Skip to main content
SpringerLink
Log in

Ultrastructural cytochemistry of the human adrenal medulla

  • Published:
Histochemistry Aims and scope Submit manuscript

Summary

A cytochemical study of the human adrenal medulla showed that it is made up of two cell types, the adrenaline (A-) and noradrenaline (N-) storing cells. A- and N-storing granules were argentaphobic when ultrathin sections of Araldite-embedded medullae were stained according to the periodic acid-thiocarbohydrazide silver proteinate technique of Thiery. A small amount of glycogen (which disappeared after digestion with alpha amylase) in the form of B-particles, as well as lysosomes were, however, visualized by this technique. The entire core of A granules was markedly positive after ultrathin sections of glutaraldehyde-fixed, glycol methacrylate-(GMA-) embedded medullae were stained with phosphotungstic acid (PTA) at a low pH (0.3). The N granules, in contrast, were mostly unreactive. PTA stained a large part of the Golgi complex of A cells, whereas it generally had no such effect on that of the N cells. In both cell types, the cell coat, lysosomes and multivesicular bodies reacted to PTA. The periodic acid —schiff (PAS) technique showed A but not N granules in semithin sections of GMA- or Araldite-embedded medullae. The PTA and PAS stains were abolished by acetylation, restored by saponification, unchanged by methylation and greatly diminished by sulfation or by digestion with beta glucuronidase after oxidation by perchloric acid. These results indicate that in man the A granules and the Golgi complex of A cells, unlike the same structures in N cells, are rich in glycoproteins.

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

Access this article

Log in via an institution

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

  • Al-Lami, F.: Light and electron microscopy of the adrenal medulla of Macaca mulata monkey. Anat. Rec. 164, 317–332 (1969)

    Google Scholar 

  • Babai, F., Bernhard, W.J.: Détection cytochimique par l'acide phosphotungstique de certains polysaccharides sur coupes à congélation ultrafines. J. Ultrastruct. Res. 37, 601–617 (1971)

    Google Scholar 

  • Bargmann, W., Lindner, E.: Über den Feinbau des Nebennierenmarkes des Igels (Erinaceus europeus L.). Z. Zellforsch. 64, 868–912 (1964)

    Google Scholar 

  • Bässler, R., Habighorst, L.V.: Vergleichende licht- und elektronenmikroskopische Untersuchungen am Nebennierenmark und Pheochromozytom. Beitr. Pathol. Anat. 130, 446–488 (1964)

    Google Scholar 

  • Benchimol, S., Cantin, M.: Radioautographic study of synthesis and migration of glycoproteins in the cells of the rat adrenal medulla. J. Microsc. Biol. Cell. (Paris) (1976) (in print)

  • Benedeczky, I., Lapis, K.: Electron microscopy of human adrenal medulla and pheochromozytoma. Beitr. Pathol. Anat. 137, 403–438 (1968)

    Google Scholar 

  • Benedeczky, I., Smith, A.C.: Ultrastructural studies on the adrenal medulla of golden hamster: origin and fate of secretory granules. Z. Zellforsch. 124, 367–386 (1972)

    Google Scholar 

  • Bennett, G., Leblond, C.P., Hadded, A.: Migration of glycoproteins from the Golgi apparatus to the surface of various cell types as shown by radioautography after labelled fucose injection into rats. J. Cell Biol. 60, 258–284 (1974)

    Google Scholar 

  • Brown, W.J., Barajas, L., Latta, H.: The ultrastructure of the human adrenal medulla: with comparative studies of white rat. Anat. Rec. 169, 173–184 (1971)

    Google Scholar 

  • Cannata, M.A., Chiocchio, S.R., Tramezzani, J.H.: Specificity of the glutaraldehyde silver technique for catecholamines and related compounds. Histochemie 12, 253–264 (1968)

    Google Scholar 

  • Cantin, M., Benchimol, S.: Localization and characterization of carbohydrates in adrenal medullary cells. J. Cell Biol. 65, 463–479 (1975)

    Google Scholar 

  • Cantin, M., Benchimol, S., Castonguay, Y., Berlinguet, J.C., Huet, M.: Ultrastructural cytochemistry of atrial muscle cells. V. Characterization of the specific granules in the human left atrium. J. Ultrastruct. Res. 52, 179–192 (1975)

