Skip to main content
Log in

Electron microscopic studies on pigment granules in the substantia nigra and locus coeruleus of the Japanese monkey (Macaca fuscata yakui)

  • Published:
Zeitschrift für Zellforschung und Mikroskopische Anatomie Aims and scope Submit manuscript

Summary

The so-called neuromelanin pigments in the substantia nigra and locus coeruleus ofMacaca fuscata yakui were studied electron microscopically and cytochemically. Eight Japanese monkeys were perfused with buffered 4% formaldehyde solutions. The materials were post-fixed in buffered 2% osmium tetroxide solutions for 2 hours or immersed in an incubation medium for acid phosphatase before post-osmification. They were dehydrated and embedded in Epon mixture.

The neuromelanin pigment granules measure up to 1 μ in diameter and consist of three structural components which are similar to those of lipofuscin except that the former contain electron dense coarse patches. A conspicuous round and homogenous inclusion body without any crystalline structure occurs in the mitochondrial matrix.

The probable process of neuromelanin formation is discussed, as well as the functional significance of intra-mitochondrial inclusions and acid phosphatase activity. It is suggested that neuromelanin pigments originate from lysosomes, in which altered catecholamines accumulate as coarse patches.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Adler, A.: Melanin pigment in the central nervous system of vertebrate. J. comp. Neurol.70, 315–325 (1939).

    Google Scholar 

  • —: Melanin pigment in the brain of the gorilla. J. comp. Neurol.76, 501–507 (1942).

    Google Scholar 

  • Andén, N., A. Dahlström, K. Fuxe, andK. Larsson: Further evidence for the presence of nigrostriatal dopamine neurons in the rat. Amer. J. Anat.116, 329–333 (1965).

    Google Scholar 

  • Bak, I. J.: The ultrastructure of the substantia nigra and caudate nucleus of the mouse and the cellular localization of catecholamines. Exp. Brain Res.3, 40–57 (1967).

    Google Scholar 

  • Beaver, D. L., H. L. Moses, andC. E. Ganote: Electron microscopy of the trigeminal ganglion. II. Autopsy study of human ganglia. Arch. Path.79, 557–570 (1965).

    Google Scholar 

  • Brown, J. O.: Pigmentation of substantia nigra and locus coeruleus in certain carnivores. J. comp. Neurol.79, 393–405 (1943).

    Google Scholar 

  • Christensen, A. K., andD. W. Fawcett: The normal fine structure of opossum testicular interstitial cells. J. biophys. biochem. Cytol.9, 653–670 (1961).

    Google Scholar 

  • D'Agostino, A. J., andS. Luse: Electron microscopic observations on the human substantia nigra. Neurology (Minneap.)14, 529–536 (1964).

    Google Scholar 

  • Deschner, E. E.: A membrane bounded intramitochondrial granules in untreated mouse sigmoid-rectal epithelial cells. Exp. Cell Res.31, 428–432 (1963).

    Google Scholar 

  • Duffy, P. E., andV. M. Tennyson: Phase and electron microscopic observations of Lewy bodies and melanin granules in the substantia nigra and locus coeruleus in Parkinson's disease. J. Neuropath. exp. Neurol.24, 398–414 (1965).

    Google Scholar 

  • Ebe, T., S. Kobayashi, andT. Yamamoto: Intramitochondrial inclusion bodies in the urinary epithelium of striped snake (Elaphe quadrivirgata) (in Japanese). J. Electronmicroscop. (Tokyo)14, 203–209 (1965).

    Google Scholar 

  • Essner, E., andA. B. Novikoff: Human hepatocellular pigments and lysosomes. J. Ultrastruct. Res.3, 374–391 (1960).

    Google Scholar 

  • Foley, J. M., andD. Baxter: On the nature of pigment granules in the cells of the locus coeruleus and substantia nigra. J. Neuropath. exp. Neurol.17, 586–578 (1958).

