Summary
Immunocytochemistry with a rod-specific antiserum was used to study the post-hatch development (2 days–300 days) of photoreceptor elements within the pineal of the Japanese quail. At all ages staining was restricted to limited numbers of pinealocytes scattered throughout the gland. An enzyme-linked immunosorbent assay (ELISA), with the same rod-specific antibody, was then used to obtain a quantitative measure of rod opsin in total eye and pineal extracts in both the developing retina and pineal. The opsin content of both tissues shows a marked increase during the first 30 days after hatch and then plateaued to 0.84±0.02 nmoles opsin in the eye and 2.20±0.11 pmoles opsin equivalents in the pineal. The increase in opsin in the retina may be associated with continued post-hatch development of the photoreceptors. We then attempted to demonstrate the presence of the rhodopsin chromophore within pineal and retinal extracts using HPLC analysis. In both retinal and pineal extracts, 11-cis retinaldehyde was identified and a light-induced shift from the 11-cis to the all-trans isomer was clearly shown. This analysis also allowed us to calculate the total content of 11-cis and all-trans retinaldehyde (derived from both rod and non-rod photoreceptors) of the eye and pineal (eye: 1.7±0.2 nmoles; pineal: 4.6±0.5 pmoles). In the quail eye, the total amount of retinaldehyde is more than twice the amount of rod-like opsin. This probably reflects the large contribution of cones in the quail retina; the cone pigments will contribute to the retinaldehyde content but are not recognized by the rodspecific antibodies. In the pineal, we also found more than double the concentration of retinaldehyde than we would have predicted from the amount of rod-like opsin. These results, coupled with our immunocytochemical findings, suggest that the quail pineal contains at least two classes of photoreceptor, some ‘rod-like’, others ‘non rod-like’.
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Abbreviations
- HPLC :
-
high-performance liquid chromatography
- ELISA :
-
enzyme-linked immunosorbent assay
References
Bischoff MB (1969) Photoreceptoral and secretory structures in the avian pineal organ. J Ultrastruct Res 28:16–26
Bowmaker JK (1977) The visual pigments, oil droplets and spectral sensitivity of the pigeon. Vision Res 17:1129–1138
Boya J, Calvo J (1980) Ultrastructural study of the post-hatching evolution of the pineal gland of the chicken (Gallus). Acta Anat 107:143–168
Bridges CDB (1984) Retinoids in photosensitive systems. In: Sporn MB, Roberts AB, Goodman DS (eds) The retinoids. Academic Press, New York, pp 125–176
Collin JP (1971) Differentiation and regression of the cells of the sensory line in the epiphysis cerebri. In: Wolstenholm GEW, Knight J (eds) The pineal gland. Churchill Livingstone, Edinburgh London, pp 79–125
Collin JP (1979) Recent advances in pineal cytochemistry: evidence of the production of indolamines and proteinaceous substances by rudimentary photoreceptor cells and pinealocytes of amniota. In: Kapper JA, Pevet P (eds) The pineal gland of vertebrates including man. Progr Brain Res 52:271–296
Curd MR (1968) Dilute H2O2-NH4OH; A rapid bleach for retinal melanin. Stain Technology 43:42–43
De Grip WJ, Daemen FJM, Bonting SL (1980) Isolation and purification of bovine rhodopsin. Methods Enzymol 67:301–320
Deguchi T (1979) Circadian rhythm of serotonin N-acetyltransferase activity in organ culture of chicken pineal gland. Science 203:1245–1247
Deguchi T (1981) Rhodopsin-like photosensitivity of isolated chicken pineal gland. Nature 290:702–704
Dodt E, Meissl H (1982) The pineal and parietal organs of lower vertebrates. Experientia 38:996–1000
Ekström P, Foster RG, Korf H-W, Schalken JJ (1987) Antibodies against retinal photoreceptor-specific proteins reveal axonal projections from the photosensory pineal organ in teleosts. J Comp Neurol 265:25–33
Foster RG, Korf H-W, Schalken JJ (1987) Immunocytochemical markers revealing retinal and pineal but not hypothalamic photoreceptor systems in the Japanese quail. Cell Tissue Res 248:161–167
Foster RG, Timmers AM, Schalken JJ, De Grip WJ (1989) A comparison of some photoreceptor characteristics in the pineal and retina: II. The Djungarian Hamster (Phodopussungorus). J Comp Physiol 165:565–572
Frisch K von (1911) Beiträge zur Physiologie der Pigmentzellen in der Fischhaut. Pflügers. Arch 138:319–387
Groenendijk GWT, De Grip WJ, Daemen FJM (1979) Identification and characterization of syn- and anti-isomers of retinal oximes. Analyt Biochem 99:304–310
Groenendijk GWT, De Grip WJ, Daemen FJM (1980) Quantitative determination of retinals with complete retention of their geometric configuration. Biochim Biophys Acta 617:430–438
Hartwig HG (1980) The structure of the pineal gland. In: Epple A, Stetson MH (eds) Avian endocrinology. Academic Press, New York, pp 31–51
Hartwig HG (1984) Cyclic renewal of whole pineal photoreceptor outer segments. Ophthalmic Res 16:102–106
Hartwig HG, Oksche A (1982) Neurobiological aspects of extraretinal photoreceptive systems: structure and function. Experientia 38:991–996
