Hostname: page-component-586b7cd67f-vdxz6 Total loading time: 0 Render date: 2024-11-23T04:04:25.708Z Has data issue: false hasContentIssue false
  • English
  • Français

Correlation between a bicuculline-resistant response to GABA and GABAA receptor ρ1 subunit expression in single rat retinal bipolar cells

Published online by Cambridge University Press:  02 June 2009

Hermes H. Yeh ,
Elena V. Grigorenko  and
Margaret L. Veruki
Hermes H. Yeh
Affiliation:
Department of Physiology and Pharmacology, Bowman Gray School of Medicine, Winston-Salem
Elena V. Grigorenko
Affiliation:
Department of Physiology and Pharmacology, Bowman Gray School of Medicine, Winston-Salem
Margaret L. Veruki
Affiliation:
Department of Physiology and Pharmacology, Bowman Gray School of Medicine, Winston-Salem
Get access Rights & Permissions [Opens in a new window]

Abstract

Using patch-clamp recording in combination with reverse transcriptase-polymerase chain reaction (RT-PCR), we show in individual bipolar cells acutely dissociated from the adult rat retina a correlation between the expression of the GABAA receptor ρ1 subunit mRNA and a bicuculline-resistant, diazepam-insensitive component of the GABA-activated whole-cell current response. This “GABAC-like” response, contributing to approximately 42% of the GABA-activated whole-cell current and displaying variable sensitivity to picrotoxin, was found in bipolar cells but not in any of the ganglion cells examined. Expression profiling of GABAA receptor subunit mRNAs in individual electrophysiologically tested retinal neurons revealed that, while both bipolar cells and ganglion cells may express numerous GABAA receptor subunit isoforms, including that of ρ2, the expression of the ρ1 subunit was strictly limited to bipolar cells. We propose a possible link between the presence of a receptor with GABAC-like pharmacological profile and the expression of the retina-specific ρ1 subunit isoform. The results presented in this study constitute the first direct demonstration of such a correlation at the single-cell level.

Keywords

Rat retinaBipolar cellGanglion cellBicuculline-resistant GABA responseGABAA receptor ρ subunitCombined patch clamp/single-cell RT-PCR
Type
Research Articles
Information
Visual Neuroscience , Volume 13 , Issue 2 , March 1996 , pp. 283 - 292
Copyright
Copyright © Cambridge University Press 1996

