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Functional localization of the nitric oxide/cGMP pathway in the salamander retina

Published online by Cambridge University Press:  01 May 2009

JAN J. BLOM ,
TODD A. BLUTE  and
WILLIAM D. ELDRED
JAN J. BLOM
Affiliation:
Department of Biology, Boston University, Boston, Massachusetts
TODD A. BLUTE
Affiliation:
Department of Biology, Boston University, Boston, Massachusetts
WILLIAM D. ELDRED*
Affiliation:
Department of Biology, Boston University, Boston, Massachusetts
*
*Address correspondence and reprint requests to: William D. Eldred, Department of Biology, Boston University, 5 Cummington Street, Boston, MA 02215. E-mail: [email protected]
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Abstract

Nitric oxide (NO) is a gaseous neuromodulator that has physiological functions in every cell type in the retina. Evidence indicates that NO often plays a role in the processing of visual information in the retina through the second messenger cyclic guanosine monophosphate (cGMP). Despite numerous structural and functional studies of this signaling pathway in the retina, none have examined many of the elements of this pathway within a single study in a single species. In this study, the NO/cGMP pathway was localized to specific regions and cell types within the inner and outer retina. We have immunocytochemically localized nitric oxide synthase, the enzyme that produces NO, in photoreceptor ellipsoids, four distinct classes of amacrine cells, Müller and bipolar cells, somata in the ganglion cell layer, as well as in processes within both plexiform layers. Additionally, we localized NO production in specific cell types using the NO-sensitive dye diaminofluorescein. cGMP immunocytochemistry was used to functionally localize soluble guanylate cyclase that was activated by an NO donor in select amacrine and bipolar cell classes. Analysis of cGMP and its downstream target, cGMP-dependent protein kinase II (PKGII), showed colocalization within processes in the outer retina as well as in somata in the inner retina. The results of this study showed that the NO/cGMP signaling pathway was functional and its components were widely distributed throughout specific cell types in the outer and inner salamander retina.

Keywords

NOcGMPsGCPKGRetina
Type
Research Articles
Information
Visual Neuroscience , Volume 26 , Issue 3 , May 2009 , pp. 275 - 286
Copyright
Copyright © Cambridge University Press 2009

