Hostname: page-component-8448b6f56d-qsmjn Total loading time: 0 Render date: 2024-04-25T02:01:24.878Z Has data issue: false hasContentIssue false

Immunocytochemical and histochemical localization of nitric oxide synthase in the turtle retina

Published online by Cambridge University Press:  02 June 2009

Todd A. Blute
Affiliation:
Department of Biology, Boston University, Boston
Bernd Mayer
Affiliation:
Department of Pharmacology and Toxicology, University of Graz, Graz, Austria

Abstract

Recent interest in nitric oxide and its relationship to cGMP has produced many attempts to anatomically localize the enzyme synthesizing nitric oxide, nitric oxide synthase. In the retina, numerous previous studies have used the NADPH-diaphorase enzyme activity of nitric oxide synthase as a histochemical method to localize nitric oxide synthase. However, all NADPH-diaphorase activity is not necessarily nitric oxide synthase, because several enzymes have similar biochemical activity. Additionally, various histochemical methods have been used to demonstrate NADPH-diaphorase activity, which makes comparisons between studies difficult. The purpose of this study was twofold. First, we wanted to examine the histochemical labeling of NADPH-diaphorase in the turtle retina to allow comparisons to previous studies. Second, we wanted to compare the histochemical localization of NADPH-diaphorase activity to the immunocytochemical localization of nitric oxide synthase in the turtle retina. Our histochemical localization of NADPH-diaphorase activity and our localization of nitric oxide synthase-like immunoreactivity in the turtle retina both produced similar results. Both the histochemistry and immunocytochemistry consistently labeled photoreceptor inner segments, at least three amacrine cell types, and processes in the inner plexiform layer. In optimized double-labeled preparations, all cells with NADPH-diaphorase activity were also positive for nitric oxide synthase-like immunoreactivity, although some somata in the ganglion cell layer only had nitric oxide synthase-like immunoreactivity. The immunocytochemical localization of nitric oxide synthase in photoreceptors, amacrine cells, and putative ganglion cells indicates that nitric oxide may function at several levels of visual processing in the turtle retina.

