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A light and electron microscopic study of GAT-1-positive cells in the cerebral cortex of man and monkey

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Journal of Neurocytology

Abstract

Summary

Specimens of human cerebral cortex were obtained during neurosurgical operations and studied by immunocytochemistry and electron microscopy, using antibodies to the GABA transporter GAT-1. Cortical material from macaque monkeys was prepared similarly. Large numbers of GAT-1-positive non-pyramidal neurons were observed in layers I, II, V, and VI of the cortex. Electron microscopy also showed that the GAT-1-positive axon terminals formed symmetrical and not asymmetrical synapses, suggesting that they were the terminals of non-pyramidal neurons. Processes of cells in the walls of blood vessels were also labelled. We conclude that GAT-1 is present in cell bodies and axon terminals of non-pyramidal neurons, and a population of mural cells in blood vessels, in the primate cerebral cortex.

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References

  • Brodmann, K. (1909) Vergleichende Lokalisationslehre der Grosshirnrinde in ihren Prinzipien dargestellt auf Grund des Zellesbauses. Leipzig: Barth. Translated by L.J. Garey (1994) as Brodmann′s Localisation in the Cerebral Cortex. London: Smith-Gordon.

    Google Scholar 

  • Borden, L.A. (1996) GABA transporter heterogeneity: pharmacology and cellular localization. Neurochemistry International 29, 335-356.

    Google Scholar 

  • Brecha, N.C., Casini, G., Evans, C. & Rickman, D. (1993) Localization of GABA transporter (GAT-1) immunoreactivity in the rat nervous system. Society for Neuroscience Abstracts 19, 496.

    Google Scholar 

  • Clark, J.A., Deutch, A.Y., Gallipoli, P.Z. & Amara, S.G. (1992) Functional expression and CNS distribution of a beta-alanine-sensitive neuronal GABA transporter. Neuron 9, 337-48.

    Google Scholar 

  • Conti, F., Melone, M., de Biasi, S., Minelli, A., Brecha, N.C. & Ducatt, A. (1998) Neuronal and glial localization of GAT-1, a high affinity gamma-aminobutyric acid plasma membrane transporter, in human cerebral cortex: with a note on its distribution in monkey cortex. Journal of Comparative Neurology 396, 51-63.

    Google Scholar 

  • de Felipe, J. & Gonzalez-Albo, M.D. (1998) Chandelier cell axons are immunoreactive for GAT-1 in the human cortex. NeuroReport 9, 46-70.

    Google Scholar 

  • Durkin, M.M., Smith, K.E., Borden, L.A., Weinshank, R.L., Branchek, T.A. & Gustafson, E.L.(1995) Localization of messenger RNAs encoding three GABA transporters in rat brain: an in situ hybridization study. Molecular Brain Research 33, 7-21.

    Google Scholar 

  • Feldman, M.L. (1984) Morphology of the neocortical pyramidal neuron. In: Cerebral Cortex, Vol. 1: Cellular Components of the Cerebral Cortex (edited by Peter A. & Jones, E.G.), pp. 123-200. New York and London: Plenum Press.

    Google Scholar 

  • Guastella, J., Nelson, N., Nelson, H., Czyzyk, L., Keynan, S., Miedel, M.C., Davidson, N., Lester, H.A. & Kanner, B.I. (1990) Cloning and expression of a rat brain GABAtransporter. Science 249, 1303-6.

    Google Scholar 

  • Ikegaki, N., Saito, N., Hashima, M. & Tanaka, C. (1994) Production of specific antibodies against GABA transporter subtypes (GAT-1, GAT-2, GAT-3) and their application to immunocytochemistry. Molecular Brain Research 26, 47-54.

    Google Scholar 

  • Iversen, L.L. & Kelly, J.S. (1975) Uptake and metabolism of gamma-aminobutyric acid by neurones and glial cells. Biochemical Pharmacology 24, 933-8.