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Akaike, N., Hattori, K., Oomura, Y. & Carpenter, D. (1985). Bicuculline and picrotoxin block γ-aminobutyric acid-gated Cl− conductance by different mechanisms. Experentia 41, 70–71.CrossRefGoogle ScholarPubMed
Brecha, N.C. (1992). Expression of GABAA receptors in the vertebrate retina. Progress in Brain Research, 90, 3–27.CrossRefGoogle ScholarPubMed
Cutting, G.R., Lu, L., O'Hara, B.F., Kasch, L.M., Montrose-Rafizadeh, C., Gonovan, D.M., Shimada, S., Antonarkakis, S.E., Guggino, W.B., Uhl, G.R. & Kazazian, H.H. (1991). Cloning of the γ-aminobutyric acid ρ1 cDNA: A GABA receptor subunit highly expressed in the retina. Proceedings of the National Academy of Sciences of the U.S.A. 88, 2673–2677.CrossRefGoogle Scholar
Cutting, G.R., Curristin, S., Zoghbi, H., O'Hara, B., Seldin, M.F. & Uhl, G.R. (1992). Identification of a putative γ-aminobutyric acid (GABA) receptor subunit rho2 cDNA and colocalization of the genes encoding rho2 (GABRR2) and rho1 (GABRR1) to human chromosome 6q14–q21 and mouse chromosome 4. Genomics 12, 801–806.CrossRefGoogle ScholarPubMed
Cutting, G.R., Wang, T-L. & Giggino, W.G. (1993). Retina-specific GABA subunits rho1 and rho2 expressed in Xenopus laevis oocytes form receptors with distinct pharmacological and physiological properties. Investigative Ophthalmology and Visual Science 34, 1380.Google Scholar
Dolphin, A.C. & Scott, R.H. (1987). Calcium channel currents and their inhibition ny (−)-baclofen in rat sensory neurones: modulation by guanine nucleotides. Journal of Physiology (London) 386, 1–17.CrossRefGoogle Scholar
Dutar, P. & Nicoll, R.A. (1988). A physiological role for GABAB receptors in the central nervous system. Nature 332, 156–158.CrossRefGoogle ScholarPubMed
Enz, R., BrandstÄTter, J.H., Hartveit, E., WÄSsle, H. & Bormann, J. (1995). Expression of GABA receptor ρ1 and ρ2 subunit in the retina and brain of the rat. Proceedings of the 23rd Göttingen Neurobiology Conference, Vol. 2, #637.0Google Scholar
Feigenspan, A., WÄSsle, H. & Bormann, J. (1993). Pharmacology of GABA receptor Cl− channels in rat retinal bipolar cells. Nature 361, 159–162.CrossRefGoogle ScholarPubMed
Feigenspan, A. & Bormann, J. (1994). Differential pharmacology of GABAA and GABAC receptors on rat retinal bipolar cells. European Journal of Pharmacology 288, 97–104.CrossRefGoogle ScholarPubMed
Greferath, U., MÜLler, F., WÄSsle, H., Shivers, B. & Seeburg, P. (1993). Localization of GABAA receptors in the rat retina. Visual Neuroscience 10, 551–561.CrossRefGoogle ScholarPubMed
Grigorenko, E.V. & Yeh, H.H. (1994). Expression profiling of GABAA receptor β-subunits in the rat retina. Visual Neuroscience 11, 379–387.CrossRefGoogle ScholarPubMed
Hales, T.G. & Tyndale, R.F (1994). Few cell lines with GABAA mRNAs have functional receptors. Journal of Neuroscience 14, 5429–5436.CrossRefGoogle ScholarPubMed
Hamill, O.P., Marty, A., Neher, E., Sakmann, B. & Sigworth, F.J. (1981). Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflügers Archives 391, 85–100.CrossRefGoogle ScholarPubMed
Holz, G.G., Rane, S.G. & Dunlap, K. (1986). GTP-binding proteins mediate transmitter inhibition of voltage-dependent calcium channels. Nature 319, 670–672.CrossRefGoogle ScholarPubMed
Hughes, T.E., GrÜNert, U. & Karten, H.J. (1991). GABAA receptors in the retina of the cat: An immunohistochemical study of whole-mounts, sections, and dissociated cells. Visual Neuroscience 6, 229–238.CrossRefGoogle Scholar
Johnston, G.A.R. (1986). Multiplicity of GABA receptors. In Benzodiazepine/GABA Receptors and Chloride Channels. Receptor Biochemistry and Methodology, ed. Olsen, R.W. & Venter, J.C., pp. 57–71. New York: Alan R. Liss.Google Scholar
Karschin, A. & WÄSsle, H. (1990). Voltage- and transmitter-gated currents in isolated rod bipolar cells of the rat retina. Journal of Neurophysiology 63, 860–876.CrossRefGoogle ScholarPubMed
Kusama, T., Wang, T-L., Guggino, W.B., Cutting, G.R. & Uhl, G.R. (1993). GABA ρ2 receptor pharmacological profile: GABA recognition site similarities to ρ 1. European Journal of Pharmacology 245, 83–84.CrossRefGoogle Scholar
Lambolez, B., Audinat, E., Bochet, P., Crepel, F. & Rossier, J. (1992). AMPA receptor subunits expressed by single Purkinje cells. Neuron 9, 247–258.CrossRefGoogle ScholarPubMed
