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The appearance and distribution of microglia in the developing retina of the rat

Published online by Cambridge University Press:  02 June 2009

K. W. S. Ashwell ,
H. Holländer ,
W. Streit  and
J. Stone
K. W. S. Ashwell
Affiliation:
Department of Anatomy, University of Sydney
H. Holländer
Affiliation:
Abteilung für Neuromorphologie, Max-Planck-Institut für Psychiatrie, München
W. Streit
Affiliation:
Abteilung für Neuromorphologie, Max-Planck-Institut für Psychiatrie, München
J. Stone
Affiliation:
Department of Anatomy, University of Sydney
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Abstract

We have examined the development of microglia in the rat retina, using a peroxidase-conjugated lectin derived from Griffonia simplicifolia. Retinas were studied from animals aged from E(embryonic day)12, just after the invagination of the optic cup and prior to the closure of the optic fissure, to adulthood. The lectin also proved a sensitive label for the endothelial cells of the developing retina. Our results provide some support for the view that microglia are derived from the monocyte-macrophage series of blood cells. At E12, most labeled cells were found at the vitreal surface, suggesting that they had come from the hyaloid circulation, while some had entered the retina and appeared to be migrating towards its ventricular surface. From E14 to early postnatal ages, most labeled cells had processes and resembled the amoeboid microglial cells described in silver carbonate staining studies (Ling, 1982). The number of labeled cells rose from about 700 to E14 to a peak of about 27,000 at P(postnatal day)7, and fell to about 19,600 by P12. As early as E16, a regularity was apparent in the distribution of microglial cells over the surface of the retina, the cells tending to avoid each other. Microglial cells are found throughout the thickness of the very young retina, but as the layers of the retina differentiate, they are increasingly restricted to the inner half of the retina. Our findings indicate that microglia enter the retina well before the period of neuronal death, making it unlikely that they invade the retina solely in response to cell death. Our results confirm however that, once in the retina, microglia become associated with, and appear to phagocytose, the pyknotic debris which appears during the period of neuronal death. They also become closely associated with the retinal vasculature. In the adult, the intensity of the labeling of microglia was much reduced. Those cells which were labeled appeared more differentiated, resembling the “resting microglia” described in earlier studies.

Keywords

MicrogliaLectinsRetinal vasculatureMicroglial-vascular interactionsPhagocytosisCell death
Type
Research Article
Information
Visual Neuroscience , Volume 2 , Issue 5 , May 1989 , pp. 437 - 448
Copyright
Copyright © Cambridge University Press 1989