    Google Scholar 

  • Jones, E.G. & Hendry, S.H.C. (1984) Basket cells. In: Cerebral Cortex, Vol. 1 Cellular Components of the Cerebral Cortex (edited by Peters, A. & Jones, E.G.), pp. 309-36. New York and London: Plenum Press.

    Google Scholar 

  • Kanner, B.I., Keynan, S. & Radian, R. (1989) Structural and functional studies on the sodium-and chloride-coupled gamma-aminobutyric acid transporter: deglycosylation and limited proteolysis. Biochemistry 28, 3722-8.

    Google Scholar 

  • Kisvarday, Z.F., Gulyas, A., Beroukas, D., North, J.B., Chubb, I.W. & Somogyi, P. (1990) Synapses, axonal and dendritic patterns of GABA-immunoreactive neurons in human cerebral cortex. Brain 113, 793-812.

    Google Scholar 

  • Krogsgaard-Larsen, P., Falch, E., Larsson, O.M. & Schousboe, A. (1987) GABA uptake inhibitors: relevance to antiepileptic drug research. Epilepsy Research 1, 77-93.

    Google Scholar 

  • Kruger, L., Ghosdian, S. & Brecha, N.C. (1994) Distribution of GABA transporter (GAT-1) mRNA and immunoreactivity in the rat visual system. Society for Neuroscience Abstracts 20, 919.

    Google Scholar 

  • Larsson, O.M., Griffiths, R., Allen, I.C. & Schousboe A. (1986) Mutual inhibition kinetic analysis of gamma-aminobutyric acid, taurine, and beta-alanine high-affinity transport into neurons and astrocytes: evidence for similarity between the taurine and beta-alanine carriers in both cell types. Journal of Neurochemistry 47, 426-32.

    Google Scholar 

  • Liu, Q.R., Mandiyan, S., Nelson, H. & Nelson, N. (1992) A family of genes encoding neurotransmitter transporters. Proceedings of the National Academy of Science USA 89, 6639-43.

    Google Scholar 

  • Lopez-Corcuera, B., Liu, Q.R., Mandiyan, S., Nelson, H. & Nelson, N. (1992) Expression of a mouse brain cDNA encoding novel gamma-aminobutyric acid transporter. Journal of Biological Chemistry 267, 17491-3.

    Google Scholar 

  • Lund, J.S. (1984) Spiny stellate neurons. In: Cerebral Cortex, Vol. 1: Cellular Components of the Cerebral Cortex (edited by Peters, A. & Jones, E.G.), pp. 255-308. New York and London: Plenum Press.

    Google Scholar 

  • Mabjeesh, N.J., Frese, M., Rauen, T., Jeserich, G. & Kanner, B.I. (1992) Neuronal and glial gamma-aminobutyric acid transporters are distinct proteins. FEBS Letters 299, 99-102.

    Google Scholar 

  • Mager, S., Neave, J., Quick, M., Labarca, C., Davidson, M., Lester, H.A. (1993) Steady states, charge movements, and rates for a cloned GABA transporter expressed in Xenopus oocytes. Neuron 10, 177-188.

    Google Scholar 

  • Miller, J.W., Kleven, D.T., Domin, B.A. & Fremeau, R.T. (1997) Cloned sodium-(and chloride-) dependent high-affinity transporters for GABA, glycine, proline, betaine, taurine and creatine. In: Neurotransmitter Transporters. Structure, Function, and Regulation (edited by Reith, M.E.A.), pp. 101-50. Ottawa: Humana Press.

    Google Scholar 

  • 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. Journal of Neuroscience 15, 7734-46.

  • Nelson, H., Mandiyan, S. & Nelson, M. (1990) Cloning of the human brain GABA transporter. FEBS Letters 26, 181-4.

    Google Scholar 

  • Ong, W.Y. & Garey, L.J. (1991a) Ultrastructural characteristics of human adult and infant cerebral cortical neurons. Journal of Anatomy 175, 79-104.