Lukasiewicz, P.D., Maple, B.R. & Werblin, F.S. (1994). A novel GABA receptor on bipolar cell terminals in the tiger salamander retina. Journal of Neuroscience 14, 1202–1212.CrossRefGoogle ScholarPubMed
Lukasiewicz, P.D. & Werblin, F.S. (1994). A novel GABA receptor modulates synaptic transmission from bipolar to ganglion and amacrine cells in the tiger salamander retina. Journal of Neuroscience 14, 1213–1223.CrossRefGoogle ScholarPubMed
Macdonald, R.L. & Barker, J.L. (1979). Enhancement of GABA-mediated postsynaptic inhibition in cultured mammalian neurons: A common mode of anticonvulsant action. Brain Research 167, 323–336.CrossRefGoogle ScholarPubMed
Matthews, G., Ayoub, G.S. & Heidelberg, R. (1994). Presynaptic inhibition by GABA is mediated via two distinct GABA receptors with novel pharmacology. Journal of Neuroscience 14, 1079–1090.CrossRefGoogle ScholarPubMed
Nelson, R. & Kolb, H. (1983). Synaptic patterns and response properties of bipolar cells and ganglion cells in the cat retina. Vision Research 23, 1183–1195.CrossRefGoogle ScholarPubMed
Qian, H. & Dowling, J.E. (1993). Novel GABA responses from rod-driven retinal horizontal cells. Nature 361, 162–164.CrossRefGoogle ScholarPubMed
Sambrook, J.E., Fritsch, E.F. & Maniatis, T. (1989). Molecular Cloning. A Laboratory Manual. Michigan: Cold Spring Harbor Laboratory Press.Google Scholar
Shimada, S., Cutting, G. & Uhl, G.R. (1992). γ-aminobutyric acid A or C receptor? γ-aminobutyric acid ρ1 receptor RNA induces bicuculline-, barbiturate, and benzodiazepine-insensitive γ-aminobutyric acid responses in Xenopus oocytes. Molecular Pharmacology 41, 683–687.Google ScholarPubMed
Sivilotti, L. & Nistri, A. (1989). Pharmacology of a novel effect of γ-aminobutyric acid on the frog optic tectum in vitro. European Journal of Pharmacology 164, 205–212.CrossRefGoogle ScholarPubMed
Sivilotti, L. & Nistri, A. (1991). GABA receptor mechanisms in the central nervous system. Progress in Neurobiology 36, 35–92.CrossRefGoogle ScholarPubMed
Stelzer, A., Kay, A.R. & Wong, R.S.K. (1988). GABAA receptor function in hippocampal cells is maintained by phosphorylation factors. Science 241, 339–341.CrossRefGoogle ScholarPubMed
Study, R.E. & Barker, J.L. (1981). Diazepam and (−) pentobarbital: Fluctuation analysis reveals different mechanisms for potentiation of γ-aminobutyric acid responses in cultured central neurons. Proceedings of the National Academy of Sciences of the U.S.A. 83, 4071–4075.Google Scholar
Tauck, D.L., Frosch, M.P. & Lipton, S.A. (1988). Characterization of GABA- and glycine-induced currents in solitary ganglion cells. Neuroscience 27, 193–203.CrossRefGoogle Scholar
Twyman, R.E., Rogers, C.J. & Macdonald, R.L. (1989). Differential regulation of γ-aminobutyric acid receptor channels by diazepam and phenobarbital Annals Neurology 25, 213–220.CrossRefGoogle ScholarPubMed
Tyndale, R.F., Hales, T.G. & Tobin, A.J. (1994). Distinctive patterns of GABAA receptor subunit mRNAs in 13 cell lines. Journal of Neuroscience 14, 5417–5428.CrossRefGoogle ScholarPubMed
Veruki, M.L. & Yeh, H.H. (1992). Vasoactive intestinal polypeptide modulates GABAA receptor function in bipolar cells and ganglion cells of the rat retina. Journal of Neurophysiology 67, 791–797.CrossRefGoogle ScholarPubMed
Veruki, M.L. & Yeh, H.H. (1994). Vasoactive intestinal polypeptide modulates GABAA receptor function through activation of cyclic AMP. Visual Neuroscience 11, 899–908.CrossRefGoogle ScholarPubMed
Woodward, R.M., Polenzani, L. & Miledi, R. (1993). Characterization of bicuculline/baclofen-insensitive (ρ-like) γ-aminobutyric acid receptors expressed in Xenopus oocytes 11. Pharmacology of γ-aminobutyric acidA and γ-aminobutyric acidB receptor agonists and antagonists. Molecular Pharmacology 43, 609–625.Google Scholar
Yeh, H.H., Lee, M.B. & Cheun, J.E. (1990). Properties of GABA-activated whole-cell currents in bipolar cells of the rat retina. Visual Neuroscience 4, 349–357.CrossRefGoogle ScholarPubMed
Zhang, D. & Yeh, H.H. (1991). Protein kinase C-like immunoreactivity in rod bipolar cells of the rat retina: A developmental study. Visual Neuroscience 6, 429–437.CrossRefGoogle ScholarPubMed