Summary
The postnatal development of the tapetum lucidum cellulosum of the cat was studied with cytochemical, histochemical, microspectrofluorimetric, and chemical methods. At birth, the prospective tapetal cells exhibit a cytoplasmic, formaldehyde-induced catechol fluorescence which, by spectrographical criteria, is due to the presence of a thioether of DOPA, most likely 5-S-cysteinyldopa. These cells show a positive DOPA-reaction in the GERL, a Golgi-associated system of smooth endoplasmic reticulum. Beyond the third postnatal week, tyrosinase activity is found in the GERL and in the premelanosomal-like tapetal rods. Shortly thereafter, cells in the innermost layers of the tapetum reveal a change in the colour of the fluorophore from green (formaldehyde-induced) to orange-yellow (autofluorescent). Concomitant with the appearance of the yellow fluorophore (having spectral characteristics similar to authentic riboflavin), the DOPA-reactivity in the tapetal cells is no longer detectable and the cells attain the feature of mature tapetal elements with typical elongated, parallelly arranged, electron-dense rods. The increases and decreases in tyrosinase activity are parallelled by similar time-dependent changes in DOPA and cysteinyldopa content. Both DOPA and cysteinyldopa are considered as potential precursors of melanin polymers. Thus, these data support the concept that the tapetal cells represent uniquely differentiated and highly specialized choroidal melanocytes. The compact arrangement of these cells in the tapetum lucidum renders it an ideal tissue for studying the developmental biology of melanocytes.
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References
Agrup, G., Hansson, C., Rorsman, H., Rosengren, A.M., Rosengren, E.: Mass spectrometric analysis of enzymatically synthetized cysteinyldopa isomers. Comm. Dept. Anat., No 5, University of Lund, Sweden (1976)
Agrup, G., Björklund, A., Falck, B., Jacobsson, S., Lindvall, O., Rorsman, H., Rosengren, E.: Fluorescence histochemical demonstration of DOPA thioethers by condensation with gaseous formaldehyde. Histochemistry 52, 179–186 (1977)
Baumgarten, H.G.: Biogenic monoamines in the cyclostome and lower vertebrate brain. Progr. Histochem. Cytochem. 4, 1–90 (1972)
Bernstein, M.H., Pease, D.C.: Electron microscopy of the tapetum lucidum of the cat. J. Biophys. Biochem. Cytol. 5, 35–41 (1959)
Björklund, A., Falck, B., Lindvall, O.: Microspectrofluorimetric analysis of cellular monoamines after formaldehyde or glyoxylic acid condensation. In: Methods in Brain Research (P.B. Bradley, ed.), pp. 249–294. London: John Wiley and Sons 1975
Büssow, H.: Zur Histogenese und Cytogenese des Tapetum lucidum cellulosum der Katze. Eine licht- und elektronenoptische Untersuchung. Anat. Embryol. 146, 141–156 (1974)
Büssow, H.: Aufbau und Entwicklung des Tapetum lucidum der Katze. Verh. Anat. Ges. 69, 625–630 (1975)
Corrodi, H., Hillarp, N.A., Jonsson, G.: Fluorescence methods for the histochemical demonstration of monoamines. 3. Sodium borohydride reduction of the fluorescent compounds as a specificity test. J. Histochem. Cytochem. 12, 582–586 (1964)
Dunn, D.R., Barth, R.E.: Identification of melanoma cells by formaldehyde-induced fluorescence. Cancer 33, 701–706 (1974)
Ehinger, B., Olivecrona, H., Rorsman, H.: Malignant melanomas of the eyes as studied with a specific fluorescence method. Acta Pathol. Microbiol. Scand. 69, 179–184 (1967)
Ehinger, B., Rosengren, E.: DOPA in ocular pigment cells in mammalian albionotic embryos. Experientia (Basel) 23, 441 (1967)
Ehinger, B., Hannesson, O.B.: Ocular melanomas—formaldehyde-induced fluorescence in relation to mortality. A. v. Graefes Arch. Ophthal. 203, 133–137 (1977)
