Skip to main content
Log in

β2-Adrenoreceptor immunoreactivity in cardiac ganglia of the guinea pig

  • Papers
  • Published:
The Histochemical Journal Aims and scope Submit manuscript

Summary

Previous pharmacological studies in co-culture systems have indicated, the presence of β-adrenoreceptors on intrinsic cardiac neurons of the guinea pig (Horackovaet al., 1993) but radiologand binding studies of tissue sections failed to provide a definite answer as to the presence of such receptors on cardiac neuronsin situ, due to the iodine-binding properties of cardiac nerve bundles and ganglia (Molenaaret al., 1992). We therefore addressed this question by immunohistochemistry, using antisera raised against synthetic peptides of the β2-adrenoreceptor. For comparison, cholinergic and catecholaminergic neurons were identified immunohistochemically by means of antibodies against the enzymes involved in the synthesis of acetylcholine (choline acetyltransferase), and of catecholamines (tyrosine hydroxylase). Virtually all intrinsic cardiac neurons contained both β2-adrenoreceptor- and choline acetyltransferase-immunoreactivities. In addition, some nerve fibre bundles exhibited β2-adrenoreceptor-immunoreactivity. Several ganglia were innervated by tyrosine hydroxylase-immunoreactive axons, but the majority of ganglia did not receive tyrosine hydroxylase-immunoreactive nerve terminals, and additional intraganglionic sources of catecholamine synthesis could not be identified. Thus, the results are in favour of β-adrenergic modulation of guinea pig cardiac ganglia by humorally and, partially, by locally released catecholamines.

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.

Similar content being viewed by others

References

  • Allen, T. G. J. &Burnstock, G. (1987) Intracellular studies of the electrophysiological properties of cultured intracardiac neurones of the guinea-pig.J. Physiol. 388, 349–66.

    CAS  PubMed  Google Scholar 

  • Aoki, C. (1992) β-Adrenergic receptors: astrocytic localization in the adult visual cortex and their relation to catecholamine axon terminals as revealed by electron microscopic immunocytochemistry.J. Neurosci. 12, 781–92.

    CAS  PubMed  Google Scholar 

  • Barnes, P. J. (1992) Modulation of neurotransmission in airways.Physiol. Rev. 72, 699–729.

    CAS  PubMed  Google Scholar 

  • Cheng, P. Y., Svingos, A. L., Wang, H., Clarke, C. L., Jenab, S., Beczowska, I. W., Inturris, C. E. &Pickel, V. M. (1995) Ultrastructural immunolabelling shows prominent presynaptic vesicular localization of δ-opioid receptor within both enkephalin- and non-enkephalin-containing axon terminals in the superficial layers of the rat cervical spinal cord.J. Neurosci. 15, 5976–88.

    CAS  PubMed  Google Scholar 

  • Choate, J. K., Edwards, F. R., Hirst, G. D. S. &O'Shea, J. E. (1993) Effects of sympathetic nerve stimulation on the sinoatrial node of the guinea-pig.J. Physiol. 471, 707–27.

    CAS  PubMed  Google Scholar 

  • Crowe, R. &Burnstock, G. (1982) Fluorescent histochemical localisation of quinacrine-positive neurones, in the guinea-pig and rabbit atrium.Cardiovasc. Res. 16, 384–90.

    CAS  PubMed  Google Scholar 

  • Csillag, A., Hajos, F., Zilles, K., Schleicher, A. &Schröder, H. (1993) Matching localization of vasoactive intestinal polypeptide (VIP) and VIP-receptor at pre- and postsynaptic sites in the mouse visual cortex.J. Neurocytol. 22, 491–7.

    Article  CAS  PubMed  Google Scholar 

  • Dalsgaard, C.-J., Franco-Cereceda, A., Saria, A., Lundberg, J.M., Theodorsson-Norheim, E. &Hökfelt, T. (1986) Distribution and origin of substance P- and neuropeptide Y-immunoreactive nerves in the guinea-pig heart.Cell Tissue Res. 243, 477–85.

    Article  CAS  PubMed  Google Scholar 

  • Dixon, R. A. F., Kobilka, B. K., Strader, D. J., Benovic J. L., Dohlman, H. G., Frielle, T., Bolanowski, M. A., Bennett, C. D., Rands, E., Diehl, R. E., Mumford, R. A., Slater, E. E., Sigal, I. S., Caron, M. G., Lefkowitz, R. J. &Strader, C. D. (1986) Cloning of the gene and cDNA for mammalian beta-adrenergic receptor and homology with rhodopsin.Nature 321, 75–9.

