Abstract
Peptide YY (PYY) release was studied by measuring radioimmunoassayable PYY in the arterial plasma of anaesthetized rats receiving into the duodenum, ileum or colon either a complete semi-liquid meal (3 ml, 21 kJ) or elemental nutrients as isocaloric or isoosmolar solutions. PYY release induced by the intraduodenal meal peaked at 60 min and lasted more than 120 min. The integrated response of PYY over 120 min was larger when the meal was administered into the duodenum than into the ileum. The undigested meal induced no release of PYY over a 120-min period when administered into the colon. When injected into the duodenum in isocaloric amounts to the meal, glucose and amino acids led to the release of as much PYY as did the meal, whereas oleic acid led to the release of less PYY. Part of these responses were due to osmolarity, since administration of intraduodenal hyperosmolar saline led to the release of about half as much PYY as did hyperosmolar glucose. In moderate amounts, and injected as a solution isoosmolar to plasma, oleic acid was a major PYY releaser; the amounts released were at least two times larger when oleic acid was administered into the duodenum than into the ileum and colon. Isoosmolar glucose and amino acids led to the release of no PYY when injected into the duodenum, but were nearly as active as oleic acid in the colon. Short-chain fatty acids induced the release of PYY when injected into the colon, but not into the ileum. Hexamethonium suppressed PYY release induced by the intraduodenal meal, but did not change PYY release induced by glucose or oleic acid in the colon. Urethane anaesthesia did not reduce PYY release induced by the intraduodenal meal. These results suggest that two mechanisms at least contribute to PYY release in the rat. An indirect, neural mechanism, involving nicotinic synapses, is prominent in the proximal small intestine; the stimulation is transmitted to ileal and colonic L-cells by undetermined pathways, but contact of nutrients with L-cells is not needed. Another mechanism, probably direct and quantitatively smaller, occurs in the distal intestine when nutrients come into contact with the mucosa containing L-cells. Glucose, fatty acids and amino acids stimulate differentially the proximal and distal mechanisms.
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References
Adrian TE, Ferri GL, Bacarese-Hamilton AJ, Fuessl HS, Polak JM, Bloom SR (1985) Human distribution and release of a putative new gut hormone, peptide YY. Gastroenterology 89:1070–1077
Adrian TE, Savage AP, Sagor GR, Allen JM, Bacarese Hamilton AJ, Tatemoto K, Polak M, Bloom SR (1985) Effect of peptide YY on gastric, pancreatic, and biliary function in humans. Gastroenterology 89:494–499
Adrian TE, Ballantyne GH, Longo WE, Bilchik AJ, Graham S, Basson MD, Tierney RP, Modlin IM (1993) Deoxycholate is an important releaser of peptide YY and enteroglucagon from the human colon. Gut 34:1219–1224
Aponte GW, Taylor IL, Soll AH (1988) Primary culture of PYY cells from canine colon. Am J Physiol 254:G829-G836
Aponte GW, Park K, Hess R, Garcia R, Taylor IL (1989) Mealinduced peptide tyrosine tyrosine inhibition of pancreatic secretion in the rat. FASEB J 3:1949–1955
Bado A, Cloarec D, Moizo L, Laigneau JP, Bataille D, Lewin MJM (1993) Neurotensin and oxyntomodulin-(30–37) potentiate PYY regulation of gastric acid and somatostatin secretions. Am J Physiol 265:G113-G117
Ballantyne GH, Longo WE, Savoca PE, Adrian TE, Vukasin AP, Bilchik AJ, Sussman J, Modlin IM (1989) Deoxycholatestimulated release of peptide YY from the isolated perfused rabbit left colon. Am J Physiol 257:G715-G722
Bilchik AJ, Hines OJ, Adrian TE, McFadden DW, Berger JJ, Zinner MJ, Ashiley SW (1993) Peptide YY is a physiological regulator of water and electrolyte absorption in the canine small bowel in vivo. Gastroenterology 105:1441–1448
Bilski J, Hladij M, Jaworek J, Konturek SJ, Varga G (1988) Effects of peptide YY on dog and rat pancreatic secretion in vivo and in vitro. Int J Pancreatol 3:309–322
Brubaker PL (1991) Regulation of intestinal proglucagonderived peptide secretion by intestinal regulatory peptides. Endocrinology 128:3175–3182
Brubaker PL, Drucker DJ, Asa SL, Greenberg GR (1991) Regulation of peptide YY synthesis and secretion in fetal rat intestinal cultures. Endocrinology 129:3351–3358
Gomez G, Lluis F, Greeley GH, Thompson JC (1986) Bile enhances fat-stimulated release of peptide YY (abstract). Can J Physiol Pharmacol 64:37 (A)
Grandt D, Layer P, Rippel K, Schimiczek M, Kölbel C, Ahrens O, Beglinger C, Reeve JR Jr, Eysselein VE, Goebell H (1992) Peptide YY (PYY) inhibits endogenously stimulated pancreatic enzyme secretion in man (abstract). Regul Pept 40:160
Greeley GH Jr, Hill FLC, Spannagel A, Thompson JC (1987) Distribution of peptide YY in the gastrointestinal tract of the rat, dog, and monkey. Regul Pept 19:365–372
