Hostname: page-component-cd9895bd7-gbm5v Total loading time: 0 Render date: 2024-12-25T13:42:01.413Z Has data issue: false hasContentIssue false
  • English
  • Français

Nitric oxide production and the expression of two nitric oxide synthases in the avian retina

Published online by Cambridge University Press:  30 May 2013

MERVE TEKMEN-CLARK  and
EVANNA GLEASON
MERVE TEKMEN-CLARK*
Affiliation:
Department of Biological Sciences, Louisiana State University, Baton Rouge, Louisiana
EVANNA GLEASON*
Affiliation:
Department of Biological Sciences, Louisiana State University, Baton Rouge, Louisiana
*
Address correspondence to: Evanna Gleason, Department of Biological Sciences, Louisiana State University, 202 Life Sciences Building, Baton Rouge, LA 70803. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Nitric oxide (NO) is known to exert multiple effects on the function of many retinal neurons and their synapses. Therefore, it is equally important to understand the potential sources of NO within the retina. To explore this, we employ a combination of 4-amino-5-methylamino-2′,7′-difluorofluorescein diacetate (DAF-FM) based NO detection and immunohistochemistry for the NO synthetic enzymes, neuronal and endothelial nitric oxide synthase (nNOS and eNOS). We find DAF signals in photoreceptors, horizontal cells, amacrine cells, efferent synapses, Müller cells, and cells in the ganglion cell layer (GCL). nNOS immunoreactivity was consistent with the DAF signal with the exception that horizontal cells and Müller cells were not clearly labeled. eNOS-like immunoreactivity (eNOS-LI) was more widespread with photoreceptors, horizontal cells, occasional bipolar cells, amacrine cells, Müller cells, and cells in the GCL all showing labeling. Double labeling with antibodies raised against calretinin, syntaxin, and glutamine synthetase confirmed that horizontal cells, amacrine cells, and Müller cells (respectively) were expressing eNOS-LI. Although little or no nNOS labeling is observed in horizontal cells or Müller cells, the expression of eNOS-LI is consistent with the ability of these cells to produce NO. Together these results suggest that the capability to produce NO is widespread in the chicken retina. We propose that multiple forms of regulation for nNOS and eNOS play a role in the patterning of NO production in the chicken retina.

Keywords

Chicken retinaHorizontal cellsMüller cells
Type
Research Articles
Information
Visual Neuroscience , Volume 30 , Issue 3 , May 2013 , pp. 91 - 103
Copyright
Copyright © Cambridge University Press 2013 

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

Arnold, W.P., Mittal, C.K., Katsuki, S. & Murad, F. (1977). Nitric oxide activates guanylate cyclase and increases guanosine 3’:5’-cyclic monophosphate levels in various tissue preparations. Proceedings of the National Academy of Sciences of the United States of America 74, 3203–3207.CrossRefGoogle Scholar
Barnstable, C.J., Hofstein, R. & Akagawa, K. (1985). A marker of early amacrine cell development in rat retina. Brain Research 352, 286–290.CrossRefGoogle ScholarPubMed
Blom, J.J., Blute, T.A. & Eldred, W.D. (2009). Functional localization of the nitric oxide/cGMP pathway in the salamander retina. Visual Neuroscience 26, 275–286.CrossRefGoogle ScholarPubMed
Blute, T.A., Lee, M.R. & Eldred, W.D. (2000). Direct imaging of NMDA-stimulated nitric oxide production in the retina. Visual Neuroscience 17, 557–566.CrossRefGoogle ScholarPubMed
Brown, G.C. (2010). Nitric oxide and neuronal death. Nitric Oxide 23, 153–165.CrossRefGoogle ScholarPubMed
