Springer Nature is making Coronavirus research free. View research | View latest news | Sign up for updates

Catecholaminergic innervation of the chicken ovary

With special reference to the follicular wall

Summary

The innervation of the chicken ovary was investigated with special emphasis on adrenergic nerves in the follicular wall. Quantitative determinations of catecholamines (CA) by high-performance liquid chromatography and electrochemical detection (hplc-ed) revealed 15.4±3.3 ng/mg protein of norepinephrine (NE) and 3.14 ng/mg protein of epinephrine (E), with even larger amounts in the cranial part of the ovary close to the adrenal gland. Serial sections that had been processed for the visualisation of aminergic nerves (Falck-Hillarp- or glyoxylic acid technique) showed CA localized in nerve-fibre bundles; cell bodies of chromaffin and sympathetic neurons were only found at the ovarianadrenal junction suggesting that ovarian nerves stored considerable quantities of E. An antiserum against bovine phenylethanolamine N-methyltransferase (PNMT, the E-synthesizing enzyme) produced no immunostaining in chicken ovary or adrenal gland, due to a lack of crossreactivity between the antiserum and chicken PNMT.

Serial sections processed alternately for the visualisation of aminergic nerves and myosin (from chicken gizzard) immunoreactivity revealed a scarce nerve supply of contractile cells in the theca externa compared to an extraordinarily dense innervation of the endocrine interstitial tissue of the theca interna. This distribution pattern of nerve fibres in the follicular wall was confirmed by electron microscopy in ovarian tissue that had been pretreated with 5- or 6-hydroxydopamine (OHDA). More than 90% of the terminal axons were specifically labeled by these false adrenergic transmitters. Many of these terminals were seen in close contact (20 nm) with steroidogenic cells suggesting a neuromodulatory function of CA in hormone synthesis and/or release. It is yet unclear whether E and NE are stored in separate or identical axon moieties and within the same organelles. Choline acetyltransferase activity, which was taken as a measure for a cholinergic nerve component in the ovary, amounted to only 7% of its adrenal activity. It is suggested that the chicken ovary may serve as an excellent model to investigate the modulatory role of nerves in the endocrine function of the ovary.

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

References

  1. Bahr J, Kao L, Nalbandov AV (1974) The role of catecholamines and nerves in ovulation. Biol Reprod 10:273–290

  2. Baumgarten HG, Holstein AF (1968) Adrenerge Innervation im Hoden und Nebenhoden vom Schwan. Z Zellforsch 91:402–410

  3. Baumgarten HG, Holstein AF (1971) Noradrenerge Nervenfasern im Hoden von Mammaliern und anderen Vertebraten. J Neuro-Visc Rel, Suppl 10:563–572

  4. Bennett T, Malmfors T (1970) The adrenergic nervous system of the domestic fowl. Z Zellforsch mikrosk Anat 106:22–50

  5. Björklund A, Falck B, Owman Ch (1972) Fluorescence microscopic and microspectrofluorometric techniques for the cellular localization and characterization of biogenic amines. In: Berson SA (ed) Methods of investigative and diagnostic endocrinology, Vol 1. Rall JE, Kopin IJ (eds) The thyroid and biogenic amines. North Holland Publ Co, Amsterdam, pp 318–368

  6. Bulmer D (1965) A histochemical study of ovarian cholinesterases. Acta Anat 62:254–265

  7. Burden HW (1972) Adrenergic innervation in ovaries of the rat and guinea-pig. Am J Anat 133:455–462

  8. Burden HW (1978a) Neural modulation of ovarian function. TINS 1:85–86

  9. Burden HW (1978b) Ovarian Innervation. In: Jones RE (ed) The vertebrate ovary. Comparative Biology and Evolution. Plenum Press, New York and London, pp 615–638

  10. Capps ML, Lawrence IE Jr, Burden HW (1978) Ultrastructure of the cells of the ovarian interstitial gland in hypophysectomized rats. Cell Tissue Res 193:433–442

  11. Connett RJ, Kirshner N (1970) Purification and properties of bovine phenylethanolamine N-methyltransferase. J Biol Chem 245:329–334

  12. Coupland RW (1972) The Chromaffin System. In: Blaschko H, Muscholl E (eds) Catecholamines. In: Handb Exp Pharm XXXIII, Springer, Berlin-Heidelberg-New York, pp 16–45

  13. Dahl E (1970) Studies of the fine structure of ovarian interstitial tissue. 3. The innervation of the thecal gland of the domsetic fowl. Z Zellforsch 109:212–226

  14. De La Torre JC, Surgeon JW (1976) Histochemical fluorescence of tissue and brain monoamines: results in 18 min using the sucrose-phosphate-glyoxylic acid (SPG) method. Neuroscience 1:451–453

  15. Fonnum F (1975) A rapid radiochemical method for the determination of choline acetyltransferase. J Neurochem 24:407–409

  16. Gilbert AB (1965) Innervation of the ovarian follicle of the domestic hen. Q J Exp Physiol 50:437–445

  17. Gilbert AB (1969) Innervation of the ovary of the domestic hen. Q J Exp Physiol 54:404–415

  18. Gilbert AB, Wood Gush DGM (1969) Innervation of ovarian transplants in the domestic hen. J Reprod Fertil 18:550–551

  19. Gröschel-Stewart U, Schreiber J, Mahlmeister C (1976) Production of specific antibodies to contractile proteins and their use in immunofluorescence microscopy. I. Antibodies to smooth and striated chicken muscle myosins. Histochemistry 46:229–236

  20. Haase E (1973) Histochemische und elektronenmikroskopische Untersuchungen über die Innervation des Hodens vom Bergfink (Fringilla montifringilla). Verh Dt Zool Ges 66:106–110