    Google Scholar 

  • Chang, W.W.L., Bencosme, S.A.: Selective staining of secretory granules of adrenal medullary cells by silver methenamine: a light and electron microscopic study. Canad. J. Physiol. Pharmacol. 46, 745–747 (1968)

    Google Scholar 

  • Coimbra, A., Leblond, C.P.: Sites of glycogen synthesis in rat liver cells as shown by electron microscope radioautography after administration of glucose-H3. J. Cell Biol. 30, 151–175 (1966)

    Google Scholar 

  • Coupland, R.E.: Catecholamines. The chromaffin system. Handbook of Experimental Pharmacology, Vol. XXXIII (Blaschko, H., Muscholl, E., ed.) pp. 16–45. Berlin-Heidelberg-New York: Springer 1972

    Google Scholar 

  • Coupland, R.E.: Subcellular organization and function in endocrine tissues. (Hiller, H., Lederis, K., ed.) pp. 611–635. London: Cambridge University Press 1971

    Google Scholar 

  • Coupland, R.E., Hopwood, D.: The mechanism of the differential staining reaction for adrenaline- and noradrenaline-storing granules in tissues fixed in glutaraldehyde. J. Anat. 100, 227–243 (1966)

    Google Scholar 

  • Coupland, R.E., Pyper, A.S., Hopwood, D.: A method for differentiating between noradrenaline- and adrenaline-storing cells in the light and electron microscope. Nature (Lond.) 201, 1240–1241 (1964)

    Google Scholar 

  • Coupland, R.E., Weakley, B.S.: Electron microscopic observation on the adrenal medulla and extra-adrenal chromaffin tissue of the postnatal rabbit. J. Anat. 106, 213–231 (1970)

    Google Scholar 

  • Diner, O.: Observations sur le développement de la medullo-surrénale du rat: l'évolution de la partie non-chromaffine. Arch Anat. microsc. Morph. exp. 54, 671–718 (1965)

    Google Scholar 

  • Elfvin, L.G.: The fine structure of the cell surface of chromaffin cells in the rat adrenal medullla. J. Ultrastruct. Res. 12, 263–286 (1965)

    Google Scholar 

  • Fillion, G., Nosál, R., Uvnäs, B.: The presence of a sulphomucopolysaccharide-protein complex in adrenal medullary cell granules. Acta Physiol. Scand. 83, 286–288 (1971)

    Google Scholar 

  • Flechon, J.E.: Validity of phosphotungstic acid staining of polysaccharide (glycogen) at very low pH on thin sections of glycolmethacrylate embedded material. J. Microsc. (Paris) 19, 207–212 (1974)

    Google Scholar 

  • Fullmer, H.M.: Effect of peracetic acid on the enzymatic digestion of various mucopolysaccharides: reversal of the PAS staining reaction of mucin. J. Histochem. Cytochem. 8, 113–121 (1960)

    Google Scholar 

  • Goldstone, A., Koenig, H.: Acid hydrolases and structural lipoproteins of kidney lysosomes. J. Histochem. Cytochem. 16, 511–512 (1968)

    Google Scholar 

  • Gorgas, K.: Über fibrillärstrukturen im Nebennierenmark von Haus- und Wildmeerschweinchen (Cavia aperea f. porcellus L. und Cavia aperea tschudii Fitzinger). Z. Zellforsch. 87, 377–388 (1968)

    Google Scholar 

  • Hervonen, A.: Fine structure of paraganglia and adrenal medulla. Acta Physiol. Scand. Suppl. 368, 46–77 (1971)

    Google Scholar 

  • Holtzman, E., Dominitz, P.: Cytochemical studies of lysosomes, Golgi apparatus and endoplasmic reticulum in secretion and protein uptake by adrenal medulla cells of the rat. J. Histochem. Cytochem. 16, 320–385 (1968)

    Google Scholar 

  • Huet, M., Benchimol, S., Castonguay, Y., Cantin, M.: Ultrastructural cytochemistry of atrial muscle cells. III. Reactivity of specific granules in man. Histochemistry 41, 87–105 (1974)

    Google Scholar 

  • Huet, M., Cantin, M.: Ultrastructural cytochemistry of atrial muscle cells. I. Characterization of the carbohydrate content of specific granules. Lab. Invest. 30, 514–524 (1974)

