Hostname: page-component-cd9895bd7-8ctnn Total loading time: 0 Render date: 2024-12-25T05:18:57.907Z Has data issue: false hasContentIssue false

Immunolocalization of TRPC channel subunits 1 and 4 in the chicken retina

Published online by Cambridge University Press:  18 November 2003

SCOTT CROUSILLAC
Affiliation:
Department of Biological Sciences, Louisiana State University, Baton Rouge
MICHELLE LEROUGE
Affiliation:
Department of Biological Sciences, Louisiana State University, Baton Rouge
MICHELE RANKIN
Affiliation:
Department of Biological Sciences, Louisiana State University, Baton Rouge
EVANNA GLEASON
Affiliation:
Department of Biological Sciences, Louisiana State University, Baton Rouge

Abstract

In the vertebrate retina, multiple cell types express G protein-coupled receptors linked to the IP3 signaling pathway. The signaling engendered by activation of this pathway can involve activation of calcium permeable transient receptor potential (TRP) channels. To begin to understand the role of these channels in the retina, we undertake an immunocytochemical localization of two TRP channel subunits. Polyclonal antibodies raised against mammalian TRPC1 and TRPC4 are used to localize the expression of these proteins in sections of the adult chicken retina. Western blot analysis indicates that these antibodies recognize avian TRPC1 and TRPC4. TRPC1 labeling is almost completely confined to the inner plexiform layer (IPL) where it labels a subset of processes that ramify in three broad stripes. Occasionally, cell bodies are labeled. These can be found in the inner nuclear layer (INL) proximal to the IPL, the IPL, and the ganglion cell layer (GCL). Double-labeling experiments using a polyclonal antibody that recognizes brain nitric oxide synthase (bNOS) in the chicken indicate that many of the TRPC1-positive processes and cell bodies also express bNOS. Labeling with the TRPC4 antibody was much more widespread with some degree of labeling found in all layers of the retina. TRPC4 immunoreactivity was found in the photoreceptor layer, in the outer plexiform layer (OPL), in radially oriented cells in the INL, diffusely in the IPL, and in vertically oriented elements below the GCL. Double-labeling experiments with a monoclonal antibody raised against vimentin indicate that the TRPC4-positive structures in the INL and below the GCL are Müller cells. Thus, TRPC1 and TRPC4 subunits have unique expression patterns in the adult chicken retina. The distributions of these two subunits indicate that different retinal cell types express TRP channels containing different subunits.

