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Voltage-dependent sodium channel alpha subunit immunoreactivity is expressed by distinct cell types of the cat and monkey retina

Published online by Cambridge University Press:  02 June 2009

José Javier Miguel-Hidalgo
Affiliation:
Department of Psychology and the Center for Neuroscience, University of California, Davis
Cara J. Snider
Affiliation:
Department of Psychology and the Center for Neuroscience, University of California, Davis
Kimon J. Angelides
Affiliation:
Department of Cell Biology, Baylor College of Medicine, One Baylor Plaza, Houston
Leo M. Chalupa
Affiliation:
Department of Psychology and the Center for Neuroscience, University of California, Davis

Abstract

Polyclonal (7493 and 7317) and monoclonal (mAb3) antibodies, generated to the α subunit of the voltage-gated sodium channel (αNaCh), were employed to assess the cell types containing αNaCh-like immunoreactivity in the mature cat and monkey retina. Immunoblot analyses of retinal proteins in the cat revealed that the polyclonal and monoclonal antibodies we employed labeled a band in the 260–kDa region which corresponds to the molecular mass of the α subunit of the NaCh. In both the cat and monkey, these antibodies immunolabeled several distinct types of retinal cells. With the polyclonal antibodies immunoreactivity was observed in ganglion cells and their intraretinal axons, in horizontal cells, and unexpectedly, in cones. In addition, in both species, a limited number of heavily labeled profiles, presumed to be bipolar cells, were seen in the inner nuclear layer. In cat and monkey the monoclonal antibody labeled axons in the fiber layer, ganglion cell somata, and a continuous band of immunoreactive cell bodies (presumed bipolar cells) situated in the outer half of the inner nuclear layer. By immunolabeling isolated cells dissociated from the cat retina, it was possible to demonstrate unequivocally that a population of bipolar cells was labeled by the monoclonal and the polyclonal antibodies we employed. The differences in the labeling observed with the monoclonal antibody as compared to the polyclonal antibodies were interpreted as reflecting the presence of different α-subunit subtypes in the mammalian retina. Collectively, our findings suggest that αNaCh-like proteins are expressed by a more diverse population of retinal cells than expected on the basis of previous physiological and immunohistochemical studies.

