Cholecystokinin regulates satiation independently of the abdominal vagal nerve in a pig model of total subdiaphragmatic vagotomy

Physiology and Behavior

Volumn 139, Issue , 2015, Pages 167-176

  Ripken, D ^a,b,c   van der Wielen, N ^a,b,c   van der Meulen, J ^c   Schuurman, T ^c   Witkamp, R F ^c   Hendriks, H F J ^a   Koopmans, S J ^c  

^a TOP INSTITUTE FOOD AND NUTRITION   (Netherlands)

^b TNO   (Netherlands)

^c WAGENINGEN UNIVERSITY   (Netherlands)

Author keywords

Cholecystokinin; Devazepide; Exendin (9 39); Food intake regulation; Glucagon like peptide 1; Vagal nerve

Indexed keywords

CHOLECYSTOKININ; CHOLECYSTOKININ A RECEPTOR; DEVAZEPIDE; GLUCAGON LIKE PEPTIDE 1; GLUCAGON LIKE PEPTIDE 1 RECEPTOR; GLUCOSE; INSULIN; PARACETAMOL; EXENDIN (9-39); GLUCAGON RECEPTOR; GLUCAGON-LIKE PEPTIDE-1 RECEPTOR; GLUCOSE BLOOD LEVEL; HORMONE ANTAGONIST; PEPTIDE FRAGMENT;

ABDOMINAL VAGAL NERVE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOPSY; CHOLECYSTOKININ BLOOD LEVEL; CONTROLLED STUDY; DRUG ABSORPTION; DRUG BLOOD LEVEL; FLUID INTAKE; FOOD INTAKE; GLUCOSE BLOOD LEVEL; HORMONAL REGULATION; HORMONE RESPONSE; INSULIN BLOOD LEVEL; INTESTINE MOTILITY; MALE; MAXIMUM PLASMA CONCENTRATION; NONHUMAN; POSTPRANDIAL STATE; SATIETY; SHAM PROCEDURE; STOMACH ABSORPTION; STOMACH CONTENT; STOMACH EMPTYING; SUBDIAPHRAGMATIC VAGOTOMY; TIME TO MAXIMUM PLASMA CONCENTRATION; VAGOTOMY; VAGUS NERVE; WEIGHT GAIN; ANIMAL; ANTAGONISTS AND INHIBITORS; BLOOD; DRUG EFFECTS; EATING; METABOLISM; PATHOPHYSIOLOGY; PHYSIOLOGY; PIG;

ACETAMINOPHEN; ANIMALS; BLOOD GLUCOSE; CHOLECYSTOKININ; DEVAZEPIDE; EATING; GLUCAGON-LIKE PEPTIDE 1; HORMONE ANTAGONISTS; INSULIN; MALE; MODELS, ANIMAL; PEPTIDE FRAGMENTS; POSTPRANDIAL PERIOD; RECEPTORS, GLUCAGON; SATIATION; SUS SCROFA; VAGOTOMY; VAGUS NERVE;

EID: 84911457362     PISSN: 00319384     EISSN: 1873507X     Source Type: Journal    
DOI: 10.1016/j.physbeh.2014.11.031     Document Type: Article

References (57)

