Distinct patterns of expression and regulation of GABAA receptors containing the δ subunit in cerebellar granule and hippocampal neurons

Journal of Neurochemistry

Volumn 94, Issue 3, 2005, Pages 659-671

  Follesa, Paolo ^a   Mostallino, Maria Cristina ^a   Biggio, Francesca ^a   Gorini, Giorgio ^a   Caria, Stefania ^a   Busonero, Fabio ^a   Murru, Luca ^a   Mura, Maria Luisa ^a   Sanna, Enrico ^a   Biggio, Giovanni ^a  

^a UNIVERSITY OF CAGLIARI   (Italy)

Author keywords

Alcohol; GABAA receptor; Neurosteroid; Patch clamp; Plasticity; Withdrawal

Indexed keywords

3ALPHA HYDROXY 5ALPHA PREGNAN 20 ONE; 4 AMINOBUTYRIC ACID A RECEPTOR; ALCOHOL; CHLORIDE CHANNEL; NEUROTRANSMITTER RECEPTOR;

ALCOHOL WITHDRAWAL; ANIMAL CELL; ARTICLE; CEREBELLUM; CONTROLLED STUDY; GENE EXPRESSION REGULATION; GRANULE CELL; HIPPOCAMPUS; IMMUNOBLOTTING; IMMUNOFLUORESCENCE; LONG TERM EXPOSURE; MORPHOMETRICS; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; RAT; RNA PROBE;

ANESTHETICS; ANIMALS; ANIMALS, NEWBORN; BLOTTING, WESTERN; CELLS, CULTURED; CENTRAL NERVOUS SYSTEM DEPRESSANTS; CEREBELLUM; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG ADMINISTRATION SCHEDULE; DRUG INTERACTIONS; ELECTRIC STIMULATION; ETHANOL; GABA AGONISTS; GENE EXPRESSION REGULATION; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; ISOXAZOLES; MEMBRANE POTENTIALS; NEURONS; PATCH-CLAMP TECHNIQUES; PREGNANOLONE; PROTEIN SUBUNITS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, GABA-A; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; TIME FACTORS;

EID: 23244463624     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2005.03303.x     Document Type: Article

References (72)

