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Different types of small granule-containing cells and neurons in the guinea-pig adrenal medulla

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An electron microscopic, histoand biochemical study was carried out on the adrenal medulla of newborn and adult guinea-pigs giving special emphasis to small granule-containing (SGC) cells. Adrenaline (A) was the predominating catecholamine (CA) both in newborn (70–90 % of total CA) and adult (85–90%) guinea-pig adrenals. In analogy to the biochemical findings electron microscopy revealed a high predominance of A cells, which contained large granular vesicles with an average diameter of 180 nm. Most noradrenaline (NA) storing cells showed granular vesicles of a considerably smaller average diameter (80 nm) and had a higher nuclear-cytoplasmic ratio. These cells were termed SGC-NA cells. NA cells with large granular vesicles (average diameter 170 nm) were extremely rare. Another type of SGC cells contained granular vesicles with cores of low to medium electron-density (SGC-NA-negative cells). Biochemical determinations made it unlikely that these cells contained predominantly dopamine (DA). SGC cells were scarcely innervated by cholinergic nerves. They formed processes, which were found both in the adrenal cortex and medulla contacting blood vessels including sinusoid capillaries, steroid producing cells of the reticularis and fasciculata zone and processes, which were interpreted to belong to medullary nerve cells.

Two types of neurons were present in the guinea-pig adrenal medulla, one resembling the principal neurons in sympathetic ganglia, the other, which, according to its morphology, occupied an intermediate position between principal neurons and SGC cells.

In adrenomedullary grafts under the kidney capsule, which were studied three weeks after transplantation, “ordinary” A cells resembled SGC-NA negative cells with respect to their ultramorphology. Processes of transplanted principal neurons showed uptake of 5-hydroxydopamine and, hence, were considered to be adrenergic. Despite the lack of extrinsic nerves to the transplants, few principal neurons received cholinergic synapses, the origin of which is uncertain to date.

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References

  • Axelrod, J.: Purification and properties of phenylethanolamine-N-methyltransferase. J. biol. Chem. 237, 1657–1660 (1962)

    Google Scholar 

  • Björklund, A., Cegrell, C., Falck, B., Ritzén, M., Rosengren, E.: Dopamine-containing cells in sympathetic ganglia. Acta physiol. scand. 78, 334–338 (1970)

    Google Scholar 

  • Brudieux, R., Delost, P.: Secretion des corticosteroids après autogreffe surrénalienne chez le rat. J. Physiol. (Paris) 60, Suppl. 2, 411 (1968)

    Google Scholar 

  • Chamley, J.H., Mark, G.E., Campell, G.R., Burnstock, G.: Sympathetic ganglia in culture. I. Neurons. Z. Zellforsch. 135, 287–314 (1972)

    Google Scholar 

  • Chiba, T.: Electron microscopic and histochemical studies on the synaptic vesicles in mouse vas déferens and atrium after 5-hydroxydopamine administration. Anat. Rec. 175, 35–48 (1973)

    Google Scholar 

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

    Google Scholar 

  • Coupland, R.E., Kobayashi, S., Tomlinson, A.: On the presence of small granule chromaffin (SGC) cells in the rodent adrenal medulla. Proc. Anat. Soc. Great Britain and Ireland 24/25, 3 (1977)

    Google Scholar 

  • Dail, W.G., Evan, A.P., Eason, H.R.: The major ganglion in the pelvic plexus of the male rat. A histochemical and ultrastructural study. Cell Tiss. Res. 159, 49–62 (1975)

    Google Scholar 

  • Diner, O.: Présence d'amas de vésicules de type synaptique du niveau des péricaryons des cellules nerveuses des la médullosurrénale du Hamster. C.R. Acad. Sci. (Paris) 266, 2441–2443 (1968)

    Google Scholar 

  • Elfvin, L.G.: A new granule containing nerve cell in the inferior mesenteric ganglion of the rabbit. J. Ultrastruct. Res. 22, 37–44 (1968)