    Google Scholar 

  • Frei, J. V., andH. Sheldon: Corpus intracristam: a dense body within hyperplastic mouse epidermis. J. biophys. biochem. Cytol.11, 724–729 (1961).

    Google Scholar 

  • Gahan, P. B.: Histochemistry of lysosomes. Int. Rev. Cytol.21, 1–63 (1967).

    Google Scholar 

  • Hirano, H.: (Personal Communication).

  • Honjin, R., A. Takahashi, T. Hanyu, andS. Murono: Electron microscopy of intracristal dense body within mitochondria of epithelial cells of mouse stomach and rectum. Okajimas Folia anat. jap.41, 267–275 (1965).

    Google Scholar 

  • Kurosumi, K., T. Matsuzawa, andN. Watari: Mitochondrial inclusions in the snake renal tubulus. J. Ultrastruct. Res.16, 269–277 (1966).

    Google Scholar 

  • Lillie, R. D.: Histopathological technic and practical histochemistry, 3rd ed. New York: McGraw-Hill Book Co. 1965.

    Google Scholar 

  • —, andH. Yamada: Histochemical studies on the neuromelanins. Okajimas Folia anat. jap.36, 155–163 (1960).

    Google Scholar 

  • — —: On the yellow brown pigments of the substantia nigra, locus coeruleus and dorsal vagus nucleus of a monkey (Macaca mulata). Okajimas Folia anat. jap.36, 181–183 (1960).

    Google Scholar 

  • Luft, J. H.: Improvements in epoxy resin embedding methods. J. biophys. biochem. Cytol.9, 409–414 (1961).

    Google Scholar 

  • Luft, R., D. Ikkos, G. Palmieri, L. Ernster, andB. Afzelius: A case of severe hypermetabolism of nonthyroid origin with a defect in the maintenance of mitochondrial respiratory control: A correlated clinical, biochemical and morphological study. J. clin. Invest.41, 1776–1804 (1962).

    Google Scholar 

  • Maeda, T., T. Abe, andN. Shimizu: Histochemical demonstration of aromatic monoamine in the locus coeruleus of the mammalian brain. Nature (Lond.)188, 326–327 (1960).

    Google Scholar 

  • Marsden, C. D.: The development of pigmentation and enzyme activity in the nucleus substantia nigra of the cat. J. Anat. (Lond.)99, 175–180 (1965).

    Google Scholar 

  • Millonig, G.: A modified procedure for lead acetate staining of thin sections. J. biophys. biochem. Cytol.11, 736–739 (1961).

    Google Scholar 

  • Moses, H. L., D. L. Beaver, andC. E. Ganote: Electron microscopy of the trigeminal ganglion. I. Comparative ultrastructure. Arch. Path.79, 541–556 (1965).

    Google Scholar 

  • —,C. E. Ganote, D. L. Beaver, andS. S. Schuffman: Light and electron microscopic studies of pigment in human and rhesus monkey substantia nigra and locus coeruleus. Anat. Rec.155, 167–184 (1966).

    Google Scholar 

  • Moyer, F.: Electron microscopic observations on the origin, development and genetic control of melanin granules in the mouse eye. In: The structure of the eye, ed. G. K. Smelser. New York and London: Academic Press 1961.

    Google Scholar 

  • Nagatsu, T.: Biosynthesis and metabolism of catecholamines. J. Jap. biochem. Soc.37, 697–715 (1965).

    Google Scholar 

  • Nakai, T., P. Shubik, andP. Feldman: An electron microscopic study of skin carcinogenesis in the mouse with special reference to the intramitochondrial body. Exp. Cell Res.27, 608–611 (1962).

    Google Scholar 

  • Nilsson, O.: Ultrastructure of mouse uterine surface epithelium under different estrogenic influences. I. Spayed animals and oestrus animals. J. Ultrastruct. Res.1, 375–396 (1958).

    Google Scholar 

  • Ogawa, K., Y. Shinonaga, andT. Suzuki: Electron histochemical demonstration of acid phosphatase activity in the rat cerebellum. J. Electronmicroscop. (Tokyo)11, 111–115 (1962).