1. Adkins C. E., Pillai G. V., Kerby J., Bonnert T. P., Haldon C., McKeman R. M., Gonzalez J. E., Oades K., Whiting P. J. and Simpson P. B. (2001) α4β3δ GABA(A) receptors characterized by fluorescence resonance energy transfer-derived measurements of membrane potential. J. Biol. Chem. 276, 38 934-38 939.
2. Banker G. A. and Cowan W. M. (1977) Rat hippocampal neurons in dispersed cell culture. Brain Res. 126, 397-342.
3. Barnard E. A., Skolnick P., Olsen R. W., Mohler H., Sieghart W., Biggio G., Braestrup C., Bateson A. N. and Langer S. Z. (1998) International Union of Pharmacology. XV. Subtypes of γ-aminobutyric acid A receptors: classification on the basis of subunit structure and receptor function. Pharmacol. Rev. 50, 291-313.
4. Bateson A. N. (2004) The benzodiazepine site of the GABAA receptor: an old target with new potential? Sleep Med. 5, S9-S15.
5. Bencsits E., Ebert V., Tretter V. and Sieghart W. (1999) A significant part of native γ-aminobutyric AcidA receptors containing α4 subunits do not contain γ or δ subunits. J. Biol. Chem. 274, 19613-19616.
6. Bollan K., Robertson L. A., Tang H. and Connolly C. N. (2003a) Multiple assembly signals in γ-aminobutyric acid (type A) receptor subunits combine to drive receptor construction and composition. Biochem. Soc. Trans. 31, 875-879.
7. Bollan K., King D., Robertson L. A., Brown K., Taylor P. M., Moss S. J. and Connolly C. N. (2003b) GABA(A) receptor composition is determined by distinct assembly signals within α and β subunits. J. Biol. Chem. 278, 4747-4755.
8. Bovolin P., Santi M. R., Puia G., Costa E. and Grayson D. (1992) Expression patterns of γ-aminobutyric acid type A receptor subunit mRNAs in primary cultures of granule neurons and astrocytes from neonatal rat cerebella. Proc. Natl Acad. Sci. USA 89, 9344-9348.
9. Brickley S. G., Cull-Candy S. G. and Farrant M. (1996) Development of a tonic form of synaptic inhibition in rat cerebellar granule cells resulting from persistent activation of GABAA receptors. J. Physiol. 497, 753-759.
10. Brickley S. G., Revilla V., Cull-Candy S. G., Wisden W. and Farrant M. (2001) Adaptive regulation of neuronal excitability by a voltage-independent potassium conductance. Nature 409, 88-92.
11. Brown N., Kerby J., Bonnert T. P., Whiting P. J. and Wafford K. A. (2002) Pharmacological characterization of a novel cell line expressing human α(4)β(3)δ GABA(A) receptors. Br. J. Pharmacol. 136, 965-974.
12. Cagetti E., Liang J., Spigelman I. and Olsen R. W. (2003) 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. 63, 53-64.
13. Concas A., Mostallino M. C., Porcu P., Follesa P., Barbaccia M. L., Trabucchi M., Purdy R. H., Grisenti P. and Biggio G. (1998) Role of brain allopregnanolone in the plasticity of γ-aminobutyric acid type A receptor in rat brain during pregnancy and after delivery. Proc. Natl Acad. Sci. USA 95, 13 284-13 289.
14. Costa E. T., Soto E. E., Cardoso R. A., Olivera D. S. and Valenzuela C. F. (2000) Acute effects of ethanol on kainate receptors in cultured hippocampal neurons. Alcohol Clin. Exp. Res. 24, 220-225.
15. Crestani F., Keist R., Fritschy J. M., Benke D., Vogt K., Prut L., Bluthmann H., Mohler H. and Rudolph U. (2002) Trace fear conditioning involves hippocampal α5 GABA(A) receptors. Proc. Natl Acad. Sci. USA 99, 8980-8985.
16. Danielson P. E., Forss-Petter S., Brow M. A., Calavetta L., Douglass J., Milner R. J. and Sutcliffe J. G. (1988) p1B15: a cDNA clone of the rat mRNA encoding cyclophilin. DNA 7, 261-267.
17. Fenelon V. S. and Herbison A. E. (1996) Plasticity in GABAA receptor subunit mRNA expression by hypothalamic magnocellular neurons in the adult rat. J. Neurosci. 16, 4872-4880.
