Summary
A study was made of the fine structure of neurons in lumbar sympathetic ganglia which were surgically removed from a 52 year old male patient. Some samples were fixed by direct immersion into osmium tetroxide, others were first prefixed with an aldehyde solution. Large vesiculated pigment granules were described, compared with similar particles, previously seen in human and animal autonomic neurons, and their glycogen and lipid-soluble components were tentatively identified. These granules increase numerically during aging, are probably derivatives of lysosomes, and may incorporate both lipofuscin and melanin in the same particle. Mitochondrial changes (enlargement, disappearance of cristae and deposit of opaque central material) in sympathetic perikarya occurred under all conditions of preservation, and were interpreted as hypoxia-induced structures which developed during life. Abnormal aggregates of mitochondria were seen in nerve processes. Laminar bodies, chiefly associated with mitochondria were present, especially, in aldehyde prefixed material. It remained undecided whether these structures occurred during life or were artifacts. Compared with direct osmium tetroxide fixation, prefixation with aldehyde, followed by osmium tetroxide proved to be a superior, but not entirely adequate method of preserving deep layers of neuronal tissue.
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References
Bassi, M., and A. Bernelli-Zazzera: Ultrastructural cytoplasmic changes of liver cells after reversible and irreversible ischemia. Exp. and molec. Path. 3, 332–350 (1964).
Bennett, H. S.: A suggestion as to the nature of the lysosome granules. J. biophys. biochem. Cytol. 2 (Suppl.), 185 (1956).
Bloom, G. D., and E. M. Ritzén: Autofluorescent granules in cells of human dermis II. Histochemical observations. Z. Zellforsch. 61, 841–854 (1964).
—: Autofluorescent granules in cells of human dermis III. Electron microscopical observations and fluorescence characteristics. Z. Zellforsch. 67, 319–337 (1965).
Breemen, V. L. van, and R. W. Bowman: Lamellar bodies in Purkinje cells of dog cerebellum. 6th Ann. Meet. Amer. Soc. Cell Biol. Houston Texas 17–19 November, 1966. In: J. Cell Biol. 31, 138 A (1966).
Clementi, F., C. Peracchia et C. Vassallo: Modifications histologiques et ultra-structurales des ganglions lombaires dans la thrombo-angéite oblitérante périphérique du type Buerger. Presse méd. 73, 537–542 (1965).
Confer, D. B., and R. J. Stenger: The evolution of lysosomes in hypoxic liver parenchyma as seen with the electron microscope. Amer. J. Path. 45, 533–546 (1964).
Cravioto, H.: Elektronenmikroscopische Untersuchungen am sympathischen Nervensystem des Menschen. Z. Zellforsch. 58, 312–330 (1962).
DeLemos, C., and J. Pick: The fine structure of thoracic sympathetic neurons in the adult rat. Z. Zellforsch. 71, 189–206 (1966).
Doolin, P. F., and K. D. Barron: Ultrastructure and histochemistry of cytoplasmic laminar bodies (CLB) in lateral geniculate neurons of the cat. Sixth internat. congr. electron micr., Kyoto, 2, 453–454 (1966).
Duve de: The function of intracellular hydrolases. Exp. Cell Res., Suppl. 7, 169–182 (1959).
—: The lysosome concept. In: Lysosomes, Ciba Found. Symp. (A. V. S. de Reuk and M. P. Cameron), p. 1–35. Boston: Little, Brown & Co. 1963.
Essner, E., and A. B. Novikoff: Human hepatocellular pigments and lysosomes. J. Ultrastruct. Res. 3, 374–391 (1960).
Forssmann, W. G.: Studien über den Feinbau des Ganglion cervicale superius der Ratte. Acta anat. (Basel) 50, 106–140 (1964).
Gatenby, J. B., and R. L. Devine: The structure and aging of sympathetic neurons. J. roy. micr. Soc. 79, 1–17 (1960).
Gedigk, P., u. E. Bontke: Über den Nachweis von hydrolytischen Enzymen in Lipopigmenten. Z. Zellforsch. 44, 495–518 (1956).
