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Specialized neuropeptide Y- and glucagon-like immunoreactive amacrine cells in the peripheral retina of the turtle

Published online by Cambridge University Press:  02 June 2009

Randall K. Wetzel  and
William D. Eldred
Randall K. Wetzel
Affiliation:
Department of Biology, Boston University, Boston
William D. Eldred
Affiliation:
Department of Biology, Boston University, Boston
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Abstract

There are many regional differences in cell morphology and neurochemistry in the retina. This study examined a specialized population of neuropeptide Y- and glucagon-like immunoreactive amacrine cells in the peripheral retina of the turtle. Some of the dendritic processes from these peptidergic amacrine cells formed a dense circumferentially oriented nerve fiber plexus which ran parallel to the ora serrata. Collaterals from this plexus projected into and innervated the nonpigmented ciliary epithelium in the pars plana region of the ciliary body. Electron microscopy revealed that the neuropeptide Y- and glucagon-like immunoreactive processes in the ciliary epithelium contained many labeled, large dense-cored vesicles. Small crystals of lipid-soluble fluorescent dye were implanted in the retina near the ora serrata in fixed retinal tissue to search for other peripheral retinal specializations. Numerous thick and thin cell processes oriented parallel to the ora serrata were labeled in the retina by the dye. In addition, many dye-labeled somata with circumferentially oriented dendritic arborizations were seen in the extreme periphery of the retina. Many of these dye-labeled cells and processes were clearly not associated with the neuropeptide Y- and glucagon-like immunoreactive cells described above. This study has shown that some peptidergic neurons in the peripheral retina have a unique morphology in comparison to more centrally located cells. The function of these specialized peripheral cells is not established, but the innervation of the ciliary epithelium by peptidergic amacrine cells suggests that they may be involved in control of aqueous inflow.

Keywords

Neuropeptide YGlucagonRetinaOra serrataCiliary epithelium
Type
Research Articles
Information
Visual Neuroscience , Volume 14 , Issue 5 , September 1997 , pp. 867 - 877
Copyright
Copyright © Cambridge University Press 1997

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References

Bartels, S.P., Lee, S.R. & Neufeld, A.H. (1987). The effects of forskolin on cyclic AMP, intraocular pressure and aqueous humor formation in rabbits. Current Eye Research 6, 307–320.CrossRefGoogle ScholarPubMed
Bataille, D. (1989). Glucagon and related peptides. In Peptide Hormones as Prohormones, ed. Martinez, J., pp. 104–126. New York: Halsted Press.Google Scholar
Bausher, L.P. & Horio, B. (1990). Neuropeptide Y and somatostatin inhibit stimulated cyclic AMP production in rabbit ciliary processes. Current Eye Research 9, 371–378.CrossRefGoogle ScholarPubMed
Brecha, N.C., Eldred, W., Kuljis, R.O. & Karten, H.J. (1984). Identification and localization of biologically active peptides in the vertebrate retina. In Progress in Retinal Research, vol. 3, ed. Osborne, N. & Chader, G., pp. 185–226. New York: Pergamon Press.Google Scholar
Brubaker, R.F. (1991). Flow of aqueous humor in humans. Investigative Ophthalmology and Visual Science 32, 3145–3166.Google ScholarPubMed
Bruun, A. (1992). The action of NPY on adenylate cyclase in rabbit retina. Investigative Ophthalmology and Visual Science 33, 1033.Google Scholar
Bruun, A., Ehinger, B. & Ekman, R. (1991). Characterization of neuropeptide Y-like immunoreactivity in vertebrate retina. Experimental Eye Research 53, 539–543.CrossRefGoogle ScholarPubMed
