 Jun;17(3):525-31 PMID: 8392817
  19. Segregation of different GABAA receptors to synaptic and extrasynaptic membranes of cerebellar granule cells.
    J Neurosci. 1998 Mar 1;18(5):1693-703 PMID: 9464994
  20. Ethanol enhances alpha 4 beta 3 delta and alpha 6 beta 3 delta gamma-aminobutyric acid type A receptors at low concentrations known to affect humans.
    Proc Natl Acad Sci U S A. 2003 Dec 9;100(25):15218-23 PMID: 14625373
  21. Formation and plasticity of GABAergic synapses: physiological mechanisms and pathophysiological implications.
    Pharmacol Ther. 2003 Jun;98(3):299-323 PMID: 12782242
  22. Increased number of synaptic GABA(A) receptors underlies potentiation at hippocampal inhibitory synapses.
    Nature. 1998 Sep 10;395(6698):172-7 PMID: 9744275
  23. GABAergic neurons and GABA(A)-receptors in temporal lobe epilepsy.
    Neurochem Int. 1999 May;34(5):435-45 PMID: 10397372
  24. Withdrawal from chronic intermittent ethanol treatment changes subunit composition, reduces synaptic function, and decreases behavioral responses to positive allosteric modulators of GABAA receptors.
    Mol Pharmacol. 2003 Jan;63(1):53-64 PMID: 12488536
  25. Absence of association between delta and gamma2 subunits in native GABA(A) receptors from rat brain.
    Eur J Pharmacol. 1998 Apr 24;347(2-3):347-53 PMID: 9653902
  26. Stoichiometry and assembly of a recombinant GABAA receptor subtype.
    J Neurosci. 1997 Apr 15;17(8):2728-37 PMID: 9092594
  27. GABA(A) receptor changes in delta subunit-deficient mice: altered expression of alpha4 and gamma2 subunits in the forebrain.
    J Comp Neurol. 2002 Apr 29;446(2):179-97 PMID: 11932935
  28. A significant part of native gamma-aminobutyric AcidA receptors containing alpha4 subunits do not contain gamma or delta subunits.
    J Biol Chem. 1999 Jul 9;274(28):19613-6 PMID: 10391897
  29. Targeted disruption of the GABA(A) receptor delta subunit gene leads to an up-regulation of gamma 2 subunit-containing receptors in cerebellar granule cells.
    J Biol Chem. 2001 Mar 30;276(13):10532-8 PMID: 11136737
  30. Diminished allopregnanolone enhancement of GABA(A) receptor currents in a rat model of chronic temporal lobe epilepsy.
    J Physiol. 2001 Dec 1;537(Pt 2):453-65 PMID: 11731578
  31. The glucose oxidase-DAB-nickel method in peroxidase histochemistry of the nervous system.
    Neurosci Lett. 1988 Feb 29;85(2):169-71 PMID: 3374833
  32. Tonic inhibition in mouse hippocampal CA1 pyramidal neurons is mediated by alpha5 subunit-containing gamma-aminobutyric acid type A receptors.
    Proc Natl Acad Sci U S A. 2004 Mar 9;101(10):3662-7 PMID: 14993607
  33. Development of a tonic form of synaptic inhibition in rat cerebellar granule cells resulting from persistent activation of GABAA receptors.
    J Physiol. 1996 Dec 15;497 ( Pt 3):753-9 PMID: 9003560
  34. GABAA-receptor heterogeneity in the adult rat brain: differential regional and cellular distribution of seven major subunits.
    J Comp Neurol. 1995 Aug 14;359(1):154-94 PMID: 8557845
  35. GABAA receptor subunit gamma2 and delta subtypes confer unique kinetic properties on recombinant GABAA receptor currents in mouse fibroblasts.
    J Physiol. 1999 Jan 1;514 ( Pt 1):27-45 PMID: 9831714
  36. Loss of glutamate decarboxylase mRNA-containing neurons in the rat dentate gyrus following pilocarpine-induced seizures.