18. Follesa P., Floris S., Tuligi G., Mostallino M. C., Concas A. and Biggio G. (1998) Molecular and functional adaptation of the GABA(A) receptor complex during pregnancy and after delivery in the rat brain. Eur. J. Neurosci. 10, 2905-2912.
19. Follesa P., Concas A., Porcu P., Sanna E., Serra M., Mostallino M. C., Purdy R. H. and Biggio G. (2001) Role of allopregnanolone in regulation of GABA(A) receptor plasticity during long-term exposure to and withdrawal from progesterone. Brain Res. Brain Res. Rev. 37, 81-90.
20. Follesa P., Mancuso L., Biggio F., Mostallino M. C., Manca A., Mascia M. P., Busonero F., Talani G., Sanna E. and Biggio G. (2003) γ-Hydroxybutyric acid and diazepam antagonize a rapid increase in GABA(A) receptors α(4) subunit mRNA abundance induced by ethanol withdrawal in cerebellar granule cells. Mol. Pharmacol. 63, 896-907.
21. Follesa P., Biggio F., Caria S., Gorini G. and Biggio G. (2004a) Modulation of GABA(A) receptor gene expression by allopregnanolone and ethanol. Eur. J. Pharmacol. 500, 413-425.
22. Follesa P., Biggio F., Mancuso L., Cabras S., Caria S., Gorini G., Manca A., Orru A. and Biggio G. (2004b) Ethanol withdrawal-induced up-regulation of the α2 subunit of the GABAA receptor and its prevention by diazepam or γ-hydroxybutyric acid. Brain Res. Mol. Brain Res. 120, 130-137.
23. Hamann M., Rossi D. J. and Attwell D. (2002) Tonic and spillover inhibition of granule cells control information flow through cerebellar cortex. Neuron 33, 625-633.
24. Hevers W. and Luddens H. (1998) The diversity of GABAA receptors. Pharmacological and electrophysiological properties of GABAA channel subtypes. Mol. Neurobiol. 18, 35-86.
25. Holt R. A., Bateson A. N. and Martin I. L. (1996) Chronic treatment with diazepam or abecamil differently affects the expression of GABAA receptor subunit mRNAs in the rat cortex. Neuropharmacology 35, 1457-1463.
26. Jechlinger M., Pelz R., Tretter V., Klausberger T. and Sieghart W. (1998) Subunit composition and quantitative importance of hetero-oligomeric receptors: GABAA receptors containing α6 subunits. J. Neurosci. 18, 2449-2457.
27. Jones A., Korpi E. R., McKeman R. M. et al. (1997) Ligand-gated ion channel subunit partnerships: GABAA receptor α6 subunit gene inactivation inhibits δ subunit expression. J. Neurosci. 17, 1350-1362.
28. Laurie D. J., Wisden W. and Seeburg P. H. (1992a) The distribution of thirteen GABAA receptor subunit mRNAs in the rat brain. III. Embryonic and postnatal development. J. Neurosci. 12, 4151-4172.
29. Laurie D. J., Seeburg P. H. and Wisden W. (1992b) The distribution of 13 GABAA receptor subunit mRNAs in the rat brain. II. Olfactory bulb and cerebellum. J. Neurosci. 12, 1063-1076.
30. Lee J. J. and Costlow N. A. (1987) A molecular titration assay to measure transcript prevalence levels. Meth. Enzymol. 152, 633-648.
31. Levi G., Aloisi F., Ciotti M. T. and Gallo V. (1984) Autoradiographic localization and depolarization-induced release of acidic amino acids in differentiating cerebellar granule cell cultures. Brain Res. 290, 77-86.
32. Low K., Crestani F., Keist R. et al. (2000) Molecular and neuronal substrate for the selective attenuation of anxiety. Science 290, 131-134.
33. Luscher B. and Keller C. A. (2004) Regulation of GABAA receptor trafficking, channel activity, and functional plasticity of inhibitory synapses. Pharmacol. Ther. 102, 195-221.
34. McKeman R. M., Quirk K., Prince R., Cox P. A., Gillard N. P., Ragan C. I. and Whiting P. (1991) GABAA receptor subtypes immunopurified from rat brain with α subunit-specific antibodies have unique pharmacological properties. Neuron 7, 667-676.
