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Periodic fluctuations of gut regulatory peptides in phase with the duodenal migrating myoelectric complex in preruminant calves: effect of different sources of dietary protein

Published online by Cambridge University Press:  09 March 2007

Romuald Zabielski ,
Claude Dardillat ,
Isabelle Le Huërou-Luron ,
Christine Bernard ,
Jean Alain Chayvialle  and
Paul Guilloteau
Romuald Zabielski
Affiliation:
Laboratoire du Jeune Ruminant, INRA, 65 rue de St Brieuc, 35042 Rennes, France Department of Animal Physiology, Warsaw Agricultural University, 02-787 Warsaw, Poland
Claude Dardillat
Affiliation:
Station de Recherches sur la Nutrition des Herbivores, INRA, Theix, 63122 Saint-Genès-Champanelle, France
Isabelle Le Huërou-Luron
Affiliation:
Laboratoire du Jeune Ruminant, INRA, 65 rue de St Brieuc, 35042 Rennes, France
Christine Bernard
Affiliation:
INSERM U45, Hôpital Edouard Herriot, 69374 Lyon, France
Jean Alain Chayvialle
Affiliation:
INSERM U45, Hôpital Edouard Herriot, 69374 Lyon, France
Paul Guilloteau*
Affiliation:
Laboratoire du Jeune Ruminant, INRA, 65 rue de St Brieuc, 35042 Rennes, France
*
*Corresponding author:Dr Paul Guilloteau, fax +33 2 99 28 53 70, email [email protected]
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Abstract

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Four preruminant calves with implanted electrodes in the duodenum and a catheter in the external jugular vein were used for investigation of plasma gut regulatory peptide profiles during different phases of migrating myoelectric complex (MMC) in the small intestine. The effects of different dietary proteins on the rhythmic activity of gut peptides and gastrointestinal motility were compared. In particular, the effects of skimmed-milk protein (retaining physiological patterns of abomasal clotting, and abomaso-intestinal digesta flow) v. fish protein (devoid of clotting activity and modifying the digesta flow) were studied. In calves fed on the milk diet, plasma concentrations of pancreatic polypeptide, motilin, secretin, cholecystokinin (CCK) and somatostatin, but not vasoactive intestinal polypeptide or gastrin, fluctuated in phase with the duodenal MMC in the preprandial period. Feeding transiently affected the intestinal MMC and abolished the peptide fluctuations in a specimen-specific manner. In contrast, calves fed on the fish-protein diet showed more profound changes in intestinal MMC. In these animals the MMC-related fluctuations were significant only for plasma CCK. In conclusion, the source of dietary protein has an impact on the physiological endocrine function of the small intestine. Observed fluctuations of plasma gut regulatory peptides seem to be secondary to duodenal motility cycles.

Keywords

Gut peptidesDuodenumMyoelectrical activityDietary protein
Type
Animal Nutrition
Information
British Journal of Nutrition , Volume 79 , Issue 3 , March 1998 , pp. 287 - 296
Copyright
Copyright © The Nutrition Society 1998

