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ON cone bipolar cells in rat express the metabotropic receptor mGluR6

Published online by Cambridge University Press:  02 June 2009

Noga Vardi  and
Katsuko Morigiwa
Noga Vardi
Affiliation:
Department of Neuroscience, University of Pennsylvania, Philadelphia
Katsuko Morigiwa
Affiliation:
Department of Neuroscience, University of Pennsylvania, Philadelphia
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Abstract

The rod bipolar cell and about five types of ON cone bipolar cells depolarize to light by employing a sign-reversing metabotropic glutamate receptor. Glutamate responses are similar in both rod bipolar and cone bipolar cells, but the receptor mediating this response (mGluRo) was so far demonstrated only in rod bipolar cells. To test if ON cone bipolar cells also express mGluR6, we immunoreacted rat retina with an antibody specific for mGluRo, and studied the staining from serial ultrathin sections. We demonstrate that mGluR6 is indeed expressed in the dendritic tips of cone bipolar cells, the majority of which receive a ribbon synapse, and thus probably are ON cone bipolar cells. We further show that half of the dendritic tips contacting the cones stain for mGluR6, thus implying that all ON cone bipolar cell types express mGluR6.

Keywords

L-AP4Rod bipolarG-protein
Type
Short Communications
Information
Visual Neuroscience , Volume 14 , Issue 4 , July 1997 , pp. 789 - 794
Copyright
Copyright © Cambridge University Press 1997