Husain OAN, Millett JA, Grainger JM (1980) Use of polylysine-coated slides in the preparation of cell samples for diagnostic cytology with special reference to urine samples. J Clin Pathol 33:309–311
Jansen HG, Sanyal S, De Grip WJ, Schalken JJ (1987) Development and degeneration of retina in rds mutant mice: Ultraimmunohistochemical localization of opsin. Exp Eye Res 44:347–361
Kappers JA (1971) The pineal organ: an introduction. In: Wolstenholm GEW, Knight J (eds) The pineal gland. Churchill Livingstone, Edinburgh London
Korf H-W, Vigh-Teichmann I (1984) Sensory and central nervous elements in the avian pineal organ. Ophthalmic Res 16:96–101
Lythgoe JN (1979) The ecology of vision. Oxford University Press, Oxford
Margry RJCF, Jacobs CWM, Bonting SL, De Grip WJ, Daemen FJM (1983) Detergent-induced specificity of anti-rhodopsin serum for opsin micro-complement fixation studies. Biochim Biophys Acta 742:465–470
Menaker M, Oksche A (1974) The avian pineal organ. In: Farner DS, King JR (eds) Avian biology, vol IV. Academic Press, New York
Menaker M, Wisner S (1983) Temperature-compensated circadian clock in the pineal ofAnolis. Proc Natl Acad Sci USA 80:6119–6121
Morita T (1966) Absence of electrical activity of the pigeon's pineal organ in response to light. Experientia 22:402
Papermaster DS (1982) Preparation of antibodies to rhodopsin and the large protein of outer segments. Methods Enzymol 81:240–246
Ralph CL, Dawson DC (1968) Failure of the pineal body of two species of birds (Coturnix japonica andPasser domesticus) to show electrical responses to illumination. Experientia 24:147–148
Schalken JJ (1987) The visual pigment rhodopsin: Immunocytochemical aspects and induction of experimental autoimmune uveoretinitis. PhD thesis, Dept Biochemistry, Center for Eye Research, University of Nijmegen, The Netherlands
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 43:431–439
Semm P, Demaine C (1983) Electrical responses to direct and indirect photic stimulation of the pineal gland in the pigeon. J Neural Transmiss 58:281–289
Sheffield J, Fischmann D (1970) Intercellular junctions in the developing neural retina of the chick embryo. Z Zellforsch 104:405–418
Slonaker JR (1921) The development of the eye and its accessory parts in the English sparrow (Passer domesticus). J Morphol 35:263–357
Sternberger LA (1979) Immunocytochemistry. Wiley, New York Chichester Brisbane Toronto
Tabata M, Suzuki T, Niwa H (1985) Chromophores in the extraretinal photoreceptor (pineal organ) of teleosts. Brain Res 338:173–176
Veen TH van, 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
Veen TH van, Ostholm T, Gierschik P, Spiegel A, Somers R, Korf H-W, Klein DC (1986b) alpha-Transducin immunoreactivity in the retinae and sensory pineal organs of adult vertebrates. Proc Natl Acad Sci USA 834:912–916
Vigh B, Vigh-Teichmann I (1981) Light- and electron-microscopic demonstration of immunoreactive opsin in the pinealocytes of various vertebrates. Cell Tissue Res 221:451–463
Vigh B, Vigh-Teichmann I (1986) Three types of photoreceptors in the pineal and frontal organs of frogs: ultrastructural and opsin immunoreactivity. Arch Histol Jpn 49:495–518
Vigh B, Vigh-Teichmann I, Aros B (1975) Comparative ultrastructure of cerebrospinal fluid-contacting neurons and pinealocytes. Cell Tissue Res 158:409–424
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, Aros B, Oksche A (1985) Sensory cells of the ‘rod-’ and ‘cone-type’ in the pineal organ ofRana esculenta, as revealed by immunoreaction against opsin and by the presence of an oil (lipid) droplet. Cell Tissue Res 240:143–148
Vigh B, Vigh-Teichmann I, Reinhard A, Szèl A, Van Veen T (1986) Opsin immunoreactions in the developing and adult pineal organ. In: Gupta D, Reiter RJ (eds) The pineal gland during development: From fetus to adult. Croom Helm, London Sydney, pp 31–42
Vigh-Teichmann I, Vigh B (1979) A comparison of epithalamic, hypothalamic and spinal neurosecretory terminals. Acta Biol Acad Sci Hungaricae 30:1–39
Vigh-Teichmann I, Vigh B, Szèl A, Röhlich P, Wirtz GH (1988) Immunocytochemical localization of vitamin A in the retina and pineal organ of the frog,Rana esculenta. Histochemistry 88:533–543
Wainwright SD, Wainwright LK (1981) Regulation of the cycle in chick pineal serotonin N-acetyltransferase activity in vitro by light. J Neurochem 35:451–457
Wald G (1968) Molecular basis of visual excitation. Science 162:230–239
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Work conducted while member of the AFRC Research Group on Photoperiodism and Reproduction, Department of Zoology, University of Bristol, Bristol, BS8 1UG, United Kingdom
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Foster, R.G., Schalken, J.J., Timmers, A.M. et al. A comparison of some photoreceptor characteristics in the pineal and retina. J. Comp. Physiol. 165, 553–563 (1989). https://doi.org/10.1007/BF00611241
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DOI: https://doi.org/10.1007/BF00611241