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Cholecystokinin-dependent selective inhibitory effect on ‘minute rhythm’ in the ovine small intestine

Published online by Cambridge University Press:  19 November 2008

K. W. Romański
K. W. Romański*
Affiliation:
Department of Animal Physiology, Veterinary School, Wrocław University of Environmental and Life Sciences, Norwida 31, 50-375 Wrocław, Poland
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Abstract

Cholecystokinin (CCK) can exert multiple actions on intestinal motility but its effect on the small-intestinal ‘minute rhythm’ (MR) is virtually unknown. Therefore, the electrical activity from the abomasal antrum, duodenal bulb, duodenum, jejunum and ileum was continuously recorded in six sheep before, during and after slow intravenous administration, of three doses each, of cholecystokinin-octapeptide (CCK-OP) and cerulein. In four of these sheep, two additional electrodes and the strain gauge force transducer were also inserted in the duodenum. Chronic experiments were performed in the fasted and non-fasted animals and saline or CCK peptides were injected during phases 1, 2a or 2b of the duodenal migrating myoelectric complex (MMC). The administration of both CCK peptides in various doses evoked an inhibitory effect mostly in the duodenal bulb, except for the lowest dose of cerulein. The effects of 20 times greater doses of CCK-OP than that of cerulein were more pronounced. The introduction of both CCK peptides during phase 1 of the MMC produced no marked or significant response. In non-fasted animals, the effects of both hormonal peptides, given during phase 2b of the MMC, were often stronger than those given during phase 2a, while in fasted animals the effects of CCK peptides, administered in the course of phases 2a and 2b of the MMC, were similar. Both higher doses of CCK peptides increased the number of spike bursts within the given MR pattern in the duodenum and decreased the incidence of MR mostly in the duodenal bulb. The inhibitory effects of both CCK peptides on the bulbar MR exhibited a dose-response character, though the lowest dose often evoked the slight stimulatory response. It is concluded that CCK principally exerts an inhibitory effect upon the MR in the duodenal bulb and modifies the MR in the duodenum by increasing the spike burst number in a given MR pattern. Both these actions of CCK peptides seem to be physiological. There is a positive relationship between the intensity of the refractory period and the demonstrated effect of CCK in the duodenum.

Keywords

sheepcholecystokinin-octapeptideceruleinduodeno-jejunumminute rhythm
Type
Full Paper
Information
animal , Volume 3 , Issue 2 , February 2009 , pp. 275 - 286
Copyright
Copyright © The Animal Consortium 2008