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References

Akazawa, C., Ohishi, H., Nakajima, Y., Okamoto, N., Shigemoto, R., Nakanishi, S. & Mizuno, N. (1994). Expression of mRNAs of L-AP4-sensitive metabotropic glutamate receptors (mGluR4. mGluR6. mGluR7) in the rat retina. Neuroscience Letters 171, 52–54.CrossRefGoogle ScholarPubMed
Ashmore, J.F. & Falk, G. (1979). Transmission of visual signals to bipolar cells near absolute threshold. Vision Research 19, 419–423.CrossRefGoogle ScholarPubMed
Ashmore, J.F. & Falk, G. (1980). Responses of rod bipolar cells in the dark-adapted retina of the dogfish, Scyliorhinus canicula. Journal of Physiology 300, 115–150.CrossRefGoogle ScholarPubMed
Bolz, J., Wässle, H. & Thier, P. (1984). Pharmacological modulation of on and off ganglion cells in the cat retina. Neuroscience 12, 875–885.CrossRefGoogle Scholar
Calkins, D., Tsukamoto, Y. & Sterling, P. (1996). Foveal cones form basal as well as invaginating contacts with diffuse ON bipolar cells. Vision Research 36, 3373–3381.CrossRefGoogle ScholarPubMed
Cohen, E. & Sterling, P. (1990). Demonstration of cell types among cone bipolar neurons of cat retina. Philosophical Transactions of the Royal Society B (London) 330, 305–321.Google ScholarPubMed
Dacheux, R.F. & Raviola, E. (1986). The rod pathway in the rabbit retina: A depolarizing bipolar and amacrine cell. Journal of Neuroscience 6, 331–345.CrossRefGoogle ScholarPubMed
De La Villa, P., Kurahashi, T. & Kaneko, A. (1995). L-glutamate-induced responses and cGMP-activated channels in retinal bipolar cells dissociated from the cat. Journal of Neuroscience 15, 3571–3582.CrossRefGoogle ScholarPubMed
Dowling, J.E. & Boycott, B.B. (1966). Organization of the primate retina: Electron microscopy. Proceedings of the Royal Society B (London) 166, 80–111.Google ScholarPubMed
Duvoisin, R.M. & Vardi, N. (1996). The mGluR6 L-AP4 receptor is expressed in both rod and cone ON bipolar cells in primate retina. Society of Neuroscience 21 (Abstracts), p. 880.Google Scholar
Euler, T., Schneider, H. & Wässle, H. (1996). Glutamate responses of bipolar cells in a slice preparation of the rat retina. Journal of Neuroscience 16, 2934–2944.CrossRefGoogle Scholar
Euler, T. & Wässle, H. (1995). Immunocytochemical identification of cone bipolar cells in the rat retina. Journal of Comparative Neurology 361, 461–478.CrossRefGoogle ScholarPubMed
Hirano, A.A. & MacLeish, P.R. (1991). Glutamate and 2-amino-4-phosphonobutyrate evoke an increase in potassium conductance in retinal bipolar cells. Proceedings of the National Academy of Sciences of the U.S.A. 88, 805–809.CrossRefGoogle ScholarPubMed
Hopkins, J.M. & Boycott, B.B. (1995). Synapses between cones and diffuse bipolar cells of a primate retina. Journal of Neurocytology 24, 680–694.CrossRefGoogle ScholarPubMed
Hughes, T.E., Hermans-Borgmeyer, I. & Heinemann, S. (1992). Differential expression of glutamate receptor genes (GluR1-5) in the rat retina. Visual Neuroscience 8, 49–55.CrossRefGoogle ScholarPubMed
Kolb, H., Linberg, K.A. & Fisher, S.K. (1992). Neurons of the human retina: A Golgi study. Journal of Comparative Neurology 318, 147–187.CrossRefGoogle ScholarPubMed
Kolb, H. & Nelson, R. (1995). The organization of photoreceptor to bipolar synapses in the outer plexiform layer. In Neurobiology and Clinical Aspects of the Outer Retina, ed. Djamgoz, M.B.A., Archer, S.N. & Vallerga, S., pp. 273–296. London: Chapman & Hall.CrossRefGoogle Scholar
Kolb, H., Nelson, R. & Mariani, A. (1981). Amacrine cells, bipolar cells and ganglion cells of the cat retina: A Golgi study. Vision Research 21, 1081–1114.CrossRefGoogle ScholarPubMed
Lasansky, A. (1972). Cell junctions at the outer synaptic layer of the retina. Investigative Ophthalmology 11, 265–275.Google ScholarPubMed
Lasansky, A. (1973). Organization of the outer synaptic layer in the retina of the larval tiger salamander. Philosophical Transactions of the Royal Society B (London) 265, 471–489.Google ScholarPubMed
Lasater, E.M. (1988). Membrane currents of retinal bipolar cells in culture. Journal of Neurophysiology 60. 1460–1480.CrossRefGoogle ScholarPubMed
Massey, S.C., Redburn, D.A. & Crawford, M.L. (1983). The effects of 2-amino-4-phosphonobutyric acid (APB) on the ERG and ganglion cell discharge of rabbit retina. Vision Research 23. 1607–1613.CrossRefGoogle ScholarPubMed
