Developmental expression of γ-aminobutyric acid transporters (GAT-1 and GAT-3) in the rat cerebellum: Evidence for a transient presence of GAT-1 in Purkinje cells

Developmental Brain Research

Volumn 111, Issue 2, 1998, Pages 253-269

  Yan, Xiao Xin ^a   Ribak, Charles E ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Astrocyte; Dentate nucleus; Interneuron; Purkinje cell; Zonal organization

Indexed keywords

4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID TRANSPORTER PROTEIN GAT 1; 4 AMINOBUTYRIC ACID TRANSPORTER PROTEIN GAT 3; CARRIER PROTEIN; UNCLASSIFIED DRUG;

4 AMINOBUTYRIC ACID UPTAKE; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CEREBELLUM CORTEX; FEMALE; GOLGI COMPLEX; IMMUNOCYTOCHEMISTRY; MALE; NEUROPIL; NONHUMAN; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; PURKINJE CELL; RAT; STELLATE CELL;

ANIMALS; ANTIBODIES; ASTROCYTES; CARRIER PROTEINS; CEREBELLAR NUCLEI; FEMALE; GABA PLASMA MEMBRANE TRANSPORT PROTEINS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; INTERNEURONS; MALE; MEMBRANE PROTEINS; MEMBRANE TRANSPORT PROTEINS; ORGANIC ANION TRANSPORTERS; PURKINJE CELLS; RATS; RATS, SPRAGUE-DAWLEY;

ANIMALIA;

EID: 0032495111     PISSN: 01653806     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0165-3806(98)00144-8     Document Type: Article

References (72)