—, u. R. Fischer: Über die Entstehung von Lipopigmenten in Muskelfasern. Untersuchungen beim experimentellen Vitamin E-Mangel der Ratte und an Organen des Menschen. Virchows Arch. path. Anat. 332, 431–468 (1959).
Goldfischer, S., H. Villaverde, and R. Forschirm: The demonstration of acid hydrolase, thermostable reduced diphosphopyridine nucleotide tetrazolium reductase and peroxidase activities in human lipofuscin pigment granules. J. Histochem. Cytochem. 14, 641–652 (1966).
Graham, R. C., and M. J. Karnovsky: The early stages of absorption of injected horseradish peroxidase in the proximal tubules of mouse kidney: Ultrastructural cytochemistry by a new technique. J. Histochem. Cytochem. 14, 291–302 (1966).
Hager, H., W. Hirschberger, and W. Scholz: Electron microscopic changes in brain tissue of Syrian hamsters following acute hypoxia. Aerospace Med. 31, 379–387 (1960).
Heidenreich, O., u. G. Siebert: Untersuchungen an isoliertem, unverändertem Lipofuscin aus Herzmuskulatur. Virchows Arch. path. Anat. 327, 112–126 (1955).
Herdson, P. B., P. J. Garvin, and R. B. Jennings: Fine structural changes produced in rat liver by partial starvation. Amer. J. Path. 45, 157–181 (1964).
Herndon, R. M.: Lamellar bodies, an unusual arrangement of the granular endoplasmic reticulum. J. Cell Biol. 20, 338–342 (1964).
Hess, A.: The fine structure of young and old spinal ganglia. Anat. Rec. 123, 399–423 (1955).
Hydén, H., and B. Lindström: Microspectrographic studies on the yellow pigment in nerve cells. Discussions Faraday Soc. 9, 436–441 (1950).
Issidorides, M., and W. M. Shanklin: Histochemical reactions of cellular inclusions in the human neurone. J. Anat. (Lond.) 95, 151–159 (1961).
Jezequel, A. M.: Dégénérescence myélinique des mitochondries de foie humain dans un épithélioma du cholédoque et un ictère viral. J. Ultrastruct. Res. 3, 210–215 (1959).
Jordan, S. W.: Electron microscopy of hepatic regeneration. Exp. and molec. Path. 3, 183–200 (1964).
Karlsson, U., and R. L. Schulz: Fixation of the central nervous system for electron microscopy by aldehyde perfusion. I. Preservation with aldehyde perfusates versus direct perfusion with osmium tetroxide with special reference to membranes and the extra cellular space. J. Ultrastruct. Res. 12, 160–186 (1965).
Koneff, H.: Beiträge zur Kenntniss der Nervenzellen in den peripheren Ganglien. Mitt. naturforsch. Ges. Bern 13–44 (1887).
Lafontaine, J. G., and C. Allard: A light and electron microscope study of the morphological changes induced in rat liver cells by the azo dye 2-Me-DAB. J. Cell Biol. 22, 143–172 (1964).
Mercer, E. H.: The evolution of intracellular phospholipid membrane systems. In: The interpretation of ultrastructure (R. Harris, ed.), vol. 1, p. 369–384. New York: Academic Press 1962.
Miller, F., and G. E. Palade: Lytic activities in renal protein absorption droplets. An electron microscopical cytochemical study. J. Cell Biol. 23, 519–552 (1964).
Mishima, Y.: Macromolecular changes in pigmentary disorders. Arch. Derm. 91, 519–558 (1965).
Morales, R., D. Duncan, and R. Rehmet: A distinctive laminated cytoplasmic body in the lateral geniculate body neurons of the cat. J. Ultrastruct. Res. 10, 116–123 (1964).
Nelson, B. D.: Hepatic lysosome and serum enzyme alterations in rats exposed to high altitude. Amer. J. Physiol. 211, 651–655 (1966).
Nilsson, O.: Ultrastructure of mouse uterine surface epithelium under different estrogenic influences. I. Spayed animals and oestrous animals. J. Ultrastruct. Res. 1, 375–396 (1958).
Oshuga, N., S. Shionoya, K. Kamiya, and M. Hoshino: An electron microscopic study of the human sympathetic ganglion cell. I. Inclusion bodies. J. Electronmicr. 15, 26–27 (1966).
