Bergmann glia GABAA receptors concentrate on the glial processes that wrap inhibitory synapses

Journal of Neuroscience

Volumn 22, Issue 24, 2002, Pages 10720-10730

  Riquelme, Raquel ^a   Miralles, Celia P ^a   De Blas, Angel L ^a  

^a UNIVERSITY OF CONNECTICUT   (United States)

Author keywords

Astrocyte; Bergmann glia; Cerebellum; Electron microscopy; GABAA receptor; Glia; Immunocytochemistry; Immunogold; Neuron; Purkinje cell; Synapse

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR;

ANIMAL TISSUE; ARTICLE; CELL MEMBRANE; CEREBELLUM; DENDRITIC SPINE; GABAERGIC SYSTEM; GLIA; IMMUNOGOLD ELECTRON MICROSCOPY; IMMUNOHISTOCHEMISTRY; NERVE FIBER; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PURKINJE CELL; SYNAPTIC TRANSMISSION;

EID: 0037114957     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.22-24-10720.2002     Document Type: Article

References (67)

1. Amin J, Weiss DS (1993) GABAA receptor needs two homologous domains of the beta-subunit for activation by GABA but not by pentobarbital. Nature 366:565-569.
2. 2+ elevations in astrocytes in hippocampal slices. J Neurosci 22:2443-2450.
3. Barnard EA, Skolnick P, Olsen RW, Mohler H, Sieghart W, Biggio G, Braestrup C, Bateson AN, Langer SZ (1998) International Union of Pharmacology. XV. Subtypes of gamma-aminobutyric acidA receptors: Classification on the basis of subunit structure and receptor function. Pharmacol Rev 50:291-313.
4. Beaulieu C, Somogyi P (1990) Targets and quantitative distribution of GABAergic synapses in the visual cortex of the cat. Eur J Neurosci 2:296-303.
5. + currents in adult hippocampal glial cells in situ. Glia 26:129-138.
6. Berthele A, Platzer S, Weis S, Conrad B, Tolle TR (2001) Expression of GABAB1 and GABAB2 mRNA in the human brain. NeuroReport 12:3269-3275.
7. Blankenfeld GV, Kettenmann H (1992) Glutamate and GABA receptors in vertebrate glial cells. Mol Neurobiol 1:31-43.
8. A receptor in cultured murine cells of the oligodendrocyte lineage. Eur J Neurosci 3:310-316.
9. - channels in cultured astrocytes. Proc Natl Acad Sci USA 85:9336-9340.
10. Bovolin P, Santi MR, Puia G, Costa E, Grayson D (1992) Expression patterns of gamma-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.
11. Chaudhry FA, Lehre KP, van Lookeren Campagne M, Ottersen OP, Danbolt NC, Storm-Mathisen J (1995) Glutamate transporters in glial plasma membranes: Highly differentiated localizations revealed by quantitative ultra structural immunocytochemistry. Neuron 15:711-720.
12. A receptor clustering in cultured hippocampal neurons. J Neurosci 22:684-697.
13. A receptor and gephyrin clusters. Prog Brain Res 136:157-180.
14. Conti F, Zuccarello LV, Barbaresi P, Minelli A, Brecha NC, Melone M (1999) Neuronal, glial and epithelial localization of γ-aminobutyric acid transporter 2, a high-affinity γ-aminobutyric acid plasma membrane transporter, in the cerebral cortex and neighboring structures. J Comp Neurol 409:482-494.
15. De Blas AL (1984) Monoclonal antibodies to specific astroglial and neuronal antigens reveal the cytoarchitecture of the Bergmann glia fibers in the cerebellum. J Neurosci 4:265-273.
16. A receptors studied with subunit-specific antibodies. Mol Neurobiol 12:55-71.
17. De Blas AL, Cherwinski HM (1985) The development of the Bergmann fiber palisades in the cerebellum of the normal rat and in the weaver mouse. Brain Res 342:234-241.
18. - channel complex. J Neurosci 8:602-614.
19. A receptors is recognized by two different monoclonal antibodies. Brain Res 569:57-62.
