Skip to main content
SpringerLink
Log in

Enkephalin- and serotonin-like immunoreactivity in the aortico-pulmonary paraganglia of the white-belly opossumDidelphis albiventris (Marsupialia)

  • Published:
The Histochemical Journal Aims and scope Submit manuscript

Summary

Serial histological sections of the interatrial septum and basal heart vessels of the weaned and juvenile white-belly opossum (Didelphis albiventris) were obtained in order to study the presence of paraganglia and their content of regulatory peptides and serotonin. Paraganglion groups were mapped between the aorta and pulmonary arteries and close to the bifurcation of the pulmonary trunk and were found to contain cells with immunoreactivity to serotonin and to the neuroendocrine markers PGP 9.5 and NSE. When these paraganglia were tested for immunoreactivity to a battery of regulatory peptides, all were found to be positive for methionin-enkephalin, leucine-enkephalin and galanin. The hypothesis is raised that these peptides and serotonin, besides catecholamines, produced by these paraganglia may play a physiological role in the functions of the cardiovascular system of the white-belly opossum.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Almeida, H. O., Cobbi, H., Teixeira, V. P. A. &Brandão, M. C. (1984) Paragânglios interatriais no coração humano adulto.Arq. Bras. Cardiol. 43, 251–4.

    Google Scholar 

  • Barnard, W. G. (1946) A paraganglion related to the ductus arteriosus.J. Pathol. Bacteriol. 58, 631–2.

    Google Scholar 

  • Becker, A. E. (1966) The glomera of the region of the heart and great vessels.Pathol. Europ. 1(4), 410–24.

    Google Scholar 

  • Boyd, J. D. (1981) The inferior aortico-pulmonary glomus.Brit. Med. Bull. 17(2), 127–31.

    Google Scholar 

  • Busachi, P. (1913) I corpi chromaffini del cuore umano.Arch. Ital. Anat. Embriol. 11, 352–76.

    Google Scholar 

  • Dail, W. G. &Palmer, G. C. (1973) Localization and correlation of cathecolamine-containing cells with adenyl-cyclase and phosphodiesterase activities in the human fetal heart.Anat. Rec. 177, 265–88.

    Google Scholar 

  • Edwards, C. &Heath, D. (1969) Microanatomy of glomic tissue of the pulmonary trunk.Thorax 24, 209–17.

    Google Scholar 

  • Glenner, G. G. &Grimley, P. M. (1974)Tumors of the Extraadrenal Paraganglion System. 2nd edn. Washington DC: Armed Forces Institute of Pathology.

    Google Scholar 

  • Gobbi, H., Teixeira, V. P. A., Brandão, M. C. Almeido, H. O. (1985) Paragânglio atrial humano intramiocárdico; relato de caso.Arq. Bras. Cardiol. 44, 277–8.

    Google Scholar 

  • Gobbi, H., Barbosa, A. J. A., Teixeira, V. P. A. &Almeida, H. O. (1991) Immunocytochemical identification of neuroendocrine markers in human cardiac paraganglion-like structures.Histochemistry 95, 337–40.

    Google Scholar 

  • Goormaghtigh, N. &Pannier, R. (1930) Les paraganglions du coeur et des zones vasosensibles carotidienne et aorticopulmonaire chez le chat adult.Arch. Biol. 50,455–533.

    Google Scholar 

  • Hacker, G. W., Bishop, A. E., Terenghi, G., Varndell, I. M., Aghaowa, J., Pollard, K., Thurner, J. &Polak, J. M. (1988) Multiple peptide production and presence of general neuroendocrine markers detected in 12 cases of human phaechromocytoma and in mammalian adrenal glands.Virchows Archiv A Pathol. Anat. Histopathol. 412, 399–411.

    Google Scholar 

  • Hansen, J. T., Brokaw, J., Christie, D. &Karasek, M. (1982) Localization of enkephalin-like immunoreactivity in the cat carotid ann aortic body chemoreceptors.Anat. Rec. 203, 405–10.

    Google Scholar 

  • Hervonen, A. (1971) Development of cathecolamine-storing cells in human fetal paraganglia and adrenal medulla.Acta Physiol. Scand. 368(suppl), 1–94.

