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Distribution of two GABA receptor-like subunits in theDrosophila CNS

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Invertebrate Neuroscience

Abstract

Previously we have described the distribution of theRdl GABA receptor subunit in theDrosophila CNS. Knowing thatRdl can coassemble with LCCH3 (aDrosophila GABA receptor-like subunit showing sequence similarity to vertebrate Β subunit GABAA receptors) in baculovirus infected insect cells, we compared the localization of these two receptor subunits in order to identify any potential overlap in their spatial or temporal distribution. The two subunits show very different patterns of localization. Early in development LCCH3 is found in the majority of developing neuroblasts and later is localized to the cell bodies of the embryonic nerve cord and brain, and the neuronal cell bodies surrounding the adult brain. In contrast,Rdl receptor subunits appear confined to the neuropil in all developmental stages. These results have two important implications. Firstly, they suggest that although these two subunits can coassemble in heterologous expression systems, they may not be found in the same tissues in the nervous system. Secondly, production of LCCH3 before neuronal differentiation leads us to speculate on the role of that LCCH3 containing receptors in the developing nervous system.

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References

  • Aronstein, K. and ffrench-Constant, R. (1995) Immunocytochemistry of a novel GABA receptor subunitRdl inDrosophila melanogaster.Invertebr. Neurosci.,1, 25–31.

    Google Scholar 

  • Ashburner, M. (1989) Drosophila:a laboratory manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.

    Google Scholar 

  • Barnard, E. A., Darlison, M. G., and Seeburg, P. (1987) Molecular biology of the GABAA receptor: the receptor/channel superfamily.Trends Neurosci.,10, 502–509.

    Google Scholar 

  • Buchner, E., Bader, R., Buchner, S., Cox, J., Emson, P. C., Flory, E., Heizmann, C. W., Hemm, S., Hofbauer, A., and Oertel, W. H. (1988) Cell-specific immuno-probes for the brain of normal and mutantDrosophila melanogaster.Cell Tissue Res.,253, 357–370.

    Google Scholar 

  • Buckingham, S. D., Hosie, A. M., Roush, R. T. and Sattelle, D. B. (1994). Actions of agonists and convulsant antagonists on aDrosophila melanogaster GABA receptor (Rdl) homo-oligomer expressed inXenopus oocytes.Neurosci. Lett.,181, 137–140.

    Google Scholar 

  • Campos-Ortega, J. A. and Hartenstein, V. (1985)The embryonic development of Drosophila melanogaster. Berlin: Springer-Verlag.

    Google Scholar 

  • Chen, R., Belelli, D., Lambert, J. L., Peters, J. A., Reyes, A. and Lan, N. C. (1994) Cloning and functional expression of aDrosophila γ-aminohutyric acid receptor.Proc. Nat. Acad. Sci. USA,91, 6069–6073.

    Google Scholar 

  • Cherubini, E., Gaiarsa, J. L. and Yehezkel, B.-A. (1991) GABA: an excitatory transmitter in early postnatal life.Trends Neurosci.,14, 515–519.

    Google Scholar 

  • ffrench-Constant, R. H., Mortlock, D. P., Shaffer, C. D., MacIntyre, R. J. and Roush, R. T. (1991) Molecular cloning and transformation of cyclodiene resistance inDrosophila: an invertebrate GABAA receptor locus.Proc. Nat. Acad. Sci. USA,88, 7209–7213.

    Google Scholar 

  • ffrench-Constant, R. H. and Rocheleau, T. (1992)Drosophila cyclodiene resistance gene shows conserved genomic organization with vertebrate γ-aminobutyric acidA receptors.J. Neurochem.,59, 1562–1565.

    Google Scholar 

  • ffrench-Constant, R. H., Rocheleau, T. A., Steichen, J. C. and Chalmers, A. E. (1993) A point mutation in aDrosophila GABA receptor confers insecticide resistance.Nature,363, 449–451.

    Google Scholar 

  • Fritschy, J.-M., Paysan, J., Enna, A. and Mohler, H. (1994) Switch in the expression of rat GABAA-receptor subtypes during postnatal development: an immunohistochemical study.J. Neurosci.,14, 5302–5324.

    Google Scholar 

  • Harvey, R. J., Schmitt, B., Hermans-Borgmeyer, I., Gundelfinger, E. D., Betz, H. and Darlison, M. G. (1994) Sequence of aDrosophila ligand-gated ion-channel polypeptide with an unusual amino-terminal extracellular domain.J. Neurochemi.,62, 2480–2483.

    Google Scholar 

  • Henderson, J. E., Soderlund, D. M. and Knipple, D. C. (1993) Characterization of a putative γ-aminobutyric acid (GABA) receptor Β subunit gene fromDrosophila melanogaster.Biochem. Biophys. Res. Commun.,193, 474–482.

    Google Scholar 

  • Homberg, U., Kingan, T. G. and Hildebrand, J. G. (1987) Immunocytochemistry of GABA in the brain and suboesophageal ganglion ofManduca sexta.Cell Tissue Res.,248, 1–24.

    Google Scholar 

  • Lee, H.-J., Rocheleau, T., Zhang, H.-G., Jackson, M. B. and ffrench-Constant, R. H. (1993) Expression of aDrosophila GABA receptor in a baculovirus insect cell system: functional expression of insecticide susceptible and resistant GABA receptors from the cyclodiene resistance geneRdl.FEBS Lett.,335, 315–318.

    Google Scholar 

  • Michelson, H. B. and Wong, K. S. (1991) Excitatoty synaptic responses mediated by GABAA receptors in the hippocampus.Science,253, 1420–1422.

    Google Scholar 

  • Olsen, R. W. and Tobin, A. J. (1990) Molecular biology of GABAA receptors.FASEB J.,4(5), 1469–1480.

    Google Scholar 

  • Patel, N. H., Snow, P. M. and Goodman, C. S. (1987) Characterization and cloning of fasciclin III: a glycoprotein expressed on a subset of neurons and axon pathways inDrosophila.Cell,48, 975–988.

    Google Scholar 

  • Schofield, P. R., Darlison, M. G., Fujita, N., Burt, D. R., Stephenson, F. A., Rodriguez, H., Rhee, L. M., Ramachandran, J., Reale, V., Glencorse, T. A., Seeburg, P. H. and Barnard, E. A. (1987) Sequence and functional expression of the GABAA teceptor shows a ligand-gated receptor super-family.Nature,328, 221–227.

    Google Scholar 

  • Ymer, S., Draguhn, A., Wisden, W., Werner, P., Keinanen, K., Schofield, P. R., Sprengel, R., Pritchett, D. B. and Seeburg, P. H. (1990) Structural and functional characterization of the gamma 1 subunit of GABAA/benzodiazepine receptors.EMBO J.,9 (10), 3261–3267.

    Google Scholar 

  • Zhang, H.-G., Lee, H.-J., Rocheleau, T., ffrench-Constant, R. H. and Jackson, M. B. (1995) Subunit composition determines picrotoxin and bicuculline sensitivity ofDrosophila GABA receptors.Mol. Pharmacol.,48, 1–6.

    Google Scholar 

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Correspondence to R. Ffrench-Constant.

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Aronstein, K., Auld, V. & Ffrench-Constant, R. Distribution of two GABA receptor-like subunits in theDrosophila CNS. Invertebrate Neuroscience 2, 115–120 (1996). https://doi.org/10.1007/BF02214114

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