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References

Adelson, DW, Million, M, Kanamoto, K, Palanca, T, Tache, Y 2004. Coordinated gastric and sphincter motility evoked by intravenous CCK-8 as monitored by ultrasonomicrometry in rats. American Journal of Physiology – Gastrointestinal and Liver Physiology 286, G321–G332.CrossRefGoogle ScholarPubMed
Bertaccini, G, De Caro, G, Endean, R, Erspamer, V, Impicciatore, M 1968. The actions of caerulein on the smooth muscle of the gastrointestinal tract and the gall bladder. British Journal of Pharmacology 34, 291–310.CrossRefGoogle ScholarPubMed
Bueno, L, Praddaude, F 1979. Electrical activity of the gallbladder and biliary tract in sheep and its relationships with antral and duodenal motility. Annales de Biologie Animale, Biochemie et Biophysique 19, 1109–1121.CrossRefGoogle Scholar
Calingasan, NY, Kitamura, N, Yamada, J, Oomori, Y, Yamashita, T 1984. Immunocytochemical study of the gastroenteropancreatic endocrine cells of the sheep. Acta Anatomica 118, 171–180.CrossRefGoogle ScholarPubMed
Code, CF, Marlett, JA 1975. The interdigestive myoelectric complex of the stomach and small bowel of dogs. Journal of Physiology 246, 289–309.CrossRefGoogle ScholarPubMed
Cottrell, DF, Gregory, PC 1991. Regulation of gut motility by luminal stimuli in the ruminant. In Physiological aspects of digestion and metabolism in ruminants. Proceedings of the 7th International Symposium on Ruminant Physiology (ed. T Tsuda, Y Sasaki and R Kawashima), pp. 3–32. Academic Press, Inc., San Diego, USA.CrossRefGoogle Scholar
Dent, J, Dodds, WJ, Sekiguchi, T, Hogan, WJ, Arndorfer, RC 1983. Interdigestive phasic contractions of the human lower esophageal sphincter. Gastroenterology 84, 453–460.CrossRefGoogle ScholarPubMed
Dockray, GJ 1994. Physiology of enteric neuropeptides. In Physiology of the gastrointestinal tract (ed. LR Johnson), pp. 169–209. Raven Press, New York, USA.Google Scholar
Dockray, GJ 2006. Gastrointestinal hormones: gastrin, cholecystokinin, somatostatin, and ghrelin. In Physiology of the gastrointestinal tract (ed. LR Johnson), pp. 91–120. Academic Press, Amsterdam, The Netherlands.CrossRefGoogle Scholar
Ducrotte, P, Peillon, C, Guillemot, F, Testart, J, Denis, P 1991. Could recurrent cholangitis after Roux-en-Y hepaticojejunostomy be explained by motor intestinal anomalies? A manometric study. American Journal of Gastroenterology 86, 1255–1258.Google ScholarPubMed
Faustini, R, Beretta, C, Cheli, R, De Gresti, A 1973. Some effects of caerulein on the motility of sheep forestomach and gall bladder. Pharmacological Research Communications 5, 383–387.CrossRefGoogle Scholar
Fioramonti, J, Bueno, L 1988. Hormonal control of gut motility in ruminants and non-ruminants and its nutritional implications. Nutritional Research Reviews 1, 169–188.CrossRefGoogle ScholarPubMed
Fleckenstein, P, Bueno, L, Fioramonti, J, Ruckebusch, Y 1982. Minute rhythm of electrical spike bursts of the small intestine in different species. American Journal of Physiology – Gastrointestinal and Liver Physiology 242, G654–G659.CrossRefGoogle ScholarPubMed
Grybäck, P, Jacobsson, H, Blomquist, L, Schnell, PO, Hellström, PM 2002. Scintigraphy of the small intestine: a simplified standard for study of transit with reference to normal values. European Journal of Nuclear Medicine and Molecular Imaging 29, 39–45.CrossRefGoogle ScholarPubMed
Li, W, Zheng, TZ, Qu, SY 2000. Effect of cholecystokinin and secretin on contractile activity of isolated gastric muscle strips in guinea pigs. World Journal of Gastroenterology 6, 93–95.CrossRefGoogle ScholarPubMed
Li, Y, Zhu, J, Owyang, C 1999. Electrical physiological evidence for high- and low-affinity vagal CCK-A receptors. American Journal of Physiology – Gastrointestinal and Liver Physiology 277, G469–G477.CrossRefGoogle ScholarPubMed
Liddle, RA 1994. Cholecystokinin. In Gut peptides (ed. JH Walsh and G J Dockray), pp. 175–216. Raven Press, New York, USA.Google Scholar
Rasmussen, L, Øster-Jørgensen, E, Qvist, N, Holst, JJ, Rehfeld, JF, Hovendal, CP, Pedersen, SA 1996. The relationship between gut hormone secretion and gastric emptying in different phases of the migrating motor complex. Scandinavian Journal of Gastroenterology 31, 458–462.CrossRefGoogle ScholarPubMed
Rayner, CK, Park, HS, Doran, SM, Chapman, IM, Horowitz, M 2000. Effects of cholecystokinin on appetite and pyloric motility during physiological hyperglycemia. American Journal of Physiology – Gastrointestinal and Liver Physiology 278, G98–G104.CrossRefGoogle ScholarPubMed
Romański, KW 2002. Characteristics and cholinergic control of the ‘minute rhythm’ in ovine antrum, small bowel and gallbladder. Journal of Veterinary Medicine A 49, 313–320.CrossRefGoogle ScholarPubMed
Romański, KW 2003. Character and cholinergic control of myoelectric activity in ovine duodenal bulb: relationships to adjacent regions. Veterinarski Arhiv 73, 1–16.Google Scholar