  21. Holzbauer M, Sharman DF (1972) The distribution of catecholamines in vertebrates. In: Blaschko H, Muscholl E (eds) Catecholamines. In: Handb Exp Pharm XXXIII, Springer, Berlin-Heidelberg-New York, pp 110–185

  22. Ignarro LJ, Shideman FE (1968) Appearance and concentrations of catecholamines and their biosynthesis in the embryonic and developing chick. J Pharmacol Exp Ther 159:38–48

  23. Jacobowitz D, Wallach EE (1967) Histochemical and chemical studies of the autonomic innervation of the ovary. Endocrinology 81:1132–1139

  24. Lindmar R, DeSantis VP (1974) The significance of noradrenaline and adrenaline as adrenergic transmitters in the chicken. Naunyn-Schmiedeberg's Arch Pharmacol 282:R58

  25. Lindvall O, Björklund A (1974) The glyoxylic acid fluorescence histochemical method: A detailed account of the methodology for the visualization of central catecholamine neurons. Histochemistry 39:97–127

  26. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275

  27. Müller TH, Unsicker K (1981) High performance liquid chromatography with electrochemical detection as a highly efficient tool for studying catecholaminergic systems. I. Quantification of noradrenaline, adrenaline and dopamine in cultured adrenal medullary cells. J Neurosci Meth 4:39–52

  28. Owman Ch, Sjöberg N-O, Svensson KG, Walles B (1975) Autonomic nerves mediating contractility in the human Graafian follicle. J Reprod Fertil 45:553–556

  29. Owman Ch, Sjöberg N-O, Wallach EE, Walles B, Wright KH (1979) Neuromuscular mechanisms of ovulation. In: Hafez ESE (ed) Human ovulation: Mechanisms, prediction, detection and regulation. Elsevier/North Holland, Amsterdam, pp 57–100

  30. Rosengren E, Sjöberg N-O (1967) The adrenergic nerve supply to the female reproductive tract of the cat. Am J Anat 121:271–284

  31. Soliman KFA, Walker ChA (1976) In vitro motility of the avian ovarian follicles. Gen Comp Endocrinol 30:372–377

  32. Stefenson A, Owman Ch, Sjöberg NO, Sporrong B, Walles B (1981) Comparative study of the autonomic innervation of the mammalian ovary, with particular regard to the follicular system. Cell Tissue Res 215:47–62

  33. Svensson KG, Owman Ch, Sjöberg NO, Sporrong B, Walles B (1975) Ultrastructural evidence for adrenergic innervation of the interstitial gland in the guinea pig ovary. Neuroendocrinol 17:40–47

  34. Taxi J (1979) The chromaffin and chromaffin-like cells in the autonomic nervous system. Int Rev Cytol 57:283–343

  35. Unsicker K (1970) Zur Innervation der interstitiellen Drüse im Ovar der Maus (Mus musculus L.). Z Zellforsch 109:46–54

  36. Unsicker K (1982 in press) Innervation of endocrine tissues. In: Motta PM (ed) Electron microscopy in biology and medicine. Nijhoff Publ Hingham MA USA

  37. Unsicker K, Seidel F, Gröschel-Stewart U, Lindmar R, Löffelholz K, Wolf U (1980) Zur adrenergen Innervation des Hühnerovars. Verh Anat Ges 74:443–445

  38. Unsicker K, Tschechne B, Tschechne D (1981) Differentiation and transdifferentiation of adrenal chromaffin cells of the guinea-pig. Cell Tissue Res 215:341–367

  39. Walles B, Edvinsson L, Nybell G, Owman Ch, Sjöberg NO (1974) Amine-induced influence on spontaneous ovarian contractility in the guinea-pig and the cat. Fertil Steril 25:602–611

  40. Walles B, Edvinsson L, Falck B, Owman Ch, Sjöberg NO, Svensson KG (1975) Evidence for a neuromuscular mechanism involved in the contractility of the ovarian follicular wall: Fluorescence and electron microscopy and effects of tyramine on follicle strips. Biol Reprod 12:239–248

  41. Walles B, Edvinsson L, Owman Ch, Sjöberg NO, Sporrong B (1976) Cholinergic nerves and receptors mediating contraction of the Graafian follicle. Biol Reprod 15:565–572

  42. Walles B, Falck B, Owman Ch, Sjöberg NO (1977a) Characterization of autonomic receptors in the smooth musculature of human Graafian follicle. Biol Reprod 17:423–431

  43. Walles B, Edvinsson L, Owman Ch, Sjöberg NO, Sporrong B, Stefenson A (1977b) Influence of sympathetic nerves, amine receptors and anti-adrenergic drugs on follicular contractility and ovulation. Acta Physiol Scand Suppl 452:113–120

  44. Walles B, Gröschel-Stewart U, Owman Ch, Sjöberg NO, Unsicker K (1978) Fluorescence histochemical demonstration of a relationship between adrenergic nerves and cells containing actin and myosin in the rat ovary, with special reference to the follicle wall. J Reprod Fertil 52:175–178

Download references

Author information

Correspondence to Professor K. Unsicker.

Additional information

Dedicated to Professor H. Leonhardt, Kiel, in honour of his 65th birthday

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Unsicker, K., Seidel, F., Hofmann, H.-. et al. Catecholaminergic innervation of the chicken ovary. Cell Tissue Res. 230, 431–450 (1983). https://doi.org/10.1007/BF00213816

Download citation

Key words

  • Chicken ovary
  • Adrenergic innervation
  • Cholinergic innervation
  • Steroidogenic interstitial cells
  • Myosin immunoreactivity
  • PNMT
  • Choline acetyltransferase