20. Fifková E, Eason H, Schaner P (1992) Inhibitory contacts on dendritic spines of the dentate fascia. Brain Res 577:331-336.
21. Fraser DD, Mudrick-Donnon LA, MacVicar BA (1994) Astrocytic GABA receptors. Glia 11:83-93.
22. A/benzodiazepine receptors in acutely isolated hippocampus astrocytes. J Neurosci 15:2720-2732.
23. A-Receptor heterogeneity in the adult rat brain: Differential regional and cellular distribution of seven major subunits. J Comp Neurol 359:154-194.
24. Gonchar Y, Pang L, Malitschek B, Bettler B, Burkhalter A (2001) Subcellular localization of GABA(B) receptor subunits in rat visual cortex. J Comp Neurol 431:182-197.
25. A receptor immunoreactivity in the white matter. NeuroReport 3:169-172.
26. Hansen GH, Hosli E, Belhage B, Schousboe A, Hosli L (1991) Light and electron microscopic localization of GABAA-receptors on cultured cerebellar granule cells and astrocytes using immunohistochemical techniques. Neurochem Res 16:341-346.
27. Haydon PG (2001) Glia: Listening and talking to the synapse. Nat Neurosci Rev 2:185-193.
28. Isaacson JS, Solis JM, Nicoll RA (1993) Local and diffuse synaptic actions of GABA in the hippocampus. Neuron 10:165-175.
29. Kang J, Jiang L, Goldman SA, Nedergaard M (1998) Astrocyte-mediated potentiation of inhibitory synaptic transmission. Nat Neurosci 1:683-692.
30. Khan ZU, Gutierrez A, Miralles CP, De Blas AL (1996) The γ subunits of the native GABAA/benzodiazepine receptors. Neurochem Res 21:147-159.
31. Kellenberger E, Hayat MA (1991) Some basic concepts for the choice of methods. In: Colloidal gold: principles, methods and applications, Vol 3 (Hayat MA, ed), pp 1-30. New York: Academic.
32. Kulik A, Nakadate K, Nyíri G, Notomi T, Malitschek B, Bettler B, Shigemoto R (2002) Distinct localization of GABAB receptors relative to synaptic sites in the rat cerebellum and ventrobasal thalamus. Eur J Neurosci 15:291-307.
33. A receptor subunit mRNAs in the rat brain. II. Olfactory bulb and cerebellum. J Neurosci 12:1063-1076.
34. 2+-permeable AMPA receptors in Bergmann glia. Science 292:926-929.
35. Matsubara M, Laake JH, Davanger S, Usami S, Ottersen OP (1996) Organization of AMPA receptor subunits at a glutamate synapse: A quantitative immunogold analysis of hair cell synapses in rat organ of Corti. J Neurosci 16:4457-4467.
36. Matsutani S, Yamamoto N (1997) Neuronal regulation of astrocyte morphology in vitro is mediated by GABAergic signaling. Glia 20:1-9.
37. Matsutani S, Yamamoto N (1998) GABAergic neuron-to-astrocyte signaling regulates dendritic branching in coculture. J Neurobiol 37:251-264.
38. Mehta AK, Ticku MK (1999) An update on GABAA receptors. Brain Res Rev 29:196-217.
39. A receptor in the rat brain. J Comp Neurol 413:535-548.
40. Moreno JI, Piva MA, Miralles CP, De Blas AL (1994) Immunocytochemical localization of the beta 2 subunit of the gamma-aminobutyric acidA receptor in the rat brain. J Comp Neurol 350:260-271.
41. Mugnaini E (1972) The histology and cytology of the cerebellar cortex. In: The Comparative Anatomy and Histology of the Cerebellum: The Human Cerebellum, Cerebellar Connections and Cerebellar Cortex, Vol 3 (Larsell O, Jansen J, eds), pp 201-264. Minneapolis: University of Minnesota.
42. Mugnaini E, Forstronen PF (1967) Ultrastructural studies on the cerebellar histogenesis. I. Differentiation of granule cells and development of glomeruli in the chick embryo. J Zellforsch Mikrosk Anat 77:115-143.
43. A receptor expression in Bergmann glial cells. J Neurosci 14:2503-2514.