1. Albin R., Gilman S. Parasagittal zonation of GABA-B receptors in molecular layer of rat cerebellum. Eur. J. Pharmacol. 173:1989;113-114.
2. Attwell D., Barbour B., Szatkowski M. Nonvesicular release of neurotransmitter. Neuron. 11:1993;401-407.
3. +-stimulated release of GABA in the developing rat cortex. Dev. Brain Res. 10:1983;309-311.
4. Bernath S., Zigmond M.L. Calcium-independent GABA release from striatal slices: the role of calcium channels. Neuroscience. 36:1990;677-682.
5. Borden L.A., Smith K.E., Branchek T.A., Weieshank R.L. Molecular heterogeneity of the γ-aminobutyric acid (GABA) transport system. J. Biol. Chem. 267:1992;21098-21104.
6. Brecha N., Weigmenn C. Expression of GAT-1, a high-affinity gamma-aminobutyric acid plasma membrane transporter in the rat retina. Comp. Neurol. 345:1994;602-611.
7. 3H ]GABA in dispersed cell cultures of rat cerebellums: II. The development of GABAergic synapses Brain Res. 151:1978;19-29.
8. V. Chan-Palay, Cerebellar Dentate Nucleus: Organization, Cytology, and Neurotransmitters, Springer, Berlin, 1977.
9. Chan-Palay V., Nilaver G., Palay S.L., Beinfeld M.C., Zimmerman E.A., Wu J.Y., O'Donohue T.L. Chemical heterogeneity in cerebellar Purkinje cells: existence and coexistence of glutamic acid decarboxylase-like and motilin-like immunoreactivities. Proc. Natl. Acad. Sci. U.S.A. 79:1982;4221-4225.
10. Cherubini E., Gaiarsa J.L., Ben-Ari Y. GABA: an excitatory transmitter in early postnatal life. Trends Neurosci. 14:1991;515-519.
11. Clark J.A., Deutch A.Y., Gallipoli P.Z., Amara S.G. Functional expression and CNS distribution of a β-alanine sensitive neuronal GABA transporter. Neuron. 9:1992;337-348.
12. Coyle J.T., Enna S.J. Neurochemical aspects of the ontogenesis of GABAergic neurons in the rat brain. Brain Res. 111:1976;119-133.
13. Dingledine R., Korn S.J. γ-Aminobutyric acid uptake and the termination of inhibitory synaptic potentials in the rat hippocampal slice. J. Physiol. (London). 366:1985;387-409.
14. Drejer J., Meier E., Schousboe A. Novel neuron-related regulatory mechanisms for astrocytic glutamate and GABA high affinity uptake. Neurosci. Lett. 37:1983;301-306.
15. Durkin M.M., Smith K.E., Borden L.A., Weinshank P.L., Branchek T.A., Gustafson E.L. Localization of messenger RNAs encoding three GABA transporters in the brain: an in situ hybridization study. Mol. Brain Res. 33:1995;7-21.
16. J.C. Eccles, M. Ito, J. Szentágothai, The Cerebellum as a Neuronal Machine, Springer, Berlin, 1967.
17. Esclapez M., Tillakaratne N.J.K., Tobin A.J., Houser C.R. Comparative localization of mRNAs encoding two forms of glutamic acid decarboxylase with nonradioactive in situ hybridization methods. J. Comp. Neurol. 331:1993;339-362.
18. Esclapez M., Tillakaratne N.J., Kaufman D.L., Tobin A.J., Houser C.R. Comparative localization of two forms of glutamic acid decarboxylase and their mRNAs in rat brain supports the concept of functional differences between the forms. J. Neurosci. 14:1994;1834-1855.
19. Evans J.E., Frostholm A., Rotter A. Embryonic and postnatal expression of four gamma-aminobutyric acid transporter mRNAs in the mouse brain and leptomeninges. J. Comp. Neurol. 376:1996;431-446.
20. Gabbott P.L., Somogyi J., Stewart M.G., Hamori J. GABA-immunoreactive neurons in the rat cerebellum: a light and electron microscope study. J. Comp. Neurol. 251:1986;474-490.
21. Greif K.F., Erlander M.G., Tillakaratne N.J., Tobin A.J. Postnatal expression of glutamate decarboxylases in developing rat cerebellum. Neurochem. Res. 16:1991;235-342.
22. Guastella J., Brecha N., Nelson H., Czyzyx L., Keynan S., Miedel M.C., Davidson N., Lester H.A., Kanner B.I. Cloning and expression of a rat brain GABA transporter. Science. 249:1990;1303-1306.
23. 3H ]γ-aminobutyric acid: visualization of developing γ-aminobutyric acid-utilizing neurons in vitro and in vivo J. Neurosci. 4:1984;1343-1353.
24. Hawkes R. An anatomical model of cerebellar modules. Prog. Brain Res. 114:1997;39-52.
