Skip to main content
Log in

Distribution of PACAP (pituitary adenylate cyclase-activating polypeptide)-like and helospectin-like peptides in the teleost gut

  • Published:
Cell and Tissue Research Aims and scope Submit manuscript

Abstract

Pituitary adenylate cyclase-activating polypeptide (PACAP) and helospectin are two vasoactive intestinal polypeptide (VIP)-related neuropeptides that have recently been demonstrated in the mammalian gut; the aim of this study was to reveal their occurrence and localisation in the gastrointestinal tract, swimbladder, urinary bladder and the vagal innervation of the gut of teleosts, using immunohistochemical methods on whole-mounts and sections of these tissues from the Atlantic cod, Gadus morhua and the rainbow trout, Oncorhynchus mykiss. Both PACAP-like and helospectin-like peptides were present in the gut wall of the two species. Immunoreactive nerve fibres were found in all layers but were most frequent in the myenteric plexus and along the circular muscle fibres. Immunoreactivity was also demonstrated in nerves innervating the swimbladder wall, the urinary bladder and blood vessels to the gut. Immunoreactive nerve cell bodies were found in the myenteric plexus of the gut and in the muscularis mucosae of the swimbladder. In the vagus nerve, non-immunoreactive nerve cells were surrounded by PACAP-immunoreactive fibres. Double staining revealed the coexistence of PACAP-like and helospectin-like peptides with VIP in all visualized nerve fibres and in some endocrine cells. It is concluded that PACAP-like and helospectin-like peptides coexist with VIP in nerves innervating the gut of two teleost species. The distribution suggests that both PACAP and helospectin, like VIP, are involved in the control of gut motility and secretion.

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

  • Absood A, Chen D, Håkanson R (1992a) Neuropeptides of the vasoactive intestinal peptide/helodermin/pituitary adenylate cyclase activating peptide family elevate plasma cAMP in mice: comparison with a range of other regulatory peptides. Regul Pept 40: 311–322

    Google Scholar 

  • Absood A, Ekblad E, Ekelund M, Håkanson R, Sundler F (1992b) Helospectin-like peptides in the gastrointestinal tract: immunocytochemical localization and immunochemical characterization. Neuroscience 46: 431–438

    Google Scholar 

  • Bjenning C, Holmgren S (1988) Neuropeptides in the fish gut. A study of evolutionary trends. Histochemistry 88: 155–163

    Google Scholar 

  • Campbell RM, Scanes CG (1992) Minireview — evolution of the growth hormone-releasing factor (GRF) family of peptides. Growth Regul 2: 175–191

    Google Scholar 

  • Chartrel N, Tonon MC, Vaudry H, Conlon JM (1991) Primary structure and biological activity of pituitary adenylate cyclaseactivating polypeptide (PACAP) from frog brain. Endocrinology 129: 3367–3371

    Google Scholar 

  • Costa M, Buffa R, Furness JB, Solcia E (1980) Immunohistochemical localization of polypeptides in peripheral autonomic nerves using whole-mount preparations. Histochemistry 65: 157–165

    Google Scholar 

  • Desai H, Uddman R, Malina J, Sundler F (1992) Helospectin-like immunoreactivity in the esophagus. Regul Pept 40: 363–371

    Google Scholar 

  • Dimaline R (1989) Vasoactive intestinal peptide. In: Holmgren S (eds) The comparative physiology of regulatory peptides. Chapman and Hall, London, pp 150–173

    Google Scholar 

  • Dimaline R, Thorndyke MC (1986) Purification and characterisation of VIP from two species of dogfish. Peptides 7: 21–25

    Google Scholar 

  • Dimaline R, Young J, Thwaites DT, Lee CM, Shuttleworth TJ, Thorndyke MC (1987) A novel vasoactive intestinal peptide (VIP) from elasmobrach intestine has full affinity for mammalian pancreatic VIP receptors. Biochem Biophys Acta 930: 97–100

    Google Scholar 

  • Dockray GJ (1992) Transmission: peptides. In: Burnstock G, Hoyle CHV (eds) Autonomic neuroeffector mechanisms, Harwood Academic, Chur Reading Paris, pp 409–464

    Google Scholar 

  • Fridolf T, Sundler F, Ahrén B (1992) Pituitary adenylate cyclase-activating polypeptide (PACAP): occurrence in rodent pancreas and effects on insulin and glucagon secretion in the mouse. Cell Tissue Res 269: 275–279

    Google Scholar 

  • Gibbins IL (1990) Target-related patterns of co-existence of neuropeptide-Y, vasoactive intestinal peptide, enkephalin and substance P in cranial parasympathetic neurons innervating the facial skin and exocrine glands of guinea-pigs. Neuroscience 38: 541–560

    Google Scholar 

  • Gottschall P, Tatsuno I, Miyata A, Arimura A (1990) Characterization and distribution of binding sites for the hypothalamic peptide, pituitary adenylate cyclase-activating polypeptide. Endocrinology 127: 271–277

    Google Scholar 

  • Grundemar L, Högestätt ED (1990) Vascular effects of helodermin, helospectin I and helospectin II: a comparison with vasoactive intestinal peptide (VIP). Br J Pharmacol 99: 526–528

    Google Scholar 

  • Jensen J, Conlon JM (1992) Characterization of peptides related to neuropeptide tyrosine and peptide tyrosine-tyrosine from the brain and gastrointestinal tract of teleost fish. Eur J Biochem 210: 405–410

