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Microglia and reactive “M” cells of degenerating central nervous system: Does similar morphology and function imply a common origin?

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Summary

Electron microscopy of subependymal cells and microglia in rat neonatal spinal cord reveals the latter to be a distinctive group of non-neuronal elements characterized by pronounced heterochromatin nuclei, many free ribosomes and rosettes, hour-glass shaped mitochondria, a moderately dense, granular cytoplasmic matrix, lipid vacuoles and a wide variety of lysosomes. Some examples are elongated and ameboid in appearance or may contain phagocytic vacuoles. Transitional forms between subependymal cells, or any other nonneuronal forms, and microglia were not observed. Ultrastructural features displayed by microglia are also strikingly characteristic of the “M” cells (Matthews and Kruger, 1973a, b) encountered in zones of thalamic degeneration two to three weeks following cortical ablation of adult rabbits. During the first and second postoperative weeks, “M” cells closely resemble the agranular leukocytes accumulating in the perivascular space of vessels coursing within the zones of degeneration. This fact, together with documentation of penetration of the vascular external lamina by elements of similar morphology, indicates a mesodermal origin for some “M” cells.

The microglia of normal CNS and “M” cells of pathologic neural tissue are sufficiently similar, both in morphology and apparent function, to warrant consideration of a mesodermal origin for the microglia of neonatal CNS and a number of criteria to substantiate this concept are presented.

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References

  • Adrian, E. K., Williams, M. G.: An electron microscopic study of reactive cells in the spinal cord labeled with 3H-thymidine before spinal cord injury. Anat. Rec. 175, 261–262 (1973a)

    Google Scholar 

  • Adrian, E. K., Williams, M. G.: Cell proliferation in injured spinal cord. An electron microscopic study. J. comp. Neurol. 151, 1–24 (1973b)

    Google Scholar 

  • Allen, E.: Cessation in mitosis in central nervous system of the albino rat. J. Comp. Neurol. 22, 547–568 (1912)

    Google Scholar 

  • Blakemore, W. F.: The ultrastructure of the subependymal plate in the rat. J. Anat. (Lond.) 104, 423–433 (1969)

    Google Scholar 

  • Blakemore, W. F.: Microglial reactions following thermal necrosis of the rat cortex: An electron microscopic study. Acta neuropath. (Berl.) 21, 11–22 (1972)

    Google Scholar 

  • Blakemore, W. F., Jolly, R. D.: The subependymal plate and associated ependyma in the dog. An ultrastructural study. J. Neurocytol. 1, 69–84 (1972)

    Google Scholar 

  • Boulder Committee: Embryonic vertebrate central nervous system: revised terminology. Anat. Rec. 166, 257–262 (1970)

    Google Scholar 

  • Cammermeyer, J.: Juxtavascular karyokinesis and microglial cell proliferation during retrograde degeneration in the mouse facial nucleus. Ergebn. Anat. Entwickl.-Gesch. 38, 1–22 (1965a)

    Google Scholar 

  • Cammermeyer, J.: Histiocytes, juxtavascular mitotic cells and microglia cells during retrograde changes in the facial nucleus of rabbits of varying age. Ergebn. Anat. Entwickl-Gesch. 38, 195–229 (1965b)

    Google Scholar 

  • Frederickson, R. G., Low, F. N.: Blood vessels and tissue space associated with the brain of the rat. Amer. J. Anat. 125, 123–146 (1969)

    Google Scholar 

  • Fujita, H., Fujita, S.: Electron microscopic studies on the differentiation of the ependymal cells and the glioblast in the spinal cord of domestic fowl. Z. Zellforsch. 64, 262–272 (1964)

    Google Scholar 

  • Fujita, S.: An autoradiographic study on the origin and fate of the sub-pial glioblast in the embryonic chick spinal cord. J. comp. Neurol. 124, 51–60 (1965)

    Google Scholar 

  • Fujita, S.: Genesis of glioblasts in the human spinal cord as revealed by Feulgen cytophotometry. J. comp. Neurol. 151, 25–34 (1973)

    Google Scholar 

  • Hildebrand, C.: Ultrastructural and light microscopic studies of the developing feline spinal cord white matter. II. Cell death and myelin sheath disintegration in the early postnatal period. Acta physiol. scand., Suppl. 364, 109–144 (1971)

    Google Scholar 

  • Hinds, J. W.: Autoradiographic study of histogenesis in the mouse olfactory bulb. II. Cell proliferation and migration. J. comp. Neurol. 134, 305–322 (1968)

    Google Scholar 

  • Hinds, J. W., Ruffett, T. L.: Cell proliferation in the neural tube: An electron microscopic and Golgi analysis in the mouse cerebral vesiclea. Z. Zellforsch. 115, 226–264 (1971).