Oudea, P. R.: Anoxic changes of liver cells electron microscopic study after injection of colloidal mercury. Lab. Invest. 12, 386–394 (1963).
Palay, S. L., S. M. McGee-Russell, G. Spencer jr., and M. A. Grillo: Fixation of neural tissues for electron microscopy by perfusion with solutions of osmium tetroxide. J. Cell Biol. 12, 385–410 (1962).
—, and G. E. Palade: The fine structure of neurons. J. biophys. biochem. Cytol. 1, 69–88 (1955).
Pick, J.: The submicroscopic organization of the sympathetic ganglion in the frog. J. comp. Neurol. 120, 409–462 (1963).
- The fine structure of human sympathetic neurons in adolescence. Third Europ. Reg. Confer. on Electron Micr. Czechosl. Acad. Sci. 1964, p. 303.
- Sympathetic neurons in x-irradiated rats. (In preparation).
—, C. DeLemos, and C. Gerdin: The fine structure of sympathetic neurons in man. J. comp. Neurol. 122, 19–68 (1964).
—, C. Gerdin, and C. Delemos: An electron microscopical study of developing sympathetic neurons in man. Z. Zellforsch. 62, 402–415 (1964).
Sachs, H. W.: Über die autogenen Pigmente, besonders das Lipofuszin und seine Abgrenzung von Melanin. Beitr. path. Anat. 108, 267–314 (1943).
Samorajski, T., J. Keefe. and J. M. Ordy: Intracellular localization of lipofuscin age pigments in the nervous system. J. Geront. 19, 262–276 (1964).
—, J. M. Ordy, and J. R. Keefe: The fine structure of lipofuscin age pigment in the nervous system of aged mice. J. Cell Biol. 16, 779–795 (1965).
Schaffner, F., and P. Felig: Changes in hepatic structure in rats produced by breathing pure oxygen. J. Cell Biol. 27, 505–517 (1965).
Siebert, G., P. B. Diezel, K. Jahr, E. Krug, A. Schmitt, E. Grunberger u. I. Bottke: Isolierung und Eigenschaften von Lipofuscin aus Herzgewebe des Menschen. Histochemie 3, 17–45 (1962).
Strehler, B. L., and A. S. Mildvan: Studies on the chemical properties of lipofuscin pigment. In: Biological aspects of aging (N. Shock, ed.), p. 174–181. New York: Columbia University Press 1962.
Sulkin, N.: The distribution of mucopolysaccharides in the cytoplasm of vertebrate nerve cells. J. Neurochem. 5, 231–235 (1960).
Terry, R. D., and M. Weiss: Studies in Tay-Sachs disease. II. Ultrastructure of the cerebrum. J. Neuropath. exp. Neurol. 22, 18–55 (1963).
Trump, B. F., P. J. Goldblatt, G. C. Griffen, V. S. Waravdekar, and R. E. Stowell: Effects of freezing and thawing on the ultrastructure of mouse hepatic parenchymal cells. Lab. Invest. 13, 967–1002 (1964).
Watrach, A. M.: Degeneration of mitochondria in lead poisoning. J. Ultrastruct. Res. 10, 177–181 (1964).
Webster, F. H., de, and A. Ames: Reversible and irreversible changes in the fine structure of nervous tissue during oxygen and glucose deprivation. J. Cell Biol. 26, 885–909 (1965).
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This investigation was supported (in whole) by United States Public Health Service Grant NB 1879-09, Institute for Nervous Diseases and Blindness.
The author is greatly indebted to Dr. Jere W. Lord, Jr., Department of Surgery, New York University Medical Center, for the surgically removed tissues used in this study; he is grateful to Dr. Sanford L. Palay, Department of Anatomy, Harvard Medical School, for suggesting the use of the then unpublished method of prefixation with the aldehyde solution. It is a pleasure to acknowledge the expert skill with which Miss Carmen DeLemos and Mr. Arnlod Cianella assisted in completing this work.
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Pick, J. Pigment, abnormal mitochondria and laminar bodies in human sympathetic neurons. Z. Zellforsch. 82, 118–135 (1967). https://doi.org/10.1007/BF00326105
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DOI: https://doi.org/10.1007/BF00326105