1. Blundell J., de Graaf C., Hulshof T., Jebb S., Livingstone B., Lluch A., et al. Appetite control: methodological aspects of the evaluation of foods. Obes Rev 2010, 11(3):251-270.
2. de Graaf C., Blom W., Smeets P., Stafleu A., Hendriks H. Biomarkers of satiation and satiety. Am J Clin Nutr 2004, 79(6):946-961.
3. Mithieux G. Nutrient control of hunger by extrinsic gastrointestinal neurons. Trends Endocrinol Metab 2013, 24(8):378-384.
4. Blundell J., Halford J. Regulation of nutrient supply - the brain and appetite control. Proc Nutr Soc 1994, 53(2):407-418.
5. Berthoud H.R. The vagus nerve, food intake and obesity. Regul Pept 2008, 149(1-3):15-25.
6. Ogawa N., Ito M., Yamaguchi H., Shiuchi T., Okamoto S., Wakitani K., et al. Intestinal fatty acid infusion modulates food preference as well as calorie intake via the vagal nerve and midbrain-hypothalamic neural pathways in rats. Metabolism 2012, 61(9):1312-1320.
7. Holst J.J. The physiology of glucagon-like peptide 1. Physiol Rev 2007, 87(4):1409-1439.
8. Iwasaki Y., Yada T. Vagal afferents sense meal-associated gastrointestinal and pancreatic hormones: mechanism and physiological role. Neuropeptides 2012, 46(6):291-297.
9. Cantor P., Rehfeld J.F. Cholecystokinin in pig plasma: release of components devoid of a bioactive COOH-terminus. Am J Physiol 1989, 256(1 Pt 1):G53-G61.
10. Rehfeld J.F., Friis-Hansen L., Goetze J.P., Hansen T.V. The biology of cholecystokinin and gastrin peptides. Curr Top Med Chem 2007, 7(12):1154-1165.
11. Ji Z., Hadac E.M., Henne R.M., Patel S.A., Lybrand T.P., Miller L.J. Direct identification of a distinct site of interaction between the carboxyl-terminal residue of cholecystokinin and the type A cholecystokinin receptor using photoaffinity labeling. J Biol Chem 1997, 272(39):24393-24401.
12. Ritter R.C. Increased food intake and CCK receptor antagonists: beyond abdominal vagal afferents. Am J Physiol Regul Integr Comp Physiol 2004, 286(6):R991-R993.
13. Kanoski S.E., Fortin S.M., Arnold M., Grill H.J., Hayes M.R. Peripheral and central GLP-1 receptor populations mediate the anorectic effects of peripherally administered GLP-1 receptor agonists, liraglutide and exendin-4. Endocrinology 2011, 152(8):3103-3112.
14. Gribble F.M. The gut endocrine system as a coordinator of postprandial nutrient homoeostasis. Proc Nutr Soc 2012, 71(4):456-462.
15. Deacon C.F., Holst J.J. Immunoassays for the incretin hormones GIP and GLP-1. Best Pract Res Clin Endocrinol Metab 2009, 23(4):425-432.
16. Dailey M.J., Moran T.H. Glucagon-like peptide 1 and appetite. Trends Endocrinol Metab 2013, 24(2):85-91.
17. Chelikani P.K., Haver A.C., Reidelberger R.D. Intravenous infusion of glucagon-like peptide-1 potently inhibits food intake, sham feeding, and gastric emptying in rats. Am J Physiol Regul Integr Comp Physiol 2005, 288(6):R1695-R1706.
18. Gutzwiller J.P., Göke B., Drewe J., Hildebrand P., Ketterer S., Handschin D., et al. Glucagon-like peptide-1: a potent regulator of food intake in humans. Gut 1999, 44(1):81-86.
19. Parrott R., Ebenezer I., Baldwin B., Forsling M. Central and peripheral doses of cholecystokinin that inhibit feeding in pigs also stimulate vasopressin and cortisol release. Exp Physiol 1991, 76(4):525-531.
20. Zhang J., Ritter R.C. Circulating GLP-1 and CCK-8 reduce food intake by capsaicin-insensitive, nonvagal mechanisms. Am J Physiol Regul Integr Comp Physiol 2012, 302(2):R264-R273.
21. Ritter R.C., Ladenheim E.E. Capsaicin pretreatment attenuates suppression of food intake by cholecystokinin. Am J Physiol 1985, 248(4 Pt 2):R501-R504.
22. Joyner K., Smith G., Gibbs J. Abdominal vagotomy decreases the satiating potency of cck-8 in sham and real feeding. Am J Physiol 1993, 264(5):R912-R916.
23. Smith G.P., Jerome C., Norgren R. Afferent axons in abdominal vagus mediate satiety effect of cholecystokinin in rats. Am J Physiol 1985, 249(5 Pt 2):R638-R641.
24. Richards P., Parker H.E., Adriaenssens A.E., Hodgson J.M., Cork S.C., Trapp S., et al. Identification and characterization of glucagon-like peptide-1 receptor expressing cells using a new transgenic mouse model. Diabetes 2014, 63(4):1224-1233.
25. Reidelberger R. Abdominal vagal mediation of the satiety effects of exogenous and endogenous cholecystokinin in rats. Am J Physiol 1992, 263(6):R1354-R1358.
26. Reidelberger R., Hernandez J., Fritzsch B., Hulce M. Abdominal vagal mediation of the satiety effects of CCK in rats. Am J Physiol Regul Integr Comp Physiol 2004, 286(6):R1005-R1012.
27. Clouard C., Meunier-Salauen M.C., Val-Laillet D. Food preferences and aversions in human health and nutrition: how can pigs help the biomedical research?. Animal 2012, 6(1):118-136.
28. Miller E.R., Ullrey D.E. The pig as a model for human nutrition. Annu Rev Nutr 1987, 7:361-382.
29. CVB.centraal veevoederbureau Dutch norms for livestock feeding and nutritive values for feedstuffs 2000, CVB Press, Lelystad (The Netherlands). 24th edition.
