Skip to main content

Species-specific effects of neurotensin on gallbladder contractionin vitro

Digestive Diseases and Sciences volume 34, pages 21–26 (1989)Cite this article

Abstract

We have previously shown that an in vivoadministration of neurotensin (NT) stimulates contraction of dog gallbladder (GB), but produces dilatation of GB in humans. The objective of this study was to examine the effect of NT on human, dog, guinea pig, and rabbit GB in vitro,in order to delineate direct versus indirect actions of NT in different species and to evaluate the structure-activity relationships of NT. The effect of NT on the canine sphincter of Oddi (SOD) was also examined in vitro.Isolated longitudinal strips of GB from the four species given above and SOD from dogs were suspended in oxygenated Krebs buffer, and the isometric tension responses to various doses of NT, NT 8–13, NT 1–11, and xenopsin (XP) were determined. All the NT homologs, except NT 1–11, stimulated contraction of the dog GB and SOD in a dose-dependent manner. NT also caused dose-related stimulation of GB contraction from guinea pigs but did not stimulate or depress the contractile activity of human and rabbit GB strips. These results suggest that NT action on GB contraction is species-specific. Tetrodotoxin did not modify the contraction of dog GB and SOD in response to NT, indicating that NT mediates its contractile effects directly. The relaxing effect of NT on GB of humans in vivo,as previously reported by us, thus appears to be an indirect action. The fact that structural changes in the NT molecule resulted in marked changes in the biological activity of NT on GB activity in dogs indicates that the effects of NT on dog GB contraction are probably mediated through binding of NT to specific receptors that requires both the C-terminal amino group and the two C-terminal amino acids to produce a contractile response. Based on these results, we suggest that NT may participate in the regulation of GB and SOD contraction in dogs.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

43,34 €

Price includes VAT (Finland)
Tax calculation will be finalised during checkout.

References

  1. Carraway R, Leeman SE: The isolation of a new hypotensive peptide, neurotensin, from bovine hypothalami. J Biol Chem 248:6854–6861, 1973

    PubMed  Google Scholar 

  2. Kitabgi P, Carraway R, Leeman SE: Isolation of a tridecapeptide from bovine intestinal tissue and its partial characterization as neurotensin. J Biol Chem 251:7053–7058, 1973

    Google Scholar 

  3. Hammer RA, Leeman SE, Carraway R, Williams RH: Isolation of human intestinal neurotensin. J Biol Chem 255:2476–2480, 1980

    PubMed  Google Scholar 

  4. Doyle H, Greeley GH Jr, Mate L, Sakamoto T, Townsend CM Jr, Thompson JC: Distribution of neurotensin in the canine gastrointestinal tract. Surgery 87:337–341, 1985

    Google Scholar 

  5. Helmstaedter V, Taugner CH, Feurle GE, Forssmann WG: Localization of neurotensin-immunoreactive cells in the small intestine of man and various mammals. Histochemistry 53:35–41, 1977

    PubMed  Google Scholar 

  6. Polack JM, Sullivan SN, Bloom SR, Buchan AMJ, Facer, P, Brown MR, Pearse AGE: Specific localization of neurotensin to the N cell in human intestine by radioimmunoassay and immunocytochemistry. Nature 270:183–184, 1977

    PubMed  Google Scholar 

  7. Brown DR, Miller RJ: Neurotensin. Br Med Bull 38:239–245, 1982

    PubMed  Google Scholar 

  8. Holzer P, Bucsics A, Saria A, Lembeck A: A study of the concentrations of substance P and neurotensin in the gastro-intestinal tract of various mammals. Neuroscience 7:2919–2924, 1982

    PubMed  Google Scholar 

  9. Baca I, Feurle GE, Schwab A, Mittmann U, Kna W, Lehnert T: Effect of neurotensin on exocrine pancreatic secretion in dogs. Digestion 23:174–183, 1982

    PubMed  Google Scholar 

  10. Sakamoto T, Newman J, Fujimura M, Greeley GH Jr, Townsend CM Jr, Thompson JC: Role of neurotensin in pancreatic secretion. Surgery 96:146–153, 1984.

    PubMed  Google Scholar 

  11. Hellstrom PM, Rosell S: Effects of neurotensin, substance P and methionine-enkephalin on colonic motility. Acta Physiol Scand 113:147–154, 1981

    PubMed  Google Scholar 

  12. Rossel S, Al-Saffar A, Thor K: The role of neurotensin in gut motility. Scand J Gastroenterol19:69–75, 1984

    Google Scholar 

  13. Andersson S, Chang D, Folkers K, Rosell S: Inhibition of gastric acid secretion in dogs by neurotensin. Life Sci 19:367–370, 1976

    PubMed  Google Scholar 

  14. Blackburn AM, Bloom SR, Long RG, Fletcher DR, Christofides ND, Fitzpatrick ML: Effect of neurotensin on gastric function in man. Lancet 1:987–989, 1980

    PubMed  Google Scholar 

  15. Ayers EA, Fulginiti JT, Porreca F, Peterson LJ, Shook JE, Burks TF: The effects of neurotensin on gastrointestinal motility in rodents. Proc West Pharmacol Soc 28:153–155, 1985

    PubMed  Google Scholar 

  16. Rossel S, Thor K, Nyquist O, Lewenhaupt A, Kager L, Folkers K: Plasma concentration of neurotensin-like immunoreactivity (NTLI) and lower esophageal sphincter (LES) pressure in man following infusion of (Gln4)-neurotensin. Acta Physiol Scand 109:369–375, 1980