Masu, M., Iwakabe, H., Tagawa, Y, Miyoshi, T., Yamashita, M., Fukuda, Y., Sasaki, H., Hiroi, K., Nakamura, Y. & Shigemoto, R. (1995). Specific deficit on the ON response in visual transmission by targeted disruption of the mGluRo gene. Cell 80, 757–765.CrossRefGoogle ScholarPubMed
McGuire, B.A., Stevens, J.K. & Sterling, P. (1984). Microcircuitry of bipolar cells in cat retina. Journal of Neuroscience 4, 2920–2938.CrossRefGoogle ScholarPubMed
Missotten, L. (1965). The Ultrastructure of the Human Retina. Brussels: Editions Arscia S.A.Google Scholar
Nakajima, Y., Iwakabe, H., Akazawa, C., Nawa, H., Shigemoto, R., Mizuno, N. & Nakanishi, S. (1993). Molecular characterization of a novel retinal metabotropic glutamate receptor mGluR6 with a high agonist selectivity for L-2-amino-4-phosphonobutyrate. Journal of Biological Chemistry 268, 11868–11873.CrossRefGoogle ScholarPubMed
Nawy, S. & Copenhagen, D.R. (1987). Multiple classes of glutamate receptor on depolarizing bipolar cells in retina. Nature 325, 56–58.CrossRefGoogle ScholarPubMed
Nawy, S. & Jahr, C.E. (1990). Suppression by glutamate of cGMP-activated conductance in retinal bipolar cells. Nature 346, 269–271.CrossRefGoogle ScholarPubMed
Nawy, S. & Jahr, C.E. (1991). cGMP-gated conductance in retinal bipolar cells is suppressed by the photoreceptor transmitter. Neuron 7, 677–683.CrossRefGoogle ScholarPubMed
Nelson, R. & Kolb, H. (1983). Synaptic patterns and response properties of bipolar and ganglion cells in the cat retina. Vision Research 23, 1183–1195.CrossRefGoogle ScholarPubMed
Nomura, A., Shigemoto, R., Nakamura, Y., Okamoto, N., Mizuno, N. & Nakanishi, S. (1994). Developmentally-regulated postsynaptic localization of a metabotropic glutamate-receptor in rat rod bipolar cells. Cell 77, 361–369.CrossRefGoogle ScholarPubMed
Peng, Y.-W., Blackstone, C.D., Huganir, R.L. & Yau, K.-W. (1995). Distribution of glutamate receptor subtypes in the vertebrate retina. Neuroscience 66, 483–497.CrossRefGoogle ScholarPubMed
Pin, J.-P. & Duvoisin, R.M. (1995). Neurotransmitter receptors I. The metabotropic glutamate receptors: Structure and functions. Neuropharmacology 34, 1–26.CrossRefGoogle ScholarPubMed
Rao-Mirotznik, R., Harkins, A., Buchsbaum, G. & Sterling, P. (1995). Mammalian rod terminal: Architecture of a binary synapse. Neuron 14, 561–569.CrossRefGoogle ScholarPubMed
Raviola, E. & Gilula, N.B. (1975). Intramembrane organization of specialized contacts in the outer plexiform layer of the retina. Journal of Cell Biology 65, 192–222.CrossRefGoogle ScholarPubMed
Saito, T., Kondo, H. & Toyoda, J.-I. (1981). Ionic mechanisms of two types of on-center bipolar cells in the carp retina. II. The responses to annular illumination. Journal of General Physiology 78, 569–589.CrossRefGoogle ScholarPubMed
Sassoè-Pognetto, M., Wässle, H. & Grünert, U. (1994). Glycinergic synapses in the rod pathway of the rat retina: Cone bipolar cells express the alpha-l subunit of the glycine receptor. Journal of Neuroscience 14, 5131–5146.CrossRefGoogle Scholar
Shiells, R.A. & Falk, G. (1990). Glutamate receptors of rod bipolar cells are linked to a cyclic GMP cascade via a G-protein. Proceedings of the Royal Society B (London) 242, 91–94.Google ScholarPubMed
Shiells, R.A. & Falk, G. (1992 a). The glutamate-receptor linked cGMP cascade of retinal on bipolar cells is pertussis and cholera sensitive. Proceedings of the Royal Society B (London) 247, 17–20.Google ScholarPubMed
Shiells, R.A. & Falk, G. (1992 b). Properties of the cGMP-activated channel of retinal on-bipolar cells. Proceedings of the Royal Society B (London) 247, 21–25.Google ScholarPubMed
Stell, W.K., Ishida, A.T. & Lightfoot, D.O. (1977). Structural basis for On- and Off-center responses in retinal bipolar cells. Science 198, 1269–1271.CrossRefGoogle ScholarPubMed
Sterling, P., Smith, R.G., Rao, R. & Vardi, N. (1995). Functional architecture of mammalian outer retina and bipolar cells. In Neurobiology and Clinical Aspects of the Outer Retina, ed. Archer, S., Djamgoz, M.B.A. & Vallerga, S., pp. 325–348. London, UK: Chapman & Hall, Ltd.CrossRefGoogle Scholar
Van Den Pol, A.N. (1988). Silver intensification of colloidal gold or horseradish peroxidase for dual ultrastructural immunocytochemistry. In Molecular Neuroanatomy, ed. Van Leeuwen, F.W., Buijs, R.M., Pool, C.W. & Pach, O., pp. 315–336. Elsevier Science.Google Scholar
Vardi, N. & Sterling, P. (1996). GO Might mediate the mGluR6 light response of ON bipolar cells. Society of Neuroscience 21 (Abstracts).Google Scholar