References

Chayvialle, JA, Descos, F, Bernard, C, Martin, A, Barbe, C & Parthensky, C (1978) Somatostatin in mucosa of stomach and duodenum in gastroduodenal disease. Gastroenterology 75, 13–19.Google Scholar
Chayvialle, JA, Migata, M, Rayford, PL & Thompson, JC (1980) Effects of test meal, intragastric nutrients and intraduodenal bile on plasma concentration of immunoreactive somatostatin and vasoactive intestinal peptide in dogs. Gastroenterology 79, 844–852.CrossRefGoogle ScholarPubMed
Chen, MH, Joffe, SN, Magee, DF, Murphy, RF & Naruse, S (1983) Cyclic changes of plasma pancreatic polypeptide and pancreatic secretin in fasting dogs. Journal of Physiology 341, 453–461.Google Scholar
Code, CF & Marlett, JA (1975) The interdigestive myo-electric complex of the stomach and small bowel of dogs. Journal of Physiology 246, 289–309.Google Scholar
Cuber, JC, Bernard, C, Laplace, JP & Chayvialle, JA (1985) Comparative assessment of secretin and motilin responses to graded duodenal acidification in anaesthetized pigs. Digestion 32, 35–41.Google Scholar
Cuber, JC, Bernard, C, Laplace, JP, Levenez, F & Chayvialle, JA (1986) Plasma cholecystokinin like immunoreactivity varies cyclically during the migrating myoelectric complexes in the pig. Canadian Journal of Physiology and Pharmacology 64, 45.Google Scholar
Dardillat, C (1977) Analyse électromyographique et débimètrique du transit alimentaire chez le veau nouveau-né. (Electromyo-graphic and flow measurement analysis of the alimentary flow in newborn calves). Journal of Physiology (Paris) 73, 925–944.Google Scholar
Dardillat, C & Marrero, E (1977) Etude de l'électromyogramme global chronique de la paroi intestinale du veau préruminant: migration des phases d'activité régulière et relation avec le transit (Electromyographical analysis of preruminant calf intestine. Relation between migrating activity front and transit time). Annales de Biologie Animale Biochimie Biophysique 17, 523–550.Google Scholar
Dardillat, C & Ruckebusch, Y (1973) Aspects fonctionnels de la jonction gastroduodénale chez le veau nouveau-né. (Functional characteristics of the gastroduodenal junction of the newborn calf). Annales de Recherche Vétérinaire 4, 31–56.Google Scholar
DiMagno, EP, Hendricks, JC, Go, VLW & Dozois, RR (1979) Relationships among canine fasting pancreatic and biliary secretions, pancreatic duct pressure, and duodenal phase III motor activity – Boldyreff revisited. Digestive Diseases and Sciences 24, 689–693.Google Scholar
Dockray, GJ (1994) Vasoactive intestinal polypeptide and related peptides. In Gut Peptides, pp. 447–472 [Walsh, JH and Dockray, GJ, editors]. New York: Raven Press.Google Scholar
Fioramonti, J, Bueno, L & Ruckebusch, M (1982) Blood sugar oscillations and duodenal migrating myoelectric complexes. American Journal of Physiology 242, G15–G20.Google ScholarPubMed
Girard, CL & Sissons, JW (1992) The role of migrating myoelectric complexes in the regulation of digesta transport in the preruminant calf. Canadian Journal of Physiology and Pharmacology 70, 1142–1147.Google Scholar
Guilloteau, P (1986) Digestion des protéines chez de jeune ruminant (Digestion of proteins in young ruminants). PhD Thesis, Université Pierre et Marie Curie, Paris.Google Scholar
Guilloteau, P, Corring, T, Chayvialle, JA, Bernard, C, Sissons, JW & Toullec, R (1986 a) Effects of soya protein on digestive enzymes, gut hormone and anti-soya antibody plasma levels in the preruminant calf. Reproduction, Nutrition, Development 26, 717–728.Google Scholar