    Google Scholar 

  • Jensen J, Holmgren S (1994) The gastrointestinal canal. In: Nilsson S, Holmgren S (eds) Comparative physiology and evolution of the autonomic nervous system. Harwood Academic, Chur Reading Paris, [in press]

    Google Scholar 

  • Karila P, Jönsson AC, Jensen J, Holmgren S (1993) Galanin-like immunoreactivity in extrinsic and intrinsic nerves to the gut of the Atlantic cod, Gadus morhua, and the effect of galanin on the smooth muscle of the gut. Cell Tissue Res: 271: 537–544

    Google Scholar 

  • Kimura C, Ohkubo S, Ogi K, Itoh Y, Onda H, Miyata A, Jiang LD,R, Stibbs HH, Arimura A, Fujino M (1990) A novel peptide which stimulates adenylate cyclase: molecular cloning and characterization of the ovine and human cDNAs. Biochem Biophs Res Commun 166: 81–89

    Google Scholar 

  • Köves K, Arimura A, Somogyvári-Vigh A, Vigh S, Miller J (1990) Immunohistochemical demonstration of a novel hypothalamic poptide, pituitary adenylate cyclase-activating polypeptide, in the ovine hypothalamus. Endocrinology 127: 264–271

    Google Scholar 

  • Köves K, Arimura A, Vigh S, Somogyvári-Vigh A, Miller J (1993) Immunohistochemical localization of PACAP in the ovine digestive system. Peptides 14: 449–455

    Google Scholar 

  • Miyata A, Arimura A, Dahl RR, Minamino N, Uehara A, Jiang L, Culler MD, Coy DH (1989) Isolation of a novel 38 residue hypothalamic polypeptide which stimulates adenylate cyclase in pituitary cells. Biochem Biophys Res Commun 164: 567–574

    Google Scholar 

  • Miyata A, Jiang L, Dahl RR, Kitada C, Kubo K, Fujino M, Minamino N, Arimura A (1990) Isolation of a neuropeptide corresponding to the N-terminal 27 residues of the pituitary adenylate cyclase activating polypeptide with 38 residues (PACAP 38). Biochem Biophys Res Commun 170: 643–648

    Google Scholar 

  • Mungan Z, Arimura A, Ertan A, Rossowski WJ, Coy DH (1992) Pituitary adenylate cyclase-activating polypeptide relaxes rat gastrointestinal smooth muscle. Scand J Gastroenterol 25: 375–380

    Google Scholar 

  • Mutt V, Said SI (1974) Structure of the porcine vasoactive intestinal octosapeptide. The amino acid sequence. Use of kallikrein in its determination. Eur J Biochem 42: 581–589

    Google Scholar 

  • Ogi K, Kimura C, Onda H, Arimura A, Fujino M (1990) Molecular cloning and characterization of cDNA for the precursor of rat pituitary adenylate cyclase activating polypeptide (PACAP). Biochem Biophys Res Commun 173: 1271–1279

    Google Scholar 

  • Parker DS, Raufman JP, O'Donaghue TL, Bledsoe M, Yoshida H, Pisano JJ (1984) Amino acid sequences of helospectins, new members of the glucagon superfamily, found in the Gila monster venom. J Biol Chem 259: 11751–11755

    Google Scholar 

  • Said SI, Mutt V (1969) Long acting vasodilator peptide from lung tissue. Nature 224: 699–700

    Google Scholar 

  • Smart D, Johnston CF, Curry WJ, Shaw C, Halton DW, Fairweather I, Buchanan KD (1992) Immunoreactivity of two specific regions of chromogranin A in the nervous system of Ascaris suum: an immunohistochemical study. Parasitol Res 78: 329–335

    Google Scholar 

  • Sundler F, Ekblad E, Absood A, Håkanson R, Köves K, Arimura A (1992) Pituitary adenylate cyclase activating peptide: a novel vasoactive intestinal peptide-like neuropeptide in the gut. Neuroscience 46: 439–454

    Google Scholar 

  • Thwaites DT, Young J, Thorndyke MC, Dimaline R (1989) The isolation and chemical characterization of a novel vasoactive intestinal peptide-related peptide from a teleost fish, the cod, Gadus morhua. Biochim Biophys Acta 999: 217–220

    Google Scholar 

  • Vandermeers A, Vandermeers-Piret MC, Robberecht P, Waelbroeck J, Dehaye P, Winand J, Christophe J (1984) Purification of a novel pancreatic secretory factor (PSF) and a novel peptide with VIP-and secretin-like properties (helodermin) from Gila monster venom. FEBS Lett 166: 273–276

    Google Scholar 

  • Vandermeers A, Gourlet P, Vandermeers-Piret MC, Cauvin A, De Neef P, Rathe J, Svoboda M, Robberecht P, Christophe J (1987) Chemical, immunological and biological properties of peptides like vasoactive-intestinal-peptide and peptide-histidine-isoleucinamide extracted from the venom of two lizards (Heloderma horridum and Heloderma suspectum). Eur J Biochem 164: 321–327

    Google Scholar 

  • Yon L, Feuilloley M, Chartrel N, Arimura A, Conlon JM, Fournier A, Vaudry H (1992) Immunohistochemical distribution and biological activity of pituitary adenylate cyclase-activating polypeptide (PACAP) in the central nervous system of the frog Rana ridibunda. J Comp Neurol 324: 485–499

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Olsson, C., Holmgren, S. Distribution of PACAP (pituitary adenylate cyclase-activating polypeptide)-like and helospectin-like peptides in the teleost gut. Cell Tissue Res 277, 539–547 (1994). https://doi.org/10.1007/BF00300227

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00300227

Key words

Navigation