Bruun, A., Ehinger, B., Sytsma, V. & Tornqvist, K. (1985). Retinal neuropeptides in the skates, Raja clavata, R. radiata R. oscellata (Elas- mobranchii). Cell and Tissue Research 241, 17–24.CrossRefGoogle Scholar
Bruun, A., Ehinger, B., Sundler, E, Tornqvist, K. & Uddman, R. (1984). Neuropeptide Y immunoreactive neurons in the guinea-pig uvea and retina. Investigative Ophthalmology and Visual Science 25, 1113–1123.Google ScholarPubMed
Burstein, N.L., Sears, M.L. & Mead, A. (1984). Aqueous flow in human eyes is reduced by forskolin, a potent adenylate cyclase activator. Experimental Eye Research 39, 745–749.CrossRefGoogle ScholarPubMed
Caprioli, J. & Sears, M. (1984). The adenylate cyclase receptor complex and aqueous humor formation. Yale Journal of Biology and Medicine 57, 283–300.Google ScholarPubMed
Caprioli, J., Sears, M., Bausher, L., Gregory, D. & Mead, A. (1984). Forskolin lowers intraocular pressure by reducing aqueous flow. Investigative Ophthalmology and Visual Science 25, 268–277.Google Scholar
Cepelik, J. & Hynie, S. (1990). Inhibitory effects of neuropeptide Y on adenylate cyclase of rabbit ciliary processes. Current Eye Research 9, 121–128.CrossRefGoogle ScholarPubMed
Cervetto, L., Marchiafava, P.L. & Pasino, E. (1976). Influence of efferent retinal fibers on responsiveness of ganglion cells to light. Nature 260, 56–57.CrossRefGoogle ScholarPubMed
Coca-Prados, M. & Lopez-Briones, G. (1987). Evidence thai the α and α(+) isoforms of the catalytic subunit of (Na +, K+) ATPase reside in distinct ciliary epithelial cells of the mammalian eye. Biochemical and Biophysical Research Communications 145, 460–466.CrossRefGoogle Scholar
Conlon, J.M. & Hicks, J.W. (1990). Isolation and structural characterization of insulin, glucagon, and somatostatin from the turtle, Pseudemys scripta. Peptides 11, 461–466.CrossRefGoogle ScholarPubMed
Crook, R.B., Lui, G.M., Alvarado, J.A., Fauss, D.J. & Polansky, J.R. (1994). High affinity vasoactive intestinal peptide receptors on fetal human nonpigmented ciliary epithelial cells. Current Eye Research 13, 271–279.CrossRefGoogle ScholarPubMed
Das, A., Pansky, B. & Budd, G.C (1985). Glucagon-like immunoreactivity in mouse and rat retina. Neuroscience Letters 60, 215–218.CrossRefGoogle ScholarPubMed
Eldred, W.D., Zucker, C, Karten, H.J. & Yazulla, S. (1983). Comparison of fixation and penetration techniques for use in ultrastructural immunocytochemistry. Journal of Histochemistry and Cytochemistry 31, 285–292.CrossRefGoogle ScholarPubMed
Eldred, W.D. & Karten, H.J. (1983). Characterization and quantification of peptidergic amacrine cells in the turtle retina: Enkephalin, neurotensin, and glucagon. Journal of Comparative Neurology 221, 371–381.CrossRefGoogle ScholarPubMed
Eldred, W.D. & Cheung, K. (1988). Immunocytochemical localization of glycine in the retina of the turtle (Pseudemys scripta). Visual Neuroscience 2, 333–338.Google Scholar
Fernandez-Durango, R., Sanchez, D. & Fernandez-Cruz, A. (1990). Identification of glucagon receptors in rat retina. Journal of Neuro-chemistry 54, 1233–1237.CrossRefGoogle ScholarPubMed
Ferriero, D.M. & Sagar, S.M. (1989). Development of neuropeptide Y-immunoreactive neurons in the rat retina. Brain Research and Developmental Brain Research 48, 19–26.CrossRefGoogle ScholarPubMed
Flugel, C. & Lütjen-Drecoll, E. (1988). Presence and distribution of Na+/K+-ATPase in the ciliary epithelium of the rabbit. Histochemistry 88, 613–621.CrossRefGoogle ScholarPubMed
Flugel, C, Lütjen-Drecoll, E., Zadunaisk, J.A. & Wiederholt, M. (1989). Regional differences in the morphology and enzyme distribution of the spiny dogfish (Squalus acanthias) ciliary epithelium. Experimental Eye Research 49, 1097–1114.CrossRefGoogle ScholarPubMed