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References

Adams, J.C. (1981). Heavy-metal intensification of DAB-based HRP reaction product. Journal of Histochemistry and Cytochemistry 29, 775.CrossRefGoogle ScholarPubMed
Akiyama, H., Itagaki, S. & McGeer, P.L. (1988). Major histocompatability complex antigen expression on rat microglia following epidural kainic acid lesions. Journal of Neuroscience Research 20, 147–157.CrossRefGoogle ScholarPubMed
Ashwell, K.W.S., Holländer, H., Streit, W. & Stone, J. Lectin binding by microglia and blood vessels in the developing rat retina. Journal of Anatomy (in press).Google Scholar
Boya, J., Calvo, J. & Carbonell, A.L. (1987). Appearance of microglial cells in the postnatal rat retina. Archivum Histologicum Japonicum 50, 223–228.CrossRefGoogle ScholarPubMed
Boycott, B.B. & Hopkins, J.M. (1981). Microglia in the retina of monkey and other mammals; its distinction from other types of glia and horizontal cells. Neuroscience 6, 679–688.CrossRefGoogle ScholarPubMed
Braekevelt, C.R. & Hollenberg, M.J. (1970). The development of the retina of the albino rat. American Journal of Anatomy 127, 281–302.CrossRefGoogle ScholarPubMed
Cammermeyer, J. (1965). The hypendymal microglia cell. Zeitschrift für Anatomie und Entwicklungsgeschichte 124, 543–561.CrossRefGoogle Scholar
Dougherty, T.F. (1944). Studies on the cytogenesis of microglia and their relation to cells of the reticulo-endothelial system. American Journal of Anatomy 74, 61–96.CrossRefGoogle Scholar
Hebel, R. & Stromberg, M.W. (1986). Anatomy and embryology of the laboratory rat. Section L Sensory Organs. Worthsee: BioMed Verlag.Google Scholar
Hickey, W.F. & Kimura, H. (1988). Perivascular microglial cells of the CNS are bone marrow-derived and present antigen in vivo. Science 239, 290–292.CrossRefGoogle ScholarPubMed
Horsburgh, G.M. & Sefton, A.J. (1987). Cellular degeneration and synaptogenesis in the developing retina of the rat. Journal of Comparative Neurology 263, 553–566.CrossRefGoogle ScholarPubMed
Hume, D.A., Perry, V.H. & Gordon, S. (1983). Immunohistochemical localization of a macrophage specific antigen in developing mouse retina: phagocytosis of dying neurons and differentiation of microglial cells to form a regular array in the plexiform layers. Journal of Cell Biology 97, 253–257.CrossRefGoogle Scholar
Imamoto, K. & Leblond, C.P. (1978). Radioautographic investigation of gliogenesis in the corpus callosum of young rats. II. Origin of microglial cells. Journal of Comparative Neurology 180, 139–164.CrossRefGoogle ScholarPubMed
Lewis, P.D. (1968). The fate of the subependymal cell in the adult rat brain, with a note on the origin of microglia. Brain 91, 721–736.CrossRefGoogle ScholarPubMed
Ling, E.A. (1981). The origin and nature of microglia. Advances in Cellular Neurobiology 2, 33–82.CrossRefGoogle Scholar
Ling, E.A. (1982). A light-microscopic demonstration of amoeboid microglia and microglial cells in the retina of rats of various ages. Archivum Histologicum Japonicum 45, 37–44.CrossRefGoogle ScholarPubMed
McCail, M.J., Robinson, S.R. & Dreher, B. (1987). Differential retinal growth appears to be the primary factor producing the ganglion cell density gradient in the rat. Neuroscience Letters 79, 78–84.CrossRefGoogle Scholar
Oehmichen, M. (1975). Monocytic origin of microglia cells. In Mononuclear Phagocytes in Immunity, Infection, and Pathology, ed. van Furth, R., Oxford: Blackwell, pp. 223–240.Google Scholar
Oehmichen, M. (1980). Enzyme-histochemical differentiation of neuroglia and microglia: a contribution to the cytogenesis of microglia and globoid cells. Pathology Research and Practice 168, 344–373.CrossRefGoogle Scholar
Perry, V.H., Hume, D.A. & Gordon, S. (1985). Immunohistochemical localization of macrophages and microglia in the adult and developing mouse brain. Neuroscience 15, 313–326.CrossRefGoogle ScholarPubMed
Potts, R.A., Dreher, B. & Bennett, M.R. (1982). The loss of ganglion cells in the developing retina of the rat. Developmental Brain Research 3, 481–486.CrossRefGoogle Scholar
Richardson, K.C., Janett, L. & Finke, E.H. (1960). Embedding in epoxy resins for ultrathin sections in electron microscopy. Stain Technology 35, 313–323.CrossRefGoogle ScholarPubMed
Rio del Hortega, P. (1932). Microglia Section X. In Cytology and Cellular Pathology of the Nervous System, ed. Penfold, W., New York: Paul B. Hoebber, pp. 481–534.Google Scholar
Russel, G.V. (1962). The compound granular corpuscle or Gitter cell: a review, together with notes on the origin of this phagocyte. Texas Report of Biology and Medicine 20, 338–351.Google Scholar
Santha, K. & Juba, A. (1933). Weitere Untersuchungen über die Entwicklung der Hortegaschen Mikroglia. Archiv für Psychiatrie und Nervenkr 98, 598–613.CrossRefGoogle Scholar
Sanyal, S. & DeRuiter, A. (1985). Inosine dephosphatase as a histochemical marker of retinal microvasculature, with special reference to transformation of microglia. Cell and Tissue Research 241, 291–297.CrossRefGoogle Scholar
Stone, J. (1981). The Wholemount Handbook. Sydney: Maitland.Google Scholar
Streit, W.J. & Kreutzberg, G.W. (1987). Lectin binding by resting and reactive microglia. Journal of Neurocytology 16, 249–260.CrossRefGoogle ScholarPubMed
Streit, W.J., Graeber, M.B. & Kreutzberg, G.W. (1988). Functional plasticity of microglia: a review. Glia 1, 301–307.CrossRefGoogle ScholarPubMed
Terubayashi, H., Murabe, Y., Fujisawa, H., Itoi, M. & Ibata, Y. (1984). Enzymehistochemical identification of microglial cells in the rat retina: Light- and electron-microscopic studies. Experimental Eye Research 39, 595–603.CrossRefGoogle Scholar
Vrabec, Fr. (1970). Microglia in the monkey and rabbit retina. Journal of Neuropathology and Experimental Neurology 29, 217–224.CrossRefGoogle ScholarPubMed
Wässle, H. & Riemann, H.J. (1978). The mosaic of nerve cells in the mammalian retina. Proceedings of the Royal Society B (London) 200, 441–461.Google Scholar