25. Hawkes R., Gravel C. The modular cerebellum. Prog. Neurobiol. 36:1991;309-327.
26. Herrup K., Kuemerle B. The compartmentalization of the cerebellum. Annu. Rev. Neurosci. 20:1997;61-90.
27. 3H ]GABA in rat cerebellar cortex: an autoradiographic study Brain Res. 22:1970;391-396.
28. Honda S.M., Yamamoto M., Saito N. Immunocytochemical localization of three subtypes of GABA transporter in rat retina. Mol. Brain Res. 33:1995;319-325.
29. Ikegaki N., Saito N., Hashima M., Tanaka C. Production of specific antibodies against GABA transporter subtypes (GAT-1, GAT-2, GAT-3) and their application to immunocytochemistry. Mol. Brain Res. 26:1994;47-54.
30. Itouji A., Sakai N., Hashima M., Saito N. Neuronal and glial localization of two GABA transporters (GAT-1 and GAT-3) in the rat cerebellum. Mol. Brain Res. 37:1996;309-316.
31. Iversen L.L., Kelly J.S. Uptake and metabolism of γ-aminobutyric acid by neurons and glial cells. Biochem. Pharmacol. 24:1975;933-938.
32. Johnson J., Chen T.K., Rickman D.W., Evans C., Brecha N.C. Multiple γ-aminobutyric acid plasma membrane transporter (GAT-1, GAT-2, GAT-3) in the rat retina. J. Comp. Neurol. 375:1996;212-224.
33. Kanner B.I., Shuldiner S. Mechanism of transport and storage of neurotransmitters. CRC Crit. Rev. Biochem. 22:1987;1-39.
34. 3H ]GABA into single folia of the cerebellum Cold Spring Harb. Symp. Quant. Biol. 40:1970;93-106.
35. Kontro P., Oja S.S. Release of taurine and GABA from cerebellar slices from developing and adult mice. Neuroscience. 29:1989;413-423.
36. 3H ]GABA and differentiation of stellate neurons in cultures of dissociated postnatal rat cerebellum Brain Res. 69:1974;235-254.
37. Levi G., Raiteri M. Carrier-mediated release of neurotransmitters. Trends Neurosci. 16:1993;415-418.
38. Liu Q.-R., Lopez-Caarcuera B., Mandiyan S., Nelson H., Nelson N. Molecular characterization of four pharmacological distinct γ-aminobutyric acid transporters in the mouse brain. J. Biol. Chem. 268:1993;2106-2112.
39. Lopez-Corcuera B., Liu Q.-R., Mandiyan H., Helson H., Helson N. Expression of a mouse brain cDNA encoding novel γ-aminobutyric acid transporter. J. Biol. Chem. 267:1992;17491-17493.
40. Miale I.L., Sidman R.L. An autoradiographic analysis of histogenesis in mouse cerebellum. Exp. Neurol. 4:1961;277-296.
41. Meier E., Jorgensen O.S. Gamma-aminobutyric acid affects the developmental expression of neuron-associated proteins in cerebellar granule cell cultures. J. Neurochem. 46:1986;1256-1262.
42. A receptor complex in an inhibitory synaptic circuit in the rat cerebellum. Dev. Brain Res. 55:1990;73-86.
43. Minelli A., Brecha N.C., Karschin C., DeBiasi S., Conti F. GAT-1, a high-affinity GABA plasma membrane transporter, is localized to neurons and astroglia in the cerebral cortex. J. Neurosci. 15:1995;7734-7748.
44. Minelli A., DeBiasi S., Brecha N.C., Zuccarello L.V., Conti F. GAT-3, a high-affinity GABA plasma membrane transporter, is localized to astrocytic processes, and it is not confined to the vicinity of GABAergic synapses in the cerebral cortex. J. Neurosci. 16:1996;6255-6264.
45. Morara S., Brecha N.C., Marcotti W., Provini L., Rosina A. Neuronal and glial localization of the GABA transporter GAT-1 in the cerebellar cortex. Neuroreport. 7:1996;2993-2996.
46. Obata K. Excitatory and trophic action of GABA and related substances in newborn mice and organotypic cerebellar culture. Dev. Neurosci. 19:1997;117-119.
47. Obata K., Takeda K., Shinozaki H. Further study in pharmacological properties of cerebellar-induced inhibition of Deiter's neurons. Exp. Brain Res. 11:1970;327-342.
48. Oertel W.H., Schmechel D.E., Mugnaini E., Tappaz M.L., Kopin I.J. Immunocytochemical localization of glutamate decarboxylase in rat cerebellum with a new antiserum. Neuroscience. 7:1981;2715-2735.
49. O'Hearn E., Long D.B., Molliver M.E. Ibogaine induces glial activation in parasagittal zones of the cerebellum. Neuroreport. 4:1993;299-302.