Caminos, E., Velasco, A., Jarrin, M., Aijon, J. & Lara, J.M. (1999). Protein kinase C-like immunoreactive cells in embryo and adult chicken retinas. Brain Research. Developmental Brain Research 118, 227–230.CrossRefGoogle ScholarPubMed
Cao, L. & Eldred, W.D. (2001). Subcellular localization of neuronal nitric oxide synthase in turtle retina: Electron immunocytochemistry. Visual Neuroscience 18, 949–960.CrossRefGoogle ScholarPubMed
Cobcroft, M., Vaccaro, T. & Mitrofanis, J. (1989). Distinct patterns of distribution among NADPH-diaphorase neurones of the guinea pig retina. Neuroscience Letters 103, 1–7.CrossRefGoogle ScholarPubMed
Crousillac, S., Colonna, J., McMains, E. & Gleason, E.L. (2009). Sphingosine-1-phosphate elicits receptor-dependent calcium signaling in retinal amacrine cells. Journal of Neurophysiology 102, 3295–3309.CrossRefGoogle ScholarPubMed
Crousillac, S., LeRouge, M., Rankin, M. & Gleason, E. (2003). Immunolocalization of TRPC channel subunits 1 and 4 in the chicken retina. Visual Neuroscience 20, 453–463.CrossRefGoogle ScholarPubMed
Davis, K.L., Martin, E., Turko, I.V. & Murad, F. (2001). Novel effects of nitric oxide. Annual Review of Pharmacology and Toxicology 41, 203–236.CrossRefGoogle ScholarPubMed
Dawson, T.M., Bredt, D.S., Fotuhi, M., Hwang, P.M. & Snyder, S.H. (1991). Nitric oxide synthase and neuronal NADPH diaphorase are identical in brain and peripheral tissues. Proceedings of the National Academy of Sciences of the United States of America 88, 7797–7801.CrossRefGoogle ScholarPubMed
DeVries, S.H. & Schwartz, E.A. (1989). Modulation of an electrical synapse between solitary pairs of catfish horizontal cells by dopamine and second messengers. The Journal of Physiology 414, 351–375.CrossRefGoogle ScholarPubMed
Eldred, W.D. & Blute, T.A. (2005). Imaging of nitric oxide in the retina. Vision Research 45, 3469–3486.CrossRefGoogle ScholarPubMed
Ellis, J.H., Richards, D.E. & Rogers, J.H. (1991). Calretinin and calbinding in the retina of the developing chick. Cell and Tissue Research 264, 192–208.CrossRefGoogle Scholar
Fischer, A.J., Stanke, J.J., Aloisio, G., Hoy, H. & Stell, W.K. (2007). Heterogeneity of horizontal cells in the chicken retina. The Journal of Comparative Neurology 500, 1154–1171.CrossRefGoogle ScholarPubMed
Fischer, A.J. & Stell, W.K. (1999). Nitric oxide synthase-containing cells in the retina, pigmented epithelium, choroid, and sclera of the chick eye. The Journal of Comparative Neurology 405, 1–14.3.0.CO;2-U>CrossRefGoogle ScholarPubMed
Garcia-Cardena, G., Oh, P., Liu, J., Schnitzer, J.E. & Sessa, W.C. (1996). Targeting of nitric oxide synthase to endothelial cell caveolae via palmitoylation: implications for nitric oxide signaling. Proceedings of the National Academy of Sciences of the United States of America 93, 6448–6453.CrossRefGoogle ScholarPubMed
Gleason, E., Borges, S. & Wilson, M. (1993). Synaptic transmission between pairs of retinal amacrine cells in culture. The Journal of Neuroscience 13, 2359–2370.CrossRefGoogle ScholarPubMed
Goureau, O., Regnier-Ricard, F., Jonet, L., Jeanny, J.C., Courtois, Y. & Chany-Fournier, F. (1997). Developmental expression of nitric oxide synthase isoform I and III in chick retina. Journal of Neuroscience Research 50, 104–113.3.0.CO;2-B>CrossRefGoogle ScholarPubMed
Hare, W.A. & Owen, W.G. (1998). Effects of bicarbonate versus HEPES buffering on measured properties of neurons in the salamander retina. Visual Neuroscience 15, 263–271.CrossRefGoogle ScholarPubMed
Haverkamp, S. & Eldred, W.D. (1998). Localization of nNOS in photoreceptor, bipolar and horizontal cells in turtle and rat retinas. Neuroreport 9, 2231–2235.CrossRefGoogle ScholarPubMed