Ghosh, S., Hernando, N., Martin-Alonso, J.M., Martin-Vasallo, P. & Coca-Prados, M. (1991). Expression of multiple Na+, K+-ATPase genes reveals a gradient of isoforms along the nonpigmented ciliary epithelium: Functional implications in aqueous humor secretion. Journal of Cellular Physiology 149, 184–194.CrossRefGoogle ScholarPubMed
Gregory, D., Sears, M., Bausher, L., Mishima, H. & Meade, A. (1981). Intraocular pressure and aqueous flow are decreased by cholera toxin. Investigative Ophthalmology and Visual Science 20, 371–381.Google ScholarPubMed
Grün, G. (1982). The development of the vertebrate retina: A comparative survey. Advances in Anatomy Embryology and Cell Biology 78, 1–85.CrossRefGoogle ScholarPubMed
Grundemar, L., Wahlestedt, C & Wang, Z. (1993). Neuropeptide Y suppresses the neurogenic inflammatory response in the rabbit eye; mode of action. Regulatory Peptides 43, 57–64.CrossRefGoogle ScholarPubMed
Hiscock, J. & Straznicky, C. (1989). Neuropeptide Y-like immunoreactive amacrine cells in the retina of Bufo marinus. Brain Research 494, 55–64.CrossRefGoogle ScholarPubMed
Hitchcock, P.F. & Easter, S.S. Jr (1986). Retinal ganglion cells in goldfish: A qualitative classification into four morphological types, and a quantitative study of the development of one of them. Journal of Neuroscience 6, 1037–1050.CrossRefGoogle Scholar
Holthofer, H., Siegel, G.J., Tarkkanen, A. & Tervo, T. (1991). Im-munocytochemical localization of carbonic anhydrase, NaK-ATPase and the bicarbonate chloride exchanger in the anterior segment of the human eye. Acta Ophthalmologica 69, 149–154.CrossRefGoogle ScholarPubMed
Isayama, T. & Eldred, W.D. (1988). Neuropeptide Y-immunoreactive amacrine cells in the retina of the turtle Pseudemys scripta elegans. Journal of Comparative Neurology 271, 56–66.CrossRefGoogle ScholarPubMed
Isayama, T.Polak, J. & Eldred, W.D. (1988). Synaptic analysis of amacrine cells with neuropeptide-Y-like immunoreactivity in turtle retina. Journal of Comparative Neurology 275, 452–459.CrossRefGoogle ScholarPubMed
Johns, P.R. (1977). Growlh of the adult goldfish eye. III. Source of the new retinal cells. Journal of Comparative Neurology 176, 343–357.CrossRefGoogle Scholar
Jumblatt, J.E. & Gooch, J.M. (1990). Neuropeptide Y modulates adenylate cyclase in the rabbit iris ciliary body and ciliary epithelium. Experimental Eye Research 51, 229–231.CrossRefGoogle ScholarPubMed
Katayama, Y, Kiyama, H., Arai, Y. & Tohyama, M. (1984). Immuno-reactive avian pancreatic polypeptide in the chicken retina: Overall distribution. Brain Research 310, 164–167.CrossRefGoogle Scholar
Koh, S.M., Kyritsis, A. & Chader, G.J. (1984). Interaction of neuropeptides and cultured glial (Müller) cells of the chick retina: Elevation of intracellular cyclic AMP by vasoactive intestinal peptide and glucagon. Journal of Neurochemistry 43, 199–203.CrossRefGoogle ScholarPubMed
Kuwayama, I.Ismmoto, I., Flikuda, M., Shimizu, Y, Shiosaka, S., Inagki, S., Senba, E., Sakanaka, M., Takagi, H., Takatsuki, K., Hara, Y., Kawai, Y. & Tohyama, M. (1982). Overall distribution of glucagon-like immunoreactivity in the chicken retina: An immunohis-tochemical study with flat-mounts. Investigative Ophthalmology and Visual Science 22, 681–686.Google Scholar
Larhammar, D., Soderberg, C. & Blomquist, A.G. (1993). Evolution of the neuropeptide Y family of peptides. In The Biology of Neuropeptide Y and Related Peptides, ed. Colmers, W.F. & Wahlestedt, C, pp. 1–41. Totowa, New Jersey: Humana Press, Inc.Google Scholar
