Skip to main content
Log in

Demonstration of the neural crest origin of type I (APUD) cells in the avian carotid body, using a cytochemical marker system

  • Published:
Histochemie Aims and scope Submit manuscript

Summary

The biogenic amines present in the carotid body Type 1 cells of two avian species (Japanese quail and chicken) were identified, by microspectrofluorometry of formaldehyde-induced fluorescence, as dopamine and 5-hydroxytryptamine respectively. These and other cytochemical properties establish the cells as members of the APUD series.

Grafts of the neural rhombencephalic primordium from 6 to 10-somite quail embryos were implanted in the appropriate region of chick embryos of the same age. After up to 11 days incubation the carotid bodies of the host were freeze-dried and treated with hot formaldehyde vapour. The carotid body Type 1 cells in the chick host were identified, by the presence of dopamine and the absence of 5-HT, as cells from the quail neural crest.

The dopamine phenotype in cells of quail origin thus provides a cytochemical marker which may be used for other allograft experiments. The present work confirms earlier findings, using a biological (nuclear chromatin) marker, which showed the avian carotid body to be of neural crest origin.

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

  • Al-Lami, F., Murray, R.G.: Fine structure of the carotid body of Macaca mulata monkey. J. Ultrastruct. Res. 24, 465–478 (1968a).

    Google Scholar 

  • Al-Lami, F., Murray, R.G.: Fine structure of the carotid body of normal and anoxic cats. Anat. Rec. 160, 697–718 (1968b).

    Google Scholar 

  • Banister, R.J., Portic, P.J., Vogt, M.: The content and localization of catechol amines in the carotid labyrinths and aortic arches of Rana temporaria. J. Physiol. (Lond.) 192, 529–535 (1967).

    Google Scholar 

  • Becker, A.E., Drukker, J., Meijer, H.E.F.H.: Histochemical characteristics of chemoreceptor organs (glomera). Histochemie 11, 195–204 (1967).

    Google Scholar 

  • Biscoe, T.J.: Carotid body: Structure and function. Physiol. Rev. 51, 437–495 (1971).

    Google Scholar 

  • Biscoe, T.J., Stehbens, W.E.: Ultrastructure of the carotid body. J. Cell Biol. 30, 563–568 (1966).

    Google Scholar 

  • Björklund, A., Ehinger, B., Falck, B.: Analysis of fluorescence excitation peak ratios for the cellular identification of noradrenaline, dopamine or their mixtures. J. Histochem. Cytochem. 20, 56–64 (1972).

    Google Scholar 

  • Boyd, J.D.: The development of the human carotid body. Contr. Embryol. Carneg. Instn 26, 1–31 (1937).

    Google Scholar 

  • Capella, C., Solcia, E.: Optical and electron microscopical study of cytoplasmic granules in human carotid body, carotid body tumours and glomus jugulare tumours. Virchows Arch. Abt. B 7, 37–53 (1971).

    Google Scholar 

  • Celestino Da Costa, A.: La notion de métaneurogonie. C. R. Ass. Anat. (41st réunion) 644–653 (1955).

  • Chen, I-Li, Yates, R.D.: Electron microscopic radioautographic studies of the carotid body following injections of labeled biogenic amine precursors. J. Cell Biol. 42, 794–803 (1969).

    Google Scholar 

  • Chiocchio, S.R., Biscardi, A.M., Tramezzani, J.H.: Catecholamines in the carotid body of the cat. Nature (Lond.) 212, 843–845 (1966).

    Google Scholar 

  • Dearnaley, D.P., Fillenz, M., Woods, R.I.: The identification of dopamine in the carotid body of the rabbit. In: R.W. Torrance, Arterial chemoreceptors, p. 189–192. Oxford-Edinburgh: Blackwell Sci. Publ. 1968.

    Google Scholar 

  • Eränkö, O.: The practical histochemical demonstration of catecholamines by formaldehyde induced fluorescence. J. roy. micr. Soc. 87, 259–276 (1967).

    Google Scholar 

  • Falck, B.: Observations on the possibility of the cellular localization of monoamines by a fluorescence method. Acta physiol. scand. 56, Suppl. 197 (1962).

    Google Scholar 

  • Grimley, P.M., Glenner, G.G.: Ultrastructure of the human carotid body. A perspective on the mode of chemoreception. Circulation 37, 648–665 (1968).

    Google Scholar 

  • Hamberger, B., Ritzen, M., Wersäll, J.: Demonstration of catecholamines and 5-hydroxytryptamine in the human carotid body. J. Pharmacol. exp. Ther. 152, 197–201 (1966).