El-Hifnawi, E., Hinrichsen, K.: Melanogenesis in the pigment epithelium of chicken embryos. I. Topogenesis of pigment in the iris anlage. Anat. Embryol. 147, 177–187 (1975)
Elliott, J.E., Futterman, S.: Fluorescence in the tapetum of the cat's eye. Identification assay and localization of riboflavin in the tapetum and a proposed mechanism by which it may facilitate vision. Arch. Ophthal. 70, 531–534 (1963)
Endo, H., Hu, F.: Pigment cell development in rhesus monkey eyes: an electron microscopic and histochemical study. Develop. Biol. 32, 69–81 (1973)
Eppig, J.J., Dumont, J.N.: Cytochemical localization of tyrosinase activity in pigmented epithelial cells of Rana pipiens and Xenopus laevis larvae. J. Ultrastruct. Res. 39, 397–410 (1972)
Eppig, J.J., Dumont, J.N.: Oogenesis in Xenopus leavis (Daudin). II. The induction and subcellular localization of tyrosinase activity in developing oocytes. Develop. Biol. 36, 330–342 (1974)
Falck, B., Owman, Ch.: A detailed methodological description of the fluorescence method for the cellular demonstration of biogenic monoamines. Acta Univ. Lund II 7, 1–23 (1965)
Falck, B., Jacobsson, S., Olivecrona, H., Rosman, H.: Pigmented nevi and malignant melanomas as studied with a specific fluorescence method. Science 149, 439–440 (1965)
Fitzpatrick, T.B., Kukita, A.: Tyrosinase activity in vertebrate melanocytes. In: Pigment Cell Biology (M. Gordon, ed.), pp. 489–524. New York: Academic Press 1959
Graham, D.G., Tiffany, S.M., Vogel, F.S.: Toxicity of melanin precursors. J. Invest. Dermatol. 70, 113–116 (1978a)
Graham, D.G., Tiffany, S.M., Bell, W.R., Gutknecht, W.F.: Autoxidation versus covalent binding of quinones as the mechanism of toxicity of dopamine, 6-hydroxydopamine, and related compounds toward C1300 neuroblastoma cells in vitro. Molec. Pharmacol. 14, 644–653 (1978b)
Hansson, C., Edholm, L.-E., Agrup, G., Rorsman, H., Rosengren, A.-M., Rosengren, E.: The quantitative determination of 5-S-cysteinyldopa and DOPA in normal serum and in serum from patients with malignant melanoma by means of high-pressure liquid chromatography. Clin. Chim. Acta 88, 419–427 (1978)
Hebel, R.: Entwicklung und Struktur der Retina und des Tapetum lucidum des Hundes. Ergebn. Anat. Entwickl.-Gesch. 45/2, 1–93 (1971)
Ide, C.: The development of melanosomes in the pigment epithelium of the chick embryo. Z. Zellforsch. 131, 171–186 (1972)
Jimbow, K., Quevedo, W.C., Fitzpatrick, T.B., Szabo, G.: Some aspects of melanin biology: 1950–1975. J. Invest. Dermatol. 67, 72–89 (1976)
Lauber, H.: Die Aderhaut (Chorioidea). In: Handbuch der mikroskopischen Anatomie des Menschen (W. v. Möllendorff, ed.), Vol. III/2, pp. 91–133. Berlin: Springer 1936
Lucchi, M.L., Callegari, E., Bortolami, R.: The development of the rods in the tapetal cells of the cat. J. Anat. (Lond.) 127, 505–513 (1978)
Luft, J.H.: Improvements in epoxy resin embedding methods. J. Biophys. Biochem. Cytol. 9, 409–414 (1961)
Maul, G.G., Brumbaugh, J.A.: On the possible function of coated vesicles in melanogenesis of the regenerating fowl feathers. J. Cell Biol. 48, 41–48 (1971)
Mishima, H., Hasebe, H., Fujita, H.: Melanogenesis in retinal pigment epithelial cell of chick embryo. DOPA-reaction and electron microscopic autoradiography of H-3 dopa. Invest. Ophthalmol. Vis. Sci. 17, 403–411 (1978)
Novikoff, A.B., Albala, A., Biempica, L.: Ultrastructural and cytochemical observations on B-16 and Harding-Passey melanomas. (The origin of premelanosomes and compound melanosomes.) Histochem. Cytochem. 16, 299–319 (1968)
Novikoff, A.B., Leuenberger, P.M., Novikoff, P.M., Quintana, N.: Retinal pigment epithelium: interrelations of endoplasmic reticulum and melanolysosomes in the black mouse and its beige mutant. Lab. Invest. 40, 166–171 (1979)