    Google Scholar 

  • Hervonen, A., Pickel, V. M., Joh, T. H., Reis, D. J., Linnoila, I., Kanerva, L. &Miller, R. J. (1980) Immunocytochemical demonstration of catecholamine-synthesizing enzymes and neuropeptides in the cathecolamine-storing cells of human fetal sympathetic nervous system.Adv. Biochem. Psychopharmacol. 25, 373–8.

    Google Scholar 

  • Hervonen, A., Pickel, V. M., Joh, T. H., Reis, D. J., Linnoila, I. &Miller, R. J. (1981) Immunohistochemical localization of catecholamine-synthesizing enzymes, substance P and enkephalin in the human fetal sympathetic ganglion.Cell Tissue Res. 214, 33–42.

    Google Scholar 

  • Jacobowitz, D. (1967) Histochemical studies of the relationship of chromaffin cells and adrenergic nerve fibers to the cardiac ganglia of several species.J. Pharmacol. Exp. Therap. 158, 227–40.

    Google Scholar 

  • Jarvi, R., Helen, P., Pelto-Huikko, M. &Hervonen, A. (1986) Neuropeptide Y (NPY)-like immunoreactivity in rat sympathetic neurons and small granule-containing cells.Neurosci. Lett. 67, 223–7.

    Google Scholar 

  • Junqueira, L. C. U., Bignolas, G. &Brentani, R. R. (1979) Picrosirius staining plus polarization microscopy, a specific method for collagen detection in tissue sections.Histochem. J. 11, 447–55.

    Google Scholar 

  • Kobayashi, S., Ohashi, T., Fujita, T., Nakao, K., Yoshimasa, T., Imura, H., Mochizuki, T., Yanaihara, C., Yanaihara, N. &Verhofstad, A. A. J. (1983a) An immunohistochemical study on the co-storage of met-enkephalin-arg-gly-leu and met-enkephalin-arg-phe with adrenaline and/or noradrenaline in the adrenal chromaffin cells of rat, dog and cat.Biomed. Res. 4(5), 433–42.

    Google Scholar 

  • Kobayashi, S., Uchida, T., Ohashi, T., Fujita, T., Nakao, K., Yoshimasa, T., Imura, H., Mochisuki, T., Yanaihara, C., Yanaihara, N. &Verhfstad, A. A. J. (1983b) Immunocytochemical demonstration of the co-storage of noradrenaline with met-enkephalin-arg-phe and met-enkephalin-arg-glyleu in the carotid body chief cells of dog.Arch. Histol. Jap. 46(5), 713–22.

    Google Scholar 

  • Kohn, A. (1903) Die paraganglion.Arch. Mikrobiol. 62, 61–79.

    Google Scholar 

  • Linnoila, R. I., Diaugustine, R. P., Hervonen, A. &Miller, R. J. (1980) Distribution of met- and leu-enkephalin-, vasoactive intestinal polypeptide- and substance P-like immunoreactivities in human adrenal glands.Neurosci. 5, 2247–59.

    Google Scholar 

  • Lloyd, R. V., Sisson, J. C., Shapiro, B. &Verhofstad, A. A. J. (1986) Immunohistochemical localization of epinephrine, norepinephrine, catecholamine-synthesizing enzymes and chromogranin in neuroendocrine cells and tumors.Am. J. Pathol. 125, 45–54.

    Google Scholar 

  • Lundberg, J. M., Hamberger, B., Schultzberg, M., Hokfelt, T., Granberg, P. O., Efendic, S., Terenius, L., Goldstein, M. &Luft, R. (1979a) Enkephalin- and somatostatin-like immunoreactivities in human adrenal medulla and pheochromocytoma.Proc. Natl Acad. Sci. USA 76(8), 4079–83.

    Google Scholar 

  • Lundberg, J. M., Hokfelt, T., Fahrenkrug, J., Nilsson, G. &Terenius, L. (1979b) Peptides in the carotid body (glomus carotidum): VIP-, enkephalin-, and substance P-like immunoreactivity.Acta Physiol. Scand. 107, 279–81.

    Google Scholar 

  • Monro, R. S. (1950) The morphology of the branchial glomera and their tumours, with a report of a case of aorticopulmonary glomus tumour.Brit. J. Surg. 38, 105–9.