    Google Scholar 

  • Iglesias, J.R., Bernier, R., Simard, R.: Ultracryotomie: a routine procedure. J. Ultrastruct. Res. 36, 271–289 (1971)

    Google Scholar 

  • Jacobs, M.M., Nyc, J.F., Brown, D.M.: Isolation and chemical properties of a repressible acid phosphatase in Neurospora crassa. J. Biol. Chem. 246, 1419–1428 (1971)

    Google Scholar 

  • Lauro, G., Caravita, S., Palladini, G.: Observations histochimiques sur les glycoprotéines de la médullo-surrénale du rat. Arch. Anat. Microsc. 61, 5–15 (1972)

    Google Scholar 

  • Margolis, R.U., Margolis, R.K.: Isolation of chondroitin sulfate and glycopeptides from chromaffin granules of adrenal medulla. Biochem. Pharmacol. 22, 2195–2197 (1973)

    Google Scholar 

  • Marinozzi, V.: Fourth european regional conference of electron microscopy (Steve Bocciarelli, D., ed.) p. 55. Rome, 2, 1968

  • Mayor, H.D., Hampton, J.C., Rosario, B.: A simple method for removing the resin from epoxyembedded tissue. J. Biophys. Biochem. Cytol. 9, 909–910 (1961)

    Google Scholar 

  • McDowell, E.M., Barrett, L.A., Trump, B.F.: Observations on small granule cells in adult human bronchial epithelium and in carcinoid and oat cell tumors. Lab. Invest. 34, 202–206 (1976)

    Google Scholar 

  • McManus, J.F.A.: Staining method, histologic and histochemical. New York: Harper and Row 1960

    Google Scholar 

  • Neutra, M., Leblond, C.P.: Synthesis of the carbohydrate of mucus in the Golgi complex as shown by electron microscope radioautography of goblet cells from rats injected with glucose-H3. J. Cell Biol. 30, 119–136 (1966)

    Google Scholar 

  • Neutra, M., Leblond, C.P.: Radioautographic comparison of the uptake of galactose-H3 and glucose-H3 in the Golgi region of various cells secreting glycoproteins or mucopolysaccharides. J. Cell Biol. 30, 137–150 (1966)

    Google Scholar 

  • Pearse, A.G.E.: Endocrine pathology decennial (Sommers, S.C., ed.) pp. 147–163. New York: Appleton-Century-Crofts 1975

    Google Scholar 

  • Pease, D.C.: Polysaccharides associated with the exterior surface of epithelial cells: kidney, intestine, brain. J. Ultrastruct. Res. 15, 555–588 (1966)

    Google Scholar 

  • Pease, D.C.: Phosphotungstic acid as a specific electron stain for complex carbohydrates. J. Histochem. Cytochem. 18, 455–458 (1970)

    Google Scholar 

  • Pelletier, G.: Détection des glycoprotéines dans les cellules corticotropes de l'hypophyse du rat. J. Microsc. (Paris) 11, 327–330 (1971)

    Google Scholar 

  • Piezzi, R.S.: Two types of chromaffin cells in the adrenal gland of the “Bufo arenarum”. Acta Physiol. Lat. Amer. 15, 96–100 (1965)

    Google Scholar 

  • Quintarelli, G., Bellocci, M., Geremia, R.: On phosphotungstic acid staining. IV. Selectivity of the staining reaction. J. Histochem. Cytochem. 21, 155–160 (1973)

    Google Scholar 

  • Rambourg, A.: Détection des glycoprotéines en microscopie électronique: coloration de la surface cellulaire et de l'appareil de Golgi par un mélange acide chromique-phosphotungstique. C.R. Acad. Sci. [D] (Paris) 265, 1426–1428 (1967)

    Google Scholar 

  • Rambourg, A.: Fourth european regional conference on electron microscopy (Steve Bocciarelli, D., ed.) p. 57. Rome, 2: 1968

  • Rambourg, A.: Morphological and histochemical aspects of glycoproteins at the surface of animal cells. Int. Rev. Cytol. 31, 57–114 (1971)

    Google Scholar 

  • Schaff, Z., Barry, D.W., Grimley, P.M.: Cytochemistry of tubuloreticular structures in lymphocytes from patients with systemic lupus erythematosus and in cultured human lymphoid cells: comparison to a paramyxovirus. Lab. Invest. 29, 577–586 (1973)