Guilloteau, P, Le Huërou-Luron, I, Chayvialle, JA, Toullec, R, Zabielski, R & Blum, JW (1997) Gut regulatory peptides in young cattle and sheep. Journal of Veterinary Medicine A 44, 1–23.Google Scholar
Guilloteau, P, Paruelle, JL, Toullec, R & Mathieu, CM (1975) Utilization of protein by the preruminant fattening calf. III. Gastric emptying as affected by the substitution of milk protein by fish protein. Annales de Zootechnie 24, 243–253.Google Scholar
Guilloteau, P, Toullec, R, Grongnet, JF, Patureau-Mirand, P, Prugnaud, J & Sauvant, D (1986 b) Digestion of milk, fish and soya-bean protein in the preruminant calf: flow of digesta, apparent digestibility at the end of the ileum and amino acid composition of ileal digesta. British Journal of Nutrition 55, 571–592.Google Scholar
Guilloteau, P, Toullec, R, Patureau-Mirand, P & Prugnaud, J (1981) Importance of the abomasum in digestion in the preruminant calf. Reproduction, Nutrition, Development 21, 885–899.CrossRefGoogle ScholarPubMed
Keane, FB, DiMagno, EP & Dozois, RR (1980) Relationships among canine interdigestive exocrine pancreatic and biliary flow, duodenal motor activity, plasma pancreatic polypeptide and motilin. Gastroenterology 78, 310–316.CrossRefGoogle ScholarPubMed
Konturek, SJ, Thor, PJ, Bilski, J, Bielański, W & Laskiewicz, J (1986) Relationships between duodenal motility and pancreatic secretion in fasted and fed dogs. American Journal of Physiology 250, G570–G574.Google Scholar
Lee, KY, Shiratori, K, Chen, YF, Chang, T-M & Chey, WY (1986) A hormonal mechanism for the interdigestive pancreatic secretion in dogs. American Journal of Physiology 251, G759–G764.Google Scholar
Le Dréan, G, Le Huërou-Luron, I, Chayvialle, JA, Philouze-Romé, V, Gestin, M, Bernard, C, Toullec, R & Guilloteau, P (1997) Kinetics of pancreatic exocrine secretion and plasma gut regulatory peptide release in response to feeding in preruminant and ruminant calves. Comparative Biochemistry and Physiology 117, 245–255.CrossRefGoogle ScholarPubMed
Le Meuth, V, Philouze-Romé, V, Le Huërou-Luron, I, Formal, M, Vaysse, N, Gespach, C, Guilloteau, P & Fourmy, D (1993) Differential expression of A- and B-subtypes of cholecystoki-nin/gastrin receptors in the developing calf pancreas. Endocrinology 133, 1182–1191.CrossRefGoogle ScholarPubMed
Liddle, RA (1994) Cholecystokinin. In Gut Peptides, pp. 175–216 [Walsh, JH and Dockray, GJ, editors]. New York: Raven Press.Google Scholar
Magee, DF & Naruse, S (1983) Neural control of periodic secretion of the pancreas and the stomach in fasting dogs. Journal of Physiology 344, 153–160.CrossRefGoogle ScholarPubMed
Miazza, B, Palma, R, Lachance, JR, Chayvialle, JA, Jomard, PP & Modigliani, R (1985) Jejunal secretory effect of intraduodenal food in man: a comparison of mixed nutrients, proteins, lipids and carbohydrates. Gastroenterology 88, 1215–1222.CrossRefGoogle Scholar
Pelletier, MJ, Chayvialle, JA & Minaire, Y (1978) Uneven and transient secretin release after a liquid test-meal. Gastroenterology 75, 1124–1132.CrossRefGoogle ScholarPubMed
Pieramico, O, Dominguez-Muñoz, JE, Nelson, DK, Böck, W, Büchler, M & Malfertheiner, P (1995) Interdigestive cycling in chronic pancreatitis: altered coordination among pancreatic secretion, motility, and hormones. Gastroenterology 109, 224–230.Google Scholar
Pierzynowski, SG, Zabielski, R, Podgurniak, P, Kiela, P, Sharma, P, Weström, B, Kato, S & Barej, W (1992) Effect of reversible cold vagal blockade and atropinization on exocrine pancreatic function during liquid food consumption in calves. Journal of Animal Physiology and Animal Nutrition 67, 268–273.Google Scholar