    Google Scholar 

  • Helpap, B., Hempel, K.: Über den Katecholamin-Stoffwechsel des Carotiskörperchens der Ratte. Virchows Arch. Abt. B 3, 270–281 (1969).

    Google Scholar 

  • Hervonen, A., Korkala, O.: The histochemically demonstrable monoamines of human fetal carotid body. Experientia (Basel) 28, 449–450 (1972).

    Google Scholar 

  • Höglund, R.: An ultrastructural study of the carotid body of horse and dog. Z. Zellforsch. 76, 568–576 (1967).

    Google Scholar 

  • Kobayashi, S.: Catecholamines in the avian carotid body. Experientia (Basel) 25, 1075–1076 (1969).

    Google Scholar 

  • Kohn, A.: Über den Bau und die Entwicklung der sog. Carotisdrüse. Arch. mikr. Anat. 56, 81–148 (1900).

    Google Scholar 

  • Le Douarin, N.: Particularités du noyau interphasique chez la Caille japonaise (Coturnix coturnix japonica). Utilisation de ces particularités comme ≪marquage biologique≫ dans des recherches sur les interactions tissulaires et les migrations cellulaires au cours de l'ontogenèse. Bull. biol. France Belg. 103, 435–452 (1969).

    Google Scholar 

  • Le Douarin, N.: Caractéristiques ultrastructurales du noyau interphasique chez la caille et chez le poulet et utilisation de cellules de caille comme ≪marqueurs biologiques≫ en embryologie expérimentale. Ann. d'Embryol. Morphogen. 4, 125–135 (1971).

    Google Scholar 

  • Le Douarin, N., Le Lièvre, C.: Démonstration de l'origine neurale des cellules à calcitonine du corps ultimobranchial chez l'embryon de Poulet. C. R. Acad. Sci. (Paris), Série D 270, 2857–2860 (1970).

    Google Scholar 

  • Le Douarin, N., Le Lièvre, C., Fontaine. J.: Recherches experimentales sur l'origine embryologique du corps carotidien chez les Oiseaux. C. R. Acad. Sci. (Paris), Série D 275, 583–586 (1972).

    Google Scholar 

  • Le Douarin, N., Teillet, M.A.: Localization, par le méthode des greffes interspécifiques, du territoire neural dont dérivent les cellules adrénales surrénaliennes chez l'embryon d'Oiseau. C. R. Acad. Sci. (Paris), Série D 272, 481–484 (1971).

    Google Scholar 

  • Lever, J.D., Lewis, P.R., Boyd, J.D.: Observations on the fine structure and histochemistry of the carotid body in the cat and rabbit. J. Anat. (Lond.) 93, 478–491 (1959).

    Google Scholar 

  • Melander, A., Owman, Ch., Sundler, F.: Concomitant depletion of dopamine and secretory granules from cells in the ultimobranchial gland of vitamin D2-treated chicken. Histochemie 25, 21–31 (1971).

    Google Scholar 

  • Millonig, G.: Further observations on a phosphate buffer for osmium solutions in fixation. In: Proc. 5th Int. Congr. Electron Microscopy. Edit. S.S. Breese. New York: Acad. Press 1962.

    Google Scholar 

  • Model, P.G., Dalton, H.C.: The uptake and localization of radioactive DOPA by amphibian melanoblasts in vitro. Develop. Biol. 17, 245–271 (1968).

    Google Scholar 

  • Mönckeberg, I.G.: Die Tumoren der Glandula carotica. Beitr. path. Anat. 38, 1–66 (1905).

    Google Scholar 

  • Morita, R., Chiocchio, S.R., Tramezzani, J.H.: Four types of main cells in the carotid body of the cat. J. Ultrastruct. Res. 28, 399–410 (1969).

    Google Scholar 

  • Muscholl, E., Rahn, K.H., Watzka, M.: Nachweis von Noradrenalin in Glomus caroticum. Naturwissenschaften 47, 325 (1960).

    Google Scholar 

  • Niemi, M., Ojala, K.: Cytochemical demonstration of catecholamines in the human carotid body. Nature (Lond.) 203, 539–540 (1964).

    Google Scholar 

  • Pearse, A.G.E.: 5-hydroxytryptophan uptake by dog thyroid C cells and its possible significance in polypeptide hormone production. Nature (Lond.) 211, 598 (1966a).

    Google Scholar 

  • Pearse, A.G.E.: Common cytochemical properties of cells producing polypeptide hormones. with particular reference to calcitonin and the thyroud C cells. Vet. Rec. 79, 587–590 (1966b).