Lee, P.Y., Podos, S.M., Severin, C. & Mittag, T.W. (1984). The effect of topically applied forskolin on aqueous humor dynamics in cynomolgus monkeys. Investigative Ophthalmology and Visual Science 25, 1206–1209.Google Scholar
Maccarrone, C. & Jarrott, B. (1985). Differences in regional brain concentrations of neuropeptide Y in spontaneously hypertensive (SH) and Wistar-Kyoto (WKY) rats. Brain Research 345, 165–169.CrossRefGoogle ScholarPubMed
Marchiafava, PL. (1976). Centrifugal actions on amacrine and ganglion cells in the retina of the turtle. Journal of Physiology 255, 137–155.CrossRefGoogle ScholarPubMed
McNellis, E.L. & Bausher, L.P. (1991). Stimulatory and inhibitory cyclic AMP responses in rabbit ciliary processes after cervical ganglion-ectomy. Current Eye Research 10, 399–407.CrossRefGoogle Scholar
Meyer-Bothling, U., Bron, A.J. & Osborne, N.N. (1993). Topical application of serotonin or the 5-HT1agonist 5-CT intraocular pressure in rabbits. Investigative Ophthalmology and Visual Science 34, 3035–3042.Google ScholarPubMed
Mishima, H.K., Kiuchi, Y., Yokoyama, T., Yasumoto, T. & Yamazaki, M. (1991). A cyclic AMP phosphodiesterase inhibitor, 8'-pival-oyloxymethyl ester (POM-ester) of griseolic acid, lowers rabbit intraocular pressure. Current Eye Research 10, 817–822.CrossRefGoogle ScholarPubMed
Mittag, T.W. & Tormay, A. (1985). Drug responses of adenylate cyclase in iris-ciliary body determined by adenine labeling. Investigative Ophthalmology and Visual Science 26, 396–399.Google Scholar
Mittag, T.W., Tormay, A. & Podos, S.M. (1987). Vasoactive intestinal peptide and intraocular pressure: Adenylate cyclase activation and binding sites for vasoactive intestinal peptide in membranes of ocular ciliary processes. Journal of Pharmacology and Experimental Therapeutics 241, 230–235.Google ScholarPubMed
Mittag, T.W., Tormay, A., Taniguchi, T. & Ortega, M. (1993 a). Calmodulin activated adenylyl cyclase in ciliary processes: Additivity of calcium and cyclic adenosine monophosphate signals on intraocular pressure response on the rabbit eye. Investigative Ophthalmology and Visual Science 34, 2041–2048.Google ScholarPubMed
Mittag, T.W., Tormay, A., Severin, C, Taniguchi, T, Lee, P., Wang, R. & Podos, S.M. (1993 b). Effects of Al3+ and Be2+ ions combined with NaF on ciliary process adenylyl cyclase activity and aqueous humor dynamics in the rabbit eye. Investigative Ophthalmology and Visual Science 34, 606–612.Google ScholarPubMed
Mittag, T.W. & Tormay, A. (1993). Interactions between forskolin, Gs, and divalent cations on ciliary process adenylyl cyclase and intraocular pressure in the rabbit eye. Experimental Eye Research 57, 13–19.CrossRefGoogle ScholarPubMed
Nakano, T., Fujimoto, K., Honda, Y. & Ogawa, K. (1992). Cytochemistry of protein kinase C and Na-K-ATPase in rabbit ciliary processes treated with phorbol ester. Investigative Ophthalmology and Visual Science 33, 3455–3462.Google ScholarPubMed
Nilsson, S.F.E., Sperber, G.O. & Bill, A. (1986). Effects of vasoactive intestinal polypeptide (VIP) on intraocular pressure, facility of outflow and formation of aqueous humor in the monkey. Experimental Eye Research 43, 849–857.CrossRefGoogle ScholarPubMed
Osborne, N.N., Patel, S., Terenghi, G., Allen, J.M., Polak, J.M. & Bloom, S.R. (1985). Neuropeptide Y (NPY)-like immunoreactive amacrine cells in retinas of frog and goldfish. Cell and Tissue Research 241, 651–656.CrossRefGoogle ScholarPubMed
Riley, M.V. & Kishida, K. (1986). ATPases of ciliary epithelium: Cellular and subcellular distribution and probable role in secretion of aqueous humor. Experimental Eye Research 42, 559–568.CrossRefGoogle ScholarPubMed
Sagar, S.M. (1987). Somatostatin-like immunoreactive material in the rabbit retina: Immunohistochemical staining using monoclonal antibodies. Journal of Comparative Neurology 266, 291–299.CrossRefGoogle ScholarPubMed
