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Ultrastructural changes in neurons of the spinal anterior horn of ageing mice with particular reference to the accumulation of lipofuscin pigment

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Journal of Neurocytology

Summary

Structural changes in neurons in the cervical anterior horn of ageing mice have been studied. The main age-related neurocytological change observed during this study is progressive accumulation of lipofuscin. The pigment was present in some nerve cells as early as six weeks after birth. Various types of membrane-bound granules encountered in the anterior horn cells were characterized on the basis of their shape, size and fine structure into primary lysosome-like (L1) granules (dense bodies), autophagic vacuole-like (L2) granules and mature (L3) pigment granules of complex substructure and irregular configuration.L1,L3 andL3 types of granules appear to represent respectively early, intermediate and mature stages in a developmental continuum of lipofuscin pigment granules. Transitional stages suggest that matureL3 pigment granules evolve by gradual alteration of lysosome-likeL1 andL2 granules. A probable sequence of morphologic events accompanying the transformation of lysosome-like granules into mature lipofuscin pigment granules is suggested.

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References

  • Andrew, W. (1939) The Golgi apparatus in the nerve cells of the mouse from youth to senility.American Journal of Anatomy 64, 351–76.

    Google Scholar 

  • Andrews, J. M. andMaxwell, D. S. (1969) Motor neuron diseases in animals. InMotor Neuron Diseases, Research On Amyotrophic Lateral Sclerosis and Related Disorders (Edited byNorris, Jr., F. H. andKurland, L. T.), pp. 369–85. Grune and Stratton, New York and London.

    Google Scholar 

  • Barden, H. (1970) Relationship of Golgi thiaminepyrophosphatase and lysosomal acid phosphatase to neuromelanin and lipofuscin in cerebral neurons of the aging rhesus monkey.Journal of Neuropathology and Experimental Neurology 29, 225–40.

    PubMed  Google Scholar 

  • Barka, T. andAnderson, P. J. (1963) InHistochemistry;Theory, Practice and Bibliography, pp. 190–92. Hoeber Div., Harper & Row, Inc., New York.

    Google Scholar 

  • Biava, C. andWest, M. (1965) Lipofuscin-like granules in vascular smooth muscle and juxtaglomerular cells of human kidneys.American Journal of Pathology 47, 287–313.

    PubMed  Google Scholar 

  • Bondareff, W. (1959) Morphology of the aging nervous system. InHandbook of Aging and the Individual (Edited by Birren, J. E.), pp. 136–72. University Chicago Press, Chicago.

    Google Scholar 

  • Bondareff, W. (1964) Histophysiology of the aging nervous system. InAdvances in Gerontological Research (Edited byStrehler, B. L.), vol.I, pp. 1–22. Academic Press, New York and London.

    Google Scholar 

  • Bourne, G. H. (1957) Aging from a biological and cellular point of view. InModern Trends in Geriatrics. (Edited byHobsen, W.), pp. 22–49. Hoeber, New York.

    Google Scholar 

  • Brandes, D. (1965) Observations on the apparent mode of formation of ‘pure’ lysosomes.Journal of Ultrastructure Research 12, 63–80.

    PubMed  Google Scholar 

  • Brizzee, K. R., Cancilla, P. A., Sherwood, N. andTimiras, P. S. (1969) The amount and distribution of pigments in neurons and glia of the cerebral cortex. Autofluorescent and ultrastructural studies.Journal of Gerontology 24, 127–35.

    PubMed  Google Scholar 

  • De Duve, C. (1959) Lysosomes: A new group of cytoplasmic particles. InSubcellular Particles (Edited byHayashi, T.), pp. 128–59. Ronald Press, New York.

    Google Scholar 

  • De Duve, C. (1963) The lysosome.Scientific American 208, 64–72.

    PubMed  Google Scholar 

  • De Duve, C. (1964) From cytases to lysosomes.Federation Proceedings 23, 104–9.

    Google Scholar 

  • Ducken, L. W. andStrich, S. J. (1968) An hereditary motor neuron disease with progressive denervation of muscle in the mouse: the mutant ‘wobbler.’Journal of Neurology, Neurosurgery and Psychiatry.31, 535–42.

    Google Scholar 

  • Elliot, A. andBak, I. J. (1964) The fate of mitochondria during aging inTetrahymena pyriformis.Journal of Cell Biology 20, 113–29.