    Google Scholar 

  • Elfvin, L.G., Hökfelt, T., Goldstein, M.: Fluorescence microscopical, immunohistochemical and ultrastructural studies on sympathetic ganglia of the guinea-pig, with special reference to the SIF-cells and their catecholamine content. J. Ultrastruct. Res. 51, 377–396 (1975)

    Google Scholar 

  • Eränkö, O.: Distribution of fluorescing islets, adrenaline and noradrenaline in the adrenal medulla of the hamster. Acta endocr. (Kbh.) 18, 180–188 (1955)

    Google Scholar 

  • Eränkö, O., Härkonen, M.: Histochemical demonstration of fluorogenic amines in the cytoplasm of sympathetic ganglion cells of the rat. Acta physiol. scand. 58, 285–286 (1963)

    Google Scholar 

  • Falk, B., Hillarp, N.-Å., Thieme, G., Torp, A.: Fluorescence of catecholamines and related compounds condensed with formaldehyde. J. Histochem. Cytochem. 10, 348–354 (1962)

    Google Scholar 

  • Gorgas, K., Böck, P.: Identification of chromaffin and enterochromaffin cells in semithin sections by means of the argentaffin reaction. Mikroskopie 32, 57–63 (1976a)

    Google Scholar 

  • Gorgas, K., Böck, P.: Morphology and histochemistry of the adrenal medulla I. Various types of primary catecholamine-storing cells in the mouse adrenal medulla. Histochemistry 50, 17–31 (1976b)

    Google Scholar 

  • Grillo, M.A.: Electron microscopy of sympathetic tissues. Pharmacol. Rev. 18, 387–399 (1966)

    Google Scholar 

  • Grillo, M.A., Jacobs, L., Conroe, J.H., Jr.: A combined fluorescence histochemical and electron microscopic method for studying special monoamine-containing cells(S.I.F. cells). J. comp. Neurol. 153, 1–14 (1974)

    Google Scholar 

  • Grynszpan-Winograd, O.: Ultrastructure of the chromaffin cell. In: Handbook of Physiology, Sect. 7, Vol. VI, Adrenal gland, pp. 295–308. Washington D.C.: Americ. Physiol. Soc. 1975

    Google Scholar 

  • Gutmann, Y., Boonyaviroy, P.: Suppression by noradrenaline of catecholamine secretion from adrenal medulla. Europ. J. Pharmacol. 28, 384–386 (1974)

    Google Scholar 

  • Heym, Ch.: Ganglion cells and paraganglionic cells in the developing superior cervical ganglion of normal and p-chlorophenylalanine treated rats. Cell Tiss. Res. 163, 249–262 (1975)

    Google Scholar 

  • Heym, Ch.: Monoamine storage sites in the rat superior cervical ganglion following synthesis inhibition. Cell Tiss. Res. 165, 239–248 (1976)

    Google Scholar 

  • Heym, Ch., Grube, D.: Effects of guanethidine on paraganglionic cells in the superior cervical ganglion of the rat. Anat. Embryol. 148, 89–97 (1975)

    Google Scholar 

  • Hökfelt, T.: Distribution of noradrenaline storing particles in peripheric adrenergic neurons as revealed by electron microscopy. Acta physiol. scand. 76, 427–440 (1969)

    Google Scholar 

  • Hopwood, D.: The histochemistry and electron histochemistry of chromaffin tissue. Progr. Histochem. Cytochem. 3, No. 1 (1971)

    Google Scholar 

  • Jacobowitz, D.: Catecholamine fluorescence studies of adrenergic neurons and chromaffin cells in sympathetic ganglia. Fed. Proc. 29, 1929 (1970)

    Google Scholar 

  • Kebabian, J.W., Greengard, P.: Dopamine-sensitive adenylcyclase: possible role in sympathetic transmission. Science 174, 1346 (1971)

    Google Scholar 

  • Kobayashi, S., Coupland, R.E.: Two populations of microvesicles in the SGC (small granule chromaffin) cells of the mouse adrenal medulla. Arch. histol. jap. 40, 251–259 (1977)

