Hostname: page-component-586b7cd67f-g8jcs Total loading time: 0 Render date: 2024-11-22T22:29:44.910Z Has data issue: false hasContentIssue false
  • English
  • Français

Identification and localization of K+ channels in the mouse retina

Published online by Cambridge University Press:  02 June 2009

David J. Klumpp ,
Eun Joo Song  and
Lawrence H. Pinto
David J. Klumpp
Affiliation:
Department of Biochemistry, Molecular Biology and Cell Biology, Northwestern University, Evanston
Eun Joo Song
Affiliation:
Department of Neurobiology and Physiology, Northwestern University, Evanston
Lawrence H. Pinto
Affiliation:
Department of Neurobiology and Physiology, Northwestern University, Evanston
Get access Rights & Permissions [Opens in a new window]

Abstract

Voltage-gated potassium channels are differentially expressed in the brain, and recent studies have shown that K+ channels show subcellular localization. We characterized the distribution of five different K+ channels in the mouse retina. Each channel was distributed in a unique pattern in the retina and was localized to specific subcellular domains within a given retinal neuron. Kvl.4 and Kv4.2 were consistently found in axonal and somatodendritic portions, respectively, consistent with previous studies in brain. In contrast, Kvl.2, Kvl.3, and Kv2.1 showed variable subcellular distribution depending upon cellular context. These results suggest that no one K+ channel is distributed over the entire length of the neuron to provide a “housekeeping” level of membrane potential stabilization. Instead, we propose that each K+ channel is associated with a specific subcellular functional module, and each local K+ conductance responds uniquely to local voltage and second messenger signals.

Keywords

K+ channelRetinaLocalizationMouseRT PCR
Type
Research Articles
Information
Visual Neuroscience , Volume 12 , Issue 6 , November 1995 , pp. 1177 - 1190
Copyright
Copyright © Cambridge University Press 1995