30. Koopmans S.J., VanderMeulen J., Wijdenes J., Corbijn H., Dekker R. The existence of an insulin-stimulated glucose and non-essential but not essential amino acid substrate interaction in diabetic pigs. BMC Biochem 2011, 12. [25-2091-12-25].
31. Koopmans S., van der Meulen J., Dekker R., Corbijn H., Mroz Z. Diurnal rhythms in plasma cortisol, insulin, glucose, lactate and urea in pigs fed identical meals at 12-hourly intervals. Physiol Behav 2005, 84(3):497-503.
32. Clements J.A., Heading R.C., Nimmo W.S., Prescott L.F. Kinetics of acetaminophen absorption and gastric emptying in man. Clin Pharmacol Ther 1978, 24(4):420-431.
33. Heading R.C., Nimmo J., Prescott L.F., Tothill P. The dependence of paracetamol absorption on the rate of gastric emptying. Br J Pharmacol 1973, 47(2):415-421.
34. Willems M., Quartero A.O., Numans M.E. How useful is paracetamol absorption as a marker of gastric emptying? A systematic literature study. Dig Dis Sci 2001, 46(10):2256-2262.
35. Schirra J., Sturm K., Leicht P., Arnold R., Goke B., Katschinski M. Exendin(9-39)amide is an antagonist of glucagon-like peptide-1(7-36)amide in humans. J Clin Invest 1998, 101(7):1421-1430.
36. Edwards C.M., Todd J.F., Mahmoudi M., Wang Z., Wang R.M., Ghatei M.A., et al. Glucagon-like peptide 1 has a physiological role in the control of postprandial glucose in humans - studies with the antagonist exendin 9-39. Diabetes 1999, 48(1):86-93.
37. + channel. Diabetes 2012, 61(10):2585-2591.
38. Ebenezer I., Delariva C., Baldwin B. Effects of the CCK receptor antagonist mk-329 on food-intake in pigs. Physiol Behav 1990, 47(1):145-148.
39. Reidelberger R.D., Heimann D., Kelsey L., Hulce M. Effects of peripheral CCK receptor blockade on feeding responses to duodenal nutrient infusions in rats. Am J Physiol Regul Integr Comp Physiol 2003, 284(2):R389-R398.
40. Ruttimann E.B., Arnold M., Geary N., Langhans W. GLP-1 antagonism with exendin (9-39) fails to increase spontaneous meal size in rats. Physiol Behav 2010, 100(4):291-296.
41. Williams D.L., Baskin D.G., Schwartz M.W. Evidence that intestinal glucagon-like peptide-1 plays a physiological role in satiety. Endocrinology 2009, 150(4):1680-1687.
42. Vahl T.P., Drazen D.L., Seeley R.J., D'Alessio D.A., Woods S.C. Meal-anticipatory glucagon-like peptide-1 secretion in rats. Endocrinology 2010, 151(2):569-575.
43. Bessell J.R., Pike G., Jamieson G.G., Maddern G.J. Physiological outcome following laparoscopic highly selective vagotomy. A controlled study in a pig model. Surg Endosc 1995, 9(12):1283-1288.
44. Lepre L., Costa G., Liotta G., Mazzoni G., Tocchi A. Comparison of four minimally invasive methods of laparoscopic vagotomy in a porcine model. Surg Endosc 1998, 12(5):440-443.
45. Prescott L.F. Kinetics and metabolism of paracetamol and phenacetin. Br J Clin Pharmacol 1980, 10(Suppl. 2):291S-298S.
46. Medhus A.W., Lofthus C.M., Bredesen J., Husebye E. Gastric emptying: the validity of the paracetamol absorption test adjusted for individual pharmacokinetics. Neurogastroenterol Motil 2001, 13(3):179-185.
47. Moran T.H., Baldessarini A.R., Salorio C.F., Lowery T., Schwartz G.J. Vagal afferent and efferent contributions to the inhibition of food intake by cholecystokinin. Am J Physiol 1997, 272(4 Pt 2):R1245-R1251.
48. Fujiwara K., Gotoh K., Chiba S., Masaki T., Katsuragi I., Kakuma T., et al. Intraportal administration of DPP-IV inhibitor regulates insulin secretion and food intake mediated by the hepatic vagal afferent nerve in rats. J Neurochem 2012, 121(1):66-76.
49. Russek M. Participation of hepatic glucoreceptors in the control of intake of food. Nature 1963, 197:79-80.
50. Niijima A. Afferent discharges from osmoreceptors in the liver of the guinea pig. Nutrition 1996, 12(5):390.
51. Udit S., Gautron L. Molecular anatomy of the gut-brain axis revealed with transgenic technologies: implications in metabolic research. Front Neurosci 2013, 7. 10.3389/fnins.2013.00134.
52. Grabauskas G., Zhou S.Y., Lu Y., Song I., Owyang C. Essential elements for glucosensing by gastric vagal afferents: immunocytochemistry and electrophysiology studies in the rat. Endocrinology 2013, 154(1):296-307.
53. Phillips R., Powley T. Tension and stretch receptors in gastrointestinal smooth muscle: re-evaluating vagal mechanoreceptor electrophysiology. Brain Res Rev 2000, 34(1-2):1-26.
54. Banks W.A., During M.J., Niehoff M.L. Brain uptake of the glucagon-like peptide-1 antagonist exendin (9-39) after intranasal administration. J Pharmacol Exp Ther 2004, 309(2):469-475.
55. Powley T.L., Phillips R.J. Musings on the wanderer: what's new in our understanding of vago-vagal reflexes? I. morphology and topography of vagal afferents innervating the GI tract. Am J Physiol Gastrointest Liver Physiol 2002, 283(6):G1217-G1225.
56. Witkamp R.F. Current and future drug targets in weight management. Pharm Res 2011, 28(8):1792-1818.
57. Luttikhold J., de Ruijter F.M., van Norren K., Diamant M., Witkamp R.F., van Leeuwen P.A., et al. Review article: the role of gastrointestinal hormones in the treatment of delayed gastric emptying in critically ill patients. Aliment Pharmacol Ther 2013, 38(6):573-583.