Type
Research Article
Copyright
2003 Cambridge University Press

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

Anderson, C.R., Furness, J.B., Woodman, H.L., Edwards, S.L., Crack, P.J., & Smith, A.I. (1995). Characterisation of neurons with nitric oxide synthase immunoreactivity that project to prevertebral ganglia. Journal of Autonomic Nervous System 52, 107116.Google Scholar
Borges, S., Gleason, E., Frerking, M., & Wilson, M. (1996). Neurotensin induces calcium oscillations in cultured amacrine cells. Visual Neuroscience 13, 311318.Google Scholar
Cai, W. & Pourcho, R.G. (1999). Localization of metabotropic glutamate receptors mGluR1α and mGluR2/3 in the cat retina. The Journal of Comparative Neurology 407, 427437.Google Scholar
Clapham, D.E., Runnels, L.W., & Strubing, C. (2001). The TRP ion channel family. Nature Reviews Neuroscience 2, 387396.Google Scholar
Cook, J.E. & Sharma, S.C. (1995). Large retinal ganglion cells in the channel catfish (Ictalurus punctatus): Three types with distinct dendritic stratification patterns form similar but independent mosaics. Journal of Comparative Neurology 362, 331349.Google Scholar
Dacey, D.M. (1989). Axon-bearing amacrine cells of the macaque monkey retina. Journal of Comparative Neurology 284, 275293.Google Scholar
Famiglietti, E.V. (1992). Polyaxonal amacrine cells of rabbit retina: Morphology and stratification of PA1 cells. Journal of Comparative Neurology 316, 391405.Google Scholar
Fischer, A.J. & Stell, W.K. (1999). Nitric oxide synthase-containing cells in the retina, pigmented epithelium, choroid, and sclera of the chick eye. Journal of Comparative Neurology 405, 114.Google Scholar
Fischer, A.J., McKinnon, L.A., Nathanson, N.M., & Stell, W.K. (1998). Identification and localization of muscarinic acetylcholine receptors in the ocular tissues of the chick. Journal of Comparative Neurology 392, 273284.Google Scholar
Gleason, E., Mobbs, P., Nuccitelli, R., & Wilson, M. (1992). Development of functional calcium channels in cultured avian photoreceptors. Visual Neuroscience 8, 315327.Google Scholar
Gleason, E., Borges, S., & Wilson, M. (1993). Synaptic transmission between pairs of retinal amacrine cells in culture. Journal of Neuroscience 13, 23592370.Google Scholar
Harteneck, C., Plant, T.D., & Schultz, G. (2000). From worm to man: Three subfamilies of TRP channels. Trends in Neurosciences 23, 159166.Google Scholar
Huber, A., Sander, P., Bahner, M., & Paulsen, R. (1998). The TRP Ca2+ channel assembled in a signaling complex by the PDZ domain protein INAD is phosphorylated through the interaction with protein kinase C (ePKC). FEBS Letters 425, 317322.Google Scholar
Kinoshita, M., Akaike, A., Satoh, M., & Kaneko, S. (2000). Positive regulation of capacitative Ca2+ entry by intracellular Ca2+ in Xenopus oocytes expressing rat TRP4. Cell Calcium 28, 151159.Google Scholar
Koulen, P., Kuhn, R., Wassle, H., & Brandstatter, J.H. (1997). Group I metabotropic glutamate receptors mGluR1α and mGluR5a: localization in both synaptic layers of the rat retina. Journal of Neuroscience 17, 22002211.Google Scholar
Kreimborg, K.M., Lester, M.L., Medler, K.F., & Gleason, E.L. (2001). Group I metabotropic glutamate receptors are expressed in the chicken retina and by cultured retinal amacrine cells. Journal of Neurochemistry 77, 452465.Google Scholar
Lemmon, V. & Rieser, G. (1983). The developmental distribution of vimentin in the chick retina. Brain Research 313, 191197.Google Scholar
Lintschinger, B., Balzer-Geldsetzer, M., Baskaran, T., Graier, W.F., Romanin, C., Zhu, M.X., & Groschner, K. (2000). Coassembly of Trp1 and Trp3 proteins generates diacylglycerol- and Ca2+-sensitive cation channels. Journal of Biological Chemistry 275, 2779927805.Google Scholar
Liu, Y. & Wakakura, M. (1998). P1-/P2-purinergic receptors on cultured rabbit retinal Müller cells. Japan Journal of Ophthalmology 42, 3340.Google Scholar
Liu, M., Parker, L.L., Wadzinski, B.E., & Shieh, B.H. (2000). Reversible phosphorylation of the signal transduction complex in Drosophila photoreceptors. Journal of Biological Chemistry 275, 1219412199.Google Scholar
McKay, R.R., Szymeczek-Seay, C.L., Lievremont, J.P., Bird, G.S., Zitt, C., Jungling, E., Luckhoff, A., & Putney, J.W., Jr. (2000). Cloning and expression of the human transient receptor potential 4 (TRP4) gene: Localization and functional expression of human TRP4 and TRP3. Biochemical Journal 351, 735746.Google Scholar
Moyer, M., Bullrich, F., & Sheffield, J.B. (1990). Emergence of flat cells from glia in stationary cultures of embryonic chick neural retina. In Vitro Cell and Developmental Biology 26, 10731078.Google Scholar
Neal, M.J., Cunningham, J.R., & Matthews, K.L. (2001). Activation of nicotinic receptors on GABAergic amacrine cells in the rabbit retina indirectly stimulates dopamine release. Visual Neuroscience 18, 5564.Google Scholar
Obukhov, A.G. & Nowycky, M.C. (2002). TRPC4 can be activated by G-protein-coupled receptors and provides sufficient Ca2+ to trigger exocytosis in neuroendocrine cells. Journal of Biological Chemistry 277, 1617216178.Google Scholar
Philipp, S., Cavalie, A., Freichel, M., Wissenbach, U., Zimmer, S., Trost, C., Marquart, A., Murakami, M., & Flockerzi, V. (1996). A mammalian capacitative calcium entry channel homologous to Drosophila TRP and TRPL. EMBO Journal 15, 61666171.Google Scholar
Philipp, S., Hambrecht, J., Braslavski, L., Schroth, G., Freichel, M., Murakami, M., Cavalie, A., & Flockerzi, V. (1998). A novel capacitative calcium entry channel expressed in excitable cells. EMBO Journal 17, 42744282.Google Scholar
Philipp, S., Trost, C., Warnat, J., Rautmann, J., Himmerkus, N., Schroth, G., Kretz, O., Nastainczyk, W., Cavalie, A., Hoth, M., & Flockerzi, V. (2000). TRP4 (CCE1) protein is part of native calcium release-activated Ca2+-like channels in adrenal cells. Journal of Biological Chemistry 275, 2396523972.Google Scholar
Sosa, R., Hoffpauir, B., Rankin, M.L., Bruch, R.C., & Gleason, E.L. (2002). Metabotropic glutamate receptor 5 and calcium signaling in retinal amacrine cells. Journal of Neurochemistry 81, 973983.Google Scholar
Strübing, C., Krapivinsky, G., Krapivinsky, L., & Clapham, D.E. (2001). TRPC1 and TRPC5 form a novel cation channel in mammalian brain. Neuron 29, 645655.Google Scholar
Tang, Y., Tang, J., Chen, Z., Trost, C., Flockerzi, V., Li, M., Ramesh, V., & Zhu, M.X. (2000). Association of mammalian trp4 and phospholipase C isozymes with a PDZ domain-containing protein, NHERF. Journal of Biological Chemistry 275, 3755937564.Google Scholar
Teranishi, T. & Negishi, K. (1992). Dendritic morphology of interstitial amacrine cells with monostratified dendrites in different-sized carp retinas. Brain Research Developmental Brain Research 67, 327332.Google Scholar
Tomita, Y., Kaneko, S., Funayama, M., Kondo, H., Satoh, M., & Akaike, A. (1998). Intracellular Ca2+ store-operated influx of Ca2+ through TRP-R, a rat homolog of TRP, expressed in Xenopus oocytes. Neuroscience Letters 248, 195198.Google Scholar
Trost, C., Bergs, C., Himmerkus, N., & Flockerzi, V. (2001). The transient receptor potential, TRP4, cation channel is a novel member of the family of calmodulin binding proteins. Biochemical Journal 355, 663670.Google Scholar
Warr, C.G. & Kelly, L.E. (1996). Identification and characterization of two distinct calmodulin-binding sites in the Trp1 ion-channel protein of Drosophila melanogaster. Biochemical Journal 314, 497503.Google Scholar
Zitt, C., Zobel, A., Obukhov, A.G., Harteneck, C., Kalkbrenner, F., Luckhoff, A., & Schultz, G. (1996). Cloning and functional expression of a human Ca2+-permeable cation channel activated by calcium store depletion. Neuron 16, 11891196.Google Scholar