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Comparative light and electron microscopic study of retinal histogenesis in normal and rd mutant mice

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Summary

Mice, homozygous for the mutant gene rd show selective degeneration of the photoreceptor cells after their initial differentiation. Phenotypic expression in the mutant and in normal mice was studied by light and electron microscopy. The sequential emergence of developmental deviations in the mutant retina falls into three categories. First, predegenerative differences are manifest within the photoreceptor cells during 4–8 days after birth in retarded growth of the inner segments, reduced outer segment production, delayed development of the outer plexiform layer and slower segregation of the perikarya. Next, degenerative changes are recognized from 6 day onwards with swelling and vacuolization of the Golgi cisternae in the inner segments followed by cytolytic alterations affecting the ultrastructure of the entire cell. Lastly, with increasing loss of photoreceptor cells post-degenerative effects are seen in deepening of the basal infoldings and microvilli of the pigment epithelium and increase of Müller's fibres. The progress of degeneration in the mutant retina corresponds to the phase of rapid growth of the Golgi apparatus and rod outer segments in the normal retina. The role of the Golgi apparatus in the differentiation of the photoreceptor cells and its relation to the expression of the rd gene are discussed.

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References

  • Akiya, S.: Electron microscopic study on the retina. Jap. J. Ophthal. 6, 87–92 (1962)

    Google Scholar 

  • Bok, D., Young, R. W.: The renewal of diffusely distributed protein in the outer segments of rods and cones. Vision Res. 12, 161–168 (1972)

    Google Scholar 

  • Braekevelt, C. R., Hollenberg, M. J.: Development of the retinal pigment epithelium, choriocapillaries and Bruch's membrane in the albino rat. Exp. Eye Res. 9, 124–131 (1970)

    Google Scholar 

  • Caley, D. W., Johnson, C., Liebelt, R. A.: The postnatal development of the retina in the normal and rodless CBA mouse: A light and electron microscopic study. Amer. J. Anat. 133, 179–212 (1972)

    Google Scholar 

  • Caravaggio, L. L., Bonting, S. L.: The rhodopsin cycle in the developing vertebrate retina. II. Correlative study in normal mice and in mice with hereditary retinal degeneration. Exp. Eye Res. 2, 12–19 (1963)

    Google Scholar 

  • Dantzker, D. R., Gernstein, D. D.: Retinal vascular changes following toxic effects on visual cells and pigment epithelium. Arch. Ophthal. 81, 106–114 (1969)

    Google Scholar 

  • Droz, B.: Dynamic conditions of proteins in the visual cells of rats and mice as shown by radioautography with labeled amino acids. Anat. Rec. 145, 157–166 (1963)

    Google Scholar 

  • Gerstein, D. D., Dantzker, D. R.: Retinal vascular changes in hereditary visual cell degeneration. Arch. Ophthal. 81, 99–105 (1969)

    Google Scholar 

  • Green, E. L.: Breeding systems. In: Biology of the laboratory mouse (ed.: Green, E. L., p. 11–22. New York: McGraw-Hill 1966

    Google Scholar 

  • Karli, P., Stoeckel, M. E., Porte, A.: Dégénérescence des cellules visuelles photoréceptrices et persistance d'une sensibilité de la rétine à la stimulation photique. Z. Zellforsch. 65, 238–252 (1965)

    Google Scholar 

  • Kleinschuster, S. J., Moscona, A. A.: Interactions of embryonic and fetal neural retina cells with carbohydrate binding phytoagglutinins: cell surface changes with differentiation. Exp. Cell Res. 70, 397–410 (1972)

    Google Scholar 

  • Lasansky, A., De Robertis, E.: Sub-microscopic analysis of the genetic dystrophy of visual cells in C3H mice. J. biophys. biochem. Cytol. 7, 678–694 (1960)

    Google Scholar 

  • Lavail, M. M., Reif-Lehrer, L.: Glutamine synthetase in the normal and dystrophic mouse retina. J. Cell Biol. 51, 348–354 (1971)

    Google Scholar 

  • Lolley, R. N.: Changes in glucose and energy metabolism in vivo in developing retinae from visually competent (DBA/1J) and mutant (C3H/HeJ) mice. J. Neurochem. 19, 175–185 (1972)

    Google Scholar 

  • Lolley, R. N.: RNA and DNA in developing retinae: Comparison of a normal with the degenerating retinae of C3H mice. J. Neurochem. 20, 175–182 (1973)

    Google Scholar 

  • Lucas, D. R.: Retinal dystrophy strains. Mouse News Letter 19, 43 (1958a)

    Google Scholar 

  • Lucas, D. R.: Inherited retinal dystrophy in the mouse: its appearance in eyes and retinae cultured in vitro. J. Embryol. exp. Morph. 6, 589–592 (1958b)

    Google Scholar 

  • Lucas, D. R., Newhouse, J. P.: The effects of nutritional and endocrine factors on an inherited retinal degeneration in the mouse. Arch. Ophthal. 57, 224–235 (1957)