    Google Scholar 

  • Libet, B., Owman, Ch.: Concomitant changes in formaldehyde-induced fluorescence of dopamine interneurons and in slow inhibitory postsynaptic potentials of the rabbit superior cervical ganglion, induced by stimulation of the preganglionic nerve or by a muscarinic agent. J. Physiol. (Lond.) 237, 635–662 (1974)

    Google Scholar 

  • Libet, B., Tosaka, T.: Dopamine as a sympathetic transmitter and modulator in sympathetic ganglia: A different mode of synaptic action. Proc. nat. Acad. Sci. (Wash.) 67, 667–673 (1970)

    Google Scholar 

  • Lu, K.-S., Lever, J.D., Santer, R.M., Presley, R.: Small granulated cell types in rat superior cervical and coeliac-mesenteric ganglia. Cell Tiss. Res. 172, 331–343 (1976)

    Google Scholar 

  • Matthews, M.R., Raisman, G.: The ultrastructure and somatic efferent synapses of small granule-containing cells in the superior cervical ganglion. J. Anat. (Lond.) 105, 255–282 (1969)

    Google Scholar 

  • O'Lague, P.H., MacLeish, P.R., Nurse, C.A., Claude, P., Furshpan, E.J., Potter, D.D.: Physiological and morphological studies on developing sympathetic neurons in dissociated cell culture. Cold Spr. Harb. Symp. quant. Biol. 40, 399–407 (1975)

    Google Scholar 

  • Patterson, P.H., Reichhardt, L.F., Chun, L.L.Y.: Biochemical studies on the development of primary sympathetic neurons in cell culture. Cold Spr. Harb. Symp. quant. Biol. 40, 389–397 (1975)

    Google Scholar 

  • Santer, R.M., Lu, K.-S., Lever, J.D., Presley, R.: A study of the distribution of chromaffin-positive (CH+) and small intensely fluorescent (SIF) cells in sympathetic ganglia of the rat at various ages. J. Anat. (Lond.) 119, 589–599 (1975)

    Google Scholar 

  • Siegrist, G., Dolivo, M., Dunant, Y., Foroglou-Kerannens, C., Ribaupierre, F. de, Rouiller, Ch.: Ultrastructure and junction of the chromaffin cells in the superior cervical ganglion of the rat. J. Ultrastruct. Res. 25, 381–407 (1968)

    Google Scholar 

  • Singh, J.: A modification of the Masson-Hamperl method for staining of argentaffin cells. Anat. Anz. 115, 81–82 (1964)

    Google Scholar 

  • Starke, K., Gorlitz, B.D., Montel, H., Schümann, H.J.: Local α-adrenoreceptor mediated feed-back inhibition of catecholamine release from the adrenal medulla? Experientia (Basel) 30, 1170–1171 (1974)

    Google Scholar 

  • Taxi, J., Gantron, J., L'Hermite, P.: Donne ultrastructurale sur une eventuelle modulation adrenergique de l'activite du ganglion cervical superieur du rat. C.R. Acad. Sci. (Paris) 269, 1281–1284 (1969)

    Google Scholar 

  • Thoenen, H.: Surgical immunological and chemical sympathectomy. Their application in the investigation of the physiology and pharmacology of the sympathetic nervous system. In: Handbook of Experimental Pharmacology, Vol. XXXIII, Catecholamines (H. Blaschko and E. Muscholl, eds.), pp. 813–844. Berlin-Heidelberg-New York: Springer 1972

    Google Scholar 

  • Tranzer, J.P., Thoenen, H.: Ultramorphologische Veränderungen der synaptischen Nervenendigungen der Katze nach Vorbehandlung mit 5-und 6-Hydroxy-Dopamin. Naunyn-Schmiedebergs Arch. Pharmak. exp. Path. 257, 343–344 (1967)

    Google Scholar 

  • Torre, J.C. de la, Surgeon, J.W.: A methodological approach to rapid and sensitive monoamine histofluorescence using a modified glyoxylic acid technique. The SPG method. Histochemistry 49, 81–93 (1976)

    Google Scholar 

  • Unsicker, K.: Über die Ganglienzellen in Nebennierenmark des Goldhamsters (Mesocricetus auratus). Ein Beitrag zur Frage der peripheren Neurosekretion. Z. Zellforsch. 76, 187–219 (1967)