Type
Research Articles
Copyright
Copyright © Cambridge University Press 1994

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References

Attwell, D. (1986). On channels and signal processing in the outer retina. Quarterly Journal of Experimental Physiology 71, 497536.Google Scholar
Attwell, D., Werblin, F.S. & Wilson, M. (1982). The properties of single cones isolated from tiger salamander retina. Journal of Physiology (London) 328, 259283.CrossRefGoogle ScholarPubMed
Auld, V.J., Goldin, A.L., Krafte, D.S., Marshall, J., Dunn, J.M., Catterall, W.A., Lester, H.A., Davidson, N. & Dunn, R.J. (1988). A rat brain Na+ channel α subunit with novel gating properties. Neuron 1, 449461.CrossRefGoogle ScholarPubMed
Barhanin, J., Pauron, D., Lombet, A., Norman, R.I., Vijverberg, H.P.M., Giglio, J.R. & Lazdunski, M. (1983). Electrophysiological characterization, solubilization, and purification of the Tityus g toxin receptor associated with the gating component of the Na+ channel from rat brain. EMBO Journal 2, 915920.CrossRefGoogle Scholar
Beckh, S., Noda, M., LÜBbert, H. & Numa, S. (1989). Differential regulation of three sodium channel messenger RNAs in the rat central nervous system during development. EMBO Journal 8, 36113616.CrossRefGoogle ScholarPubMed
Black, J.A., Waxman, S.G., Friedman, B., Elmer, L.W. & Angelides, K.J. (1989 a). Sodium channels in astrocytes of rat optic nerve in situ: Immuno-electron microscopic studies. Glia 2, 353369.Google Scholar
Black, J.A., Friedman, B., Waxman, S.G., Elmer, L.W. & Angelides, K.J. (1989 b). Immunoultrastructural localization of sodium channels at nodes of Ranvier in rat optic nerve. Proceedings of the Royal Society B (London) 238, 3951.Google ScholarPubMed
Catterall, W.A. (1988). Structure and function of voltage-sensitive ion channels. Science 242, 5061.CrossRefGoogle ScholarPubMed
Chalupa, L.M., Skaliora, I. & Scobey, R.P. (1993). Responses of isolated cat retinal ganglion cells to injected currents during development. In Progress in Brain Research: The Visually Responsive Neuron—From Basic Neurophysiology to Behavior, ed. Molotchnikoff, S. & Hicks, T.P., pp. 2531. Amsterdam: Elsevier Science Publishers.Google Scholar
Devor, M., Govrin-Lipmann, R. & Angelides, K.J. (1993). Na+ channel immunolocalization in peripheral mammalian axons and changes following nerve injury and neuroma formation. Journal of Neuroscience 13, 19761992.CrossRefGoogle ScholarPubMed
Dowling, J.E. (1987). The Retina an Approachable Part of the Brain. Cambridge: Belknap Harvard.Google Scholar
Eliasof, S., Barnes, S. & Werblin, F. (1987). The interaction of ionic currents mediating single spike activity in retinal amacrine cells of the tiger salamander. Journal of Neuroscience 7, 35123524.Google Scholar
Elmer, L.W., O’Brien, B., Nutter, T.J. & Angelides, K.J. (1985). Physicochemical characterization of the α peptide of the Na channel protein from rat brain. Biochemistry 24, 78967908.Google Scholar
Elmer, L.W., Black, J.A., Waxman, S.G. & Angelides, K.J. (1990). The voltage-dependent sodium channel in mammalian CNS and PNS: Antibody characterization and immunocytochemical localization. Brain Research 532, 222231.CrossRefGoogle ScholarPubMed
Elmer, L.W. (1988). Mammalian sodium channel physicochemical characterization and immunocytochemical localization and interaction with the neuronal cytoskeleton as a mechanism of restricted distribution. Ph.D. Dissertation, University Microfilms. Baylor College of Medicine: Houston, Texas.Google Scholar
Frelin, C., Vigne, P. & Lazdunski, M. (1983). Na channels with high and low affinity tetrodotoxin binding sites in the mammalian skeletal muscle. Journal of Biological Chemistry 258, 72567259.Google Scholar
Fuortes, M.G.F., Schwartz, E.A. & Simon, E.J. (1973). Colour-dependence of cone responses in the turtle retina. Journal of Physiology 234, 199216.CrossRefGoogle ScholarPubMed
Gordon, D., Merrick, D., Auld, V., Dunn, R., Goldin, A.L., Davidson, N. & Catterall, W.A. (1987). Tissue specific expression of the R1 and R11 sodium channel subtypes. Proceedings of the National Academy of Sciences of the U.S.A. 84, 86828686.Google Scholar
Greferath, U., GrÜNert, U. & WÄSsle, H. (1990). Rod bipolar cells in the mammalian retina show protein kinase C-like immunoreactivity. Journal of Comparative Neurology 301, 433442.Google Scholar
Hartshorne, R.P. & Catterall, W.A. (1984). The sodium channel from rat brain. Journal of Biological Chemistry 259, 16671675.Google Scholar
Joe, E.H. & Angelides, K.J. (1992). Clustering of voltage-dependent sodium channels on axons depends on Schwann cell contact. Nature 356, 333335.Google Scholar
Kaneko, A., Suzuki, S., Pinto, L.H. & Tachibana, M. (1989). Membrane currents and pharmacology of retinal bipolar cells: A comparative study on goldfīsh and mouse. Comparative Biochemistry and Physiology 98C, 115127.Google Scholar
