Summary
The coexistence of histamine, histidine decarboxylase (the enzyme synthesizing histamine), 5-hydroxytryptamine and tyrosine hydroxylase (the rate-limiting enzyme in catecholamine synthesis), was studied in the rat superior cervical ganglion with the indirect immunofluorescence method. Possible colocalization was examined by staining consecutive sections with two different antibodies, or alternatively in the same section by eluting the first antibody with a mild solution containing potassium permanganate and sulphuric acid, and by staining the same section with another antibody. It was shown that tyrosine hydroxylase immunoreactivity was found both in large principal nerve cells and in small cells, which on the basis of their size and high nucleus—cytoplasm ratio corresponded to small intensely fluorescent (SIF) cells. Histamine, histidine decarboxylase and 5-hydroxytryptamine immunoreactivities were observed only in SIF cells. Those SIF cells which were immunoreactive for histamine, histidine decarboxylase or 5-hydroxytryptamine also contained tyrosine hydroxylase immunoreactivity. On the other hand, all tyrosine hydroxylase-immunoreactive SIF cells were also immunoreactive for histidine decarboxylase or 5-hydroxytryptamine. Some of the SIF cells, which were non-reactive for histamine, were immunoreactive for tyrosine hydroxylase.
Similar content being viewed by others
References
ALTURA, B. M. & HALEVY, S. (1978) Cardiovascular actions of histamine. InHistamine II and Anti-histaminics: Chemistry, metabolism, and physiological and pharmacological actions. (edited by R. E. SILVA) Vol 18, Pt 2, pp. 1–39. Berlin, Heidelberg, New York: Springer.
BJÖRKLUND, A., CEGRELL, L., FALCK, B., RITZEN, M. & ROSENGREN, E. (1970) Dopamine-containing cells in sympathetic ganglia.Acta physiol. scand. 78, 334–8.
BÖCK, P. (1982)The Paraganglia. Berlin, Heidelberg: Springer-Verlag.
BREZENOFF, H. E. & GERTNER, S. B. (1972) The actions of polymyxin B and histamine on ganglionic transmission.Can. J. Physiol. Pharmacol. 50, 824–31.
BRIMBLE, M. J. & WALLIS, D. I. (1973) Histamine H1-and H2-receptors at a ganglionic synapse.Nature 246, 156–8.
CHAN-PALAY, V. (1982) Immunocytochemical and autoradiographic methods to demonstrate the coexistence of neuroactive substances: cerebellar Purkinje cells have glutamic acid decarboxylase and motilin immunoreactivity, the raphe neurons have serotonin and substance P immunoreactivity. InCytochemical Methods in Neuroanatomy, (edited by CHAN-PALAY, V. and PALAY, S. L.) pp. 93–118. New York: Alan R. Liss.
COONS, A. H. (1958) Fluorescent antibody methods. InGeneral Cytochemical Methods, (edited by J. F. DANIELLI) pp. 399–422. New York: Academic Press.
DUN, N. J. & KARCZMAR, A. G. (1981) Evidence for a presynaptic inhibitory action of 5-hydroxytryptamine in a mammalian sympathetic ganglion.J. Pharmacol. Exp. Ther. 217, 714–18.
ERÄNKÖ, O. (1967) The practical histochemical demonstration of catecholamines by formaldehyde-induced fluorescence.J. Roy. micr. Soc. 87, 259–76.
ERÄNKÖ, O. & HÄRKÖNEN, M. (1963) Histochemical demonstration of fluorogenic amines in the cytoplasm of sympathetic ganglion cells of the rat.Acta physiol. scand. 58, 285–6.
ERÄNKÖ, O. & HÄRKÖNEN, M. (1965) Monoamine-containing small cells in the superior cervical ganglion of the rat and an organ composed of them.Acta physiol. scand. 63, 511–12.
ERÄNKÖ, O. & ERÄNKÖ, L. (1971) Small, intensely fluorescent granule-containing cells in the sympathetic ganglion of the rat.Prog. Brain Res. 34, 39–51.
EULER, U. S. VON (1956) Histamine and nerves. InCIBA Foundation Symposium on Histamine, (edited by WOLSTENHOLME, G. E. W. and O'CONNOR, C. M.) pp. 235–41. London: Churchill.