    Google Scholar 

  • Unsicker, K.: Fine structure and innervation of the avian adrenal gland. I. Fine structure of adrenal chromaffin cells and ganglion cells. Z. Zellforsch. 145, 389–416 (1973a)

    Google Scholar 

  • Unsicker, K.: Fine structure and innervation of the avian adrenal gland. II. Cholinergic innervation of adrenal chromaffin cells. Z. Zellforsch. 145, 417–442 (1973b)

    Google Scholar 

  • Unsicker, K.: Fine structure and innervation of the avian adrenal gland. III. Non-cholinergic nerve fibres. Z. Zellforsch. 145, 557–575 (1973c)

    Google Scholar 

  • Unsicker, K.: Fine structure and innervation of the avian adrenal gland. V Innervation of interrenal cells. Z. Zellforsch. 176, 403–416 (1973d)

    Google Scholar 

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

    Google Scholar 

  • Unsicker, K., Chamley, J.H.: Growth characteristics of postnatal rat adrenal medulla in culture. Cell Tiss. Res. 177, 247–268 (1977)

    Google Scholar 

  • Unsicker, K., Gröschel-Stewart, U.: Distribution of contractile proteins and adrenergic nerves in the adrenal gland of guinea-pig, rat and ox as revealed by immunofluorescence and the glyoxylic acid technique (1977, in press)

  • Unsicker, K., Polonius, T., Lindmar, R., Löffelholz, K., Wolf, U.: Catecholamines and 5-hydroxytryptamine in corpuscles of Stannius of the salmonid, Salmo irideus L. A study correlating electron microscopical, histochemical and chemical findings. Gen. comp. Endocr. 31, 121–132 (1977a)

    Google Scholar 

  • Unsicker, K., Zwarg, U., Habura, O.: Electron microscopic evidence for the formation of synapses and synaptoid contacts in adrenal medullary grafts. Brain Res. 120, 533–539 (1977b)

    Google Scholar 

  • Vogt, M.: Observations on some conditions affecting the rate of hormone output by the suprarenal cortex. J. Physiol. (Lond.) 103, 317–332 (1944)

    Google Scholar 

  • Watanabe, H.: Adrenergic nerve elements in the hypogastric ganglion of the guinea-pig. Amer. J. Anat. 130, 305–330 (1971)

    Google Scholar 

  • Williams, T.H.W.: Electron microscopic evidence for an autonomic interneuron. Nature (Lond.) 214, 309–310 (1967)

    Google Scholar 

  • Williams, T.H.W., Black, A.C. Jr., Chiba, T., Bhalla, R.C.: Morphology and biochemistry of small intensely fluorescent cells of sympathetic ganglia. Nature (Lond.) 256, 315–317 (1975)

    Google Scholar 

  • Williams, T.H.W., Paley, S.L.: Ultrastructure of the small neurons in the superior cervical ganglion. Brain Res. 15, 17–34 (1969)

    Google Scholar 

  • Wurtman, R.J., Axelrod, J.: Control of enzymatic synthesis of adrenaline in the adrenal medulla by adrenal cortical steroids. Biol. Chemistry 241, 2301–2305 (1966)

    Google Scholar 

  • Yokota, R.: The granule containing cell somata in the superior cervical ganglion of the rat, as studied by a serial sampling method for electron microscopy. Z. Zellforsch. 141, 331–345 (1973)

    Google Scholar 

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  1. Department of Anatomy, University of Kiel, Germany

    K. Unsicker, O. Habura-Flüh & U. Zwarg

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  1. K. Unsicker
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Dedicated to Professor H. Leonhardt in honor of his 60th birthday.

Supported by a grant from Deutsche Forschungsgemeinschaft (Un 34/4)

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Unsicker, K., Habura-Flüh, O. & Zwarg, U. Different types of small granule-containing cells and neurons in the guinea-pig adrenal medulla. Cell Tissue Res. 189, 109–130 (1978). https://doi.org/10.1007/BF00223124

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