Schutte, M. & Weiler, R. (1988). Mesencephalic innervation of the turtle retina by a single serotonin-containing neuron. Neuroscience Letters 91, 289–294.CrossRefGoogle ScholarPubMed
Sears, M.L. (1985). Regulation of aqueous flow by the adenylate cyclase receptor complex in the ciliary epithelium. American Journal of Ophthalmology 100, 194–198.CrossRefGoogle ScholarPubMed
Spira, A.W., Shimizo, Y. & Rorstad, O.P. (1984). Localization, chromatographic characterization, and development of somatostatin-like immunoreactivity in the guinea pig retina. Journal of Neuroscience 4, 3069–3079.CrossRefGoogle ScholarPubMed
Tager, H.S. (1984). Glucagon-containing and glucagon-related peptides: Evolutionary, structural and biosynthetic considerations. In Evolution and Tumor Pathology of the Neuroendocrine System, ed. Falkner, S., Hakanson, R. & Sundler, F., pp. 285–310. New York, New York: Elsevier.Google Scholar
Tatemoto, K., Carlquist, M. & Mutt, V. (1982). Neuropeptide Y—a novel brain peptide with structural similarities to peptide YY and pancreatic polypeptide. Nature 296, 659–660.CrossRefGoogle ScholarPubMed
Tobin, A.B. & Osborne, N.N. (1989). Evidence for the presence pf serotonin receptors negatively coupled to adenylate cyclase in the rabbitiris-ciliary body. Journal of Neurochemistry 53, 686–691.CrossRefGoogle Scholar
Tornquist, K. & Ehinger, B. (1988). Peptide immunoreactive neurons in the human retina. Investigative Ophthalmology and Visual Science 29, 680–686.Google Scholar
Usukura, J., Fain, G.L. & Bok, D. (1988). [3H]Ouabain localization of Na-K ATPase in the epithelium of rabbit ciliary body pars plicata. Investigative Ophthalmology and Visual Science 29, 606–614.Google Scholar
Verstappen, A., Van Reeth, O., Vaudry, H., Pelletier, G. & Vander-haeghen, J.J. (1986). Demonstration of a neuropeptide Y (NPY)-like immunoreactivity in the pigeon retina. Neuroscience Letters 70, 193–197.CrossRefGoogle ScholarPubMed
Weiler, R. (1985). Mesencephalic pathway to the retina exhibits enkephalin-like immunoreactivity. Neuroscience Letters 55, 11–16.CrossRefGoogle Scholar
Wetts, R., Serbedzija, G.N. & Fraser, S.E. (1989). Cell lineage analysis reveals multipotenl precursors in the ciliary margin of the frog retina. Developmental Biology 136, 254–263.CrossRefGoogle ScholarPubMed
Wetzel, R.K. & Eldred, W.D. (1997). Localization of carbonic anhydrase in the turtle retina and ciliary epithelium using enzyme histochemistry and immunocytochemistry (in preparation).Google Scholar
Williamson, D.E. & Eldred, W.D. (1989). Amacrine and ganglion cells with corticotropin-releasing-factor-like immunoreactivity in the turtle retina. Journal of Comparative Neurology 280, 424–435.CrossRefGoogle ScholarPubMed
Yang, C. & Yazulla, S. (1986). Neuropeptide-like immunoreactive cells in the retina of the larval tiger salamander: Attention to the symmetry of dendritic projections. Journal of Comparative Neurology 248, 105–118.CrossRefGoogle Scholar
Yaqub, A. & Eldred, W.D. (1991). Localization of aspartate-like immunoreactivity in the retina of the turtle (Pseudemys scripta). Journal of Comparative Neurology 312, 584–598.CrossRefGoogle ScholarPubMed
Zhang, D. & Eldred, W.D. (1992). Colocalization of enkephalin-, glucagon-, and corticotropin-releasing factor-like immunoreactivity in GABAergic amacrine cells in turtle retina. Brain Research 596, 46–57.CrossRefGoogle ScholarPubMed
Zhang, D. & Eldred, W.D. (1994). Anatomical characterization of retinal ganglion cells that project to the nucleus of the basal optic root in the turtle (Pseudemys scripta elegans). Neuroscience 61, 707–718.CrossRefGoogle Scholar