Skip to main content
SpringerLink
Log in

Area Postrema Lesion Alters the Effects of Peptide YY on 2-DG-Stimulated Pancreatic Exocrine Secretion

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

Abstract

Previously we demonstrated that circulating peptide YY (PYY), which inhibits pancreatic exocrine secretion, binds to specific receptors in the area postrema (AP); therefore we have tested the hypothesis that the removal of the AP (APX) will alter the effects of PYY on pancreatic secretion in awake rats. One-month after AP lesion or sham lesion, rats were implanted with pancreatic, biliary, duodenal, and intravenous catheters. After recovery from the surgery, unanesthetized rats were infused with vehicle or PYY (30 pmol/kg/hr or 100 pmol/kg/hr) under basal or 2-deoxy-d-glucose (2-DG) stimulated (75 mg/kg, intravenous bolus) conditions. PYY at 30 pmol/kg/hr inhibited basal pancreatic fluid secretion in sham-operated rats, but not APX rats. PYY at 100 pmol/kg/hr stimulated basal pancreatic protein secretion in sham-operated rats, and this effect was also lost in APX rats. PYY at 30 and 100pmol/kg/hr inhibited peak 2-DG stimulated protein secretion to a greater extent in APX rats as compared to sham-operated rats (P < 0.05). Since PYY inhibition of basal pancreatic secretion is AP dependent and inhibition of 2-DG stimulated pancreatic secretion is AP independent, we conclude that the 2-DG pathway of pancreatic secretion differs from the pathway responsible for basal secretion, and that APX potentiates the inhibitory effect of PYY on the 2-DG pathway.

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. Whitcomb DC: Neuroendocine control of the exocrine pancreas. In GHJ Greeley (ed). Gastrointestinal Endocrinology. Totowa, New Jersey, Humana Press, 1999, pp:243–263

    Google Scholar 

  2. Owyang C: Physiological mechanisms of cholecystokinin action on pancreatic secretion. Am J Physiol 271:G1–G7, 1996

    Google Scholar 

  3. Solomon TE, Walsh JH, Bussjaeger L, Zong Y, Hamilton JW, Ho FJ, Lee TD, Reeve JR Jr: COOH-terminally extended secretins are potent stimulants of pancreatic secretion. Am J Physiol 276:G808–G816, 1999

    Google Scholar 

  4. Deng X, Whitcomb DC: Neurohormonal control of the exocrine pancreas. Curr Opinion Gastroenterol 14:362–368, 1998

    Google Scholar 

  5. Taylor IL, Solomon TE, Walsh JH, Grossman MI: Pancreatic polypeptide. Metabolism and effect on pancreatic secretion in dogs. Gastroenterology 76:524–528, 1979

    Google Scholar 

  6. Greeley GHJ, Jeng YJ, Gomez G, Hashimoto T, Hill FLC, Kern K, Kurosky T, Chuo HF, Thompson JC: Evidence for regulation of peptide YY release by the proximal gut. Endocrinology 124:1438–1443, 1989

    Google Scholar 

  7. Aponte GW, Park K, Hess R, Garcia R, Taylor IL: Mealinduced peptide tyrosine tyrosine inhibition of pancreatic secretion in the rat. FASEB J 3:1949–1955, 1989

    Google Scholar 

  8. Teyssen S, Grandt D, Niebergall-Roth E, Schimiczek M, Goebell H, Eysselein VE, Reeve JR Jr Singer MV: Inhibition of canine exocrine pancreatic secretion by peptide YY is mediated by PYY-preferring Y2 receptors. Pancreas 13:80–88, 1996

    Google Scholar 

  9. Hernandez EJ, Whitcomb DC, Vigna SR, Taylor IL: Saturable binding of circulating peptide YY in the dorsal vagal complex of rats. Am J Physiol 266:G511–G516, 1994