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

Adamus, G., Arendt, A. & Hargrave, P.A. (1991). Genetic control of antibody response to bovine rhodopsin in mice: Epitope mapping of rhodopsin structure. Journal of Neuroimmunology 34, 89–97.CrossRefGoogle ScholarPubMed
Attali, B., Lesage, F., Ziliani, P., Guillemare, E., Honore, E., Waldmann, R., Hugnot, J.-P., Mattei, M.-G., Lazdunski, M. & Bahanin, J. (1993). Multiple mRNA isoforms encoding the mouse cardiac Kvl-5 delayed rectifier K+ channel. Journal of Biological Chemistry 268, 24283–24289.CrossRefGoogle Scholar
Bader, C.R., Bertrand, D. & Schwartz, E.A. (1982). Voltage- activated and calcium-activated currents studies in solitary rod inner segments from the salamander retina. Journal of Physiology 331, 253–284.CrossRefGoogle Scholar
Baldwin, T.J., Tsaur, M.-L., Lopez, G.A., Jan, Y.N. & Jan, L.Y. (1991). Characterization of a mammalian cDNA for an inactivating voltage-sensitive K+ channel. Neuron 7, 471–483.CrossRefGoogle ScholarPubMed
Balkema, G.W. (1991). A synaptic antigen (B16) is localized in retinal synaptic ribbons. Journal of Comparative Neurology 312, 573–583.CrossRefGoogle ScholarPubMed
Beckh, S. & Pongs, O. (1990). Members of the RCK potassium channel family are differentially expressed in the rat nervous system. EMBO Journal 9, 777.CrossRefGoogle ScholarPubMed
Boos, R., Schneider, H. & Wässle, H. (1993). Voltage- and transmitter-gated currents of Aii-amacrine cells in a slice preparation of the rat retina. Journal of Neuroscience 13, 2874–2888.CrossRefGoogle Scholar
Cajal, S.R.y. (1972). The Structure of the Retina. Springfield, Illinois: Charles Thomas.Google Scholar
Camp, T.A., Rahal, J.O. & Mayo, K.E. (1991). Regulation of ovarian gonadotropin receptor mRNAs. Molecular Endocrinology 5, 1–13.Google Scholar
Carter-Dawson, L.D. & LaVail, M.M. (1979). Rods and cones in the mouse retina: Structural analysis using light and electron microscopy. Journal of Comparative Neurology 188, 245–262.CrossRefGoogle ScholarPubMed
Chandy, G. (1991). Simplified gene nomenclature. Nature 352, 26.CrossRefGoogle ScholarPubMed
Chandy, K.G., Williams, C.B., Spencer, R.B., Aguilar, B.A., Ghan-shani, S., Temple, B.L. & Gutman, G.A. (1990). A family of three mouse potassium channel genes with intronless coding regions. Science 247, 973–975.CrossRefGoogle ScholarPubMed
Chun, J.J.M., Schatz, D.G., Oettinger, M.A., Jaenisch, R. & Baltimore, D. (1991). The recombination activating gene-1 (RAG-1) transcript is present in the murine central nervous system. Cell 64, 189–200.CrossRefGoogle ScholarPubMed
Cook, P.B. & Werblin, F.S. (1994). Spike initiation and propagation in wide field transient amacrine cells of the salamander retina. Journal of Neuroscience 14, 3852–3861.CrossRefGoogle ScholarPubMed
DeVries, S.H. & Baylor, D.A. (1993). Synaptic circuitry of the retina and olfactory bulb. Cell/Neuron 72/10 (Suppl.), 139–149.Google ScholarPubMed
Dräger, U.C (1983). Coexistence of neurofilaments and vimentin in a neurone of adult mouse retina. Nature 303, 169–172.CrossRefGoogle Scholar
Dräger, U.C. & Olsen, J.F. (1980). Origins of crossed and uncrossed retinal projection in pigmented and albino mice. Journal of Comparative Neurology 191, 383–412.CrossRefGoogle ScholarPubMed
Dreyfuss, G., Choi, Y.D. & Adams, S.A. (1984). Characterization of heterogeneous nuclear RNA-protein complexes in vivo with monoclonal antibodies. Molecular and Cellular Biology 6, 1104–1114.Google Scholar
Eckenstein, F. & Thoenen, H. (1982). Production of specific antisera and monoclonal antibodies to choline acetyltransferase: Characterization and use for identification of cholinergic neurons. EMBO Journal 1, 363–368.CrossRefGoogle ScholarPubMed
Famiglietti, E.V. & Vaughn, J.E. (1981). Golgi impregnated amacrine cells and GABAergic retinal neurons: A comparison of dendritic, immunocytochemical, and histochemical stratification in the inner plexiform layer of rat retina. Journal of Comparative Neurology 197, 129–139.CrossRefGoogle ScholarPubMed
Ferre, F. (1992). Quantitative or semi-quantitative PCR: Reality versus myth. PCR Methods and Applications 2, 1–9.CrossRefGoogle ScholarPubMed
Froehner, S.C. (1993). Regulation of ion channel distribution at synapses. Annual Review of Neuroscience 16, 347–368.CrossRefGoogle ScholarPubMed
