Skip to main content
SpringerLink
Log in

Delta-Opioid Receptor mRNA Expression and Immunohistochemical Localization in Porcine Ileum

  • Published:
Digestive Diseases and Sciences Aims and scope Submit manuscript

Abstract

Opiates have potent antidiarrheal actions thatare mediated in part by delta-opioid receptors (DOR). Weexamined DOR localization within subregions of porcineileum, a tissue analogous to human small bowel. A partial cDNA sequence for porcine DOR wasobtained after reverse transcription-polymerase chainreaction cloning of forebrain RNA; it encoded the end oftransmembrane domain 1 through the beginning of transmembrane domain 7 and exhibited 93%nucleotide identity with human DOR. Positive signals forDOR mRNA were found in all subregions of the porcineileal wall. With an antiserum recognizing an N-terminal epitope in murine DOR, DOR-likeimmunoreactivity was localized in neurons withinmyenteric and submucous ganglia, longitudinal andcircular smooth muscle, and villous lamina propria. TheDOR agonist [D-Ser2, Leu5, Thr6]enkephalin(DSLET) attenuated circular smooth muscle contractionsin porcine ileum that were evoked by electricalstimulation of myenteric cholinergic neurons. Theseresults are consistent with previous reports of the DOR-mediatedneuromodulation that underlies the antipropulsive andantisecretory effects of opioids in the intestinaltract.

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

  1. Brown DR: Antidiarrheal drugs: pharmacologic control of intestinal hypersecretion. InPrinciples of Pharmacology: Basic Concepts and Clinical Applications. PL Munson (ed). New York, Chapman and Hall, 1995, pp 1083-1091

    Google Scholar 

  2. De Luca A, Coupar IM: Insights into opioid action in the intestinal tract. Pharmacol Ther 69:103-115, 1996

    PubMed  Google Scholar 

  3. Paton WDM: The action of morphine and related substances on contraction and on acetylcholine output of coaxially stimulated guinea-pig ileum. Br J Pharmacol 11:119 -127, 1957

    Google Scholar 

  4. Pert CB, Snyder SH: Opiate receptor: demonstration in nervous tissue. Science 179:1011-1014, 1973

    PubMed  Google Scholar 

  5. Hancock DL, Coupar IM: Evidence for functional d-opiate receptors in the rat intestine. J Pharm Pharmacol 46:805-808, 1994

    PubMed  Google Scholar 

  6. Fox-Threlkeld JET, Daniel EE, Christnick F, Hruby VJ, Cipris S, Woskowska Z: Identification of the mechanisms and sites of actions of mu and delta opioid receptor activation in the canine intestine. J Pharmacol Exp Ther 268:689 -700, 1994

    PubMed  Google Scholar 

  7. Bauer AJ, Szurszewski JH: Effect of opioid peptides on circular muscle of canine duodenum. J Physiol (London) 434:409 -422, 1991

    Google Scholar 

  8. Bauer AJ, Sarr MG, Szurszewski JH: Opioids inhibit neuromuscular transmission in circular muscle of human and baboon jejunum. Gastroenterology 101:970 -976, 1991

    PubMed  Google Scholar 

  9. Kachur JF, Miller RJ: Characterization of the opiate receptor in the guinea-pig ileal mucosa. Eur J Pharmacol 81:177-183, 1982

    PubMed  Google Scholar 

  10. Sheldon RJ, Rivière PJM, Malarchik ME, Mosberg HI, Burks TF, Porreca F: Opioid regulation of mucosal ion transport in the mouse isolated jejunum. J Pharmacol Exp Ther 253:144 - 151, 1990

    PubMed  Google Scholar 

  11. Egan TM, North RA: Both µ and δ opiate receptors exist on the same neuron. Science 214:923-924, 1981

    PubMed  Google Scholar 

  12. Galligan JJ: Peptides and enteric neural activity. InGastrointestinal Regulatory Peptides. DR Brown (ed). Heidelberg, Springer-Verlag, 1993, pp 253-276

  13. Nishimura E, Buchan AMJ, McIntosh CHS: Autoradiographic localization of m-and d-type opiate receptors in the gastrointestinal tract of the rat and guinea pig. Gastroenterology 91:1084 -1094, 1986

    PubMed  Google Scholar 

  14. Allescher HD, Ahmad S, Kostka P, Kwan CY, Daniel EE: Distribution of opioid receptors in canine small intestine: Implications for function. Am J Physiol 256:G966 -G974, 1989

    PubMed  Google Scholar 

  15. Ahmad S, Allescher HD, Manaka H, Manaka Y, Daniel EE: Biochemical studies on opioid and a 2-adrenergic receptors in canine submucosal neurons. Am J Physiol 256:G957-G965, 1989

    PubMed  Google Scholar 

  16. Kararli TT: Comparison of the gastrointestinal anatomy, physiology, and biochemistry of humans and commonly used laboratory animals. Biopharm Drug Disp 16:351-380, 1995

    Google Scholar 

  17. Malmfors G, Leander S, Brodin E, Håkanson R, Holmin T, Sundler F: Peptide-containing neurons intrinsic to the gut wall. An experimental study in the pig. Cell Tissue Res 214:225-238, 1981

    PubMed  Google Scholar 

  18. Scheuermann DW, Stach W: A simultaneous demonstration of particular ente ric neuronal cell type s with the NADH: Nitro BT-dehydrogenase reaction and of nerve fibres containing enkephalin-like immunoreactivity in the myenteric plexus of the porcine small intestine. Histochemistry 82:269 -273, 1985