Type
Research Articles
Copyright
Copyright © Cambridge University Press 1997

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

Ahmad, I. & Barnstable, C.J. (1993). Differential laminar expression of particulate and soluble guanylate cyclase genes in rat retina. Experimental Eye Research 56, 5162.CrossRefGoogle ScholarPubMed
Ahmad, I., Leinders-Zufall, T., Kocsis, J.D., Shepherd, G.M., Zufall, F. & Barnstable, C.J. (1994). Retinal ganglion cells express a cGMPgated cation conductance activatable by nitric oxide donors. Neuron 12, 155165.CrossRefGoogle ScholarPubMed
Ammermüller, J., & Kolb, H. (1995). The organization of the turtle inner retina. I. On- and Off-center pathways. Journal of Comparative Neurology 358, 134.CrossRefGoogle ScholarPubMed
Barthel, L.K. & Raymond, P.A. (1990). Improved method for obtaining 3 μm cryosections for immunocytochemistry. Journal of Histochemistry and Cytochemistry 38, 13831388.CrossRefGoogle Scholar
Belai, A., Schmidt, H.H.H.W., Hoyle, C.H.V., Hassall, C.J.S., Saffrey, M.S., Moss, J., Förstermann, U., Murad, F. & Burnstock, G. (1992). Colocalization of nitric oxide synthase and NADPHdiaphorase in the myenteric plexus of the rat gut. Neuroscience Letters 143, 6064.CrossRefGoogle ScholarPubMed
Bradshaw, D.J. & Simmons, M.A. (1995). Gamma-aminobutyric acid A receptor function is modulated by cyclic GMP. Brain Research Bulletin 37, 6772.CrossRefGoogle ScholarPubMed
Brüning, G., Wiese, S. & Mayer, B. (1995). Nitric oxide synthase in the brain of the turtle Pseudemys scripta elegans. Journal of Comparative Neurology 348, 183206.CrossRefGoogle Scholar
Bugnon, O., Schaad, N.C. & Schorderet, M. (1994). Nitric oxide modulates endogenous dopamine release in bovine retina. NeuroReport 5, 401404.CrossRefGoogle ScholarPubMed
Cobcroft, M., Vaccaro, T. & Mitrofanis, J. (1989). Distinct patterns of distribution among NADPH-diaphorase neurons of the guinea pig retina. Neuroscience Letters 103, 17.CrossRefGoogle ScholarPubMed
Dawson, V.L., Dawson, T.M., London, E.D., Bredt, D.S. & Snyder, S.H. (1991). Nitric oxide mediates glutamate neurotoxicity in primary cortical cultures. Proceedings of the National Academy of Sciences of the U.S.A. 88, 63686371.CrossRefGoogle ScholarPubMed
De la Villa, P., Kurahashi, T. & Kaneko, A. (1995). L-glutamateinduced responses and cGMP-activated channels in three subtypes of retinal bipolar cells dissociated from the cat. Journal of Neuroscience 15, 35713582.CrossRefGoogle ScholarPubMed
De Vries, S.H. & Schwartz, E.A. (1989). Modulation of an electrical synapse between solitary pairs of catfish horizontal cells by dopamine and second messengers. Journal of Physiology 414, 351375.CrossRefGoogle ScholarPubMed
Djamgoz, M.B.A., Aguilo, R., Greenstreet, E.H., Reynolds, R. & Wilkin, G.P. (1996). Histochemistry of NADPH-Diaphorase—a marker for neuronal nitric oxide synthase—in the carp retina. Neurochemical International 28, 283291.CrossRefGoogle ScholarPubMed
Dun, N.J., Dun, S.L., Förstermann, U. & Tseng, L.F. (1992). Nitric oxide synthase immunoreactivity in rat spinal cord. Neuroscience Letters 147, 217220.CrossRefGoogle ScholarPubMed
Förstermann, U., Gath, I., Schwarz, P., Closs, E.I. & Kleinert, H. (1995). Isoforms of nitric oxide synthase—Properties, cellular distribution and expressional control. Biochemical Pharmacology 50, 13211332.CrossRefGoogle ScholarPubMed
Garry, M.G., Richardson, J.D. & Hargreaves, K.M. (1994). Sodium nitroprusside evokes the release of immunoreactive calcitonin gene-related peptide and substance P from dorsal horn slices via nitric oxide-dependent and nitric oxide-independent mechanisms. Journal of Neuroscience 14, 43294337.CrossRefGoogle ScholarPubMed
Garthwaite, J. (1991). Glutamate, nitric oxide and cell-cell signaling in the nervous system. Trends in Neuroscience 14, 6067.CrossRefGoogle ScholarPubMed
Goureau, O., Hicks, D., Courtois, Y. & De Kozak, Y. (1994). Induction and regulation of nitric oxide synthase in retinal Müller glial cells. Journal of Neurochemistry 63, 310317.CrossRefGoogle ScholarPubMed
Greenstreet, E.H. & Djamgoz, M.B.A. (1994). Nitric oxide induces light adaptive morphological changes in retinal neurones. NeuroReport 6, 109112.CrossRefGoogle ScholarPubMed
Huxlin, K.R. (1995). NADPH-diaphorase expression in neurons and glia of normal rat retina. Brain Research 692, 195206.CrossRefGoogle Scholar