Plaza, MA, Arruebo, MP & Murillo, MD (1996) Involvement of somatostatin, bombesin and serotonin in the origin of the migrating myoelectric complex in sheep. Life Sciences 58, 2155–2165.Google Scholar
Qvist, N, Øster-Jørgensen, E, Rasmussen, L, Pedersen, SA, Olsen, O, Cantor, P & Schaffalitzky de Muckadell, OB (1990) Cholecystokinin, secretin, pancreatic polypeptide in relation to gallbladder dynamics and gastrointestinal interdigestive motility. Digestion 45, 130–137.CrossRefGoogle ScholarPubMed
Reid, AM, Shulkes, A & Titchen, DA (1988) Effects of the vagus nerves on gastric motility and release of vasoactive intestinal polypeptide in the anaesthetized lamb. Journal of Physiology 396, 11–24.CrossRefGoogle ScholarPubMed
Ruckebusch, Y (1970) The electrical activity of the digestive tract of the sheep as an indication of the mechanical events in various regions. Journal of Physiology 210, 857–882.Google Scholar
Ruckebusch, Y & Bueno, L (1973) The effect of weaning on the motility of the small intestine in the calf. British Journal of Nutrition 30, 491–499.Google Scholar
Schwartz, TW (1983) Pancreatic polypeptide: a hormone under vagal control. Gastroenterology 85, 1411–1425.CrossRefGoogle ScholarPubMed
Schwartz, TW, Stenquist, B, Olbe, L & Stadil, F (1979) Synchronous oscillations in the basal secretion of pancreatic polypeptide and gastric acid. Gastroenterology 76, 14–19.Google Scholar
Toullec, R (1989) Veal calves. In Ruminant Nutrition. Recommended Allowances and Feed Tables, pp. 109–119 [Jarrige, R, editor]. Paris: John Libbey Eurotext.Google Scholar
Toullec, R, Chayvialle, JA, Guilloteau, P & Bernard, C (1992) Early-life patterns of plasma gut regulatory peptide levels in calves. Effects of age, weaning and feeding. Comparative Biochemistry and Physiology 102A, 203–209.Google Scholar
Vantrappen, GR, Peeters, TL & Janssen, J (1979) The secretory component of the interdigestive migrating motor complex in man. Scandinavian Journal of Gastroenterology 14, 663–667.Google Scholar
Walsh, JH (1994) Gastrin. In Gut Peptides, pp. 75–122 [Walsh, JH and Dockray, GJ, editors]. New York: Raven Press.Google Scholar
Wang, X, Soltesz, V, Axelson, J & Anderson, R (1996) Cholecystokinin increases small intestinal motility and reduces enteric bacterial overgrowth and translocation in rats with surgically induced acute liver failure. Digestion 57, 67–72.CrossRefGoogle ScholarPubMed
Zabielski, R, Kiela, P, Leśniewska, V, Krzemiński, R, Mikolajczyk, M & Barej, W (1997) Kinetics of pancreatic juice secretion in relation to duodenal migrating myoelectric complex in preruminant and ruminant calves fed twice daily. British Journal of Nutrition 78, 427–442.Google Scholar
Zabielski, R, Kiela, P, Onaga, T, Mineo, H, Gregory, PC & Kato, S (1995) Effects of neural blockades, gastrointestinal regulatory peptides and diversion of gastroduodenal contents on periodic pancreatic secretion in the preruminant calf. Canadian Journal of Physiology and Pharmacology 73, 1616–1624.Google Scholar
Zabielski, R, Onaga, T, Mineo, H & Kato, S (1993) Periodic fluctuations in pancreatic secretion and duodenal motility investigated in neonatal calves. Experimental Physiology 78, 675–684.Google Scholar
Zabielski, R, Terui, Y, Onaga, T, Mineo, H & Kato, S (1994) Plasma secretin fluctuates in phase with periodic pancreatic secretion and the duodenal migrating myoelectric complex in calves. Research in Veterinary Science 56, 332–337.Google Scholar
Zimmerman, DW, Saar, MG, Smith, CD, Nicholson, CP, Dalton, RR, Baar, D, Perkins, JD & DiMagno, EP (1992) Cyclic interdigestive pancreatic exocrine secretion: is it mediated by neural or hormonal mechanisms? Gastroenterology 102, 1378–1384.Google Scholar