35. McKeman R. M., Rosahl T. W., Reynolds D. S. et al. (2000) Sedative but not anxiolytic properties of benzodiazepines are mediated by the GABA(A) receptor α1 subtype. Nat. Neurosci. 3, 587-592.
36. Mehta A. K. and Ticku M. K. (1999) An update on GABAA receptors. Brain Res. Brain Res. Rev. 29, 196-217.
37. Mihalek R. M., Banerjee P. K., Korpi E. R. et al. (1999) Attenuated sensitivity to neuroactive steroids in γ-aminobutyrate type A receptor δ subunit knockout mice. Proc. Natl Acad. Sci. USA 96, 12905-12910.
38. Milner R. J. and Sutcliffe J. G. (1983) Gene expression in rat brain. Nucl Acids Res. 11, 5497-5520.
39. Mody I. (2001) Distinguishing between GABA(A) receptors responsible for tonic and phasic conductances. Neurochem. Res. 26, 907-913.
40. Mody I. and Pearce R. A. (2004) Diversity of inhibitory neurotransmission through GABA(A) receptors. Trends Neurosci. 27, 569-575.
41. Morrow A. L., VanDoren M. J., Penland S. N. and Matthews D. B. (2001) The role of GABAergic neuroactive steroids in ethanol action, tolerance and dependence. Brain Res. Brain Res. Rev. 37, 98-109.
42. Moss S. J. and Smart T. G. (2001) Constructing inhibitory synapses. Nat. Rev. Neurosci. 2, 240-250.
43. Nusser Z. and Mody I. (2002) Selective modulation of tonic and phasic inhibitions in dentate gyrus granule cells. J. Neurophysiol. 87, 2624-2628.
44. Nusser Z., Sieghart W. and Somogyi P. (1998) Segregation of different GABAA receptors to synaptic and extrasynaptic membranes of cerebellar granule cells. J. Neurosci. 18, 1693-1703.
45. Pirker S., Schwarzer C., Wieselthaler A., Sieghart W. and Sperk G. (2000) GABA(A) receptors: immunocytochemical distribution of 13 subunits in the adult rat brain. Neuroscience 101, 815-850.
46. Reddy D. S. (2003) Pharmacology of endogenous neuroactive steroids. Crit. Rev. Neurobiol. 15, 197-234.
47. van Rijnsoever C., Tauber M., Choulli M. K., Keist R., Rudolph U., Mohler H., Fritschy J. M. and Crestani F. (2004) Requirement of α5-GABAA receptors for the development of tolerance to the sedative action of diazepam in mice. J. Neurosci. 24, 6785-6790.
48. Rudolph U. and Mohler H. (2004) Analysis of GABAA receptor function and dissection of the pharmacology of benzodiazepines and general anesthetics through mouse genetics. Annu. Rev. Pharmacol. Toxicol. 44, 475-498.
49. Rudolph U., Crestani F., Benke D., Brunig I., Benson J. A., Fritschy J. M., Martin J. R., Bluethmann H. and Mohler H. (1999) Benzodiazepine actions mediated by specific γ-aminobutyric acid (A) receptor subtypes. Nature 401, 796-800.
50. Sanna E., Mostallino M. C., Busonero F., Talani G., Tranquilli S., Mameli M., Spiga S., Follesa P. and Biggio G. (2003) Changes in GABA(A) receptor gene expression associated with selective alterations in receptor function and pharmacology after ethanol withdrawal. J. Neurosci. 23, 11 711-11 724.
51. Sanna E., Talani G., Busonero F., Pisu M. G., Purdy R. H., Serra M. and Biggio G. (2004) Brain steroidogenesis mediates ethanol modulation of GABAA receptor activity in rat hippocampus. J. Neurosci. 24, 6521-6530.
52. Saxena N. C. and Macdonald R. L. (1996) Properties of putative cerebellar γ-aminobutyric acid A receptor isoforms. Mol. Pharmacol. 49, 567-579.
53. Semyanov A., Walker M. C. and Kullmann D. M. (2003) GABA uptake regulates cortical excitability via cell type-specific tonic inhibition. Nat. Neurosci. 6, 484-490.
54. Semyanov A., Walker M. C., Kullmann D. M. and Silver R. A. (2004) Tonically active GABA A receptors: modulating gain and maintaining the tone. Trends Neurosci. 27, 262-269.
55. Sieghart W. (1995) Structure and pharmacology of γ-aminobutyric acid A receptor subtypes. Pharmacol. Rev. 47, 181-234.