Jones, N.M., Loiacono, R.E. & Beart, P.M. (1995). Roles for nitric oxide as an intra- and interneuronal messenger at NMDA release-regulating receptors: Evidence from studies of the NMDA-evoked release of [3H]noradrenaline and D-[3H]aspartate from rat hippocampal slices. Journal of Neurochemistry 64, 20572063.CrossRefGoogle Scholar
Koch, K.-W., Lambrecht, H.-G., Haberecht, M., Redburn, D. & Schmidt, H.H.H.W. (1994). Functional coupling of a Ca2+/calmodulindependent nitric oxide synthase and a soluble guanylyl cyclase in vertebrate photoreceptor cells. EMBO Journal 13, 33123320.CrossRefGoogle Scholar
Kolb, H. (1982). The morphology of the bipolar cells, amacrine cells and ganglion cells in the turtle retina Pseudemys scripta elegans. Philosophical Transactions Royal Society B (London) 298, 355393.Google ScholarPubMed
Kurenny, D.E., Moroz, L.L., Turner, R.W., Sharkey, K.A. & Barnes, S. (1994). Modulation of ion channels in rod photoreceptors by nitric oxide. Neuron 13, 315324.CrossRefGoogle ScholarPubMed
Kusaka, S., Dabin, I., Barnstable, C.J. & Puro, D.G. (1996). Müller cells express functional cGMP-cation channels. Investigative Ophthalmology and Visual Science (Suppl.) 37, S140.Google Scholar
Lau, K.C., So, K.-F., Tay, D. & Leung, M.C.P. (1994). NADPH-diaphorase neurons in the retina of the hamster. Journal of Comparative Neurology 350, 550558.CrossRefGoogle ScholarPubMed
Liepe, B.A., Stone, C., Koistinaho, J. & Copenhagen, D.R. (1994). Nitric oxide synthase in Müller cells and neurons of salamander and fish retina. Journal of Neuroscience 14, 76417654.CrossRefGoogle ScholarPubMed
Lonart, G., Wang, J. & Johnson, K.M. (1992). Nitric oxide induces neurotransmitter release from hippocampal slices. European Journal of Pharmacology 220, 271272.CrossRefGoogle ScholarPubMed
Marchiafava, P.L. (1976). Centrifugal actions of amacrine and ganglion cells in the retina of the turtle. Journal of Physiology 255, 137155.CrossRefGoogle ScholarPubMed
Marletta, M.A. (1993). Nitric oxide synthase structure and mechanism. Journal of Biological Chemistry 268, 1223112234.CrossRefGoogle ScholarPubMed
Matsumoto, T., Nakane, M., Pollock, J.S., Kuk, J.E. & Forstermann, U. (1993). A correlation between soluble brain nitric oxide synthase and NADPH-diaphorase activity is only seen after exposure of the tissue to fixative. Neuroscience Letters 155, 6164.CrossRefGoogle ScholarPubMed
Mayer, B., Mathias, J. & Böhme, E. (1990). Purification of a Ca2+/calmodulin-dependent nitric oxide synthase from porcine cerebellum. Federation of European Biochemical Societies 277, 215219.CrossRefGoogle ScholarPubMed
Meffert, M.K., Premack, B.A. & Schulman, H. (1994). Nitric oxide stimulates Ca2+-independent synaptic vesicle release. Neuron 12, 12351244.CrossRefGoogle Scholar
Miles, F.A. (1970). Centrifugal effects in avian retina. Science 170, 992995.CrossRefGoogle ScholarPubMed
Mills, S.L. & Massey, S.C. (1995). Differential properties of two gap junctional pathways made by All amacrine cells. Nature 377, 734737.CrossRefGoogle Scholar
Mitrofanis, J., Robinson, S.R. & Ashwell, K. (1992). Development of catecholaminergic, indoleamine-accumulating and NADPH-diaphorase amacrine cells in rabbit retinae. Journal of Comparative Neurology 319, 560585.CrossRefGoogle ScholarPubMed
Miyachi, E., Murakami, M. & Nakaki, T. (1990). Arginine blocks gap junctions between retinal horizontal cells. NeuroReport 1, 107110.CrossRefGoogle ScholarPubMed
Miyachi, E. & Murakami, M. (1991). Synaptic inputs to turtle horizontal cells analyzed after blocking of gap junctions by intracellular injections of cyclic nucleotides. Vision Research 31, 631635.CrossRefGoogle ScholarPubMed
Morgan, I.G., Miethke, P. & Lt, Z.K. (1994). Is nitric oxide a transmitter of the centrifugal projection to the avian retina. Neuroscience Letters 168, 57.CrossRefGoogle Scholar
Murphy, S. (1994). Histochemical localization of nitric oxide synthase in the CNS. Trends in Neuroscience 17, 106.CrossRefGoogle Scholar
Nawy, S. & Jahr, C.E. (1991). cGMP-gated conductance in retinal bipolar cells is suppressed by the photoreceptor transmitter. Neuron 7, 677683.CrossRefGoogle ScholarPubMed
O'Dell, T.J., Hawkins, R.D., Kandel, E.R. & Arancio, O. (1991). Tests of the roles of two diffusible substances in long-term potentiation: Evidence for nitric oxide as a possible early retrograde messenger. Proceedings of the National Academy of Sciences of the U.S.A. 88, 1128511289.CrossRefGoogle ScholarPubMed