Haverkamp, S., Kolb, H. & Cuenca, N. (1999). Endothelial nitric oxide synthase (eNOS) is localized to Müller cells in all vertebrate retinas. Vision Research 39, 2299–2303.CrossRefGoogle ScholarPubMed
Hoffpauir, B., McMains, E. & Gleason, E. (2006). Nitric oxide transiently converts synaptic inhibition to excitation in retinal amacrine cells. Journal of Neurophysiology 95, 2866–2877.CrossRefGoogle ScholarPubMed
Hope, B.T., Michael, G.J., Knigge, K.M. & Vincent, S.R. (1991). Neuronal NADPH diaphorase is a nitric oxide synthase. Proceedings of the National Academy of Sciences of the United States of America 88, 2811–2814.CrossRefGoogle ScholarPubMed
Icking, A., Matt, S., Opitz, N., Wiesenthal, A., Müller-Esterl, W. & Schilling, K. (2005). NOSTRIN functions as a homotrimeric adaptor protein facilitating internalization of eNOS. Journal of Cell Science 118, 5059–5069.CrossRefGoogle ScholarPubMed
Ishii, K., Kaneda, M., Li, H., Rockland, K.S. & Hashikawa, T. (2003). Neuron-specific distribution of P2X7 purinergic receptors in the monkey retina. The Journal of Comparative Neurology 459, 267–277.CrossRefGoogle ScholarPubMed
Ju, H., Zou, R., Venema, V.J. & Venema, RC (1997). Direct interaction of endothelial nitric-oxide synthase and caveolin-1 inhibits synthase activity. The Journal of Biological Chemistry 272, 18522–18525.CrossRefGoogle ScholarPubMed
Kim, I.B., Lee, E.J., Kim, K.Y., Ju, W.K., Oh, S.J., Joo, C.K. & Chun, M.H. (1999). Immunocytochemical localization of nitric oxide synthase in the mammalian retina. Neuroscience Letters 267, 193–196.CrossRefGoogle ScholarPubMed
Koistinaho, J., Swanson, R.A., de Vente, J. & Sagar, S.M. (1993). NADPH-diaphorase (nitric oxide synthase)-reactive amacrine cells of rabbit retina: putative target cells and stimulation by light. Neuroscience 57, 587–597.CrossRefGoogle ScholarPubMed
Kojima, H., Nakatsubo, N., Kikuchi, K., Kawahara, S., Kirino, Y., Nagoshi, H., Hirata, Y. & Nagano, T. (1998). Detection and imaging of nitric oxide with novel fluorescent indicators: diaminofluoresceins. Analytical Chemistry 70, 2446–2453.CrossRefGoogle ScholarPubMed
Koulen, P., Brandstatter, J.H., Kroger, S., Enz, R., Bormann, J. & Wassle, H. (1997). Immunocytochemical localization of the GABA(C) receptor rho subunits in the cat, goldfish, and chicken retina. The Journal of Comparative Neurology 380, 520–532.3.0.CO;2-3>CrossRefGoogle ScholarPubMed
Lane, P., Hao, G. & Gross, S.S. (2001). S-nitrosylation is emerging as a specific and fundamental posttranslational protein modification: Head-to-head comparison with O-phosphorylation. Science’s STKE: Signal Transduction Knowledge Environment 2001, re1.Google 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. The Journal of Neuroscience 14, 7641–7654.CrossRefGoogle ScholarPubMed
Lu, C. & McMahon, D.G. (1997). Modulation of hybrid bass retinal gap junctional channel gating by nitric oxide. The Journal of Physiology 499(Pt 3), 689–699.CrossRefGoogle ScholarPubMed
McMahon, D.G. & Ponomareva, L.V. (1996). Nitric oxide and cGMP modulate retinal glutamate receptors. Journal of Neurophysiology 76, 2307–2315.CrossRefGoogle ScholarPubMed
McMains, E., Krishnan, V., Prasad, S. & Gleason, E. (2011). Expression and localization of CLC chloride transport proteins in the avian retina. Plos One 6, 1–22.CrossRefGoogle ScholarPubMed
Michel, J.B., Feron, O., Sase, K., Prabhakar, P. & Michel, T. (1997). Caveolin versus calmodulin. Counterbalancing allosteric modulators of endothelial nitric oxide synthase. The Journal of Biological Chemistry 272, 25907–25912.CrossRefGoogle ScholarPubMed