    PubMed  Google Scholar 

  17. Sakamoto T, Mate L, Greeley GH Jr, Townsend CM Jr, Thompson JC: Effect of neurotensin on gallbladder contraction in dogs. Gastroenterology 86:1229, 1984

    Google Scholar 

  18. Fujimura M, Sakamoto T, Khalil T, Greeley GH Jr, Townsend CM Jr, Thompson JC: Physiologic role of neurotensin in gallbladder contraction in the dog. Surg Forum 35:192–194, 1984

    Google Scholar 

  19. Walker JP, Khalil T, Wiener I, Fagan CJ, Townsend CM Jr, Greeley GH Jr, Thompson JC: The role of neurotensin in human gallbladder motility. Ann Surg 201:678–683, 1985

    PubMed  Google Scholar 

  20. Berry H, Flower RJ: The assay of endogenous cholecystokinin and factors influencing its release in the dog and cat. Gastroenterology 60:409–420, 1971

    PubMed  Google Scholar 

  21. Lonovics J, Guzman S, Devitt P, Hejtmancik NE, Suddith RL, Rayford PL, Thompson JC: Release of pancreatic polypeptide in humans by infusion of cholecystokinin. Gastroenterology 79:817–822, 1980

    PubMed  Google Scholar 

  22. Toouli J, Watts JM: In-vitro motility studies on the canine and human extrahepatic biliary tracts. Aust NZ J Surg 40:380–387, 1971

    Google Scholar 

  23. Toouli J, Watts JM: Actions of cholecystokinin/pancreozymin, secretin and gastrin on extra-hepatic biliary tract motility in vitro. Ann Surg 175:439–447, 1972

    PubMed  Google Scholar 

  24. Quirion R, Regoli D, Rioux F, St-Pierre S: The stimulatory effects of neurotensin and related peptides in rat stomach strips and guinea-pig atria. Br J Pharmacol 68:83–91, 1980

    PubMed  Google Scholar 

  25. Kitabgi P, Poustis C, Granier C, van Rietschoten J, Rivier J, Morgat J-L, Freychet P: Neurotensin binding to extraneural and neural receptors: Comparison with biological activity and structure-activity relationships. Mol Pharmacol 18:11–19, 1980

    PubMed  Google Scholar 

  26. Huidobro-Toro JP, Kullak A: Excitatory neurotensin receptors on the smooth muscle of the rat fundus: Possible implications in gastric motility. Br J Pharmacol 84:897–910, 1985

    PubMed  Google Scholar 

  27. Kawanishi K, Goto A, Ishida T, Kawamura K, Nishina Y, Machida S, Yamamoto S, Ofuji T: The effects of xenopsin on endocrine pancreas and gastric antrum in dogs. Horm Metab Res 10:283–286, 1978

    PubMed  Google Scholar 

  28. Carraway R, Ruane SE, Feurle GE, Taylor S: Amphibian neurotensin (NT) is not xenopsin (XP): Dual presence of NT-like and XP-like peptides in various amphibia. Endocrinology 110:1094–1101, 1982

    PubMed  Google Scholar 

  29. Feurle GE, Baca I, Kna W, Schwab A, Araki T, Carraway R: Xenopsin stimulates exocrine pancreatic secretion in the dog. Experientia 38:679–680, 1982

    PubMed  Google Scholar 

  30. Zinner MJ, Kasher F, Modlin IM, Jaffe BM: Effect of xenopsin on blood flow, hormone release, and acid secretion. Am J Physiol 243:G195-G199, 1982

    PubMed  Google Scholar 

  31. Ishida T, Kawamura K, Goto A, Nishina Y, Takahara J, Yamamoto S, Kawanishi K, Ofuji T: Comparison studies of neurotensin and xenopsin in the dog. Metabolism 25:1467–1468, 1976

    PubMed  Google Scholar 

  32. Goedert M, Sturmey N, Williams BJ, Emson PC: The comparative distribution of xenopsin-and neurotensin-like immunoreactivity in xenopus laevis and rat tissues. Brain Res 308:273–280, 1984

    PubMed  Google Scholar 

  33. Feurle GE, Carraway R, Rix E, Kna W: Evidence for the presence of xenopsin-related peptide(s) in the gastric mucosa of mammals. J Clin Invest 76:156–162, 1985

    PubMed  Google Scholar 

Download references

Author information

Affiliations

  1. Department of Surgery, The University of Texas Medical Branch, 77550, Galveston, Texas

    Yan -Shi Guo MD, Pomila Singh PhD, James R. Upp Jr MD & James C. Thompson

Authors
  1. Yan -Shi Guo MD
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Pomila Singh PhD
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. James R. Upp Jr MD
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. James C. Thompson
    View author publications

    You can also search for this author in PubMed Google Scholar

Additional information

Supported by grants from the National Institutes of Health (R01 DK 15241, P01 DK 35608, and CA 38651).

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Guo, Y.S., Singh, P., Upp, J.R. et al. Species-specific effects of neurotensin on gallbladder contractionin vitro . Digest Dis Sci 34, 21–26 (1989). https://doi.org/10.1007/BF01536149

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01536149

Key words

  • neurotensin
  • gallbladder contraction
  • sphincter of Oddi
  • dog