    Google Scholar 

  • Muratori, G. (1962) Histological observations on the cervicothoracic paraganglia of amniotas.Arch. Int. Pharmacodyn. 140, 217–26.

    Google Scholar 

  • Muratori, G. (1969) Distribuzioni e caractteristiche istomorfologiche dei paragangli atriali del cuore del gatto.Arch. Ital. Anat. Embriol. 74, 1–13.

    Google Scholar 

  • Papka, R. E. (1974) A study of cathecolamine containing cells in hearts of fetal and postnatal rabbits by fluorescence electron microscopy.Cell Tissue Res. 154, 471–84.

    Google Scholar 

  • Pearse, A. G. E. &Takor Takor, T. (1979) Embryology of the diffuse endocrine system and its relationship to the common peptides.Fed. Proc. 38, 2288–94.

    Google Scholar 

  • Prechtl, J. C. &Powley, T. L. (1985) Organization of the rat subdiaphragmatic vagus and associated paraganglia.J. Comp. Neurol. 235, 182–95.

    Google Scholar 

  • Schultzberg, M., Hokfelt, T., Lundberg, J. M., Terenius, L., Elfvin, L. G. &Elde, R. (1978) Enkephalin-like immunoreactivity in nerve terminals in sympathetic ganglia and adrenal medullary gland cells.Acta Physiol. Scand. 103, 475–7.

    Google Scholar 

  • Sternberger, L. A. (1986)Immunocytochemistry. 3rd edn. pp. 90–209. New York: John Wiley.

    Google Scholar 

  • Tafuri, W. L., Almeida, H. O., Maria, T. A. &Bogliolo, L. (1975) Ultrastructure of subepicardic paraganglia of the albino mouse.Riv. Anat. Patol. Oncol. 39, 1–18.

    Google Scholar 

  • Vaalasti, A., Pelto-Huikko, M., Tainio, H. &Hervonen, A. (1985) Light- and electron-microscopic demonstration of enkephalin-like immunoreactivity in paraganglia of the urinary bladder.Cell Tissue Res. 239, 683–7.

    Google Scholar 

  • Varndell, J. M., Tapia, F. J., De Mey, J., Rush, R. A., Bloom, S. R. &Polak, J. (1982) Electron immunocytochemical localization of enkephalin-like material in cathecolamine-containing cells of the carotid body, the adrenal medulla, and in pheochromocytomas of man and other mammals.J. Histochem. Cytochem. 30(7), 682–90.

    Google Scholar 

  • Wharton, J., Polak, J. M., Pearse, A. G. E., McGregor, G. P., Bryant, M. G., Bloom, S. R., Emson, P. C., Bisgard, G. E. &Will, J. A. (1980) Enkephalin-, VIP- and substance P-like immunoreactivity in the carotid body.Nature 284, 269–71.

    Google Scholar 

  • Wharton, J., Haworth, S. G. &Polak, J. M. (1988) Postnatal development of the innervation and paraganglia in the porcine arterial bed.J. Pathol. 154, 19–27.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Pathology, School of Medicine, Federal University of Minas Gerais, Brazil

    H. Gobbi & A. J. A. Barbosa

  2. Department of Morphology, Institute of Biological Sciences, Federal University of Minas Gerais, Brazil

    J. C. Nogueira

  3. Department of Histochemistry, Royal Postgraduate Medical School, London, UK

    J. M. Polak

  4. Department of Pathology, School of Medicine, Triangulo Mineiro, Uberaba, Brazil

    V. P. A. Teixeira & H. O. Almeida

Authors
  1. H. Gobbi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. A. J. A. Barbosa
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. J. C. Nogueira
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. J. M. Polak
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. V. P. A. Teixeira
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. H. O. Almeida
    View author publications

    You can also search for this author in PubMed Google Scholar

Additional information

Work supported by grants from FINEP and CNPq (Brazil).

Rights and permissions

Reprints and permissions

About this article

Cite this article

Gobbi, H., Barbosa, A.J.A., Nogueira, J.C. et al. Enkephalin- and serotonin-like immunoreactivity in the aortico-pulmonary paraganglia of the white-belly opossumDidelphis albiventris (Marsupialia). Histochem J 24, 110–114 (1992). https://doi.org/10.1007/BF01082447

Download citation

  • Received:

  • Revised:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01082447

Keywords

Search

Navigation