56. Sieghart W. and Sperk G. (2002) Subunit composition, distribution and function of GABA(A) receptor subtypes. Curr. Top. Med. Chem. 2, 795-816.
57. Smith S. S., Gong Q. H., Li X., Moran M. H., Bitran D., Frye C. A. and Hsu F. C. (1998) Withdrawal from 3α-OH-5α-pregnan-20-1 using a pseudopregnancy model alters the kinetics of hippocampal GABAA-gated current and increases the GABAA receptor α4 subunit in association with increased anxiety. J. Neurosci. 18, 5275-5284.
58. Smothers C. T., Mrotek J. J. and Lovinger D. M. (1997) Chronic ethanol exposure leads to a selective enhancement of N-methyl-D-aspartate receptor function in cultured hippocampal neurons. J. Pharmacol. Exp. Ther. 283, 1214-1222.
59. Sperk G., Schwarzer C., Tsunashima K., Fuchs K. and Sieghart W. (1997) GABA(A) receptor subunits in the rat hippocampus I: immunocytochemical distribution of 13 subunits. Neuroscience 80, 987-1000.
60. Spigelman I., Li Z., Liang J., Cagetti E., Samzadeh S., Mihalek R. M., Homanics G. E. and Olsen R. W. (2003) Reduced inhibition and sensitivity to neurosteroids in hippocampus of mice lacking the GABA(A) receptor δ subunit. J. Neurophysiol. 90, 903-910.
61. Steiger J. L. and Russek S. J. (2004) GABAA receptors: building the bridge between subunit mRNAs, their promoters, and cognate transcription factors. Pharmacol. Ther. 101, 259-281.
62. Stell B. M. and Mody I. (2002) Receptors with different affinities mediate phasic and tonic GABA(A) conductances in hippocampal neurons. J. Neurosci. 22, RC223.
63. Stell B. M., Brickley S. G., Tang C. Y., Farrant M. and Mody I. (2003) Neuroactive steroids reduce neuronal excitability by selectively enhancing tonic inhibition mediated by δ subunit-containing GABAA receptors. Proc. Natl Acad. Sci. USA 100, 14 439-14 444.
64. Sundstrom-Poromaa I., Smith D. H., Gong Q. H., Sabado T. N., Li X., Light A., Wiedmann M., Williams K. and Smith S. S. (2002) Hormonally regulated α(4)β(2)δ GABA(A) receptors are a target for alcohol. Nat. Neurosci. 5, 721-722.
65. Wallner M., Hanchar H. J. and Olsen R. W. (2003) Ethanol enhances α4β3δ and α6β3δ γ-aminobutyric acid type A receptors at low concentrations known to affect humans. Proc. Natl Acad. Sci. USA 100, 15 218-15 223.
66. Wei W., Zhang N., Peng Z., Houser C. R. and Mody I. (2003) Perisynaptic localization of δsubunit-containing GABA(A) receptors and their activation by GABA spillover in the mouse dentate gyrus. J. Neurosci. 23, 10 650-10 661.
67. Whiting P. J., McAllister G., Vassilatis D. et al. (1997) Neuronally restricted RNA splicing regulates the expression of a novel GABAA receptor subunit conferring atypical functional properties (corrected; erratum to be published). J. Neurosci. 17, 5027-5037.
68. Wisden W, McNaughton L. A., Darlison M. G., Hunt S. P. and Barnard E. A. (1989) Differential distribution of GABAA receptor mRNAs in bovine cerebellum -localization of α2 mRNA in Bergmann glia layer. Neurosci. Lett. 106, 7-12.
69. Wisden W., Laurie D. J., Monyer H. and Seeburg P. H. (1992) The distribution of 13 GABAA receptor subunit mRNAs in the rat brain. I. Telencephalon, diencephalon, mesencephalon. J. Neurosci. 12, 1040-1062.
70. Wohlfarth K. M., Bianchi M. T. and Macdonald R. L. (2002) Enhanced neurosteroid potentiation of ternary GABA(A) receptors containing the δ subunit. J. Neurosci. 22, 1541-1549.
71. Zhao Z. Y. and Joho R. H. (1990) Isolation of distantly related members in a multigene family using the polymerase chain reaction technique. Biochem. Biophys. Res. Commun. 167, 174-182.
72. Zinn K., DiMaio D. and Maniatis T. (1983) Identification of two distinct regulatory regions adjacent to the human β-interferon gene. Cell 34, 865-879.