    Google Scholar 

  • Ong, W.Y. & Garey, L.J. (1991b) Distribution of GABA and neuropeptides in the human cerebral cortex. Alight and electron microscopic study. Anatomy and Embryology 183, 397-413.

    Google Scholar 

  • Ong, W.Y. & Garey, L.J. (1996) A light and electron microscopic study of GluR4-positive cells in human cerebral cortex. Neuroscience Letters 210, 107-10.

    Google Scholar 

  • Ong, W.Y., Garey, L.J. & Reynolds, R. (1993) Distribution of glial fibrillary acidic protein and glutamine synthetase in human cerebral cortical astrocytes-a light and electron microscopic study. Journal of Neurocytology 22, 893-902.

    Google Scholar 

  • Ong, W.Y., Leong, S.K., Garey, L.J., Tan K.K. & Zhang, H.F. (1995) A light and electron microscopic study of HLA-DR positive cells in the human cerebral cortex and subcortical white matter. Journal of Brain Research 36, 553-63.

    Google Scholar 

  • Peters, A. (1984) Chandelier cells. In: Cerebral Cortex, Vol. 1: Cellular Components of the Cerebral Cortex (edited by Peters, A. & Jones, E.G.), pp. 361-80. New York and London: Plenum Press.

    Google Scholar 

  • Peters, A. (1987) Synaptic specificity in the cerebral cortex. In: Synaptic Function (edited by Edelman, G., Gall, E. & Cowan, M.), pp. 373-97. New York: Wiley.

    Google Scholar 

  • Radian, R., Bendahan, A. & Kanner, B.I. (1986) Purification and identification of the functional sodium and chloride-coupled gamma-aminobutyric acid transport glycoprotein from rat brain. Journal of Biological Chemistry 261, 15437-41.

    Google Scholar 

  • Ribak, C., Tong, W.M.Y. & Brecha, N.C. (1994) GABA plasma membrane transporters, GAT-1 and GAT-3, display different distributions in the rat hippocampus. Journal of Comparative Neurology 367, 595-606.

    Google Scholar 

  • Swan, M., Najlerahim, A., Watson R.E.B. & Bennett, J.P, (1994) Distribution of mRNA for the GABA transporter GAT-1 in the rat brain: evidence that GABA uptake is not limited to presynaptic neurons. Journal of Anatomy 185, 315-23.

    Google Scholar 

  • Yan X.X., Cariaga, W.A. & Ribak C.E. (1997) Immunoreactivity for GABA plasma membrane transporter, GAT-1, in the developing rat cerebral cortex: transient presence in the somata of neocortical and hippocampal neurons. Developmental Brain Research 99, 1-19.

    Google Scholar 

  • Zhang, H.F., Ong, W.Y., Leong, S.K. & Garey, L.J. (1997) Ultrastructural characteristics of blood vessels in the infant and adult human cerebral cortex. Histology and Histopathology 12, 85-97.

    Google Scholar 

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Authors and Affiliations

  1. Department of Anatomy, National University of Singapore, Singapore, 119260

    W.Y. Ong

  2. Department of Neurosurgery, Tan Tock Seng Hospital, Singapore, 308433

    T.T. Yeo

  3. Department of Anatomy and Histology and Sydney Institute for Biomedical Research, University of Sydney, NSW, 2006, Australia

    V.J. Balcar

  4. Division of Neuroscience, Imperial College School of Medicine, Charing Cross Hospital, London, W6 8RF, UK

    L.J. Garey

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  1. W.Y. Ong
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  2. T.T. Yeo
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  3. V.J. Balcar
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  4. L.J. Garey
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Ong, W., Yeo, T., Balcar, V. et al. A light and electron microscopic study of GAT-1-positive cells in the cerebral cortex of man and monkey. J Neurocytol 27, 719–730 (1998). https://doi.org/10.1023/A:1006946717065

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  • DOI: https://doi.org/10.1023/A:1006946717065

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