    Google Scholar 

  • Morest, D. K.: The pattern of neurogenesis in the retina of the rat. Z. Anat. Entwickl.-Gesch. 131, 45–67 (1970)

    Google Scholar 

  • Moscona, A. A.: Embryonic and neoplastic cell surfaces: Availability of receptors for concanavalin A and wheat germ agglutinin. Science 171 905–907 (1971)

    Google Scholar 

  • Noel, W. K.: Differentiation metabolic organization and viability of the visual cell. Arch. Opthal. 60, 702–733 (1958a)

    Google Scholar 

  • Noel, W. K.: Studies on visual cell viability and differentiation. An. N. Y. Acad. Sci. 74, 337–361 (1958b)

    Google Scholar 

  • Olney, J. W.: An electron microscopic study of synapse formation, receptor outer segment development and other aspects of developing mouse retina. Invest. Ophthal. 7, 250–268 (1968)

    Google Scholar 

  • Sanyal, S.: Changes of lysosomal enzymes during hereditary degeneration and histogenesis of retina in mice. I. Acid phosphatase visualized by azo-dye and lead nitrate methods. Histochemie 23, 207–219 (1970)

    Google Scholar 

  • Sanyal, S.: Changes of lysosomal enzymes during hereditary degeneration and histogenesis of retina in mice. II. Localization of N-Acetyl-B-glucosaminidase in macrophages. Histochemie 29, 28–36 (1972)

    Google Scholar 

  • Shiose, Y., Sonohara, O.: Studies on retinitis pigmentosa. XXVI. Electron microscopic aspects of early retinal changes in inherited dystrophic mice [in Japanese with English summary]. Acta Soc. Ophthal. Jap. 72, 1126–1141 (1968)

    Google Scholar 

  • Sidman, R. L.: Histogenesis of mouse retina studied with thymidine-H3. In: The structure of the eye (ed.: G. K. Smelser) New York: Academic Press 1961

    Google Scholar 

  • Sidman, R. L.: Organ culture analysis of inherited retinal degeneration in rodents. Nat. Cancer Inst. Monogr. 11, 227–246 (1963)

    Google Scholar 

  • Sidman, R. L., Green, M. C.: Retinal degeneration in the mouse; location of the rd locus in linkage group XVII. J. Hered. 56, 23–29 (1965)

    Google Scholar 

  • Sorsby, A., Koller, P. C., Attfield, M., Davey, J. B., Lucas, D. R.: Retinal dystrophy in the mouse: Histological and genetic aspects. J. exp. Zool. 125, 171–198 (1954)

    Google Scholar 

  • Spitznas, M., Hogan, M. J.: Outer segments of photoreceptors and the retinal pigment epithelium. Arch. Ophthal. 84, 810–819 (1970)

    Google Scholar 

  • Tansley, K.: Hereditary degeneration of the mouse retina. Brit. J. Ophthal. 35, 573–582 (1951)

    Google Scholar 

  • Tansley, K.: An inherited retinal degeneration in the mouse. J. Hered. 45, 123–127 (1954)

    Google Scholar 

  • Theiler, K., Cagianut, B.: Zur erbilchen Netzhautdegeneration der Maus. Albrecht v. Graefes Arch. Ophthal. 166, 387–396 (1963)

    Google Scholar 

  • Whaley, W. G., Dauwalder, M., Kephard, J. E.: Golgi apparatus: Influence on cell surfaces. Science 175, 496–599 (1972)

    Google Scholar 

  • Yamasaki, I., Mizuno, K.: Rhodopsin and ERG of hereditary dystrophic mice and experimental retinitis pigmentosa. Jap. J. Ophthal. 14, 151–158 (1970)

    Google Scholar 

  • Young, R. W.: The renewal of photoreceptor cell outer segments. J. Cell Biol. 33, 61–72 (1967)

    Google Scholar 

  • Young, R. W.: Passage of newly formed protein through the connecting cilium of retinal rods in the frog. J. Ultrastruct. Res. 23, 462–473 (1968)

    Google Scholar 

  • Young, R. W., Droz, B.: The renewal of protein in retinal rods and cones. J. Cell Biol. 39, 169–184 (1968)

    Google Scholar 

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Supported in part by grant No. A-6207 from the National Research Council of Canada.

Authors' thanks are due to Professor Dr. J. Moll for critical reading of the manuscript, to Mr. Ian Atkinson, Mr. R. K. Hawkins and Miss A. de Ruiter for expert technical assistance; to Mr. W. van den Oudenalder and Miss P.C. Delfos for help in photography and to Mrs. L.C. Boonstra for typing the manuscript.

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Sanyal, S., Bal, A.K. Comparative light and electron microscopic study of retinal histogenesis in normal and rd mutant mice. Z. Anat. Entwickl. Gesch. 142, 219–238 (1973). https://doi.org/10.1007/BF00519723

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  • DOI: https://doi.org/10.1007/BF00519723

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