    J Neurosci. 1993 Oct;13(10):4470-85 PMID: 8410199
  37. Enhanced neurosteroid potentiation of ternary GABA(A) receptors containing the delta subunit.
    J Neurosci. 2002 Mar 1;22(5):1541-9 PMID: 11880484
  38. Five types of basket cell in the hippocampal dentate gyrus: a combined Golgi and electron microscopic study.
    J Neurocytol. 1983 Aug;12(4):577-97 PMID: 6619905
  39. Distinguishing between GABA(A) receptors responsible for tonic and phasic conductances.
    Neurochem Res. 2001 Sep;26(8-9):907-13 PMID: 11699942
  40. Epilepsy-associated plasticity in gamma-aminobutyric acid receptor expression, function, and inhibitory synaptic properties.
    Int Rev Neurobiol. 2001;45:237-52 PMID: 11130901
  41. Downregulation of the alpha5 subunit of the GABA(A) receptor in the pilocarpine model of temporal lobe epilepsy.
    Hippocampus. 2003;13(5):633-45 PMID: 12921352
  42. Perpetual inhibitory activity in mammalian brain slices generated by spontaneous GABA release.
    Brain Res. 1991 Apr 5;545(1-2):142-50 PMID: 1650273
  43. Perisynaptic localization of delta subunit-containing GABA(A) receptors and their activation by GABA spillover in the mouse dentate gyrus.
    J Neurosci. 2003 Nov 19;23(33):10650-61 PMID: 14627650
  44. Selective changes in single cell GABA(A) receptor subunit expression and function in temporal lobe epilepsy.
    Nat Med. 1998 Oct;4(10):1166-72 PMID: 9771750
  45. Spillover-mediated transmission at inhibitory synapses promoted by high affinity alpha6 subunit GABA(A) receptors and glomerular geometry.
    Neuron. 1998 Apr;20(4):783-95 PMID: 9581769
  46. Modification of seizure activity by electrical stimulation. II. Motor seizure.
    Electroencephalogr Clin Neurophysiol. 1972 Mar;32(3):281-94 PMID: 4110397
  47. Adaptive regulation of neuronal excitability by a voltage-independent potassium conductance.
    Nature. 2001 Jan 4;409(6816):88-92 PMID: 11343119
  48. GABRD encoding a protein for extra- or peri-synaptic GABAA receptors is a susceptibility locus for generalized epilepsies.
    Hum Mol Genet. 2004 Jul 1;13(13):1315-9 PMID: 15115768
  49. Assembly of GABAA receptor subunits: role of the delta subunit.
    J Neurosci. 1994 Nov;14(11 Pt 2):7077-86 PMID: 7525894
  50. Trace fear conditioning involves hippocampal alpha5 GABA(A) receptors.
    Proc Natl Acad Sci U S A. 2002 Jun 25;99(13):8980-5 PMID: 12084936
  51. Neuroactive steroids reduce neuronal excitability by selectively enhancing tonic inhibition mediated by delta subunit-containing GABAA receptors.
    Proc Natl Acad Sci U S A. 2003 Nov 25;100(24):14439-44 PMID: 14623958
  52. GABA(A) receptor subunits in the rat hippocampus III: altered messenger RNA expression in kainic acid-induced epilepsy.
    Neuroscience. 1997 Oct;80(4):1019-32 PMID: 9284057
  53. Interneurons of the hippocampus.
    Hippocampus. 1996;6(4):347-470 PMID: 8915675
  54. Proton modulation of alpha 1 beta 3 delta GABAA receptor channel gating and desensitization.
    J Neurophysiol. 2004 Sep;92(3):1577-85 PMID: 15152020
  55. Preferential coassembly of alpha4 and delta subunits of the gamma-aminobutyric acidA receptor in rat thalamus.
    Mol Pharmacol. 1999 Jul;56(1):110-5 PMID: 10385690
  56. The influence of subunit composition on the interaction of neurosteroids with GABA(A) receptors.
    Neuropharmacology. 2002 Sep;43(4):651-61 PMID: 12367610
Article Info
Journal
The Journal of neuroscience : the official journal of the Society for Neuroscience
Abbr.
J Neurosci
ISSN
1529-2401
Published
2004-09-29
Pages
8629-39
Language
English
Region
United States
NLM ID
8102140
PMCID
PMC6729896
Subset
IM
Grants
BLRD VA · I01 BX000404 · United States
NINDS NIH HHS · P01 NS035985 · United States
NINDS NIH HHS · NS35985 · United States
Corrections
CommentIn
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: product@genelibs.com