Summary
Rabbit carotid bodies were investigated by autoradiography at both the light and electron microscope levels following tritiated norepinephrine administration eitherin vivo orin vitro. Two kinds of labelled structures were found: nerve fibres (absent in sympathectomized carotid bodies) and some type I glomus cells. Desipramine (a specific norepinephrine uptake inhibitor) prevented labelling. Most of the labelled cells differed from unlabelled ones by the presence of (i) large dense-cored vesicles characterized by a large halo between the membrane and an eccentric dense core; (ii) a nucleus showing a more electron dense chromatin and a more irregular shape; and (iii) relatively abundant glycogen particles. A few weakly-labelled cells were characterized by a pyknotic nucleus and very swollen dense-cored vesicles, and were presumed to be degenerating.
Dense core diameters of dense-cored vesicles were distributed according to a unimodal distribution in labelled cells as in unlabelled ones but with an extension towards both large and very small diameters in labelled cells. The mean diameter was higher in labelled cells than in unlabelled ones (127 nm versus 113 nm,P < 0.01). The labelling intensity (as estimated by the number of silver grains per unit of cytoplasmic area) was maximum in cells having dense-cored vesicles whose mean diameter was between 130 and 170 nm, but decreased for cells with mean diameter of dense cores smaller than 130 nm, or larger than 170 nm.
Thus, in the rabbit carotid body, some glomus cells differ from others by their ability to take up tritiated norepinephrine and by the presence of larger dense-cored vesicles. However, this distinction is not clearcut and there are many intermediates. The observations suggest a phenomenon of evolution deriving from a unique cell type and typified by both metabolic norepinephrine uptake ability, glycogen accumulation) and morphologic changes (increase in diameter of dense-cored vesicles). It seems, therefore, more appropriate to consider these results in terms of different functional states rather than different types of glomus cells.
Similar content being viewed by others
References
Armengaud, C., Leitner, L. -M., Malber, C. -H., Roumy, M., Ruckebusch, M. &Sutra, J. F. (1988) Comparison of the monoamine and catabolite content in the cat and rabbit carotid bodies.Neuroscience Letters 85, 153–7.
Christie, D. S. &Hansen, J. T. (1983) Cytochemical evidence for the existence of norepinephrine-containing glomus cells in the rat carotid body.Journal of Neurocytology 12, 1041–53.
Eyzaguirre, C., Monti-Bloch, L., Baron, M., Hayashida, Y. &Woodbury, J. W. (1989) Changes in glomus cell membrane properties in response to stimulants and depressants of carotid nerve discharge.Brain Research 477, 265–79.
Fidone, S. &Gonzalez, C. (1982) Catecholamine synthesis in rabbit carotid bodyin vitro.Journal of Physiology 333, 69–79.
Fidone, S., Stensaas, L. J. &Zapata, P. (1975) Sensory nerve endings containing ‘synaptic’ vesicles: an electron microscope autoradiographic study.Journal of Neurobiology 6, 423–7.
Fidone, S., Zapata, P. &Stensaas, L. (1977) Axonal transport of labeled material into sensory nerve endings of cat carotid body.Brain Research 124, 9–28.
Fidone, S., Stensaas, L. J. &Zapata, P. (1983) Sites of synthesis, storage, release and recognition of biogenic amines in carotid bodies. InPhysiology of the Peripheral Arterial Chemoreceptors (edited byAcker, H. &O'Regan, R. G.) pp. 21–44. Amsterdam: Elsevier.
Fitzgerald, R., Garger, P., Hauer, P., Raff, M. C. &Fechter, L. (1983) Effect of hypoxia and hypercapnia on catecholamine content in cat carotid body.Journal of Applied Physiology 54, 1408–13.
Hanbauer, I. &Hellström, S. (1978) The regulation of dopamine and noradrenaline in the rat carotid body and its modification by denervation and by hypoxia.Journal of Physiology 282, 21–34.