    Google Scholar 

  10. Goumain M, Voisin T, Lorinet AM, Laburthe M: Identification and distribution of mRNA encoding the Y1, Y2, Y4, and Y5 receptors for peptides of the PP-fold family in the rat intestine and colon. Biochem Biophys Res Commun 247: 52–56, 1998

    Google Scholar 

  11. Louie DS, Williams JA, Owyang C: Action of pancreatic polypetide on rat pancreatic secreton: In vivo and in vitro. Am J Physiol 249:G489–G495, 1985

    Google Scholar 

  12. Guarita DR, Deng X, Huh YB, Wood PG, Reeve JR Jr, Whitcomb DC: PYY regulates pancreatic exocrine secretion through multiple receptors in the awake rat. Dig Dis Sci 45:1696–1702, 2000

    Google Scholar 

  13. Kalia M, Sullivan JM: Brainstem projections of sensory and motor components of the vagus nerve in the rat. J Comp Neurol 211:248–265, 1982

    Google Scholar 

  14. Whitcomb DC, Taylor IL, Vigna SR: Characterization of saturable binding sites for circulating pancreatic polypeptide in rat brain. Am J Physiol 260:G687–G691, 1990

    Google Scholar 

  15. Whitcomb DC, Puccio AM, Vigna SR, Taylor IL, Hoffman GE: Distribution of pancreatic polypeptide receptors in the rat brain. Brain Res 760:137–149, 1997

    Google Scholar 

  16. Whitcomb DC, Yin M, Curtis J, Puccio A, Reeve J, Sved AF: Centrally mediated pancreeatic secretion is stimulated through the Y1 receptor and inhibited through Y2 receptor. Gastroenterol 108:A400, 1995

    Google Scholar 

  17. Deng X, Guarita DR, Kreiss C, Wood PG, Pedroso MAR, Sved AF, Whitcomb DC: PYY inhibits CCK-stimulated pancreatic secretion through the Area Postrema in unanesthetized rats. Am J Physiol 281:R645–R653, 2001

    Google Scholar 

  18. Curtis KS, Huang W, Sved AF, Verbalis JG, Stricker EM: Impaired osmoregulatory responses in rats with area postrema lesions. Am J Physiol 277:R209–R219, 1999

    Google Scholar 

  19. Jin H, Cai L, Lee K, Chang TM, Li P, Wagner D, Chey WY: A physiological role of peptide YY on exocrine pancreatic secretion in rats. Gastroenterol 105:208–215, 1993

    Google Scholar 

  20. Rinaman L, Miselis RR: The organization of vagal innervation of rat pancreas using cholera toxin-horseradish peroxidase conjugate. J Auton Nerv Syst 21:109–125, 1987

    Google Scholar 

  21. Putnam WS, Liddle RA, Williams JA: Inhibitory regulation of rat exocrine pancreas by peptide YY and pancreatic polypeptide. Am J Physiol 256:G698–G703, 1989

    Google Scholar 

  22. Adrian TE, Savage AP, Sagor GR, Allen JM, Bacarese-Hamilton AJ, Tatemoto K, Polak JM, Bloom SR: Effect of peptide YY on gastric, pancreatic, and biliary function in humans. Gastroenterol 89:494–499, 1985

    Google Scholar 

  23. Pappas TN, Debas HT, Goto Y, Taylor IL: Peptide YY inhibits meal-stimulated pancreatic and gastric secretion. Am J Physiol 248:G118–G123, 1985

    Google Scholar 

  24. Tohno H, Sarr MG, DiMagno EP: Intraileal carbohydrate regulates canine postprandial pancreaticobiliary secretion and upper gut motility. Gastroenterol 109:1977–1985, 1995

    Google Scholar 

  25. Holst JJ, Rasmussen TN, Harling H, Schmidt P: Effect of intestinal inhibitory peptides on vagally induced secretion from isolated perfused porcine pancreas. Pancreas 8:80–87, 1993

