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Studies on the interactions between nerve fibres from para-and orthosympathetic ganglia and adreno-cortical and -medullary cells in joint culture

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Summary

The interactions between nerve fibres from para- and orthosympathetic ganglia and adreno-cortical and -medullary cells were studied in joint cultures using explanted guinea-pig ciliary and sympathetic chain ganglia and enzyme-dispersed rat adrenal gland cells. Nerve fibres from both para- and orthosympathetic ganglia made only transitory contact with cortical cells, but consistently formed associations with isolated chromaffin cells which lasted for up to 10 days. Contacts between axons and chromaffin cells often showed particularly large varicosities and frequently withstood severe tests of durability from pulls of the fibre or the cell or both. By correlating phase contrast and catecholamine histochemistry (Falck-Hillarp method) it was shown that sympathetic fibres forming long-lasting contacts with chromaffin cells were adrenergic. The functional implications of the ability of autonomic nerves to distinguish between adreno-cortical and-medullary cells and the lack of specificity shown by the para-and orthosympathetic neurons during formation of long-lasting associations with chromaffin cells are discussed.

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References

  • Bacq, Z.M.: La pharmacologie du système nerveux autonome. Ann. Physiol. Physiochim. biol. 10, 467–528 (1934)

    Google Scholar 

  • Björklund, A., Falck, B., Owman, Ch.: Fluorescence microscopic and microspectrofluorometric techniques for the cellular localization and characterization of biogenic amines. In: S.A. Berson (ed.), Methods of investigative and diagnostic endocrinology, Vol. 1: J.E. Rall and I.J. Kopin (eds.), The thyroid and biogenic amines, pp. 318–368. Amsterdam: North-Holland Publ. Co. 1972

    Google Scholar 

  • Burnstock, G.: Do some nerve cells release more than one transmitter? Neuroscience 1, 239–248 (1976)

    Google Scholar 

  • Carruba, M., Ceccarelli, B., Clementi, F., Mantegazza, P.: Selectivity in the reinnervation of iris and adrenal medulla by superior cervical ganglion after transplantation under the kidney capsule. Brain Res. 77, 39–53 (1974)

    Google Scholar 

  • Chamley, J.H., Campbell, G.R.: Isolated ureteral smooth muscle cells in culture. Including their interaction with intrinsic and extrinsic nerves. Cytobiol. 11, 358–365 (1975)

    Google Scholar 

  • Chamley, J.H., Campbell, G.R.: Tissue culture: Interaction between sympathetic nerves and vascular smooth muscle. In: Vascular neuroeffector mechanisms. 2nd Int. Symp. Odense 1975, pp. 10–18. Basel: Karger 1976

    Google Scholar 

  • Chamley, J.H., Campbell, G.R., Burnstock, G.: An analysis of the interactions between sympathetic nerve fibers and smooth muscle cells in tissue culture. Develop. Biol. 33, 344–361 (1973a)

    Google Scholar 

  • Chamley, J.H., Goller, I., Burnstock, G.: Selective growth of sympathetic nerve fibers to explants of normally densely innervated autonomic effector organs in tissue culture. Develop. Biol. 31, 362–379 (1973b)

    Google Scholar 

  • Chamley, J.H., Mark, G.E., Burnstock, G.: Sympathetic ganglia in culture. II. Accessory cells. Z. Zellforsch. 135, 315–327 (1972a)

    Google Scholar 

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

    Google Scholar 

  • Coghlan, J.P.: Personal communication (1975)

  • Coupland, R.E.: Electron microscopic observation on the structure of the rat adrenal medulla. J. Anat. (Lond.) 99, 231–272 (1965)

    Google Scholar 

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

    Google Scholar 

  • Dale, H.H., Feldberg, W.: The chemical transmission of secretory impulses to the sweat glands of the cat. J. Physiol. (Lond.), 82, 121–128 (1934)

    Google Scholar 

  • Falck, 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 

  • Feldberg, W., Minz, B., Tsudzimura, H.: Mechanisms of nervous discharge of adrenaline. J. Physiol. (Lond.) 81, 286–304 (1934)

    Google Scholar 

  • Fischbach, G.D., Henkart, M.P., Cohen, S.A., Breuer, A.C., Whysner, J., Neal, F.M.: Studies on the development of neuromuscular junctions in cell culture. In: Synaptic transmission and neuronal interaction. Ed. M.V.L. Bennett (Society of general physiologists Ser. Vo. 28), pp. 259–283. New York: Raven Press 1974

    Google Scholar 

  • Fry, D.M., Burnstock, G.: Ultrastructure and physiology of the innervation of smooth muscle in tissue culture. Eighth Intern. Congr. on Electron Microscopy, Canberra, 1974, Vol. II

  • Furness, J.B., Costa, M.: The use of glyoxylic acid for the fluorescence histochemical demonstration of peripheral stores of noradrenaline and 5-hydroxytryptamine in whole mounts. Histochemistry 41, 335–352 (1975)

    Google Scholar 

  • Hill, C.E., Purves, R.D., Watanabe, H., Burnstock, G.: Specificity of innervation of iris musculature by sympathetic nerve fibres in tissue culture. Pflügers Arch. 361, 127–134 (1976)

    Google Scholar 

  • Johnson, M., Ross, D., Meyers, M., Rees, R., Bunge, R., Wakshull, E., Burton, H.: Synaptic vesicle cytochemistry changes when cultured sympathetic neurones develop cholinergic interactions. Nature (Lond.) 262, 308–310 (1976)

    Google Scholar 

  • Mark, G., Chamley, J.H., Burnstock, G.: Interactions between autonomic nerves and smooth and cardiac muscle cells in tissue culture. Develop. Biol. 32, 194–200 (1973)