    PubMed  Google Scholar 

  • Ericcson, J. L. E., Trump, B. F., andWeisel, J. (1965) Electron microscope studies of the proximal tubule of the rat kidney. II. Cytosegresomes and cytosomes: their relationship to each other and to the lysosome concept.Laboratory Investigation 14, 1341–65.

    PubMed  Google Scholar 

  • Essner, E. andNovikoff, A. B. (1960) Human hepatocellular pigments and lysosomes.Journal of Ultrastructure Research 3, 374–91.

    PubMed  Google Scholar 

  • Essner, E. andNovikoff, A. B. (1962) Cytological studies on two functional hepatomas, Interrelations of endoplasmic reticulum, Golgi apparatus and lysosomes.Journal of Cell Biology 15, 289–312.

    Google Scholar 

  • Few, A. andGetty, R. (1967) Occurrence of lipofuscin as related to aging in the canine and porcine nervous system.Journal of Gerontology 22, 357–68.

    PubMed  Google Scholar 

  • Friend, D. S. andFarquhar, M. G. (1967) Functions of coated vesicles during protein absorption in the rat vas deferens.Journal of Cell Biology 35, 357–76.

    PubMed  Google Scholar 

  • Gatenby, J. B. (1953) The Golgi apparatus of the living sympathetic ganglion cells of the mouse, photographed by phase contrast microscopy.Journal of the Royal Microscopical Society 73, 61–8.

    PubMed  Google Scholar 

  • Glees, P. andGopinath, G. (1973) Age changes in the centrally and peripherally located sensory neurons in rat.Zeitschrift für Zellforschung und Mikroskopische Anatomie 141, 285–98.

    Google Scholar 

  • Hasan, M. andGlees, P. (1972) Genesis and possible dissolution of neuronal lipofuscin.Gerontologia 18, 217–36.

    PubMed  Google Scholar 

  • Kasan, M. andGlees, P. (1973a) Ultrastructural age changes in hippocampal nervous system and neuroglia.Experimental Gerontology 8, 75–83.

    PubMed  Google Scholar 

  • Hasan, M. andGlees, P. (1973b) Lipofuscin in monkey ‘lateral geniculate body.’ An electron microscope study.Acta Anatomica 84, 85–95.

    PubMed  Google Scholar 

  • Holtzman, E., Novikoff, A. B. andVillaverde, H. (1978) Lysosomes and GERL in normal and chromatolytic neurons of the rat ganglion nodosum.Journal of Cell Biology 33, 419–35.

    Google Scholar 

  • Kerényi, T., Havanghy, L. andHuttner, I. (1968) Investigations on experimentally produced age-pigment in the nervous system.Experimental Gerontology 3, 155–8.

    PubMed  Google Scholar 

  • Miyagishi, T., Takahata, N. andIizka, R. (1967) Electron microscopic studies on the lipopigments in the cerebral cortex nerve cells of senile and vitamin E deficient rats.Acta Neuropathologica 9, 7–17.

    PubMed  Google Scholar 

  • Moe, H., Rostgaard, J. andBehnke, O. (1965) On the morphology and origin of virgin lysosomes in the intestinal epithelium of rat.Journal of Ultrastructure Research 12, 396–403.

    PubMed  Google Scholar 

  • Nanda, B. S. andGetty, K. (1973) Occurrence of aging pigment (lipofuscin) in the nuclei and cortices of the canine brain.Experimental Gerontology 8, 1–17.

    PubMed  Google Scholar 

  • Nandy, K. (1968) Further studies on the effects of centrophenoxine on the lipofuscin pigment in the neurons of senile guinea pigs.Journal of Gerontology 23, 82–92.

    PubMed  Google Scholar 

  • Nandy, K. (1969) Histologie and histochemical study of motor neurons with specifie reference to experimental degeneration, aging and drug actions. InMotor Neuron Diseases (Edited byNorris, Jr., F. H. andKurland, L. T.), pp. 319–34. Grune and Stratton, New York.

    Google Scholar 

  • Novikoff, A. B. (1961) Lysosomes and related particles. InThe Cell, Vol. II. (Edited byBrachet, J. andMirsky, A. E.), pp. 423–88. Academic Press, New York.

    Google Scholar 

  • Novikoff, A. B. (1967) Lysosomes in nerve cells. InThe Neuron. (Edited byHydÉn, H.), pp. 319–77. Elsevier, Amsterdam.