Greferath, U., Grüuml;nert, U. & Wässle, H. (1990). Rod bipolar cells in the mammalian retina show protein kinase C-like immunoreactivity. Journal of Comparative Neurology 301, 433–442.CrossRefGoogle ScholarPubMed
Grupe, A., Schroter, K.H., Ruppersberg, J.P., Stocker, M., Drewes, T, Beckh, S. & Pongs, O. (1990). Cloning and expression of a human voltage-gated potassium channel: Novel member of the RCK potassium channel family. EMBO Journal 9, 1749–1756.CrossRefGoogle ScholarPubMed
Guillemare, E., Honore, E., Pradier, L., Lesage, F., Schweitz, H., Attali, B., Barhanin, J. & Lazdunski, M. (1992). Effects of the level of mRNA expression on biophysical properties, sensitivity to neurotoxins, and regulation of the brain delayed-rectifier K+ channel Kvl.2. Biochemistry 31, 12463–12468.CrossRefGoogle Scholar
Hille, B. (1992). Ionic Channels of Excitable Membranes. Sunderland, Massachusetts: Sinauer.Google Scholar
Hwang, P.M., Glatt, C.E., Bredt, D.S., Yellen, G. & Snyder, S.H. (1992). A novel K+ channel with unique localizations in mammalian brain: Molecular cloning and characterization. Neuron 8, 473–481.CrossRefGoogle ScholarPubMed
Hwang, P.M., Cunningham, A.M., Peng, Y.W. & Snyder, S.H. (1993). CDRK1 and DRK1 K+ channels have contrasting localizations in sensory systems. Neuroscience 55, 613–620.CrossRefGoogle ScholarPubMed
Hwang, P.M., Fotuhi, M., Bredt, D.S., Cunningham, A.M. & Snyder, S.H. (1993). Contrasting immunohistochemical localization in rat brain of two novel K+ channels of the Shab subfamily. Journal of Neuroscience 13, 1569–1576.CrossRefGoogle ScholarPubMed
Ikonen, E., Parton, R.G., Hunziker, W., Simons, K. & Dotti, C.G. (1993). Transcytosis of the polymeric immunoglobulin receptor in cultured hippocampal neurons. Current Biology 3, 635–644.CrossRefGoogle ScholarPubMed
Kaneko, A., Pinto, L.H. & Tachibana, M. (1989). Transient calcium current of retinal bipolar cells of the mouse. Journal of Physiology 410, 613–629.CrossRefGoogle ScholarPubMed
Karschin, A. & Wässle, H. (1990). Voltage- and transmitter-gated currents in isolated rod bipolar cells of rat retina. Journal of Neurophysiology 63, 860–876.CrossRefGoogle ScholarPubMed
Kawasaki, E.S. & Wang, A.M. (1989). Detection of gene expression. PCR Technology: Principles and Applications for DNA Amplification p. 246. New York: Stockton.Google Scholar
Kirsch, J., Wolters, I., Trillers, A. & Betz, H. (1993). Gephyrin antisense oligonucleotides prevent glycine receptor clustering in spinal neurons. Nature 366, 745–751.CrossRefGoogle ScholarPubMed
Klumpp, D.J., Farber, D.B., Bowes, C, Song, E.-J. & Pinto, L.H. (1991). The potassium channel MBK1 is expressed in the mouse retina. Cellular and Molecular Neurobiology 11, 611–622.CrossRefGoogle ScholarPubMed
Klumpp, D.J., Song, E.-J., Ito, S., Sheng, M.J., Jan, L.Y. & Pinto, L.H. (1995). The Shaker-like channels of the mouse rod bipolar cell and their contributions to the membrane current. Journal of Neuroscience 15, 5004–5013.CrossRefGoogle Scholar
Kues, W.A. & Wunder, F. (1992). Heterogeneous expression patterns of mammalian potassium channel genes in developing and adult rat brain. European Journal of Neuroscience 4, 1296–1308.CrossRefGoogle ScholarPubMed
Leifer, D., Lipton, S.A., Barnstable, C.J. & Masland, R.H. (1984). Monoclonal antibody to Thy-1 enhances regeneration of processes by rat retinal ganglion cells in culture. Science 224, 303–306.CrossRefGoogle ScholarPubMed
Lipton, S.A. & Tauck, D.L. (1987). Voltage-dependent conductances of solitary ganglion cells dissociated from the rat retina. Journal of Physiology 385, 361–391.CrossRefGoogle ScholarPubMed
Luneau, C.J., Williams, J.B., Marshall, J., Levitan, E.S., Oliva, C, Smith, J.S., Antanavage, J., Folander, K., Stein, R.B. et al. (1991). Alternative splicing contributes to K+ channel diversity in the mammalian central nervous system. Proceedings of the National Academy of Sciences of the U.S.A. 88, 3932–3936.CrossRefGoogle Scholar
Mangel, S. (1991). Analysis of the horizontal cell contribution to the receptive field surround of ganglion cell in the rabbit retina. Journal of Physiology 442, 211–234.CrossRefGoogle Scholar
Maricq, A.V. & Korenbrot, J.I. (1988). Calcium and calcium- dependent chloride currents generate action potentials in solitary cone photoreceptors. Neuron 1, 503–515.CrossRefGoogle ScholarPubMed