    Google Scholar 

  • Nurse, C.A., O'Lague, P.H.: Formation of cholinergic synapses between dissociated sympathetic neurons and skeletal myotubes of the rat in cell culture. Proc, nat. Acad. Sci. (Wash.) 72, 1955–1959 (1975)

    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 

  • O'Lague, P.H., Obata, K., Claude, P., Furshpan, E.J., Potter, D.D.: Evidence for cholinergic synapses between dissociated rat sympathetic neurons in cell culture. Proc. nat. Acad. Sci. (Wash.) 71, 3602–3606 (1974)

    Google Scholar 

  • Oison, M.I., Bunge. R.P.: Anatomical observations on the specificity of synapse formation in tissue culture. Brain Res. 59, 19–33 (1973)

    Google Scholar 

  • Olson, L., Seiger, A.: Brain tissue transplanted to the anterior chamber of the eye: 2. Fluorescence histochemistry of immature catecholamine- and 5-hydroxytryptamine neurons innervating the rat vas deferens. Cell Tiss. Res. 158, 141–150 (1975)

    Google Scholar 

  • Olson, L., Seiger, A.: Brain tissue transplanted to the anterior chamber of the eye. 2. Fluorescence histochemistry of immature catecholamine and 5-hydroxytryptamine neurons reinnervating the rat iris. Z. Zellforsch. 135, 175–194 (1972)

    Google Scholar 

  • Patterson, P.H., Chun, L.L.Y.: The influence of non-neuronal cells on catecholamine and acetylcholine synthesis and accumulation in cultures of dissociated sympathetic neurons. Proc. nat. Acad. Sci. (Wash.) 71, 3607–3610 (1974)

    Google Scholar 

  • Purves, R.D., Hill, C.E., Chamley, J.H., Mark, G.Ed., Fry, D.M., Burnstock, G.: Functional autonomic neuromuscular junctions in tissue culture. Pflügers Arch. 350, 1–7 (1974)

    Google Scholar 

  • Rees, R.P., Bunge, M.B., Bunge, R.P.: Morphological changes in the neuritic growth cone and target neuron during synaptic junction development. J. Cell Biol. 68, 240–263 (1976)

    Google Scholar 

  • Robinson, P.M., Perry, R.A., Hardy, H.T., Coghlan, T.P., Scoggins, B.A.: The innervation of the adrenal cortex in the sheep. J. Anat. (Lond.), in press (1976)

  • Rosenfeld, G.: Stimulative effect of acetylcholine on the adrenocortical function of isolated perfused calf adrenals. Amer. J. Physiol. 183, 272–278 (1955)

    Google Scholar 

  • Rubin, R.P., Warner, W.: Nicotine-induced stimulation of steroidogenesis in adrenocortical cells of the rat. Brit. J. Pharmacol. 53, 357–362 (1975)

    Google Scholar 

  • Uehara, Y., Burnstock, G.: Postsynaptic specialization of smooth muscle at close neuromuscular junctions in the guinea-pig sphincter pupillae. J. Cell Biol. 53, 849–853 (1972)

    Google Scholar 

  • Unsicker, K.: Zur Innervation der Nebennierenrinde vom Goldhamster. Eine fluoreszenz- und elektronenmikroskopische Studie. Z. Zellforsch. 95, 608–619 (1969)

    Google Scholar 

  • Unsicker, K.: Fine structure and innervation of the avian adrenal gland. V. Innervation of interrenal cells. Z, Zellforsch. 146, 385–402 (1973)

    Google Scholar 

  • Unsicker, K.: Innervation of adrenal cells in the lizards Lacerta dugesi and Lacerta pityusensis. Gen. comp. Endocr. 24, 409–412 (1974)

    Google Scholar 

  • Unsicker, K., Chamley, J.H.: Effects of dbcAMP and theophylline on rat adrenal medulla grown in tissue culture. Histochemistry 46, 197–201 (1976a)

    Google Scholar 

  • Unsicker, K., Chamley, J.H.: Growth characteristics of postnatal rat adrenal medulla in culture: A study correlating phase contrast, microcinematographic, histochemical, and electron microscopical observations. Cell Tiss. Res. in press. (1976b)

  • Unsicker, K., Habura, O., Zwarg, U., Lindmar. R., Löffelholz, K., Wolf, U.: Cell types in the adrenal medulla of newborn and adult guinea-pigs. A morphological, histochemical, and biochemical study. In preparation (1976)

  • 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.: The fine structure of the ciliary ganglion of the guinea-pig. Arch, histol. jap. 34, 261–276 (1972)

    Google Scholar 

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Authors and Affiliations

  1. Department of Anatomy, University of Kiel, Kiel, Germany

    K. Unsicker

  2. Department of Anatomy and Embryology, University College London, London

    Julie H. Chamley & G. Burnstock

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  1. K. Unsicker
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  2. Julie H. Chamley
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  3. G. Burnstock
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Additional information

Supported by grants from Deutsche Forschungsgemeinschaft (K.U.), the Wellcome Trust (London), the Life Insurance Medical Research Fund of Australia and New Zealand (J.H.C.) and a Research Fellowship of the University of Melbourne (K.U.). We are particulary grateful to Janet McConnell, Marlis Rall and Ingrid Riettiens for excellent technical assistance, to Heidi Waluk for the photographic work, and to Brigitte Schierhorn for typing the manuscript

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Unsicker, K., Chamley, J.H. & Burnstock, G. Studies on the interactions between nerve fibres from para-and orthosympathetic ganglia and adreno-cortical and -medullary cells in joint culture. Cell Tissue Res. 178, 533–549 (1977). https://doi.org/10.1007/BF00219573

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