    Google Scholar 

  • Novikoff, A. B., Goldfischer, S., Essner, E. andIaciofano, P. (1961) The relations between acidphosphatase rich lysosomes and the Golgi apparatus.Journal of Histochemistry and Cytochemistry 9, 630.

    Google Scholar 

  • Novikoff, A. B., Essner, E. andQuintana, N. (1964) Golgi apparatus and lysosomes.Federation Proceedings 23, 1010–22.

    PubMed  Google Scholar 

  • Novikoff, P. M., Novikoff, A. B., Quintana, N. andHauw, J.-J. (1971) Golgi apparatus, GERL, and lysosomes of neurons in rat dorsal root ganglion, studies by thick section and thin section cytochemistry.Journal of Cell Biology 50, 859–86.

    PubMed  Google Scholar 

  • Reichel, W., Hollander, J., Clark, J. H. andStrehler, B. L. (1968) Lipofuscin pigment accumulation as a function of age and distribution in rodent brain.Journal of Gerontology 23, 71–8.

    PubMed  Google Scholar 

  • Samorajski, T., Keefe, J. R. andOrdy, J. M. (1964) Intracellular localization of lipofuscin age pigments in the nervous system.Journal of Gerontology 19, 262–76.

    PubMed  Google Scholar 

  • Samorajski, T., Ordy, J. M. andKeefe, J. R. (1965) The fine structure of lipofuscin age pigment in the nervous system of aged mice.Journal of Cell Biology 26, 779–95.

    Google Scholar 

  • Samorajski, T., Ordy, J. M. andRady-Reimer, P. (1968) Lipofuscin pigment accumulation in the nervous system of aging mice.Anatomical Record 160, 555–74.

    PubMed  Google Scholar 

  • Samorajski, T. andOrdy, J. M. (1972) Neurochemistry of aging. InAging and the Brain (Advances in Behavioral Biology, Vol. 3; Edited byGaitz, C. M.), pp. 41–61. Plenum, New York.

    Google Scholar 

  • Sekhon, S. S. andMaxwell, D. S. (1970) Fine structure of developing hagfish erythrocytes with particular reference to the cytoplasmic organelles.Journal of Morphology 131, 211–36.

    PubMed  Google Scholar 

  • Sekhon, S. S., Andrews, J. M. andMaxwell, D. S. (1969) Accumulation and development of lipofuscin pigment in the aging central nervous system of the mouse.Journal of Cell Biology 43, 1233.

    Google Scholar 

  • Sosa, J. M. andDe Zorilla, N. B. (1966) Morphological variations of the Golgi apparatus in spinal ganglion nerve cells relating to ageing.Acta Anatomica 64, 475–97.

    PubMed  Google Scholar 

  • Sulkin, N. M. (1955) The properties and distribution of PAS positive substances in the nervous system of the senile dog.Journal of Gerontology 10, 135–44.

    PubMed  Google Scholar 

  • Swift, H. andHruban, Z. (1964) Focal degradation as a biological process.Federation Proceedings 23, 1026–37.

    PubMed  Google Scholar 

  • Tooze, J. andDavies, H. G. (1967) Light- and electron-microscope studies on the spleen of the newtTriturus cristatus: the fine structure of erythropoietic cells.Journal of Cell Science 2, 617–40.

    PubMed  Google Scholar 

  • Toth, S. E. (1968) The origin of lipofuscin age pigment.Experimental Gerontology 3, 19–30.

    PubMed  Google Scholar 

  • Wilcox, H. H. (1959) Structural changes in the nervous system related to the process of aging. Present status of knowledge. InThe Process of Aging in the Nervous System. (Edited byBirren, J. E., Imus, H. andWindle, W.), pp. 16–23. Charles C. Thomas, Springfield, Illinois.

    Google Scholar 

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Authors and Affiliations

  1. Veterans Administration Hospital, Long Beach, California

    Sant S. Sekhon

  2. The Department of Anatomy and the Brain Research Institute, University of California School of Medicine, Los Angeles, California

    David S. Maxwell

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  1. Sant S. Sekhon
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Sekhon, S.S., Maxwell, D.S. Ultrastructural changes in neurons of the spinal anterior horn of ageing mice with particular reference to the accumulation of lipofuscin pigment. J Neurocytol 3, 59–72 (1974). https://doi.org/10.1007/BF01111932

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  • DOI: https://doi.org/10.1007/BF01111932

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