44. A and glutamate receptors in relation to transmitter release sites on the surface of cerebellar neurons. Prog Brain Res 114:109-127.
45. A receptor is concentrated in both inhibitory and excitatory synapses on cerebellar granule cells. J Neurosci 16:103-114.
46. A receptors to synaptic and extra synaptic membranes of cerebellar granule cells. J Neurosci 18:1693-1703.
47. Ortega A, Eshhar N, Teichberg VI (1991) Properties of kainate receptor/channels on cultured Bergmann glia. Neuroscience 41:335-349.
48. Palay SL, Chan-Palay V (1974) Cerebellar Cortex. New York: Springer.
49. A receptor subunits in the rat CNS. J Comp Neurol 326:193-216.
50. Pirker S, Schwarzer C, Wieselthaler A, Sieghart W, Sperk G (2000) GABAA receptors: Immunocytochemical distribution of 13 subunits in the adult rat brain. Neuroscience 101:815-850.
51. Quirk K, Gillard NP, Ragan CI, Whiting PG, Mckernan RM (1994) Model of subunit composition of γ-amino butyric acid A receptor subtypes expressed in rat cerebellum with respect to their α and γ/δ subunits. J Biol Chem 23:16020-16028.
52. Rakic P (1971) Neuron-glia relationship during granule cell migration in developing cerebellar cortex. A Golgi and electron microscopic study in Macacus Rhesus. J Comp Neurol 141:283-312.
53. Rao A, Cha EM, Craig AM (2000) Mismatched appositions of presynaptic and postsynaptic components in isolated hippocampal neurons. J Neurosci 20:8344-8353.
54. A receptors in cat visual cortex. J Histochem Cytochem 41:685-692.
55. A receptors and glomerular geometry. Neuron 20:783-795.
56. Rubio ME, Soto F (2001) Distinct localization of P2X receptors at excitatory postsynaptic specializations. J Neurosci 21:641-653.
57. Sharma G, Vijayaraghavan S (2001) Nicotinic cholinergic signaling in hippocampal astrocytes involves calcium-induced calcium release from intracellular stores. Proc Natl Acad Sci USA 98:4148-4153.
58. Smit AB, Syed NI, Schaap D, van Minnen J, Klumperman J, Kits KS, Lodder H, van der Schors RC, van Elk R, Sorgedrager B, Brejc K, Sixma TK, Geraerts WP (2001) A glia-derived acetylcholine-binding protein that modulates synaptic transmission. Nature 411:261-268.
59. Smith GB, Olsen RW (1995) Functional domains of GABAA receptors. Trends Pharmacol Sci 16:162-168.
60. A receptors in the cerebellum of rat, cat, and monkey using monoclonal antibodies. J Neurosci 9:2197-2209.
61. A receptor is concentrated in synaptic junctions containing α1 and β2/3 subunits in hippocampus, cerebellum and globus pallidus. Neuropharmacology 35:1425-1444.
62. Ullian EM, Sapperstein SK, Christopherson KS, Barres BA (2001) Control of synapse number by glia. Science 291:657-661.
63. - channel complex. J Neurosci 8:615-622.
64. Whiting PJ, Bonnert TP, McKernan RM, Farrar S, Le Bourdelles B, Heavens RP, Smith DW, Hewson L, Rigby MR, Sirinathsinghji DJ, Thompson SA, Wafford KA (1999) Molecular and functional diversity of the expanding GABA-A receptor gene family. Ann NY Acad Sci 868:645-653.
65. A receptor mRNAs in bovine cerebellum - Localization of α2 mRNA in Bergmann glia layer. Neurosci Lett 106:7-12.
66. Ymer S, Draguhn A, Wisden W, Werner P, Keinanen K, Schofield PR, Sprengel R, Pritchett DB, Seeburg PH (1990) Structural and functional characterization of the gamma 1 subunit of GABAA/benzodiazepine receptors. EMBO J 9:3261-3267.
67. Zilberter Y, Kaiser KMM, Sakmann B (1999) Dendritic GABA release depresses excitatory transmission between layer 2/3 pyramidal and bitufted neurons in rat neocortex. Neuron 24:979-988.