Summary
The retinal proteins opsin,α-transducin, S-antigen and interstitial retinol-binding protein (IRBP) are essential for the processes of vision. By use of immunocyto-chemistry we have employed antibodies directed against these “photoreceptor proteins” in an attempt to identify the photoreceptor systems (retina, pineal and deep brain) of the Japanese quail. Opsin immunostaining was identified within many outer (basal portion) and inner segments of retinal photoreceptor cells and limited numbers of photoreceptor perikarya. Opsin immunostaining was also demonstrated in limited numbers of pinealocytes with all parts of these cells being immunoreactive. These results differ from previous observations. In contrast to the results obtained with the antibody against opsin, S-antigen andα-transducin immunostaining was seen throughout the entire outer segments and many photoreceptor perikarya of the retina. In the pineal organ immunostaining was seen in numerous pinealocytes in all follicles. These results conform to previous findings in birds. In addition, IRBP has been demonstrated for the first time in the avian retina and pineal organ. These findings underline the structural and functional similarities between the retina and pineal organ and provide additional support for a photoreceptive role of the avian pineal. No specific staining was detected in any other region of the brain in the Japanese quail; the hypothalamic photoreceptors of birds remain unidentified.
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References
Bridges CDB (1984) Retinoids in photosensitive systems. In: Sporn MB, Roberts AB, Goodman DS (eds) The retinoids. Academic Press, New York, Vol. 2, pp 125–176
Bridges CDB, Landers RA, Fong S-L, Liou GI (1986) Interstitial retinol-binding protein (IRBP) in rat and bovine pineal organs: Evolutionary vestige or functional molecule? In: O'Brien PS, Klein DC (eds) Pineal Retinal Relationships. Academic Press, New York (in Press)
Bridges CDB, Fong SL, Landers RA, Foster RG (1986) IRBP-like proteins in the pineal and other regions of the brain. Invest Opthalmol Vis Sci [Suppl] 27:191
Broekhuyse RM, Tolhuizen EFJ, Janssen APM, Winkens HJ (1985) Light induced shift and binding of S-antigen in retinal rods. Current Eye Res 4:613–618
Buzdygon B, Philp N, Zigler JS jr, Gery I, Zuckerman R (1985) Identity of S-antigen and the 48 kiloDalton protein in retinal rod outer segments. Invest Opthalmol Vis Sci [Suppl] 26:293
Chader GJ, Wiggert B (1986) Interphotoreceptor retinoid-binding protein (IRBP): a link between retinal rod cells and pineal gland? In: O'Brien P, Klein DC (eds) Pineal-retinal relationships. Academic Press, New York
Chader GJ, Wiggert B, Lai Y-L, Lee L, Fletcher RT (1983) Interphotoreceptor retinol binding protein: A possible role in retinoid transport to the retina. Prog Retinal Res 2:163–190
Deguchi T (1981) Rhodopsin-like photosensitivity of isolated chicken pineal gland. Nature 290:702–704
Foster RG, Follett BK (1985) The involvement of a rhodopsin-like photopigment in the photoperiodic response of the Japanese quail. J Comp Physiol A 157:519–528
Foster RG, Follett BK, Lythgoe JN (1985) Rhodopsin-like sensitivity of extraretinal photoreceptors mediating the photoperiodic response in quail. Nature 313:50–52
Gery I (1986) Retinal specific antigens and immunopathogenic processes they provoke. Prog Retinal Res 5:75–109
Gonzalez-Fernandez F, Landers RA, Glazebrook PA, Fong S-L, Liou GI, Lam DMK, Bridges CDB (1985) An extracellular retinol-binding glycoprotein in the rat eye - characterization, localization and biosynthesis. Neurochem Int 7:533–540
De Grip WJ (1985) Immunochemistry of rhodopsin. Prog Retinal Res 4:137–180
De Grip WJ, Deamen FJM, Bonting SL (1980) Isolation and purification of bovine rhodopsin. Methods Enzymol 67:301–320
Hartwig HG, Oksche A (1982) Neurobiological aspects of extraretinal photoreceptive systems: Structure and function. Experientia 38:991–996
