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Functional vasoactive intestinal polypeptide (VIP)-system in salt glands of the Pekin duck

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Summary

In saltwater-acclimated ducks with fully specialized supraorbital salt glands, intracarotid application of acetylcholine (5 nmoles/min/kg b.w.) or porcine vasoactive intestinal polypeptide (pVIP) (240 pmoles/min/kg b.w.) induced secretion from the salt glands at threshold conditions of secretory activity. pVIP-like immunoreactivity could be localized in fibers of the postganglionic secretory nerve ramifying throughout the glandular parenchyma. Both middle-sized arterioles and secretory tubules were innervated, and pVIP-immunoreactive varicose fibers formed peritubular baskets around the basal region of secretory tubules indicating direct innervation of the secretory tissue. pVIP-specific staining could be abolished by preabsorption of the antiserum with peptide extracts of salt-gland tissue. Synthetic pVIP and endogenous VIP from salt glands of the duck co-eluted on the HPLC system, suggesting structural similarity of the peptides. Membrane-binding studies with radioiodinated pVIP revealed the presence of high-affinity binding sites in salt-gland tissue. Affinities of unlabeled pVIP analogues to compete for these binding sites were as follows: pVIP > PHI > pVIP antagonist > secretin > pVIP (10–28) > chicken VIP (16–28). Peptide extracts of salt glands had affinities similar to pVIP. Binding sites could be localized mainly at the apical end of the radially arranged secretory tubules, as demonstrated by receptor autoradiography.

It is concluded that, in addition to the classical parasympathetic transmitter acetycholine, VIP serves as neuromodulator/transmitter in cranial parasympathetic control of avian salt-gland secretion by acting on both the arteriolar network and the secretory tubules of the gland.

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References

  • Ash RW, Pearce JW, Silver A (1969) An investigation of the nerve supply to the salt gland of the duck. QJ Exp Physiol 54:281–295

    Google Scholar 

  • Bartfai T (1985) Presynaptic aspects of the coexistence of classical neurotransmitters and peptides. TIPS 331–334

  • Borut A, Schmidt-Nielsen K (1963) Respiration of avian salt-secreting gland in tissue slice experiments. Am J Physiol 204(4): 573–581

    Google Scholar 

  • Burger JW, Hess WH (1960) Function of the rectal gland in the spiny dogfish. Science 131:670–671

    Google Scholar 

  • DeLean A, Hancock AA, Lefkowitz RJ (1982) Validation and tatistical analysis of a computer modeling method for quantitative analysis of radioligand binding data for mixtures of pharmacological receptor subtypes. Mol Pharmacol 21:5–16

    Google Scholar 

  • Dimaline R, Thorndyke MC, Young J (1986) Isolation and partial purification of elasmobranch VIP. Regul Pept 14:1–10

    Google Scholar 

  • Du BH, Eng J, Hulmes JD, Chang M, Pan YCE, Yalow RS (1985) Guinea pig has a unique mammalian VIP. Biochem Biophys Res Com 128:1093–1098

    Google Scholar 

  • Dunson WA (1969) Reptilian salt glands. In: Botelho SY, Brooks FD, Shelley WB (eds) The exocrine glands. University of Philadelphia Press, Philadelphia, pp 83–103

    Google Scholar 

  • Ernst SA, Ellis RA (1969) The development of surface specialization in the secretory epithelium of the avian salt gland in response to osmotic stress. J Cell Biol 40:305–321

    Google Scholar 

  • Fänge R, Schmidt-Nielsen K, Robinson M (1958) Control of secretion from the avian salt gland. Am J Physiol 195(2): 321–326

    Google Scholar 

  • Gerstberger R, Simon-Oppermann C, Kaul R (1984) Cephalic osmoreceptor control of salt gland activation and inhibition in the salt adapted duck. J Comp Physiol 154:449–456

    Google Scholar 

  • Gerstberger R, Healy DP, Hammel HT, Simon E (1987) Autoradiographic localization and characterization of circumventricular angiotensin II receptors in duck brain. Brain Res 400:165–170

    Google Scholar 

  • Gespach C, Hoa DHB, Rosselin G (1983) Regulation by vasoactive intestinal peptide, histamine, somatostatin-14 and -28 of cyclic adenosine monophosphate levels in gastric glands isolated from the guinea pig fundus or antrum. Endocrinology 112:1597–1606

    Google Scholar 

  • Gray DA, Simon E (1983) Mammalian and avian antidiuretic hormone: Studies related to possible species variations in osmoregulatory systems. J Comp Physiol 151:241–246

    Google Scholar 

  • Gray DA, Simon E (1985) Control of plasma angiotensin II in a bird with salt glands (Anas platyrhynchos). Gen Comp Endocr 60:1–13

    Google Scholar 

  • Hakansson CH, Malcus B (1969) Secretive response of the electrically stimulated nasal salt gland in Larus argentatus (Herring gull). Acta Physiol Scand 76:385–392

    Google Scholar 

  • Hermann K, Lang RE, Unger T, Bayer C, Ganten D (1984) Combined high-performance liquid chromatography-radioimmunoassay for the characterization and quantitative measurement of neuropeptides. J Chromatogr 312:273–284

    Google Scholar 

  • Hootman SR, Ernst SA (1982) 3H-QNB binding to muscarinic receptors in intact avian salt gland cells. Am J Physiol 243:C254-C261