    Google Scholar 

  26. Sheikh SP, Roach E, Fuhlendorff J, Williams JA: Localization of Y1 receptors for NPY and PYY on vascular smooth muscle cells in rat pancreas. Am J Physiol 260:G250–G257, 1991

    Google Scholar 

  27. Roze C, de La Tour J, Chariot J, Souchard M, Vaille C, Debray C: Pancreatic stimulation by 2-deoxy-D-glucose in the rat: A study of neural and hormonal mechanism. Gastroenterol Clin Biol 1:435–446, 1977

    Google Scholar 

  28. Kobashi M, Adachi A: Effect of topical administration of glucose on neurons innervating abdominal viscera in dorsal motor nucleus of vagus in rats. Jpn J Physiol 44:729–734, 1994

    Google Scholar 

  29. Masuda M, Kanai S, Miyasaka K: Central somatostatin prevents vagal efferent nerve excitation produced by TRH but not by 2-deoxy-D-glucose. Am J Physiol 272:G351–G356, 1997

    Google Scholar 

  30. Deng X, Guarita DR, Wood PG, Kreiss C, and Whitcomb DC: PYY potently inhibits pancreatic exocrine secretion mediated through CCK-secretin-stimulated pathways but not 2-DG stimulated pathways in awake rats. Dig Dis Sci 46:156–165, 2001

    Google Scholar 

  31. Konturek SJ, Bilski J, Pawlik W, Tasler J, Domschke W: Adrenergic pathway in the inhibition of pancreatic secretion by peptide YY in dogs. Gastroenterol 94:266–273, 1988

    Google Scholar 

  32. Nagain C, Chariot J, Roze C: Differential effects of peptide YY, neuropeptide Y, and sigma ligands on neurally stimulated external pancreatic secretion in the rat. Pancreas 10:123–130, 1995

    Google Scholar 

  33. Yang H, Kawakubo K, Tache Y: Intracisternal PYY increases gastric mucosal resistance: Role of cholinergic, CGRP, and NO pathways. Am J Physiol 277:G555–G562, 1999

    Google Scholar 

  34. Ericsson A, Arias C, Sawchenko PE: Evidence for an intramedullary prostaglandin-dependent mechanism in the activation of stress-related neuroendocrine circuitry by intravenous interleukin-1. J Neurosci 17:7166–7179, 1997

    Google Scholar 

  35. Deng X, Wood PG, Sved AF, Whitcomb DC: The area postrema lesions alter the inhibitory effects of peripherally infused pancreatic polypeptide on pancreatic secretion. Brain Res 902:18–29, 2001

    Google Scholar 

  36. Okumura TP, Pappas TN, Taylor IL: Pancreatic polypeptide microinjection into the dorsal motor nucleus inhibits pancreatic secretion in rats. Gastroenterol 108:1517–1525, 1995

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Medicine, University of Pittsburgh, Pittsburgh, Pennsylvania, USA

    Xiaoying Deng, Dulce R. Guarita, Martha R.A. Pedroso, Paul G. Wood & Christianna Kreiss

  2. Department of Neuroscience, University of Pittsburgh, Pittsburgh, Pennsylvania, USA

    Alan F. Sved

  3. Department of Medicine and Pittsburgh VAMC, University of Pittsburgh, Pittsburgh, Pennsylvania, USA

    David C. Whitcomb

Authors
  1. Xiaoying Deng
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Dulce R. Guarita
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Martha R.A. Pedroso
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Paul G. Wood
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Christianna Kreiss
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Alan F. Sved
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. David C. Whitcomb
    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

Deng, X., Guarita, D.R., Pedroso, M.R. et al. Area Postrema Lesion Alters the Effects of Peptide YY on 2-DG-Stimulated Pancreatic Exocrine Secretion. Dig Dis Sci 46, 2460–2469 (2001). https://doi.org/10.1023/A:1012380004736

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1012380004736

Search

Navigation