Okun, M.R., Edelstein, L.M., Or, N., Hamada, G., Donnellan, B., Lever, W.F.: Histochemical differentiation of peroxidase-mediated from tyrosinase-mediated melanin formation in mammalian tissues. The biologic significance of peroxidase-mediated oxidation of tyrosin to melanin. Histochemie 23, 295–309 (1970)
Paul, E.: Eine neue Methode zur feineren Melanom-Differenzierung. Die Bedeutung der Formaldehyd-induzierten Fluoreszenz für die prognostische Beurteilung maligner Melanome. Fortschr. Med. 93, 1488–1492 (1975)
Paul, E., Illig, L.: Histochemische Untersuchungen an dermalen Naevuszellnaevi. Fluoreszenzhistochemie nach Falck-Hillarp und Enzymhistochemie. Arch. Dermatol. Forsch. 251, 133–145 (1974)
Pedler, C.H.: The fine structure of the tapetum cellulosum. Exp. Eye Res. 2, 189–195 (1963)
Rodrigues, M.M., Imai, K., Shields, J.A., Laties, A.M.: Demonstration of biogenic amines and adrenergic innervation in uveal malignant melanomas by histofluorometric method. Invest. Ophthal. Vis. Sci. 16, 396–403 (1977)
Rost, F.W.D., Polak, J.M.: Fluorescence microscopy and microspectrofluorimetry of malignant melanomas, naevi and normal melanocytes. Virchows Arch. Abt. Pathol. Anat. 347, 321–326 (1969)
Stanka, P.: Die DOPA-Reaktion, eine brauchbare Methode in der Elektronenmikroskopie. Untersuchungen am retinalen Pigmentepithel von Hühnerembryonen. Mikroskopie 26, 169–174 (1970)
Stanka, P., Kinzel, V., Mohr, U.: Elektronenmikroskopische Untersuchungen über die Prämelanosomenentstehung an Melanomzellen in vitro. Virchows Arch. Abt. B 2, 91–102 (1969)
Vielkind, U., Paul, E.: Normal and malignant melanin-containing pigment cells of Xiphophorine fish as studied with formaldehyde-induced fluorescence. J. Invest. Dermatol. 70, 80–83 (1978)
Vogel, M.: Postnatal development of the cat's retina. Ergebn. Anat. Entwickl.-Gesch. 54/4, 1–66 (1978)
Weitzel, G., Buddeke, E., Fretzdorff, A.M., Strecker, F.J., Roester, U.: Struktur der im Tapetum lucidum von Hund und Fuchs enthaltenen Zinkverbindungen. Hoppe-Seylers Z. Physiol. Chem. 299, 193–213 (1955)
Wick, M.M., Byers, L., Frei, E.: L-DOPA: selective toxicity for melanoma cells in vitro. Science 197, 468–469 (1977)
Winckler, J., Turner, H.-B.: Über das Vorkommen von Katecholaminen im Pigmentepithel des Meerschweinchenauges während der Entwicklung. Histochemie 19, 272–280 (1969)
Wolff, H.H.: Enzym-histochemische und elektronenoptische Untersuchungen über die Entwicklung des Tapetum lucidum der Katze. Histochemie 13, 245–262 (1968)
Wolff, H.H.: Elektronenmikroskopische und histochemische Untersuchungen zur Entwicklung des Tapetum lucidum der Katze. Anat. Anz. 125 (Suppl.), 291–296 (1969)
Yamada, E.: The fine structure of the tapetum cells in the choroid of the kitten eye as revealed by the electron microscope. J. Ultrastruct. Res. 1, 359–364 (1958)
Yamada, E.: Some observations on the membrane-limited structure within the retinal element. In: Intracellular Membraneous Structure (S. Seno and E.V. Cowdry, eds.), pp. 49–63. Okayama: Jap. Soc. Cell. Biol. 1965
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Supported by grants of the Deutsche Forschungsgemeinschaft
Supported by grants of the Swedish Medical Research Council (B79-4x-56-15A)
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Büssow, H., Baumgarten, H.G. & Hansson, C. The tapetal cell: A unique melanocyte in the tapetum lucidum cellulosum of the cat (Felis domestica L.). Anat Embryol 158, 289–302 (1980). https://doi.org/10.1007/BF00301818
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DOI: https://doi.org/10.1007/BF00301818