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References

Ahmad, I., Leinders-Zufall, T., Kocsis, J.D., Shepherd, G.M., Zufall, F. & Barnstable, C.J. (1994). Retinal ganglion cells express a cGMP-gated cation conductance activatable by nitric oxide donors. Neuron 12, 155–165.CrossRefGoogle ScholarPubMed
Blute, T.A., Lee, H.K., Huffmaster, T., Haverkamp, S. & Eldred, W.D. (2000 a). Localization of natriuretic peptides and their activation of particulate guanylate cyclase and nitric oxide synthase in the retina. Journal of Comparative Neurology 424, 689–700.3.0.CO;2-K>CrossRefGoogle ScholarPubMed
Blute, T.A., Lee, M.R. & Eldred, W.D. (2000 b). Direct imaging of NMDA-stimulated nitric oxide production in the retina. Visual Neuroscience 17, 557–566.CrossRefGoogle ScholarPubMed
Blute, T.A., Velasco, P. & Eldred, W.D. (1998). Functional localization of soluble guanylate cyclase in turtle retina: Modulation of cGMP by nitric oxide donors. Visual Neuroscience 15, 485–498.CrossRefGoogle ScholarPubMed
Cimini, B.A., Strang, C.E., Wotring, V.E., Keyser, K.T. & Eldred, W.D. (2008). Role of acetylcholine in nitric oxide production in the salamander retina. Journal of Comparative Neurology 507, 1952–1963.CrossRefGoogle ScholarPubMed
de la Villa, P., Kurahashi, T. & Kaneko, A. (1995). L-glutamate-induced responses and cGMP-activated channels in three subtypes of retinal bipolar cells dissociated from the cat. The Journal of Neuroscience 15, 3571–3582.CrossRefGoogle ScholarPubMed
de Vente, J., Steinbusch, H.W. & Schipper, J. (1987). A new approach to immunocytochemistry of 3′,5′-cyclic guanosine monophosphate: Preparation, specificity, and initial application of a new antiserum against formaldehyde-fixed 3′,5′-cyclic guanosine monophosphate. Neuroscience 22, 361–373.CrossRefGoogle Scholar
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. The Journal of Physiology 414, 351–375.CrossRefGoogle ScholarPubMed
Eldred, W.D. (2000). Nitric oxide in the retina. Functional neuroanatomy of the nitric oxide system. In Handbook of Chemical Neuroanatomy Vol. 17, ed. Steinbusch, H.W.M., De Vente, J. & Vincent, S.R., pp. 111–145. New York: Elsevier.Google Scholar
Eldred, W.D. & Blute, T.A. (2005). Imaging of nitric oxide in the retina. Vision Research 45, 3469–3486.CrossRefGoogle ScholarPubMed
Goldstein, I.M., Ostwald, P. & Roth, S. (1996). Nitric oxide: A review of its role in retinal function and disease. Vision Research 36, 2979–2994.CrossRefGoogle Scholar
Griffiths, C. & Garthwaite, J. (2001). The shaping of nitric oxide signals by a cellular sink. The Journal of Physiology 536, 855–862.CrossRefGoogle ScholarPubMed
Hirooka, K., Kourennyi, D.E. & Barnes, S. (2000). Calcium channel activation facilitated by nitric oxide in retinal ganglion cells. Journal of Neurophysiology 83, 198–206.CrossRefGoogle ScholarPubMed
Hofmann, F., Feil, R., Kleppisch, T. & Schlossmann, J. (2006). Function of cGMP-dependent protein kinases as revealed by gene deletion. Physiological Reviews 86, 1–23.CrossRefGoogle ScholarPubMed
Hogg, N. (2002). The biochemistry and physiology of S-nitrosothiols. Annual Review of Pharmacology and Toxicology 42, 585–600.CrossRefGoogle ScholarPubMed
Kurenni, D.E., Thurlow, G.A., Turner, R.W., Moroz, L.L., Sharkey, K.A. & Barnes, S. (1995). Nitric oxide synthase in tiger salamander retina. Journal of Comparative Neurology 361, 525–536.CrossRefGoogle 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, 315–324.CrossRefGoogle ScholarPubMed
Kusaka, S., Dabin, I., Barnstable, C.J. & Puro, D.G. (1996). cGMP-mediated effects on the physiology of bovine and human retinal Muller (glial) cells. The Journal of Physiology 497(Pt 3), 813–824.CrossRefGoogle ScholarPubMed
Liepe, B.A., Stone, C., Koistinaho, J. & Copenhagen, D.R. (1994). Nitric oxide synthase in Muller 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