Michel, T. & Vanhoutte, P.M. (2010). Cellular signaling and NO production. Pflugers Archiv: European Journal of Physiology 459, 807–816.CrossRefGoogle ScholarPubMed
Mills, S.L. & Massey, S.C. (1995). Differential properties of two gap junctional pathways made by AII amacrine cells. Nature 377, 734–737.CrossRefGoogle ScholarPubMed
Miyachi, E., Murakami, M. & Nakaki, T. (1990). Arginine blocks gap junctions between retinal horizontal cells. Neuroreport 1, 107–110.CrossRefGoogle ScholarPubMed
Nemargut, J.P. & Wang, G.Y. (2009). Inhibition of nitric oxide synthase desensitizes retinal ganglion cells to light by diminishing their excitatory synaptic currents under light adaptation. Vision Research 49, 2936–2947.CrossRefGoogle ScholarPubMed
Newman, E.A. (2001). Propagation of intercellular calcium waves in retinal astrocytes and Müller cells. The Journal of Neuroscience 21, 2215–2223.CrossRefGoogle ScholarPubMed
Newman, E.A. (2005). Calcium increases in retinal glial cells evoked by light-induced neuronal activity. The Journal of Neuroscience 25, 5502–5510.CrossRefGoogle ScholarPubMed
Newman, E.A. & Zahs, K.R. (1997). Calcium waves in retinal glial cells. Science 275, 844–847.CrossRefGoogle ScholarPubMed
Norenberg, M.D., Dutt, K. & Reif-Lehrer, L. (1980). Glutamine synthetase localization in cortisol-induced chick embryo retinas. The Journal of Cell Biology 84, 803–807.CrossRefGoogle ScholarPubMed
Oh, S.J., Kim, H.I., Kim, I.B., Kim, K.Y., Huh, W., Chung, J.W. & Chun, M.H. (1999). Morphology and synaptic connectivity of nitric oxide synthase-immunoreactive neurons in the guinea pig retina. Cell and Tissue Research 297, 397–408.CrossRefGoogle ScholarPubMed
Perez, M.T., 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, 207–217.CrossRefGoogle ScholarPubMed
Puthussery, T. & Fletcher, E.L. (2004). Synaptic localization of P2X7 receptors in the rat retina. The Journal of Comparative Neurology 472, 13–23.CrossRefGoogle ScholarPubMed
Rieke, F. & Schwartz, E.A. (1994). A cGMP-gated current can control exocytosis at cone synapses. Neuron 13, 863–873.CrossRefGoogle ScholarPubMed
Rios, H., Lopez-Costa, J.J., Fosser, N.S., Brusco, A. & Saavedra, J.P. (2000). Development of nitric oxide neurons in the chick embryo retina. Brain Research. Developmental Brain Research 120, 17–25.CrossRefGoogle ScholarPubMed
Sagar, S.M. (1986). NADPH diaphorase histochemistry in the rabbit retina. Brain Research 373, 153–158.CrossRefGoogle ScholarPubMed
Sandell, J.H. (1985). NADPH diaphorase cells in the mammalian inner retina. The Journal of Comparative Neurology 238, 466–472.CrossRefGoogle ScholarPubMed
Sato, M., Ohtsuka, T. & Stell, W.K. (2011). Endogenous nitric oxide enhances the light-response of cones during light-adaptation in the rat retina. Vision Research 51, 131–137.CrossRefGoogle ScholarPubMed
Savchenko, A., Barnes, S. & Kramer, R.H. (1997). Cyclic-nucleotide-gated channels mediate synaptic feedback by nitric oxide. Nature 390, 694–698.CrossRefGoogle ScholarPubMed
Schleicher, M., Brundin, F., Gross, S., Müller-Esterl, W. & Oess, S. (2005). Cell cycle-regulated inactivation of endothelial NO synthase through NOSIP-dependent targeting to the cytoskeleton. Molecular and Cellular Biology 25, 8251–8258.CrossRefGoogle ScholarPubMed
Seth, D. & Stamler, J.S. (2011). The SNO-proteome: Causation and classifications. Current Opinion in Chemical Biology 15, 129–136.CrossRefGoogle ScholarPubMed