McCormack, T., Vega-Saenz de Miera, E.C. & Rudy, B. (1990). Molecular cloning of a member of a third class of Shaker-family K+ channel genes in mammals. Proceedings of the National Academy of Sciences of the U.S.A. 87, 5227–5231.CrossRefGoogle ScholarPubMed
McKinnon, D. (1989). Isolation of a cDNA clone coding for a putative second potassium channel indicates the existence of a gene family. Journal of Biological Chemistry 264, 8230–8236.CrossRefGoogle ScholarPubMed
Nakamura, T., Onno, M., Mariage-Samson, R., Hillova, J. & Hill, M. (1990). Nucleotide sequence of mouse L19 ribosomal protein cDNA isolated in screening with tre oncogene probes. DNA and Cell Biology 9, 697–703.CrossRefGoogle ScholarPubMed
Negishi, K., Kato, S. & Teranishi, T. (1988). Dopamine cells and rod bipolar cells contain protein kinase C-like immunoreactivity in some vertebrate retinas. Neuroscience Letters 94, 242–257.CrossRefGoogle ScholarPubMed
Nelson, R. (1982). An amacrine cells quicken time course of rod signals in the cat retina. Journal of Neurophysiology 47, 928–947.CrossRefGoogle ScholarPubMed
Newman, E.A. (1985). Voltage-dependent calcium and potassium channels in retinal glial cells. Nature 317, 809–811.CrossRefGoogle ScholarPubMed
Pak, M.D., Baker, K., Covarrubias, M., Butler, A., Ratcliffe, A. & Salkoff, L. (1991 a). mShal, a subfamily of A-type K+ channel cloned from mammalian brain. Proceedings of the National Academy of Sciences of the U.S.A. 88, 4386–4390.CrossRefGoogle ScholarPubMed
Pak, M.D., Covarrubias, M., Ratcliffe, A. & Salkoff, L. (1991 b). A mouse brain homolog of the Drosophila Shab K+ channel with conserved delayed rectifier properties. Journal of Neuroscience 11(3), 869–880.CrossRefGoogle ScholarPubMed
Peichl, L. & Gonzalez-Sorian, J. (1993). Unexpected presence of neurofilaments in axon-bearing horizontal cells of the mammalian retina. Journal of Neuroscience 13, 4091–4100.CrossRefGoogle ScholarPubMed
Perry, V.H. (1981). Evidence for an amacrine cell system in the ganglion cell layer of the rat retina. Neuroscience 6, 931–944.CrossRefGoogle ScholarPubMed
Perry, V.H. (1982). The ganglion cell layer of the mammalian retina. In Progress in Retinal Research, ed. Osborne, N.N., & Chader, G.J., pp. 53–80. Oxford: Pergamon Press.Google Scholar
Perry, V.H. & Walker, M. (1980). Amacrine cells, displaced amacrine cells and interplexiform cells in the retina of the rat. Proceedings of the Royal Society B (London) 208, 415–431.Google ScholarPubMed
Pongs, O. (1992). Molecular biology of voltage-dependent potassium channels. Physiological Reviews 4 (Suppl.), S69–S88.CrossRefGoogle Scholar
Raff, M.C (1989). Glial cell diversification in the rat optic nerve. Science 243, 1450–1455.CrossRefGoogle ScholarPubMed
Rettig, J., Wunder, F., Stocker, M., Lichtinghagen, R., Mastlaux, F., Beckh, S., Kues, W., Pedarzani, P., Schröter, K.H. et al. (1992). Characterization of a Shaw-related potassium channel family in rat brain. EMBO Journal 11, 2473–2486.CrossRefGoogle ScholarPubMed
Rosenthal, E.T., Hunt, T. & Ruderman, J.V. (1980). Selective translation of mRNA controls the pattern of protein synthesis during early development of the surf clam, Spisula solidissima. Cell 20, 487–494.CrossRefGoogle ScholarPubMed
Rudy, B., Kentros, C, Weiser, M., Fruhling, D., Serodio, P., Vega-Saenz de Miera, E., Ellisman, M.H., Pollock, J.A. & Baker, H. (1992). Region-specific expression of a K+ channel gene in brain. Proceedings of the National Academy of Sciences of the U.S.A. 89, 4603–4607.CrossRefGoogle Scholar
Salkoff, L., Baker, K., Butler, A., Covarrubias, M., Pak, M.D. & Wei, A. (1992). An essential ‘set’ of K+ channels conserved in flies, mice and humans. Trends in Neuroscience 15, 161–166.CrossRefGoogle ScholarPubMed
Sheng, M., Liao, Y.J., Jan, Y.N. & Jan, L.Y. (1993). Presynaptic A-current based on heteromultimeric K+ channels detected in vivo. Nature 365, 72–75.CrossRefGoogle ScholarPubMed
Sheng, M., Tsaur, M.-L., Jan, Y.N. & Jan, L.Y. (1992). Subcellular segregation of two A-tye K+ channel proteins in rat central neurons. Neuron 9, 271–284.CrossRefGoogle ScholarPubMed
Sheng, M., Tsuar, M.-L., Jan, Y.N. & Jan, L.Y. (1994). Contrasting subcellular localization of the Kvl.2 K+ channel subunit in different neurons of rat brain. Journal of Neuroscience 14, 2408–2417.CrossRefGoogle Scholar