HÄPPÖLÄ, O., SOINILA, S., PÄIVÄRINTA, H., PANULA, P. & ERÄNKÖ, O. (1985) Histamine-immunoreactive cells in the superior cervical ganglion and in the coeliac-superior mesenteric ganglion complex of the rat.Histochemistry 82, 1–3.
HÄPPÖLÄ, O., PÄIVÄRINTA, H., SOINILA, S. & STEIN-BUSCH, H. (1986) Pre- and postnatal development of 5-hydroxytryptamine-immunoreactive cells in the superior cervical ganglion of the rat.J. auton. Nerv. Syst. 15, 21–31.
HERTZLER, E. C. (1961) 5-hydroxytryptamine and transmission in sympathetic ganglia.Brit. J. Pharmacol. 17, 406–13.
JOH, T. H., GEGHAM, C. & REIS, D. J. (1973) Immunochemical demonstration of increased tyrosine hydroxylase protein in sympathetic ganglia and adrenal medulla elicited by reserpine.Proc. Natl. Acad. Sci. USA 70, 2767–73.
KONDO, H. (1977) Innervation of SIF cells in the superior cervical and nodose ganglia: an ultrastructural study with serial sections.Biol. Cell 30, 253–64.
KÖNIG, R. & HEYM, CH. (1978) Immunofluorescent localization of dopamine-β-hydroxylase in small intensely fluorescent cells of the superior cervical ganglion.Neurosci. Lett. 10, 187–91.
LIBET, B. (1979) Slow postsynaptic actions in ganglionic functions. InIntegrative Functions of the Autonomic Nervous System, (edited by BROOKS, C. M., KOIZUMI, K. and SATO, A.) pp. 197–222. Tokyo: University of Tokyo Press, Amsterdam: Elsevier.
LIBET, B. & OWMAN, CH. (1974) Concomitant changes in formaldehyde-induced fluorescence of dopamine interneurones and in slow inhibitory post-synaptic potentials of the rabbit superior cervical ganglion, induced by stimulation of the preganglionic nerve or by a muscarinic agent.J. Physiol. 237, 635–62.
LIUZZI, A., FOPPEN, F. H., SAAVEDRA, J. M., LEVIMONTALCINI, R. & KOPIN, I. J. (1977) Gas chromatographic-mass spectrometric assay of serotonin in rat superior cervical ganglia. Effect of nerve growth factor and 6-hydroxydopamine.Brain Res. 133, 354–7.
MACDONALD, S. M., MEZEI, M. & MEZEI, C. (1981) Effect of Wallerian degeneration on histamine concentration of the peripheral nerve.J. Neurochem. 36, 9–16.
MCGRATH, M. A. & SHEPHERD, J. T. (1978) Histamine, and 5-hydroxytryptamine — inhibition of transmitter release mediated by H2- and 5-hydroxytryptamine receptors.Federation Proc. 37, 195–8.
NORTH, R. A., HENDERSON, G., KATAYAMA, Y. & JOHNSON, S. M. (1980) Electrophysiological evidence for presynaptic inhibition of acetylcholine release by 5-hydroxytryptamine in the enteric nervous system.Neuroscience 5, 581–6.
PANULA, P., YANG, H.-Y. & COSTA, E. (1984) Histaminecontaining neurons in the rat hypothalamus.Proc. Natl. Acad. Sci. USA 81, 2572–6.
PÄIVÄRINTA, H., SOINILA, S., ERÄNKÖ, O. & JOH, T. H. (1985) Phenylethanolamine-N-methyltransferase-immunoreactive cells in developing rat superior cervical ganglion and the effect of hydrocortisone on their number.Int. J. Devl. Neuroscience 3, 9–18.
RYAN, M. J. & BRODY, M. J. (1970) Distribution of histamine in the canine autonomic nervous system.J. Pharmacol. Exp. Ther. 174, 123–32.
SAAVEDRA, J. M. & LIUZZI, A. (1976) Nerve growth factor: effects on 5-hydroxytryptamine and phenylethanolamineN-methyltransferase in the superior cervical ganglion of the rat. InSIF Cells. Structure and Function of the Small, Intensely Fluorescent Sympathetic Cells, (edited by O. ERÄNKÖ) pp. 124–30. Fogarty International Center Proceedings No. 30, U.S. Government Printing Office, Washington D.C.