    Google Scholar 

  • Scott, J.E.: Phosphotungstate: a “universal” (nonspecific) precipitant for polar polymers in acid solution. J. Histochem. Cytochem. 19, 689–691 (1971)

    Google Scholar 

  • Scott, J.E., Glick, D.: The invalidity of “phosphotungstic acid as a specific electron stain for complex carbohydrates”. J. Histochem. Cytochem. 19, 63–64 (1971)

    Google Scholar 

  • Smith, A.D.: The interaction of drugs and subcellular components on animals cells (Campbell, P.N., ed.) pp. 239–292. London: Churchill 1968

    Google Scholar 

  • Smith, A.D., Winkler, H.: Purification and properties of an acidic protein from chromaffin granules of bovine adrenal medulla. Biochem. J. 103, 483–491 (1967)

    Google Scholar 

  • Spicer, S.S., Horn, R.G., Leppi, J.: The connective tissue. International academy of pathology monograph (Wagner, B.M., ed.). Baltimore: The Williams and Wilkins Company 1967

    Google Scholar 

  • Tannenbaum, M.: Endocrine pathology decennial (Sommers, S.C., ed.) pp. 473–503. New York: Appleton-Century-Crofts 1975

    Google Scholar 

  • Thiery, J.P.: Mise en évidence des polysaccharides sur coupes fines en microscopie électronique. J. Microsc. (Paris) 6, 987–1018 (1967)

    Google Scholar 

  • Thiery, J.P.: Rôle de l'appareil de Golgi dans la synthèse des mucopolysaccharides — Etude cytochimique. I. Mise en évidence de mucopolysaccharides dans les vésicules de transition entre l'ergastoplasme et l'appareil de Golgi. J. Microsc. (Paris) 8, 689–708 (1969)

    Google Scholar 

  • Tramezzani, J.H., Chiocchio, S., Wassermann, G.F.: A technique for light and electron microscopic identification of adrenaline and noradrenaline-storing cells. J. Histochem. Cytochem. 12, 890–899 (1964)

    Google Scholar 

  • Unsicker, K.: Chromaffin, small granule-containing and ganglion cells in the adrenal gland of reptiles. Cell Tissue Res. 165, 477–508 (1976)

    Google Scholar 

  • Wassermann, G., Tramezzani, J.H.: Separate distribution of adrenaline- and noradrenaline-secreting cells in the adrenal of snakes. Gen. Comp. Endocrinol. 3, 480–489 (1963)

    Google Scholar 

  • Wood, J.G.: The relationship of nucleotidase activity of catecholamine storage sites in adrenomedullary tissue. Amer. J. Anat. 121, 671–704 (1967)

    Google Scholar 

  • Wood, J.G., Barrnett, R.J.: Histochemical differentiation of epinephrine and norepinephrine granules in the adrenal medulla with the electron microscope. Anat. Rec. 145, 301–302 (1963)

    Google Scholar 

  • Wood, J.G., Barrnett, R.J.: Histochemical demonstration of norepinephrine at a fine structural level. J. Histochem. Cytochem. 12, 197–209 (1964)

    Google Scholar 

  • Yates, R.D., Wood, J.D., Duncan, D.: Phase and electron microscopic observations of two cell types in the adrenal medulla of the Syrian hamster. Tex. Rep. Biol. Med. 20, 494–502 (1962)

    Google Scholar 

  • Yokoyama, M., Takayasu, H.: An electron microscopic study of the human adrenal medulla and pheochromocytoma. Urol. int. (Basel) 24, 79–95 (1969)

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Départment de Pathologie, Université de Montréal et Service de Pathologie, Institut de Cardiologie de Montréal, 2900, boul. Edouard-Montpetit, H3T 1J4, Montréal, Québec, Canada

    Sarita Benchimol & Marc Cantin

Authors
  1. Sarita Benchimol
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Marc Cantin
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Benchimol, S., Cantin, M. Ultrastructural cytochemistry of the human adrenal medulla. Histochemistry 54, 9–26 (1977). https://doi.org/10.1007/BF00493325

Download citation

  • Received:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00493325

Keywords

Search

Navigation