Kaneko, A., Pinto, L.H. & Tachibana, M. (1991). Transient calcium current of retinal bipolar cells of the mouse. Journal of Physiology 410, 613629.CrossRefGoogle Scholar
Karschin, A. & WÄSsle, H. (1990). Voltage- and transmitter-gated currents in isolated rod bipolar cells of rat retina. Journal of Neurophysiology 63, 860876.Google Scholar
Laemmli, U.K. (1970). Cleavage of structural proteins during the assembly of the head of the bacteriophage T4. Nature 227, 680685.CrossRefGoogle ScholarPubMed
Lasater, E.M. (1986). Ionic currents of cultured horizontal cells isolated from white perch retina. Journal of Neurophysiology 55, 499513.Google Scholar
Lipton, S.A. & Tauck, D.L. (1987). Voltage-dependent conductances of solitary ganglion cells dissociated from the rat retina. Journal of Physiology (London) 385, 361391.Google Scholar
Macleish, P.R., Burrows, M.B. & Yagi, T. (1989). Voltage-activated calcium current in solitary primate cones. Investigative Ophthalmology and Visual Science 30, 163.Google Scholar
Maricq, A.V. & Korenbrot, J.I. (1988). Calcium-dependent chloride currents generate action potentials in solitary cone photoreceptors. Neuron 1, 503515.Google Scholar
Minturn, J.E., Black, J.A., Angelides, K.J. & Waxman, S.G. (1990). Sodium channel expression detected with antibody 7493 in A2B5+ and A2B5– astrocytes from rat optic nerve in vitro. Glia 3, 358367.Google Scholar
Munson, R., Westermark, B. & Glaser, L. (1979). Tetrodotoxinsensitive sodium channels in normal human fibroblasts and normal human glia-like cells. Proceedings of the National Academy of Sciences of the U.S.A. 76, 64256429.Google Scholar
Murakami, M., Shimoda, Y., Nakatani, K., Miyachi, E. & Watanabe, S. (1982). GABA-mediated negative feedback from horizontal cells to cones in carp retina. Japanese Journal of Physiology 32, 911926.Google ScholarPubMed
Noda, M., Ikeda, T., Suzuki, H., Takeshima, H., Takahashi, T., Kuno, M. & Numa, S. (1986). Expression of functional sodium channels from cloned cDNAs. Nature 322, 826828.CrossRefGoogle Scholar
O’Bryan, P.M. (1973). Properties of the depolarizing synaptic potential evoked by peripheral illumination in cones of the turtle retina. Journal of Physiology 235, 207223.Google Scholar
Piccolino, M. & Gerschenfeld, H.M. (1980). Characteristics and ionic processes involved in feedback spikes of turtle cones. Proceedings of the Royal Society B (London) 206, 439446.Google Scholar
Ramón, Y Cajal S. (1933). La rétine des vertébrés. Travaux du Laboratoire de Recherche Biologique de l’Université de Madrid 28.Google Scholar
Shingai, R. & Christensen, B.N. (1983). Sodium and calcium currents measured in isolated catfish horizontal cells under voltage clamp. Neuroscience 10, 893897.CrossRefGoogle ScholarPubMed
Skaliora, I., Scobey, R.P. & Chalupa, L.M. (1993). Prenatal development of excitability in cat retinal ganglion cells: Action potentials and sodium currents. Journal of Neuroscience 13, 313323.CrossRefGoogle ScholarPubMed
Sontheimer, H., Black, J.A., Ransom, B.R. & Waxman, S.G. (1992). Ion channels in spinal cord astrocytes in vitro. I. Transient expression of high levels of Na+ and K+ channels. Journal of Neurophysiology 68, 9851000.CrossRefGoogle ScholarPubMed
Sontheimer, H. & Waxman, S.G. (1992). Ion channels in spinal cord astrocytes in vitro. II. Pharmacological analysis of two sodium current types. Journal of Neurophysiology 68, 10011011.CrossRefGoogle ScholarPubMed
Suzuki, H., Beckh, S., Kubo, H., Yanagi, N., Ishida, H., Kayano, T., Noda, M. & Numa, S. (1988). Functional expression of cloned cDNA encoding sodium channel III. FEBS Letters 228, 195200.CrossRefGoogle ScholarPubMed
Ueda, Y., Kaneko, A. & Kaneda, M. (1991). Voltage-gated currents in solitary horizontal cells of the cat. Investigative Ophthalmology and Visual Science 32, 1089.Google Scholar
Ueda, Y., Kaneko, A. & Kaneda, M. (1992). Voltage-dependent ionic currents in solitary horizontal cells isolated from cat retina. Journal of Neurophysiology 68, 11431150.Google Scholar
WÄSsle, H., Boycott, B.B. & RÖHrenbeck, J. (1989). Horizontal cells in the monkey retina: Cone connections and dendritic network. European Journal of Neuroscience 1, 421435.Google Scholar
Westenbroek, R.E., Merrick, D.K. & Catterall, W.A. (1989). Differential subcellular localization of the R1 and R11 Na+ channel subtypes in central neurons. Neuron 3, 695704.Google Scholar
Wollner, D.A. & Catterall, W.A. (1986). Localization of sodium channels in axon hillocks and initial segments of retinal ganglion cells. Proceedings of the National Academy of Sciences of the U.S.A. 83, 84248428.CrossRefGoogle ScholarPubMed
Wollner, D.A., Scheinman, R. & Catterall, W.A. (1988). Sodium channel expression and assembly during development of retinal ganglion cells. Neuron 1, 727737.CrossRefGoogle ScholarPubMed
Yagi, T. & Macleish, P.R. (1989). Large calcium activated currents in solitary primate cones. Investigative Ophthalmology and Visual Science 30, 62.Google Scholar