SCHIPPER, J. & TILDERS, F. J. H. (1983) A new technique for studying specificity of immunohistochemical procedures: specificity of serotonin immunostaining.J. Histochem. Cytochem. 31, 12–18.
SCHRÖDER, H., LACKNER, K. & HEYM, CH. (1982) Simultaneous demonstration of catecholamines and phenylethanolamine-N-methyltransferase in the same tissue section by means of formaldehyde-induced fluorescence (FIF) and tetramethyl-rhodamine-isothiocyanate (MRITC) immunofluorescence.J. Neurosci. Methods 6, 281–6.
SCHULTZBERG, M. (1983) The peripheral nervous system. InChemical Neuroanatomy, (edited by EMSON, P. C.) pp. 1–51. New York: Raven Press.
SIEGRIST, G., DOLIVO, M., DUNANT, Y., FOROGLOUKERAMEUS, C., DE RIBAUPIERRE, F. & ROUILLER, C. (1968) Ultrastructure and function of the chromaffin cells in the superior cervical ganglion of the rat.J. Ultrastr. Res. 25, 381–407.
STEINBUSCH, H. W. M., VERHOFSTAD, A. A. J. & JOOSTEN, H. W. J. (1978) Localization of serotonin in the central nervous system by immunohistochemistry: description of a specific and sensitive technique and some applications.Neuroscience 3, 811–19.
TRAMU, G., PILLEZ, A. & LEONARDELLI, J. (1978) An efficient method of antibody elution for the successive or simultaneous localization of two antigens by immunocytochemistry.J. Histochem. Cytochem. 26, 322–4.
VERHOFSTAD, A. A. J., STEINBUSCH, H. W. M., PENKE, B., VARGA, J. & JOOSTEN, H. W. J. (1981) Serotoninimmunoreactive cells in the superior cervical ganglion of the rat. Evidence for the existence of separate serotonin- and catecholamine-containing small ganglionic cells.Brain Res. 212, 39–49.
WALLIS, D. I. & WOODWARD, B. (1974) The facilitatory actions of 5-hydroxytryptamine and bradykinin in the superior cervical ganglion of the rabbit.Brit. J. Pharmacol. 51, 521–31.
WATANABE, T., TAGUCHI, Y., HAYASHI, H., TANAKA, J., SHIOSAKA, S., TOHYAMA, M., KUBOTA, H., TERANO, Y. & WADA, H. (1983) Evidence for the presence of a histaminergic neuron system in the rat brain: an immunohistochemical analysis.Neurosci. Lett. 39, 249–54.
WEINREICH, D. (1985) Multiple sites of histamine storage in superior cervical ganglia.Exp. Neurol. 90, 36–43.
WERLE, E. (1956) Histamine and nerves. InCIBA Foundation Symposium on Histamine, (edited by WOLSTENHOLME, G. E. W. and O'CONNOR, C. M.) pp. 264–9. London: Churchill.
WILLIAMS, T. H. (1967) Electron microscopic evidence for an autonomic interneuron.Nature (Lond) 214, 309–10.
WILLIAMS, T. H., CHIBA, T, BLACK, JR, A. C., BHALLA, R. C. & JEW, J. (1976) Species variations in SIF cells of superior cervical ganglia: are there two functional types? InSIF cells. Structure and Function of the Small, Intensely Fluorescent Sympathetic Cells, (edited by O. ERÄNKÖ) pp. 143–62. Fogarty International Center Proceedings No. 30, U.S. Government Printing Office, Washington D.C.
YAMADA, M., TOKIMASA, T. & KOKETSU, K. (1982) Effects of histamine on acetylcholine release in bullfrog sympathetic ganglia.Eur. J. Pharmacol. 82, 15–20.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Päivärinta, H., Häppölä, O., Joh, T.H. et al. Immunocytochemical colocalization of histamine, histidine decarboxylase, 5-hydroxytryptamine and tyrosine hydroxylase in the superior cervical ganglion of the rat. Histochem J 19, 319–326 (1987). https://doi.org/10.1007/BF01680447
Received:
Revised:
Issue Date:
DOI: https://doi.org/10.1007/BF01680447