Lukasiewicz, P.D., Maple, B.R. & Werblin, F.S. (1994). A novel GABA receptor on bipolar cell terminals in the tiger salamander retina. The Journal of Neuroscience 14, 1202–1212.CrossRefGoogle ScholarPubMed
Maple, B.R., Zhang, J., Pang, J.J., Gao, F. & Wu, S.M. (2005). Characterization of displaced bipolar cells in the tiger salamander retina. Vision Research 45, 697–705.CrossRefGoogle ScholarPubMed
Miyachi, E., Miyakawa, A. & Murakami, M. (1991). Modulation of electrical coupling between retinal horizontal cells by intracellular messengers. Neuroscience Research. Supplement 15, S41–S49.Google ScholarPubMed
Miyachi, E., Murakami, M. & Nakaki, T. (1990). Arginine blocks gap junctions between retinal horizontal cells. Neuroreport 1, 107–110.CrossRefGoogle ScholarPubMed
Nawy, S. & Jahr, C.E. (1991). cGMP-gated conductance in retinal bipolar cells is suppressed by the photoreceptor transmitter. Neuron 7, 677–683.CrossRefGoogle ScholarPubMed
Pang, J.J., Gao, F. & Wu, S.M. (2002). Segregation and integration of visual channels: Layer-by-layer computation of ON-OFF signals by amacrine cell dendrites. The Journal of Neuroscience 22, 4693–4701.CrossRefGoogle ScholarPubMed
Pang, J.J., Gao, F. & Wu, S.M. (2004). Stratum-by-stratum projection of light response attributes by retinal bipolar cells of Ambystoma. The Journal of Physiology 558, 249–262.CrossRefGoogle ScholarPubMed
Pow, D.V. & Crook, D.K. (1995). Immunocytochemical evidence for the presence of high levels of reduced glutathione in radial glial cells and horizontal cells in the rabbit retina. Neuroscience Letters 193, 25–28.CrossRefGoogle ScholarPubMed
Shiells, R. & Falk, G. (1992). Retinal on-bipolar cells contain a nitric oxide-sensitive guanylate cyclase. Neuroreport 3, 845–848.CrossRefGoogle ScholarPubMed
Singh, R.J., Hogg, N., Joseph, J. & Kalyanaraman, B. (1996). Mechanism of nitric oxide release from S-nitrosothiols. The Journal of Biological Chemistry 271, 18596–18603.CrossRefGoogle ScholarPubMed
Sitaramayya, A. (2002). Soluble guanylate cyclases in the retina. Molecular and Cellular Biochemistry 230, 177–186.CrossRefGoogle ScholarPubMed
Upchurch, G.R. Jr, Welch, G.N. & Loscalzo, J. (1995). S-nitrosothiols: Chemistry, biochemistry, and biological actions. Advances in Pharmacology 34, 343–349.CrossRefGoogle ScholarPubMed
Wood, J. & Garthwaite, J. (1994). Models of the diffusional spread of nitric oxide: Implications for neural nitric oxide signalling and its pharmacological properties. Neuropharmacology 33, 1235–1244.CrossRefGoogle ScholarPubMed
Wu, S.M., Gao, F. & Maple, B.R. (2000). Functional architecture of synapses in the inner retina: Segregation of visual signals by stratification of bipolar cell axon terminals. The Journal of Neuroscience 20, 4462–4470.CrossRefGoogle ScholarPubMed
Yu, D. & Eldred, W.D. (2003). GABA(A) and GABA(C) receptor antagonists increase retinal cyclic GMP levels through nitric oxide synthase. Visual Neuroscience 20, 627–637.CrossRefGoogle Scholar
Yu, D. & Eldred, W.D. (2005 a). Gycine and GABA interact to regulate the nitric oxide/cGMP signaling pathway in the turtle retina. Visual Neuroscience 22, 825–838.CrossRefGoogle ScholarPubMed
Yu, D. & Eldred, W.D. (2005 b). Nitric oxide stimulates gamma-aminobutyric acid release and inhibits glycine release in retina. Journal of Comparative Neurology 483, 278–291.CrossRefGoogle ScholarPubMed
Zai, A., Rudd, M.A., Scribner, A.W. & Loscalzo, J. (1999). Cell-surface protein disulfide isomerase catalyzes transnitrosation and regulates intracellular transfer of nitric oxide. Journal of Clinical Investigation 103, 393–399.CrossRefGoogle ScholarPubMed
Zhang, N., Beuve, A. & Townes-Anderson, E. (2005). The nitric oxide-cGMP signaling pathway differentially regulates presynaptic structural plasticity in cone and rod cells. The Journal of Neuroscience 25, 2761–2770.CrossRefGoogle ScholarPubMed
Zhang, X. & Cote, R.H. (2005). cGMP signaling in vertebrate retinal photoreceptor cells. Frontiers in Bioscience 10, 1191–1204.CrossRefGoogle ScholarPubMed