Hökfelt T, Ljungdahl A, Steinbusch H, Verhofstad A, Nilsson Brodin E, Pernow B, Goldstein M (1978) Immunohistochemical evidence of substance P-like immunoreactivity in some 5-hydroxytryptamine-containing neurones in the rat central nervous system. Neuroscience 3:517–538
Korf H-W, Vigh-Teichmann I (1984) Sensory and central nervous elements in the avian pineal organ. Opthal Res 16:96–101
Korf H-W, Møller M, Gery I, Zigler JS, Klein DC (1985a) Immunocytochemical demonstration of retinal S-antigen in the pineal organ of four mammalian species. Cell Tissue Res 239:81–85
Korf H-W, Foster RG, Ekström P, Schalken JJ (1985b) Opsin-like immunoreaction in the retinae and pineal organs of four mammalian species. Cell Tissue Res 242:645–648
Kuhn H (1984) Interactions between photoexcited rhodopsin and light-activated enzymes in rods. Prog Retinal Res 3:123–156
Margry RJCF, Jacobs CWM, Bonting SL, De Grip WJ, Daemen FJM (1983) Detergent-induced specificity of an anti-rhodopsin serum for opsin micro-complement fixation studies. Biochim Biophys Acta 742:463–470
Mirshahi M, Boucheix C, Collenot G, Thillaye B, Dorey C, Faure J-P (1984) An immunofluorescent study of the taxonomic distribution of retinal S-antigen using monoclonal antibodies. Invest Ophthalmol Vis Sci [Suppl]25:30
Møller M, Glistrup OV, Olsen W (1983) Contrast enhancement of the brownish horseradish peroxidase-activated 3,3-diaminobenzidine tetrahydrochloride reaction product in black and white photomicrography by the use of interference filters. J Histochem Cytochem 32:37–42
Nicholls TJ, Follett BK, Robinson JE (1983) A photoperiodic response in gonadectomized Japanese quail exposed to a single long day. J Endocrinol 97:212–226
Oliver J, Baylé JD (1982) Brain photoreceptors for the photoinduced testicular response in birds. Experienta 38:1021–1029
Pfister C, Dorey C, Vadot R, Mirshani M, Deterre P, Chabre M, Faure J-P (1984) Identité de la protéine dite “48k” qui interagit avec la rhodopsine illuminée dans les batonnets rétiniens et de 1'“antigène S retiniens” inducteur de l'uveo-retinite autoimmune expérimentale. CR Acad Sc Paris 299:261–265
Schalken JJ, De Grip WJ (1986) Enzyme-linked immunosorbent assay for quantitative determination of the visual pigment rhodopsin in total eye-extracts. Exp Eye Res (in Press)
Semm P, Demaine C (1983) Electrical responses to direct and indirect photic stimulation of the pineal gland in the pigeon. J Neural Transm 58:281–289
Sternberger LA (1979) Immunocytochemistry. John Wiley Sons, New York, Chichester, Brisbane, Toronto
Van Veen Th, Elofsson R, Hartwig H-G, Geri I, Mocchzuki M, Klein DC (1986a) Retinal S-antigen: immunocytochemical and immunochemical studies on the distribution in animal photoreceptors and pineal organs. Exp Biol 45:15–25
Van Veen Th, Östholm T, Gierschik P, Spiegel A, Somers R, Korf H-W, Klein DC (1986b)α-Transducin immunoreactivity in retinae and sensory pineal organs of adult vertebrates. Proc Natl Acad Sci USA 834:912–916
Vigh B, Vigh-Teichmann I, Röhlich P, Aros B (1982) Immunoreactive opsin in the pineal organ of reptiles and birds. Z Mikrosk Anat Forsch 96:113–129
Vigh B, Vigh-Teichmann I, Röhlich P, Oksche A (1983) Cerebrospinal fluid-contacting neurons, sensory pinealocytes and Landolt's clubs of the retina as revealed by means of an electronmicroscopic immunoreaction against opsin. Cell Tissue Res 233:539–548
Vigh-Teichmann I, Röhlich P, Vigh B, Aros B (1980) Comparison of the pineal complex, retina and cerebrospinal fluid-contacting neurons by immunocytochemical antirhodopsin reaction. Z Mikrosk Anat Forsch 94:623–640
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Foster, R.G., Korf, H.W. & Schalken, J.J. Immunocytochemical markers revealing retinal and pineal but not hypothalamic photoreceptor systems in the Japanese quail. Cell Tissue Res. 248, 161–167 (1987). https://doi.org/10.1007/BF01239977
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DOI: https://doi.org/10.1007/BF01239977