    Google Scholar 

  • His, W.: Histogenese und Zusammenhang der Nervenelemente. S. 93–114, Verh. X. Int. Med. Congr. Berlin (1891)

  • Juba, A.: Untersuchungen über die Entwicklung der Hortegaschen Microglia des Menschen. Arch. Psychiat. Nervenkr. 10, 577–592 (1934a)

    Google Scholar 

  • Juba, A.: Das erste Erscheinen und die Urformen der Hortegaschen Mikroglia in Zentralnervensystem. Arch. Psychiat. Nervenkr. 102, 225–232 (1934b)

    Google Scholar 

  • Kitamura, T., Hattori, H., Fujita, S.: Autoradiographic studies on histogenesis of brain macrophages in the mouse. J. Neuropath. exp. Neurol. 31, 502–518 (1972)

    Google Scholar 

  • Kruger, L., Hamori, J.: An electron microscopic study of dendrite degeneration in the cerebral cortex resulting from laminar lesions. Exp. Brain Res. 10, 1–16 (1970)

    Google Scholar 

  • Matthews, M. A., Kruger, L.: Electron microscopy of reactive vascular and hematogenous elements during thalamic degeneration. Anat. Rec. 172, 365 (1972)

    Google Scholar 

  • Matthews, M. A., Kruger, L.: Electron microscopy of non-neuronal cellular changes accompanying neural degeneration in thalamic nuclei of the rabbit. I. Reactive hematogenous and perivascular elements within the basal lamina. J. comp. Neurol. 148, 285–312 (1973a)

    Google Scholar 

  • Matthews, M. A., Kruger, L.: Electron microscopy of non-neuronal cellular changes accompanying neural degeneration in thalamic nuclei of the rabbit. II. Reactive elements within the neuropil. J. comp. Neurol. 148, 313–346 (1973b)

    Google Scholar 

  • Matthews, M. A.: Death of the central neuron: an electron microscopic study of thalamic retrograde degeneration following cortical ablation. J. Neurocytol. 2, 265–288 (1973)

    Google Scholar 

  • Matthews, M. A.: Factors affecting irreversible retrograde atrophy of “cortex-dependent” thalamic neuronsa. Anat. Rec. 178, 412–413 (1974)

    Google Scholar 

  • Metz, A., Spatz, H.: Die Hortega'schen Zellen, das sogenannte “dritte Element” und über ihre funktionelle Bedeutung. Z. Nervenheilk. 89, 138–170 (1924)

    Google Scholar 

  • Mori, S., Leblond, C. P.: Identification of microglia in light and electron microscopy. J. comp. Neurol. 135, 57–80

  • Morse, D. E., Low, F. N.: The fine structure of the pia mater of the rat. Amer. J. Anat. 133, 349–368 (1972a)

    Google Scholar 

  • Morse, D. E., Low, F. N.: The fine structure of subarachnoid macrophages in the rat. Anat, Rec. 174, 469–476 (1972b)

    Google Scholar 

  • Paterson, J. A., Privat, A., Ling, E. A., Leblond, C. P.: Investigation of glial cells in semithin sections. III. Transformation of subependymal cells into glial cells, as shown by radioautography after 3H-thymidine injection into the lateral ventricle of the brain of young rats. J. comp. Neurol. 149, 83–102 (1973)

    Google Scholar 

  • Phelps, C. H.: The development of glio-vascular relationships in the rat spinal cord. An electron microscopic study. Z. Zellforsch. 128, 555–564 (1972)

    Google Scholar 

  • Privat, A., Leblond, C. P.: The subependymal layer and neighboring region in the brain of the young rat. J. comp. Neurol. 146, 277–302 (1972)