50. S.L. Palay, V. Chan-Palay, Cerebellar Cortex: Cytology and Organization. Springer-Verlag, New York, 1974.
51. Plotkin M.D., Snyder E.Y., Hebert S.C., Delpire E. Expression of the Na-K-2Cl cotransporter is developmentally regulated in postnatal rat brains: a possible mechanism underlying GABA's excitatory role in immature brain. J. Neurobiol. 33:1997;781-795.
52. Radian R., Ottersen O.P., Storm-Mathisen J., Castel M., Kanner B.I. Immunocytochemical localization of the GABA transporter in rat brain. J. Neurosci. 10:1990;1319-1330.
53. Rattray M., Priestley J.V. Differential expression of GABA transporter-1 messenger RNA in subpopulations of GABA neurons. Neurosci. Lett. 156:1993;163-166.
54. Ribak C.E., Tong W.M.Y., Brecha N.C. Astrocytic processes compensate for the apparent lack of GABA transporters in the axon terminal of cerebellar Purkinje cells. Anat. Embryol. 194:1996;379-390.
55. Ribak C.E., Tong W.M.Y., Brecha N.C. The GABA plasma membrane transporters, GAT-1 and GAT-3, display different distributions in the rat hippocampus. J. Comp. Neurol. 367:1996;595-606.
56. Ribak C.E., Vaughn J.E., Saito K. Immunocytochemical localization of glutamic acid decarboxylase in neuronal somata following colchicine inhibition of axonal transport. Brain Res. 140:1978;315-322.
57. Saito K., Barber R., Wu J.Y., Matuda T., Roberts E., Vaughn J.E. Immunohistochemical localization of glutamate decarboxylase in rat cerebellum. Proc. Natl. Acad. Sci. U.S.A. 71:1974;269-273.
58. 3H ]GABA by stellate cells in rat cerebellar cortex in vivo Brain Res. 42:1972;503-507.
59. 3H ]GABA in tissue culture of rat cerebellum using electron microscope radioautography Brain Res. 45:1972;302-308.
60. A receptors. Science. 269:1995;977-981.
61. Swan M., Najlerahim A., Watson R.E.B., Bennett J.P. Distribution of mRNA for the GABA transporter GAT-1 in the rat brain: evidence that GABA uptake is not limited to presynaptic neurons. J. Anat. 185:1994;315-323.
62. 3H ]GABA (γ-aminobutyric acid) injected into the cat dentate nucleus Exp. Neurol. 70:1980;525-538.
63. Wong P.T.-H., McGeer E.G. Postnatal changes of GABAergic and glutaminergic parameters. Dev. Brain Res. 1:1981;519-529.
64. Wuenschell C.W., Fisher D.L., Kaufman D.L., Tobin A.J. In situ hybridization to localize mRNA encoding the neurotransmitter synthetic enzyme glutamate decarboxylase in mouse cerebellum. Proc. Natl. Acad. Sci. U.S.A. 83:1986;6193-6197.
65. Xia Y., Poosch M.S., Whitty C.J., Kapatos G., Bannon M.J. GABA transporter mRNA: in vitro expression and quantitation in neonatal rat and postmortem human brain. Neurochem. Int. 22:1993;263-270.
66. Yan X.X., Cariaga W.A., Ribak C.E. Immunoreactivity for a GABA plasma membrane transporter, GAT-1, in developing rat cerebral cortex: transient presence in the somata of neocortical and hippocampal interneurons. Dev. Brain Res. 99:1997;1-19.
67. Yan X.X., Garey L.J. Calretinin immunoreactivity in the monkey and cat cerebellum: cellular localization and modular distribution. J. Brain Res. 37:1996;409-419.
68. Yan X.X., Garey L.J. Complementary distributions of calbindin, parvalbumin and calretinin in the cerebellar vermis of the adult cat. J. Brain Res. 39:1998;9-14.
69. Yan X.X., Garey L.J., Jen L.S. Spatial periodicity of NADPH-diaphorase and synaptophysin, but not SNAP-25, reactivity in the monkey cerebellar cortex. Brain Res. 669:1995;285-290.
70. Yan X.X., Jen L.S., Garey L.J. Parasagittal patches in the granular layer of the developing and adult rat cerebellum as demonstrated by NADPH-diaphorase histochemistry. Neuroreport. 4:1993;1227-1230.
71. Yan X.X., Ribak C.E. Increased expression of GABA membrane transporters, GAT-1 and GAT-3, in deafferented superior colliculus of the rat. Brain Res. 783:1998;63-76.
72. Yang C.Y., Brecha N.C., Tsao E. Immunocytochemical localization of γ-aminobutyric acid plasma membrane transporters in the tiger salamander retina. J. Comp. Neurol. 389:1997;117-126.