Romański, KW 2004. Ovine model for clear-cut study on the role of cholecystokinin in antral, small intestinal and gallbladder motility. Polish Journal of Pharmacology 56, 247–256.Google Scholar
Romański, KW 2005a. The role of muscarinic and nicotinic receptors in the control of the ovine pyloric antral myoelectric response to nutrients during individual phases of the migrating myoelectric complex. Small Ruminant Research 57, 121–131.CrossRefGoogle Scholar
Romański, K 2005b. Cholecystokinin as a physiological regulator of abomasal motility in sheep. Medycyna Weterynaryjna 61, 1312–1316 (in Polish).Google Scholar
Romański, KW 2007. Regional differences in the effects of various doses of cerulein upon the small-intestinal migrating motor complex in fasted and non-fasted sheep. Journal of Animal Physiology and Animal Nutrition 91, 29–39.CrossRefGoogle ScholarPubMed
Romański, KW 2008. New approach to the fed pattern: feeding evokes the specific spike burst setting in the small bowel of non-fasted sheep. Research in Veterinary Science 85, 324–332.CrossRefGoogle Scholar
Romański, KW, Kuryszko, J 1995. The influence of chronic electrode implantation upon the myoelectric activity and histology of the stomach, small intestine and gallbladder in sheep. Archivum Veterinarium Polonicum 35, 127–135.Google ScholarPubMed
Ruckebusch Y 1985. Regulation of reticuloruminal motor activity and cyclical activity of the gastroduodenal junction. In Veterinary Research Communications, vol. 1. The ruminant stomach. Proceedings of an International Workshop, Antwerp, Belgium (ed. LAA Ooms, AD Degryse and R Marsboom), Published under the auspices of the Janssen Research Foundation, pp. 19–51.Google Scholar
Ruckebusch, Y 1988. Motility of the gastro-intestinal tract. In The Ruminant Animal. Digestive physiology and nutrition (ed. DC Church), pp. 64–107. Prentice Hall, Englewood Cliffs, NJ, USA.Google Scholar
Ruckebusch, Y, Soldani, G 1985. Gallbladder motility in sheep: effects of cholecystokinin and related peptides. Journal of Veterinary Pharmacology and Therapeutics 8, 263–269.CrossRefGoogle ScholarPubMed
Scarpignato, C 1997. Pharmacological stimulation of gastrointestinal motility: where we are and where are we going? Digestive Diseases 15 (suppl. 1), 112–136.CrossRefGoogle ScholarPubMed
Schemann, M, Siegle, M-L, Sahyoun, H, Ehrlein, H-J 1986. Computer analysis of intestinal motility: effects of cholecystokinin and neurotensin on jejunal contraction patterns. Zeitschrift für Gastroenterologie 24, 262–268.Google ScholarPubMed
Snedecor, GW, Cochran, WG 1971. Statistical methods, 6th edition. The Iowa State University Press, Ames, IA, USA.Google Scholar
Titchen, DA 1986. Gastrointestinal peptide hormone distribution, release, and action in ruminants. In Control of digestion and metabolism in ruminants (ed. LP Milligan, WL Grovum and A Dobson), pp. 227–248. A Reston Book, Prentice Hall, Englewood Cliffs, NJ, USA.Google Scholar
Varga, G, Balint, A, Burghardt, B, D’Amato, M 2004. Involvement of endogenous CCK and CCK1 receptors in colonic motor function. British Journal of Pharmacology 141, 1275–1284.CrossRefGoogle ScholarPubMed
Walsh, JH 1994. Gastrointestinal hormones. In Physiology of the gastrointestinal tract (ed. LR Johnson), pp. 1–128. Raven Press, New York, USA.Google Scholar
Wang, Y, Prpic, V, Green, GM, Reeve, JR Jr, Liddle, RA 2002. Luminal CCK-releasing factor stimulates CCK release from human intestinal endocrine and STC-1 cells. American Journal of Physiology – Gastrointestinal and Liver Physiology 282, G16–G22.CrossRefGoogle ScholarPubMed
Wilmer, A, Van Cutsem, E, Andrioli, A, Tack, J, Coremans, G, Janssens, J 1998. Ambulatory gastrojejunal manometry in severe motility-like dyspepsia: lack of correlation between dysmotility, symptoms, and gastric emptying. Gut 42, 235–242.CrossRefGoogle ScholarPubMed
Wood, JD 2000. Myoelectrical and contractile activities of the gastrointestinal tract. In Schuster atlas of gastrointestinal motility in health and disease (ed. MM Schuster, MD Crowell and KL Koch), pp. 19–42. BC Decker Inc, Hamilton, UK.Google Scholar
Yau, WM, Makhlouf, GM, Edwards, LE, Farrar, JT 1974. The action of cholecystokinin and related peptides on guinea pig small intestine. Canadian Journal of Physiology and Pharmacology 52, 298–303.CrossRefGoogle ScholarPubMed
Yonekura, S, Kitade, K, Furukawa, G, Takahashi, K, Katsumata, N, Katoh, K, Obara, Y 2002. Effects of aging and weaning on mRNA expression of leptin and CCK receptors in the calf rumen and abomasum. Domestic Animal Endocrinology 22, 25–35.CrossRefGoogle ScholarPubMed
Zavros, Y, Shulkes, A 1997. Cholecystokinin (CCK) regulates somatostatin secretion through both the CCK-A and CCK-B/gastrin receptors in sheep. Journal of Physiology 505, 811–821.CrossRefGoogle ScholarPubMed