Shaul, P.W., Smart, E.J., Robinson, L.J., German, Z., Yuhanna, I.S., Ying, Y., Anderson, R.G. & Michel, T. (1996). Acylation targets emdothelial nitric-oxide synthase to plasmalemmal caveolae. The Journal of Biological Chemistry 271, 6518–6522.CrossRefGoogle ScholarPubMed
Shen, Y., Liu, X.L. & Yang, X.L. (2006). N-methyl-D-aspartate receptors in the retina. Molecular Neurobiology 34, 163–179.CrossRefGoogle ScholarPubMed
Stamler, J.S., Toone, E.J., Lipton, S.A. & Sucher, N.J. (1997). (S)NO signals: Translocation, regulation, and a consensus motif. Neuron 18, 691–696.CrossRefGoogle Scholar
Sugimoto, K., Fujii, S., Takemasa, T. & Yamashita, K. (2000). Detection of intracellular nitric oxide using a combination of aldehyde fixatives with 4,5-diaminofluorescein diacetate. Histochemistry and Cell Biology 113, 341–347.CrossRefGoogle ScholarPubMed
Tracey, W.R., Nakane, M., Pollock, J.S. & Forstermann, 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, 1035–1040.CrossRefGoogle Scholar
Vaccaro, T.M., Cobcroft, M.D., Provis, J.M. & Mitrofanis, J. (1991). NADPH-diaphorase reactivity in adult and developing cat retinae. Cell and Tissue Research 265, 371–379.CrossRefGoogle ScholarPubMed
Vaney, D.I. & Young, H.M. (1988). GABA-like immunoreactivity in NADPH-diaphorase amacrine cells of the rabbit retina. Brain Research 474, 380–385.CrossRefGoogle ScholarPubMed
Vessey, K.A. & Fletcher, E.L. (2012). Rod and cone pathway signalling is altered in the P2X7 receptor knock out mouse. PLoS One 7, e29990.CrossRefGoogle ScholarPubMed
Vielma, A.H., Retamal, M.A. & Schmachtenberg, O. (2012). Nitric oxide signaling in the retina: what have we learned in two decades? Brain Research 1430, 112–125.CrossRefGoogle ScholarPubMed
Wang, G.Y., van der List, D.A., Nemargut, J.P., Coombs, J.L. & Chalupa, L.M. (2007). The sensitivity of light-evoked responses of retinal ganglion cells is decreased in nitric oxide synthase gene knockout mice. Journal of Vision 7, 7.1–7.13.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, 151–154.CrossRefGoogle ScholarPubMed
Weller, C., Lindstrom, S.H., De Grip, W.J. & Wilson, M. (2009). The area centralis in the chicken retina contains efferent target amacrine cells. Visual Neuroscience 26, 249–254.CrossRefGoogle ScholarPubMed
Wilson, M. & Lindstrom, S.H. (2011). What the bird’s brain tells the bird’s eye: the function of descending input to the avian retina. Visual Neuroscience 28, 337–350.CrossRefGoogle Scholar
Wilson, M., Nacsa, N., Hart, N.S., Weller, C. & Vaney, D.I. (2011). Regional distribution of nitrergic neurons in the inner retina of the chicken. Visual Neuroscience 28, 205–220.CrossRefGoogle ScholarPubMed
Xin, D. & Bloomfield, S.A. (2000). Effects of nitric oxide on horizontal cells in the rabbit retina. Visual Neuroscience 17, 799–811.CrossRefGoogle ScholarPubMed
Yazulla, S. (2008). Endocannabinoids in the retina: From marijuana to neuroprotection. Progress in Retina and Eye Research 27, 501–526.CrossRefGoogle ScholarPubMed
Zhou, L. & Zhu, D.Y. (2009). Neuronal nitric oxide synthase: Structure, subcellular localization, regulation, and clinical implications. Nitric Oxide 20, 223–230.CrossRefGoogle ScholarPubMed
Zemel, E., Eyal, O. & Lei, B. (1996). NADPH diaphorase activity in mammalian retina is modulated byt the state of visual adaptation. Visual Neuroscience 13, 863–871.CrossRefGoogle Scholar
Zimmermann, K., Opitz, N., Dedio, J., Renne, C., Müller-Esterl, W. & Oess, S. (2002). NOSTRIN: A protein modulating nitric oxide release and subcellular distribution of endothelial nitric oxide synthase. Proceedings of the National Academy of Sciences of the United States of America 99, 17167–17172.CrossRefGoogle ScholarPubMed