Srinivasan, Y., Lewallen, M. & Angelides, K.J. (1992). Mapping the binding site on ankyrin for the voltage-dependent sodium channel from brain. Journal of Biological Chemistry 267, 7483–7489.CrossRefGoogle ScholarPubMed
Steinberg, R.H. (1985). Interactions between the retinal pigment epithelium and the neural retina. Documenta Ophthalmologica 60, 327–346.CrossRefGoogle ScholarPubMed
Steinberg, R.H., Linsenmeier, R.A. & Griff, E.R. (1983). Three light-evoked responses of the retinal pigment epithelium. Vision Research 23, 1315–1323.CrossRefGoogle ScholarPubMed
Stühmer, W., Ruppersberg, J.P., Schroeter, K.H., Sakmann, B., Stocker, M., Giese, K.P., Perschke, A., Baumann, A. & Pongs, O. (1989). Molecular basis of functional diversity of voltage-gated potassium channels in mammalian brain. EMBO Journal 8, 3235–3244.CrossRefGoogle ScholarPubMed
Sucher, N.J., Cheng, P.O. & Lipton, S.A. (1991). Cryopreservation of postnatal rat retinal ganglion cells: Persistence of voltage- and ligand-gated ionic currents. Neuroscience 43, 135–150.CrossRefGoogle ScholarPubMed
Suzuki, H. & Pinto, L.H. (1986). Response properties of horizontal cells in the isolated retina of wild-type and pearl mutant mice. Journal of Neuroscience 6(4), 1122–1128.CrossRefGoogle ScholarPubMed
Tachibana, M. (1983). Ionic currents of solitary horizontal cells isolated from goldfish retina. Journal of Physiology 345, 329–351.CrossRefGoogle ScholarPubMed
Tamura, T., Nakatani, K. & Yau, K.-W. (1989). Light adaptation in car retinal rods. Science 245, 755–758.CrossRefGoogle Scholar
Tempel, B.L., Jan, Y.N. & Jan, L.Y. (1988). Cloning of a probable potassium channel gene from mouse brain. Nature 332, 837–839.CrossRefGoogle ScholarPubMed
Tiedge, H., Chen, W. & Brosius, J. (1993). Primary structure, neural-specific expression, and dendritic location of human BC200 RNA. Journal of Neuroscience 13, 2382–2390.CrossRefGoogle ScholarPubMed
Titius, D.E. (1991). Promega Protocols and Applications Guide, 2nd ed.Promega Corporation, Madison.Google Scholar
Trimmer, J.S. (1991). Immunological identification and characterization of a delayed rectifier K+ channel polypeptide in rat brain. Proceedings of the National Academy of Sciences of the U.S.A. 88, 10764–10768.CrossRefGoogle ScholarPubMed
Tsaur, M.-L., Sheng, M., Lowenstein, D.H., Jan, Y.N. & Jan, L.Y. (1992). Differential expression of K+ channel mRNAs in the rat brain and down-regulation in the hippocampus following seizures. Neuron 8, 1055–1067.CrossRefGoogle ScholarPubMed
Vaughn, J.E., Famiglietti, E.V., Barber, R.P., Saito, K., Roberts, E. & Ribak, C.E. (1981). GABAergic amacrine cells in rat retina: Immunocytochemical identification and synaptic connectivity. Journal of Comparative Neurology 197, 113–127.CrossRefGoogle ScholarPubMed
Vega-Saenz de Miera, E., Moreno, H., Fruhling, D., Kentros, C. & Rudy, B. (1992). Cloning of ShIII (Shaw-like) cDNAs encoding a novel high-voltage-activating, TEA-sensitive, type-A K+ channel. Proceedings of the Royal Society B (London) 248, 9–18.Google ScholarPubMed
Voigt, T. (1986). Cholinergic amacrine cells in the rat retina. Journal of Comparative Neurology 248, 19–35.CrossRefGoogle ScholarPubMed
Wang, H., Kunkel, D.D., Martin, T.M., Schwartzkroin, P.A. & Tempel, B.L. (1993). Heteromultimeric K+ channels in terminal and juxtaparanodal regions of neurons. Nature 365, 75–79.CrossRefGoogle ScholarPubMed
Wässle, H. & Boycott, B.B. (1992). Functional architecture of the mammalian retina. Physiological Reviews 71(2), 447–480.CrossRefGoogle Scholar
Wässle, H., Yamashita, M., Greferath, U., Grünert, U. & Müller, F. (1991). The rod bipolar cell of the mammalian retina. Visual Neuroscience 7, 99–112.CrossRefGoogle ScholarPubMed
Weiser, M., Vega-Saenz de Miera, E., Kentros, C, Moreno, H., Franzen, L., Hillman, D., Baker, H. & Rudy, B. (1994). Differential expression of Shaw-related K+ channels in the rat central nervous system. Journal of Neuroscience 14, 949–972.CrossRefGoogle ScholarPubMed
Wen, R., Lui, G.M. & Steinberg, R.H. (1993). Whole-cell K+ currents in fresh and cultured cell of the human and monkey retinal igment epithelium. Journal of Physiology 465, 121–147.CrossRefGoogle ScholarPubMed
Wilkinson, D.G. (1992). The theory and practice of in situ hybridization. In In Situ Hybridization: A Practical Approach, ed. Wilker-son, D.G., p. 163. Oxford: IRL Press.Google Scholar