    PubMed  Google Scholar 

  19. Scheuermann DW, Stach W: NADH-de hydrogenase reaction in combination with immunoperoxidase (PAP) staining for light microscopic observation on the interneuronal relations of the enteric nervous system of the pig. Acta Anat 124:31-34, 1985

    PubMed  Google Scholar 

  20. Timmermans JP, Scheuermann DW, Stach W, Adriaensen D, De Groodt-Lasseel MHA: Distinct distribution of CGRP-, enkephalin-, galanin-, neuromedin U-, neuropeptide Y-, somatostatin-, substance P-, VIP-, and serotonin-containing neurons in the two submucosal ganglionic neural networks of the porcine small intestine. Cell Tissue Res 260:367-379, 1990

    PubMed  Google Scholar 

  21. Quito FL, Brown DR: Neurohormonal regulation of ion transport in the porcine distal jejunum. Enhanceme nt of sodium and chloride absorption by submucosal opiate receptors. J Pharmacol Exp Ther 256:833-840, 1991

    PubMed  Google Scholar 

  22. Brown DR, Osinski MA, Kowalski TR, Poonyachoti S, Pampusch MS, Murtaugh MP: Functional modulation of the porcine small intestine: effects of opioids and characteristics of enteric opioid receptors. InAdvances in Swine in Biomedical Research, Vol 1, M Tumbleson, LB Schook (eds). New York, Plenum Press, 1997, pp 79 -87

    Google Scholar 

  23. Arviddson U, Dado RJ, Riedl M, Lee J-H, Law PY, Loh HH, Elde R, Wessendorf MW: d-Opioid receptor immunore activity: Distribution in brainstem and spinal cord, and relationship to biogenic amines and enkephalin. J Neurosci 15:1215-1235, 1995

    PubMed  Google Scholar 

  24. Chomczynski P, Sacchi N: Single-step method of RNA isolation by acid guanidinium thiocyanate -phenol-chloroform extraction. Anal Biochem 162:156 -159, 1987

    Article  PubMed  Google Scholar 

  25. Simonin F, Befort K, Gavé riaux-Ruff C, Matthes H, Nappey V, Lannes B, Micheletti G, Kieffer B: The human d-opioid receptor: Genomic organization, cDNA cloning, functional expression, and distribution in human brain. Mol Pharmacol 46:1015- 1021, 1994

    PubMed  Google Scholar 

  26. Evans CJ, Keith DE Jr, Morrison H, Magendzo K, Edwards RH: Cloning of a delta opioid receptor by functional expression. Science 258:1952-1955, 1992

    PubMed  Google Scholar 

  27. Kieffer BL, Befort K, Gavé riaux-Ruff C, Hirth CG: The d-opioid receptor: Isolation of a cDNA by expression cloning and pharmacological characterization. Proc Natl Acad Sci USA 89:12048 -12052, 1992

    PubMed  Google Scholar 

  28. Yasuda K, Raynor K, Kong H, Breder CD, Takeda J, Reisine T, Bell GI: Cloning and functional comparison of К and δ opioid receptors from mouse brain. Proc Natl Acad Sci USA 90:6736 -6740, 1993

    PubMed  Google Scholar 

  29. Knapp RJ, Malatynska E, Collins N, Fang L, Wang JY, Hruby VJ, Roeske WR, Yamamura HI: Molecular biology and pharmacology of cloned opioid receptors. FASEB J 9:516 -525, 1995

    PubMed  Google Scholar 

  30. Brown DR, Terris JM: Swine in physiological and pathophysiological research. InAdvances in Swine in Biomedical Re search, Vol 1. M Tumbleson, LB Schook (eds). New York, Plenum Press, 1996, pp 5-6

    Google Scholar 

  31. Fukuda K, Kato S, Mori K, Nishi M, Takeshima H: Primary structures and expression from cDNAs of rat opioid δ-and µ-subtypes. FEBS Lett 327:311-314, 1993

    PubMed  Google Scholar 

  32. Zaki PA, Bilsky EJ, Vanderah TW, Lai J, Evans CJ, Porreca F: Opioid receptor types and subtypes: The d receptor as a model. Annu Rev Pharmacol Toxicol 36:379 -401, 1996

    PubMed  Google Scholar 

  33. Chuang LF, Chuang TK, Killam KF Jr, Chuang AJ, Kung H, Yu L, Chuang RY: Delta opioid receptor gene expression in lymphocytes. Biochem Biophys Res Commun 202:1291-1299, 1994

    PubMed  Google Scholar 

  34. Gavé riaux C, Peluso J, Simonin F, Laforet J, Kieffer B: Identi fication of k-and d-opioid receptor transcripts in immune cells. FEBS Lett 369:272-276, 1995

    Article  PubMed  Google Scholar 

  35. Wick MJ, Minnerath SR, Roy S, R amakrishnan S, Loh HH: Differential expression of opioid receptor genes in human lymphoid cell lines and peripheral blood lymphocytes. J Neuroimmunol 64:29 -36, 1996

    Article  PubMed  Google Scholar 

Download references

Authors
  1. David R. Brown
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sutthasinee Poonyachoti
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Mark A. Osinski
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Teresa R. Kowalski
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Mary S. Pampusch
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Robert P. Elde
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Michael P. Murtaugh
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Brown, D.R., Poonyachoti, S., Osinski, M.A. et al. Delta-Opioid Receptor mRNA Expression and Immunohistochemical Localization in Porcine Ileum. Dig Dis Sci 43, 1402–1410 (1998). https://doi.org/10.1023/A:1018877823534

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1018877823534

Search

Navigation