Greeley GH Jr, Hashimoto T, Izukura M, Gomez G, Jeng J, Hill FLC, Lluis F, Thompson JC (1989) A comparison of intraduodenally and intracolonically administered nutrients on the release of peptide YY in the dog. Endocrinology 125:1761–1765
Greeley GH, Jeng YJ, Gomez G, Hashimoto T, Hill FLC, Kern K, Kurosky T, Chuo HF, Thompson JC (1989) Evidence for regulation of peptide YY release by the proximal gut. Endocrinology 124:1438–1443
Guo YS, Fuljimura M, Lluis F, Tsong Y, Greeley GH, Thompson JC (1987) Inhibitory action of peptide YY on gastric acid secretion. Am J Physiol 253:G298-G302
Hashimoto Y, Sano I, Nagahata Y, Wang ZT, Itoh A, Takeda K, Ichihara T, Moritomo H, Urakawa T, Saitoh Y (1989) Inhibitory effect of peptide YY on gastric acid output in rats. Scand J Gastroenterol 24:134–137
Hosotani R, Inoue K, Kogire M, Tatemoto K, Mutt V, Suzuki T, Rayford PL, Tobe T (1989) Effect of natural peptide YY on pancreatic secretion and cholecystokinin release in conscious dogs. Dig Dis Sci 34:468–473
Jin H, Cai L, Lee K, Chang TM, Li P, Wagner D, Chey WY (1993) A physiological role of peptide YY on exocrine pancreatic secretion in rats. Gastroenterology 105:208–215
Laburthe M, Chenut B, Rouyer-Fessard C, Tatemoto K, Couvineau A, Servin A, Amiranoff B (1986) Interaction of peptide YY with rat intestinal epithelial plasma membranes: binding of the radioiodinated peptide. Endocrinology 118:1910–1917
Lluis F, Gomez G, Fujimura M, Greeley GH, Thompson JC (1988) Peptide YY inhibits pancreatic secretion by inhibiting cholecystokinin release in the dog. Gastroenterology 94: 137–144
Lluis F, Gomez G, Hashimoto T, Fujimura M, Greeley GH Jr, Thompson JC (1989) Pancreatic juice enhances fat-stimulated release of enteric hormones in dogs. Pancreas 4:23–30
Longo WE, Ballantyne GH, Savoca PE, Adrian TE, Bilchik AJ, Modlin IM (1991) Short chain fatty acids release peptide YY in the isolated rabbit distal colon. Scand J Gastroenterol 26:442–448
McFadden DW, Rudnicki M, Kuvshinoff B, Ficher JE, Ohio C (1992) Postprandial peptide YY release is mediated by cholecystokinin. Surg Gynecol Obstet 175:145–150
Miyachi Y, Jitsuishi W, Miyoshi A, Fujita S, Mizuchi A, Tatemoto K (1986) The distribution of polypeptide YY-like immunoreactivity in rat tissues. Endocrinology 118:2163–2167
Pappas TN, Debas HT, Taylor IL (1985) Peptide YY: metabolism and effect on pancreatic secretion in dogs. Gastroenterology 89:1387–1392
Pappas TN, Debas HT, Taylor IL (1986) Enterogastrone-like effect of peptide YY is vagally mediated in the dog. J Clin Invest 77:49–53
Plaisancié P, Bernard C, Chayvialle JA, Cuber JC (1993) Release of glucagon-like peptide I (GLP-I) and PYY in the isolated vascularly perfused rat colon (abstract). Gastroenterology 104:A847
Putnam WS, Liddle RA, Williams JA (1989) Inhibitory regulation of rat exocrine pancreas by peptide YY and pancreatic polypeptide. Am J Physiol 256:G698-G703
Roberge JN, Brubaker PL (1991) Secretion of proglucagonderived peptides in response to intestinal luminal nutrients. Endocrinology 128:3169–3174
Roberge JN, Brubaker PL (1993) Regulation of intestinal proglucagon-derived peptide secretion by glucose-dependent insulinotropic peptide in a novel enteroendocrine loop. Endocrinology 133: 233–240
Rudnicki M, McFadden DW, Liwnicz BH, Balasubramaniam A, Nussbaum MS, Dayal R, Fischer JE (1990) Endogenous peptide YY is dependent on jejunal exposure to gastrointestinal contents. J Surg Res 48:485–490
Tatemoto K (1982) Isolation and characterization of peptide YY (PYY), a candidate gut hormone that inhibits pancreatic exocrine secretion. Proc Natl Acad Sci USA 79:2514–2518
Taylor IL (1985) Distribution and release of peptide YY in dog measured by specific radioimmunoassay. Gastroenterology 88:731–737
Voisin T, Rouyer-Fessard C, Laburthe M (1990) Peptide YY/neuropeptide Y receptors in small intestine. Characterization, signal transduction, and expression during cell differentiation. Ann NY Acad Sci 611:343–346
Wager-Pagé SA, Ghazali B, Anderson W, Veale WL, Davison JS (1993) The peripheral modulation of duodenal and colonic motility in rats by the pancreatic polypeptide-fold family: neuropeptide Y, peptide YY, and pancreatic polypeptide. Peptides 14:153–160
Wiley JW, Lu YX, Owyang C (1991) Mechanism of action of peptide YY to inhibit gastric motility. Gastroenterology 100:865–872
Zhang T, Brubaker PL, Thompson JC, Greeley GH Jr (1993) Characterization of peptide-YY release in response to intracolonic infusion of amino acids. Endocrinology 132:553–557
Zhang T, Uchida T, Gomez G, Liuis F, Thompson JC, Greeley GH (1993) Neural regulation of peptide YY secretion. Regul Pept 48:321–328
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Fu-Cheng, X., Anini, Y., Chariot, J. et al. Peptide YY release after intraduodenal, intraileal, and intracolonic administration of nutrients in rats. Pflügers Arch. 431, 66–75 (1995). https://doi.org/10.1007/BF00374378
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DOI: https://doi.org/10.1007/BF00374378