    CAS  PubMed  Google Scholar 

  • Dukes, I. D. &Vaughan-Williams, E. M. (1984) Effects of selective α1-, α2-, β1-,β2-adrenoceptor stimulation on potentials and contractions in the rabbit heart.J. Physiol. 355, 523–46.

    CAS  PubMed  Google Scholar 

  • Ehinger, B., Falck, B., Persson, H. &Sporrong, B. (1968) Adrenergic and cholinesterase-containing neurons of the heart.Histochemie 16, 197–205.

    Article  CAS  PubMed  Google Scholar 

  • Ellison, J. P. &Hibbs, R. G. (1974) Catecholamine-containing cells of the guinea-pig heart: an ultrastructural study.J. Mol. Cell. Cardiology 6, 17–26.

    CAS  Google Scholar 

  • Forssmann, W. G., Ito, S., Weihe, E., Aoki, A., Dym, M. &Fawcett, D. W. (1977) An improved perfusion fixation method for the testis.Anat. Rec. 188, 307–14.

    Article  CAS  PubMed  Google Scholar 

  • Frohman, E. M., Vayuvegula, B., Gupta, S. &Van Den Noort, S. (1988) Norepinephrine inhibits gamma-interferon-induced major histocompatibility class II (Ia) antigen expression on cultured astrocytes via beta-2-adrenergic signal transduction mechanisms.Proc. Natl. Acad. Sci. USA 85, 1292–6.

    CAS  PubMed  Google Scholar 

  • Hansson, E. &Rönnbäck, L. (1989) Regulation of glutamate and GABA transport by adrenoceptors in primary astroglial cell cultures.Life Sci. 44, 27–34.

    Article  CAS  PubMed  Google Scholar 

  • Hardwick, J. C., Mawe, G. M. &Parsons, R. L. (1995) Evidence for afferent fiber innervation of parasympatheitc neurons of the guinea-pig cardiac ganglion.J. Autonom. Nerv. Syst. 53, 166–74.

    Article  CAS  Google Scholar 

  • Hassall, C. J. S. &Burnstock, G. (1987a) Evidence for uptake and synthesis of 5-hydroxytryptamine by subpopulation of intrinsic neurons in the guinea-pig heart.Neuroscience 22, 413–23.

    Article  CAS  PubMed  Google Scholar 

  • Hassall, C. J. S. &Burnstock, G. (1987b) Immunocytochemical localisation of neuropeptide Y and 5-hydroxytryptamine in a subpopulation of amine-handling intracardiac neurones that do not contain dopamine β-hydroxylase in tissue culture.Brain Res. 422, 74–82.

    Article  CAS  PubMed  Google Scholar 

  • Hassall, C. J. S., Saffrey, M. J., Belai, A., Hoyle, C. H. V., Moules, E. W., Moss, J., Schmidt, H. H. H. W., Murad, F., Förstermann, U. &Burnstock, G. (1992) Nitric oxide synthase immunoreactivity and NADPH-diaphorase activity in a subpopulation of intrinsic neurones of the guinea-pig heart.Neurosci. Lett. 143, 65–8.

    Article  CAS  PubMed  Google Scholar 

  • Horackova, M., Huang, M. H., Armour, J. A., Hopkins, D. A. &Mapplebeck, C. (1993) Cocultures of adult ventricular myocytes with stellate ganglia or intrinsic cardiac neurones from guinea pigs: spontaneous activity and pharmacological properties.Cardiovasc. Res. 27, 1101–8.

    CAS  PubMed  Google Scholar 

  • Jacobowitz, D. (1967) Histochemical studies of the relationship of chromaffin cells and adrenergic nerve fibres, to the cardiac ganglia of several species.J. Pharmacol. Exp. Ther. 158, 227–39.

    CAS  PubMed  Google Scholar 

  • Kamikawa, Y. &Shimo, Y. (1990) Inhibitory effects of catecholamines on cholinergically and non-cholinergically mediated contractions of guinea-pig isolated bronchial muscles.J. Pharm. Pharmacol. 42, 121–34.

    Google Scholar 

  • Klimaschewski, L., Kummer, W., Mayer, B., Couraud, J. Y., Preissler, U., Philippin, B. &Heym C. (1992) Nitric oxide synthase in cardiac nerve fibres and neurons of rat and guinea pig heart.Circ. Res. 71, 1533–7.

    CAS  PubMed  Google Scholar 

  • Klimaschewski, L., Kummer, W. &Mayer, B. (1994) Co-localization of nitric oxide synthase with vasoactive intestinal polypeptide and neuropeptide Y in the guinea pig heart.Cell Vision 1, 131–7.

    CAS  Google Scholar 

  • Kloock, A. &Kummer, W. (1994) Lokalisation von β2-Rezeptoren im peripheren Nerven und Spinalganglion.Ann. Anat. 176, Suppl., 312.