Hansen, J. T. &Christie, D. S. (1981) Rat carotid body catecholamines determined by high performance liquid chromatography with electrochemical detection.Life Sciences 29, 1791–5.
Hellström, S. (1975) Morphometric studies of dense cored-vesicles in type I cells of the rat carotid body.Journal of Neurocytology 4, 77–86.
Hellström, S. &Koslow, S. (1975) Biogenic amines in rat carotid body of adult and infant rats: a gas chromatographic-mass spectrometric assay.Acta Physiologica Scandinavica 93, 540–8.
Leitner, L. -M., Roumy, M., Ruckebusch, M. &Sutra, J. F. (1986) Monamines and their catabolites in the rabbit carotid body; effects of reserpine, sympathectomy and carotid sinus nerve section.Pflügers Archiv 406, 552–6.
McDonald, D. M. &Mitchell, R. A. (1975) The innervation of glomus cells, ganglion cells and blood vessels in the rat carotid body: a quantitative ultrastructural analysis.Journal of Neurocytology 4, 177–230.
Mills, E., Smith, P. G., Slotkin, T. &Breese, G. (1978) Role of carotid body catecholamines in chemoreceptor function.Neuroscience 3, 1137–46.
Mir, A. K., Al-Neamy, K., Pallot, D. J. &Nahorski, S. R. (1982) Catecholamines in the carotid body of several mammalian species: effects of surgical and chemical sympathectomy.Brain Research 252, 335–42.
Morita, E., Chiocchio, S. R. &Tramezzani, J. H. (1969) Four types of main cells in the carotid body of the cat.Journal of Ultrastructure Research 28, 399–410.
Nahorski, S. R., Cook, N., Pallot, D. J. &Al-Neamy, K. (1980) Catecholamines in cat and rat carotid bodies.Journal of Anatomy 131, 749.
Pallot, D. J. (1983) Relationship between ultrastructure and function in peripheral arterial chemoreceptors. InPhysiology of the Peripheral Arterial Chemoreceptors (edited byAcker, H. &O'regan, R. G.) pp. 1–19. Amsterdam: Elsevier.
Pequignot, J. -M., Cottet-Emard, J. -M., Dalmaz, Y., De Haut De Sigy, M. &Peyrin, L. (1986) Biochemical evidence for norepinephrine stores outside the sympathetic nerves in rat carotid body.Brain Research 367, 238–43.
Smith, G. &Mills, E. (1976) Autoradiographic identification of the terminations of petrosal ganglion neurons in the cat carotid body.Brain Research 113, 174–8.
Thiery, J. -P. (1967) Mise en évidence des polysaccharides sue coupes en microscopie electronique.Journal de Microscopie 6, 987–1018.
Verna, A. (1973) Terminaisons nerveuses afferentes et efférentes dans le glomus carotidien du Lapin.Journal de Microscopie 16, 299–308.
Verna, A. (1975a) Observations on the innervation of the carotid body of the rabbit. InThe Peripheral Arterial Chemoreceptors (edited byPurves, M. J.) pp. 75–97. London: Cambridge University Press.
Verna, A. (1975b) Contribution à l'étude du glomus carotidien du Lapin (Oryctolaguscuniculus L.) Recherches cytologiques, cytochimiques et expérimentales. Thesis, Université de Bordeaux.
Verna, A. (1977) Dense-cored vesicles and cell types in the rabbit carotid body. InChemoreception in the Carotid Body (edited byAcker, H., Fidone, S., Pallot, D., Eyzaguirre, C., Lubbers, D. W. &Torrance, R. W.) pp. 216–20. Berlin: Springer-Verlag.
Verna, A. (1979) Ultrastructure of the carotid body in the mammals.International Review of Cytology 60, 271–330.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Schamel, A., Verna, A. Norepinephrine-containing glomus cells in the rabbit carotid body. I. Autoradiographic and morphometric study after tritiated norepinephrine uptake. J Neurocytol 21, 341–352 (1992). https://doi.org/10.1007/BF01191702
Received:
Revised:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF01191702