    Google Scholar 

  • Pearse, A.G.E.: Histochemistry, theoretical and applied. vol. 1, third ed. London: J. & A. Churchill Ltd. 1968.

    Google Scholar 

  • Pearse, A.G.E.: The cytochemistry and ultrastructure of polypeptide hormone-producing cells of the APUD series, and the embryologic, physiologic and pathologic implications of the concept. J. Histochem. Cytochem. 17, 303–313 (1969).

    Google Scholar 

  • Pearse, A.G.E.: Histochemistry, theoretical and applied, vol. 2, third ed. London: Churchill-Livingstone 1972.

    Google Scholar 

  • Pearse, A.G.E., Carvalheira, A.: Cytochemical evidence for an ultimobranchial origin of rodent thyroid C cells. Nature (Lond.) 214, 929–930 (1967).

    Google Scholar 

  • Pearse, A.G.E., Polak, J.M.: Cytochemical evidence for the neural crest origin of mammalian ultimobranchial C cells. Histochemie 27, 96–102 (1971 a).

    Google Scholar 

  • Pearse, A.G.E., Polak, J.M.: Neural crest origin of the endocrine polypeptide (APUD) cells of the gastrointestinal tract and pancreas. Gut 12, 783–788 (1971b).

    Google Scholar 

  • Pearse, A.G.E., Polak, J.M., Noorden, S. van: The neural crest origin of the C cells and their comparative cytochemistry and ultrastructure in the ultimobranchial gland. In: Calcium, parathyroid hormone and the calcitonins. Amsterdam: Excerpta Medica 1971.

    Google Scholar 

  • Pearse, A.G.E., Welsch, U.: Ultrastructural characteristics of thyroid C cells in the summer, autumn and winter states of the hedgehog (Erinaceus europaeus, L.), with reference to other mammalian species. Z. Zellforsch. 92, 596–609 (1968).

    Google Scholar 

  • Polak, J.M., Rost, F.W.D., Pearse, A.G.E.: Fluorogenic amine tracing of neural crest derivatives forming the adrenal medulla. Gen. comp. Endocr. 16, 132–136 (1971).

    Google Scholar 

  • Rabl, H.: Die Entwicklung der Carotisdrüse beim Meerschweinchen. Arch. mikr. Anat. 96, 315–339 (1922).

    Google Scholar 

  • Rogers, D.C.: The development of the rat carotid body. J. Anat. (Lond.) 99, 89–101 (1965).

    Google Scholar 

  • Ross, L.L.: Electron microscopic observations of the carotid body of the cat. J. biophys. biochem. Cytol. 6, 253–262 (1959).

    Google Scholar 

  • Rost, F.W.D., Pearse, A.G.E.: An improved microspectrofluorimeter with autmatic digital data logging: construction and operation. J. Microsc. 94, 93–105 (1971).

    Google Scholar 

  • Solcia, E., Capella, C., Vassallo, G.: Lead-haematoxylin as a stain of endocrine cells. Significance of staining and comparison with other selective methods. Histochemie 20, 116–126 (1969).

    Google Scholar 

  • Solcia, E., Vassallo, G., Capella, C.: Selective staining of endocrine cells by basic dyes after acid hydrolysis. Stain Technol. 43, 257–263 (1968).

    Google Scholar 

  • Stoeckel, M.E., Porte, A.: Etude ultrastructurale des corps ultimobranchiaux du poulet. I. Aspect normal développement embryonnaire. Z. Zellforsch. 94, 495–512 (1969).

    Google Scholar 

  • Szijj, I., Csapó, Z., Lásló, F.A., Kovács, K.: Medullary cancer of the thyroid gland associated with hypercorticism. Cancer (Philad.) 24, 167–173 (1969).

    Google Scholar 

  • Teillet, M.A., Le Douarin, N.: La migration des cellules pigmentaires étudiée par la methode des greffes héterospécifiques de tube nerveux chez l'embryon d'Oiseau. C. R. Acad. Sci. (Paris), Série D 270, 3095–3098 (1970).

    Google Scholar 

  • Winiwarter, H. de: Origine et développement du ganglion carotidien. Appendice: participation de l'hypoblaste à la constitution des ganglions craniens. Arch. Biol. (Paris) 50, 67–94 (1939).

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Pearse, A.G.E., Polak, J.M., Rost, F.W.D. et al. Demonstration of the neural crest origin of type I (APUD) cells in the avian carotid body, using a cytochemical marker system. Histochemie 34, 191–203 (1973). https://doi.org/10.1007/BF00303435

Download citation

  • Received:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00303435

Keywords

Navigation