Ohkuma, S., Katsura, M., Chen, D-Z., Naihara, H. & Kuriyama, K. (1996). Nitric oxide-evoked [3H]-γ-aminobutyric acid release is mediated by two distinct release mechanisms. Molecular Brain Research 36, 137144.CrossRefGoogle ScholarPubMed
Osborne, N.N., Barnett, N.L. & Herrera, A.J. (1993). NADPH diaphorase localization and nitric oxide synthetase activity in the retina and anterior uvea of the rabbit eye. Brain Research 610, 194198.CrossRefGoogle ScholarPubMed
Perez, M.T.R., Larsson, B., Alm, P., Andersson, K.-E. & Ehinger, B. (1995). Localisation of neuronal nitric oxide synthase-immunoreactivity in rat and rabbit retinas. Experimental Brain Research 104, 207217.CrossRefGoogle ScholarPubMed
Provis, J.M. & Mitrofanis, J. (1990). NADPH-diaphorase neurons of human retinae have a uniform topographical distribution. Visual Neuroscience 4, 619623.CrossRefGoogle ScholarPubMed
Roufail, E., Stringer, M. & Rees, S. (1995). Nitric oxide synthase immunoreactivity and NADPH diaphorase staining are co-localised in neurons closely associated with the vasculature in rat and human retina. Brain Research 684, 3646.CrossRefGoogle ScholarPubMed
Sagar, S.M. (1986). NADPH diaphorase histochemistry in the rabbit retina. Brain Research 373, 153158.CrossRefGoogle ScholarPubMed
Sagar, S.M. (1990). NADPH-diaphorase reactive neurons of the rabbit retina: Differential sensitivity to excitotoxins and unusual morphological features. Journal of Comparative Neurology 300, 309319.CrossRefGoogle Scholar
Sandell, J.H. (1985). NADPH diaphorase cells in the mammalian inner retina. Journal of Comparative Neurology 238, 466472.CrossRefGoogle ScholarPubMed
Sato, T. (1990). NADPH-diaphorase positive amacrine cells in the retinae of the frog (Rana esculenta) and pigeon (Columba livia). Archives of Histology and Cytology 53, 6369.CrossRefGoogle ScholarPubMed
Schnyder, H. & Künzle, H. (1983). The retinopetal system in the turtle Pseudemys scripta elegans. Cell and Tissue Research 234, 219224.CrossRefGoogle ScholarPubMed
Schuman, E.M. & Madison, D.V. (1994). Nitric oxide and synaptic function. Annual Review of Neuroscience 17, 153183.CrossRefGoogle ScholarPubMed
Shiells, R.A. & Falk, G. (1992). Properties of the cGMP-activated channel of retinal on-bipolar cells. Proceedings of the Royal Society B (London) 247, 2125.Google ScholarPubMed
Straznicky, C. & Gabriel, R. (1991). NADPH-diaphorase positive neurons in the retina of Bufo marinus: Selective staining of bipolar and amacrine cells. Archives of Histology and Cytology 54, 213220.CrossRefGoogle ScholarPubMed
Tracey, W.R., Nakane, M., Pollock, J.S. & Förstermann, U. (1993). Nitric oxide synthases in neuronal cells, macrophages and endothelium are NADPH diaphorases, but represent only a fraction of total cellular NADPH diaphorase activity. Biochemical and Biophysical Research Communications 195, 10351040.CrossRefGoogle Scholar
Vaney, D.I. & Young, H.M. (1988). GABA-like immunoreactivity in NADPH-diaphorase amacrine cells of the rabbit retina. Brain Research 474. 380385.CrossRefGoogle ScholarPubMed
Vizzard, M.A., Erdman, S.L., Roppolo, J.R., Förstermann, U. & De Groat, W.C. (1994). Differential localization of neuronal nitric oxide synthase immunoreactivity and NADPH-diaphorase activity in the cat spinal cord. Cell and Tissue Research 278, 299309.CrossRefGoogle ScholarPubMed
Wallace, M.N. & Bisland, S.K. (1994). NADPH-diaphorase activity in activated astrocytes represents inducible nitric oxide synthase. Neuroscience 59, 905919.CrossRefGoogle ScholarPubMed
Wassle, H., Chun, M.H. & Muller, F. (1987). Amacrine cells in the ganglion cell layer of the cat retina. Journal of Comparative Neurology 265, 391408.CrossRefGoogle ScholarPubMed
Weiler, R. & Kewitz, B. (1993). The marker for nitric oxide synthase, NADPH-diaphorase, co-localizes with GABA in horizontal cells and cells of the inner retina in the carp retina. Neuroscience Letters 158, 151154.CrossRefGoogle ScholarPubMed
Yamamoto, R., Bredt, D.S., Snyder, S.H. & Stone, R.A. (1993). The localization of nitric oxide synthase in the rat eye and related cranial ganglia. Neuroscience 54, 189200.CrossRefGoogle ScholarPubMed
Zemel, E., Eyal, O., Lei, B. & Perlman, I. (1996). NADPH diaphorase activity in mammalian retinas is modulated by the state of visual adaptation. Visual Neuroscience 13, 863871.CrossRefGoogle ScholarPubMed
Zhu, X.Z. & Luo, L.G. (1992). Effects of nitroprusside (nitric oxide) on endogenous dopamine release from rat striatal slices. Journal of Neurochemistry 59, 932935.CrossRefGoogle ScholarPubMed