    Google Scholar 

  • Johansson O, Lundberg JM (1981) Ultrastructural localization of VIP-like immunoreactivity in large dense-core vesicles of ‘cholinergic-type’ nerve terminals in cat exocrine glands. Neuroscience 6:847–862

    Google Scholar 

  • Kaul R, Gerstberger R, Meyer JU, Simon E (1983) Salt gland blood flow in saltwater-adapted Pekin ducks: Microsphere measurements of the proportionality to secretion rate and investigation of controlling mechanisms. J Comp Physiol 149:457–462

    Google Scholar 

  • Krejs GJ (1982) Effect of VIP infusion on water and electrolye transport in the human intestine. In: Said SI (ed) Vasoactive intestinal polypeptide. Advances in Peptide Hormone Research Series. Raven Press, New York, pp 193–200

    Google Scholar 

  • Kühnel W (1972) On the innervation of the salt gland. Z Zellforsch 134:435–438

    Google Scholar 

  • Laburthe M, Breant B, Rouyer-Fessard C (1984) Molecular identification of receptors for vasoactive intestinal peptide in rat intestinal epithelium by covalcnt crosslinking. Eur J Biochem 139:181–187

    Google Scholar 

  • Leroux P, Vaudry H, Fournier A, St.-Pierre S, Pelletier G (1984) Characterization and localization of vasoactive intestinal peptide receptors in rat lung. Endocrinology 114:1506–1512

    Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Lowy RJ, Dawson DC, Ernst SA (1985) Primary culture of duck salt gland II. Neurohumoral stimulation of active transport. Am J Physiol 249:C41-C47

    Google Scholar 

  • Lundberg JM (1981) Evidence for coexistence of vasoactive intestinal polypeptide (VIP) and acetylcholine in neurons of cat exocrine glands. Acta Phys Scand [Suppl] 496:1–57

    Google Scholar 

  • Lundberg JM, Hökfeld T, Schultzberg M, Uvnäs-Wallensten K, Köhler C, Said SI (1979) Occurrence of vasoactive intestinal polypeptide (VIP)-like immunoreactivity in certain cholinergic neurons of the cat: evidence from combined immunohistochemistry and acetylcholinesterase staining. Neuroscience 4:1539–1559

    Article  CAS  PubMed  Google Scholar 

  • Lundberg JM, Angard A, Fahrenkrug J, Hökfelt T, Mutt V (1980) Vasoactive intestinal polypeptide in cholinergic neurons of exocrine glands: Functional significance of coexisting transmitters for vasodilation and secretion. Proc Natl Acad Sci USA 77:1651–1655

    Google Scholar 

  • Mutt V (1982) Isolation and structure of vasoactive intestinal polypeptide from various species. In: Said SI (ed) Vasoactive intestinal peptide. Advances in Peptide Hormone Research Series. Raven Press, New York, pp 1–10

    Google Scholar 

  • Pandol SJ, Dharmsathaphorn K, Schoeffield MS, Vale W, Rivier J (1986) Vasoactive intestinal peptide receptor antagonist (4ClD-Phe6, Leu17)-VIP. Am J Physiol 250:G553-G557

    Google Scholar 

  • Polak JM, Bloom SR (1982) Distribution and tissue localization of VIP in the central nervous system and in seven peripheral organs. In: Said SI (ed) Vasoactive intestinal peptide. Advances in Peptide Hormone Research Series. Raven Press, New York, pp 107–120

    Google Scholar 

  • Raufman JP, Eng J, Du BH, Straus E, Yalow RS (1986) Comparison of mammalian VIP bioactivities in dispersed acini from guinea pig pancreas. Regul Pept 14:93–97

    Google Scholar 

  • Rössler W, Pierau F-K, Harti G (1987) Distribution of substance P and calcitonin gene related peptide in the spinal cord of pigeons and rats. Pflügers Arch [Suppl] 408:R61

    Google Scholar 

  • Said SI (1982) Vasodilator action of VIP: Introduction and general considerations. In: Said SI (ed) Vasoactive intestinal peptide. Advances in Peptide Hormone Research Series. Raven Press, New York, pp 145–148

    Google Scholar 

  • Schmidt-Nielsen K (1960) The salt secreting gland of marine birds. Circulation 21:955–967

    Google Scholar 

  • Solomon R, Taylor M, Stoff JS, Silva P, Epstein FH (1984) In vivo effect of volume expansion on rectal gland function. I. Humoral factors. Am J Physiol 246:R63-R66

    Google Scholar 

  • Stoff JS, Silva P, Epstein FH (1982) Effect of VIP on active chloride transport in the shark rectal gland. In: Said SI (ed) Vasoactive intestinal peptide. Advances in Peptide Hormone Research Series. Raven Press, New York, pp 223–230

    Google Scholar 

  • Sternberger L (1979) Immunocytochemistry, 2nd ed. John Wiley & Sons, New York

    Google Scholar 

Download references

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  1. Max-Planck-Institute of Physiological and Clinical Research, W.G. Kerckhoff Institute, Bad Nauheim, Federal Republic of Germany

    Rüdiger Gerstberger

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Gerstberger, R. Functional vasoactive intestinal polypeptide (VIP)-system in salt glands of the Pekin duck. Cell Tissue Res. 252, 39–48 (1988). https://doi.org/10.1007/BF00213824

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