    Google Scholar 

  • Ohsuga, N., S. Shinoya, K. Kamiya, andM. Hoshino: An electron microscopic study of the human sympathetic ganglion cell. I. Inclusion bodies. J. Electronmicroscop. (Tokyo)15, 26–27 (1965).

    Google Scholar 

  • Olszewski, J., andD. Baxter: Cytoarchitecture of the human brain stem. Basel and New York: S. Karger 1953.

    Google Scholar 

  • Pakkenberg, H.: The pigment in the substantia nigra in Parkinsonism. Microspectrophotometric comparison with other sources of human pigment. Brain Res.2, 173–180 (1966).

    Google Scholar 

  • Pick, J., C. DeLemos, andC. Gerdin: The fine structure of sympathetic neurons in man. J. comp. Neurol.122, 19–67 (1964).

    Google Scholar 

  • Poirier, L. J., andT. L. Sourkes: Influence of the substantia nigra on the catecholamine content of the striatum. Brain88, 181–192 (1965).

    Google Scholar 

  • Rappaport, H., T. Nakai, andH. Surft: The fine structure of normal and neoplastic melanocytes in the Syrian hamster with particular reference to carcinogen-induced melanotic tumors. J. Cell Biol.16, 171–186 (1963).

    Google Scholar 

  • Sato, S., andK. Kurosumi: Electron microscopic studies on the fine structure of rat lutein cells with special reference to the intramitochondrial globules. Gunma Symp. Endocrinol. (Maebashi)2, 61–69 (1965).

    Google Scholar 

  • Scherer, H. J.: Melanin pigmentation of the substantia nigra in primates. J. comp. Neurol.71, 91–93 (1939).

    Google Scholar 

  • Schnaitman, C., V. G. Erwin, andJ. W. Greenawalt: The submitochondrial localization of monoamine oxidase. An enzymatic marker for the outer membrane of rat liver mitochondria. J. Cell Biol.32, 719–735 (1967).

    Google Scholar 

  • Seiji, M., K. Shimao, M. S. C. Birbeck, andT. B. Fitzpatrick: Subcellular localization of melanin biosynthesis. Ann. N.Y. Acad. Sci.100, 497–533 (1963).

    Google Scholar 

  • Sheldon, H., andH. Zetterqvist: An electron microscope study of the corneal epithelium in the vitamin A deficient mouse. Bull. Johns Hopk. Hosp.98, 372–406 (1956).

    Google Scholar 

  • Sheridan, M. N., andW. D. Belt: Fine structure of the guinea pig adrenal cortex. Anat. Rec.149, 73–98 (1964).

    Google Scholar 

  • Whipple, H. E.: The pigmented cell molecular, biochemical and clinical aspects, ed.H. E. Whipple. Ann. N.Y. Acad. Sci.100 (1963).

  • Wurtman, R. J.: Catecholamines. Boston: Little, Brown & Co. 1965.

    Google Scholar 

  • Yamada, E.: Some observations on the fine structure of the interstitial cell in the human testis as revealed by electron microscopy. Gunma Symp. Endocrinol. (Maebashi)2, 1–17 (1965).

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Additional information

This paper is dedicated to the memory of the late Prof.Hiroshi Hosokawa, Faculty of Medicine, University of Tokyo.

This work was initiated at the suggestion of Dr.S. Sakai, Juntendo University, School of Medicine, Department of Medical History. The author is indebted to Prof.J. Nakai and Associate Prof.S. Igarashi, Department of Anatomy, Faculty of Medicine, University of Tokyo, for their criticism, reading of the manuscript and advice.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Hirosawa, K. Electron microscopic studies on pigment granules in the substantia nigra and locus coeruleus of the Japanese monkey (Macaca fuscata yakui). Z.Zellforsch 88, 187–203 (1968). https://doi.org/10.1007/BF00703907

Download citation

  • Received:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00703907

Keywords

Navigation