    Google Scholar 

  • Kummer, W., Fischer, A. &Bachmann, S. (1994) Receptor detection. InModern Methods in Analytical Histochemistry (edited byGu, J. &Hacker G. W.), pp. 341–60. New York: Plenum.

    Google Scholar 

  • Molenaar, P., Smolich, J. J., Russell, F. D., McMartin, L. R. &Summers, R. J. (1990a) Differential regulation of beta-1 and beta-2 adrenoceptors in guinea pig atrioventricular conducting system after chronic (−)-isoproterenol infusion.J. Pharmacol. Exp. Ther. 255, 393–400.

    CAS  PubMed  Google Scholar 

  • Molenaar, P., Russell, F. D., Shimada, T. &Summers, R. J. (1990b) Densitometric analysis of β2-adrenoceptors in guinea-pig atrioventricular conducting system.J. Mol. Cell. Cardiol. 22, 483–95.

    Article  CAS  PubMed  Google Scholar 

  • Molenaar, P., Kompa, A. R., Roberts, S. J., Pak, H. S. &Summers, R. J. (1992) Localization of (−)-[125I] cyanopindolol binding in guinea-pig heart: characteristics of non-β-adrenoceptor related binding in cardiac pacemaker and conducting regions.Neurosci. Lett. 136, 18–22.

    Article  Google Scholar 

  • Narumi, S., Kimelberg, H. K. &Bourke, R. L. (1978) Effects of norepinephrine on the morphology and some enzyme activities of primary monolayer cultures from rat brain.J. Neurochem. 31, 1479–80.

    CAS  PubMed  Google Scholar 

  • Schemann, M., Sann, H., Schaaf, C., &Mäder, M. (1993) Identification of cholinergic neurons in enteric nervous system by antibodies against choline acetyltransferase.Am. J. Physiol. 265, G1005–9.

    CAS  PubMed  Google Scholar 

  • Shain, W. G., Forman, D. S., Madelian, V. &Turner, J. N. (1987) Morphology of astroglial cells is controlled by betaadrenergic receptors.J. Cell Biol. 105, 2307–14.

    Article  CAS  PubMed  Google Scholar 

  • Steele, P. A., Gibbins, I. L., Morris J. L. &Mayer, B. (1994) Multiple populations of neuropeptide-containing intrinsic neurons in the guinea-pig heart.Neurosci. 62, 241–50.

    Article  CAS  Google Scholar 

  • Sternini, C. &Brecha, N. (1985) Distribution and colocalization of neuropeptide Y- and tyrosine hydroxylase-like immunoreactivity in the guinea-pig heart.Cell Tissue Res. 241, 93–102.

    Article  CAS  PubMed  Google Scholar 

  • Subbarao, K. V. &Hertz, L. (1990) Effect of adrenergic agonists on glycogenolysis in primary cultures of astrocytes.Brain Res. 536, 220–6.

    Article  CAS  PubMed  Google Scholar 

  • Tanaka, K., Hassall C. J. S. &Burnstock, G. (1993) Distribution of intracardiac neurones and nerve terminals that contain a marker for nitric oxide, NADPH-diaphorase, in the guinea-pig heart.Cell Tissue Res. 273, 293–300.

    Article  CAS  PubMed  Google Scholar 

  • Waniewski, R. A., Martin, D. L. &Shain, W. (1991) Isoproterenol selectively releases endogenous and [14C] labelled taurine from a single cytosolic compartment in, astroglial cells.Glia 4, 83–90.

    Article  CAS  PubMed  Google Scholar 

  • Weihe, E., Reinecke, M. &Forssmann, W. G. (1984) Distribution of vasoactive intestinal polypeptide-like immunoreactivity in the mammalian heart. Interrelation with neurotensin and substance P-like immunoreactive nerves.Cell Tissue Res. 236, 527–40.

    Article  CAS  PubMed  Google Scholar 

  • Xi, X., Randall, W. C. &Wurster, R. D. (1991) Morphology of intracellularly labeled canine intracardiac ganglion cells.J. Comp. Neurol. 314, 396–402.

    Article  CAS  PubMed  Google Scholar 

  • Zarbin, M. A., Palacios, J. M., Wamsley, J. K. &Kuhar, M. J. (1983) Axonal transport of β-adrenergic receptors.Mol. Pharm. 24, 341–8.

    CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Haberberger, R., Kummer, W. β2-Adrenoreceptor immunoreactivity in cardiac ganglia of the guinea pig. Histochem J 28, 827–833 (1996). https://doi.org/10.1007/BF02272155

Download citation

  • Received:

  • Revised:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02272155

Keywords

Navigation