    Google Scholar 

  • Rio-Hortega, P. Del.: El tercer element de los centros nerviosos. Bol. Soc. Esp. Biol. 9, 69–120 (1919)

    Google Scholar 

  • Rio-Hortega, P. Del: La microglia y su transformacion en celulas en bastoncito y cuerpos, granulo-adiposos. Trab. Lab. Invest. Biol. 18, 37–83 (1920)

    Google Scholar 

  • Rubinstein, L. J., Klatzo, I., Miquel, J.: Histochemical observations in oxidative enzyme activity of glial cells in a local brain injury. J. Neuropath. exp. Neurol. 21, 116–136 (1962)

    Google Scholar 

  • Rydberg, E.: On the normal microscopical anatomy of the brain of the fetus, especially of the glia tissue. Acta path. microbiol. scand., Suppl. 10, 1–247 (1932)

    Google Scholar 

  • Santha, K. von, Juba, A.: Weitere Untersuchungen über die Entwicklung der Hortegaschen Mikroglia. Arch. Psychiat. Nervenkr. 98, 598–613 (1932)

    Google Scholar 

  • Sidman, R. L.: Cell proliferation, migration and interaction in the developing mammalian central nervous system. In: The neurosciences, second study program (F. O. Schmitt, ed.), p. 100–107. The Rockefeller University Press 1970

  • Smart, I., Leblond, C. P.: Evidence for division and transformations of neuroglial cells in the mouse brain, as derived from radioautography after injection of thymidine-H3. J. comp. Neurol. 116, 349–367 (1961)

    Google Scholar 

  • Smith, B., Rubinstein, L. J.: Histochemical observations on oxidative enzyme activity in reactive microglia and somatic macrophages. J. Path. Bact. 83, 572–575 (1962)

    Google Scholar 

  • Stensaas, L. J., Gilson, B. C.: Ependymal and subependymal cells of the caudato-pallial junction in the lateral ventricle of the neonatal rabbit. Z. Zellforsch. 132, 297–322 (1972)

    Google Scholar 

  • Stensaas, L. J., Reichert, W. H.: Round and amoeboid microglial cells in the neonatal rabbit brain. Z. Zellforsch. 119, 147–163 (1971)

    Google Scholar 

  • Terry, R. D., Weiss, M.: Studies in Tay-Sacks disease. II. Ultrastructure of the cerebrum. J. Neuropath. exp. Neurol. 22, 18–55 (1963)

    Google Scholar 

  • Vaughn, J. E.: An electron microscopic analysis of gliogenesis in rat optic nerves. Z. Zellforsch. 94, 293–324 (1969)

    Google Scholar 

  • Vaughn, J. E., Peters, A.: A third neuroglial cell type. An electron microscopic study. J. comp. Neurol. 133, 269–288 (1968)

    Google Scholar 

  • Vaughn, J. E., Peters, A.: The morphology and development of neuroglial cells: In. Cellular aspects of neural growth and differentiation. D. C. Pease, ed. UCLA Forum in Medical Sciences, 14, 103–134 (1971)

  • Vaughn, J. E., Skoff, R. P.: Neuroglia in experimentally altered central nervous system. In: The structure and function of the nervous system, vol. 5 (G. W. Bourne, ed.), p. 39–72. New York: Academic Press 1972

    Google Scholar 

  • Wechsler, W., Meller, K.: Elektronenmikroskopische Befunde am Neuralrohr von Hühnerembryonen. Acta neuropath. (Berl.) 2, 491–496 (1963)

    Google Scholar 

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Authors and Affiliations

  1. Department of Anatomy, Louisiana State University, Medical Center, New Orleans, Louisiana

    Murray A. Matthews

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  1. Murray A. Matthews
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This research was supported by NIH grants DE 00241-03 and RR 05376-11. I am indebted to Mrs. Merrill Frost for her superior technical assistance, and to Mrs. Patrice Rodi for typing the manuscript.

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Matthews, M.A. Microglia and reactive “M” cells of degenerating central nervous system: Does similar morphology and function imply a common origin?. Cell Tissue Res. 148, 477–491 (1974). https://doi.org/10.1007/BF00221932

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  • DOI: https://doi.org/10.1007/BF00221932

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