The common hepatic branch of the vagus is not required to mediate the glycemic and food intake suppressive effects of glucagon-like-peptide-1

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 301, Issue 5, 2011, Pages

  Hayes, Matthew R ^a,b   Kanoski, Scott E ^a   de Jonghe, Bart C ^c   Leichner, Theresa M ^a   Alhadeff, Amber L ^a   Fortin, Samantha M ^a   Arnold, Myrtha ^d   Langhans, Wolfgang ^d   Grill, Harvey J ^a  

^a School of Arts and Sciences   (United States)

^b University School of Medicine   (United States)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

^d ETH ZURICH   (Switzerland)

Author keywords

Blood glucose; Incretin; Satiety; Vagotomy

Indexed keywords

EXENDIN 9; GLUCAGON LIKE PEPTIDE 1; GLUCAGON LIKE PEPTIDE 1 RECEPTOR; GLUCOSE; HORMONE RECEPTOR BLOCKING AGENT; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; DEAFFERENTATION; DIET RESTRICTION; DRUG EFFECT; FOOD INTAKE; GLUCOSE BLOOD LEVEL; GLUCOSE INTAKE; GLYCEMIC CONTROL; MALE; NONHUMAN; ORAL GLUCOSE TOLERANCE TEST; PARACRINE SIGNALING; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; VAGUS NERVE;

ANIMALS; APPETITE DEPRESSANTS; APPETITE REGULATION; BEHAVIOR, ANIMAL; BLOOD GLUCOSE; EATING; GLUCAGON-LIKE PEPTIDE 1; GLUCOSE TOLERANCE TEST; HORMONE ANTAGONISTS; INJECTIONS, INTRAPERITONEAL; LIVER; MALE; PARACRINE COMMUNICATION; PEPTIDE FRAGMENTS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, GLUCAGON; TIME FACTORS; VAGOTOMY; VAGUS NERVE;

EID: 80155165170     PISSN: 03636119     EISSN: 15221490     Source Type: Journal    
DOI: 10.1152/ajpregu.00356.2011     Document Type: Article

References (54)

1. Abbott CR, Monteiro M, Small CJ, Sajedi A, Smith KL, Parkinson JR, Ghatei MA, Bloom SR. The inhibitory effects of peripheral administration of peptide YY(3-36) and glucagon-like peptide-1 on food intake are attenuated by ablation of the vagal-brainstem-hypothalamic pathway. Brain Res 1044: 127-131, 2005.
2. Ackroff K, Touzani K, Peets TK, Sclafani A. Flavor preferences conditioned by intragastric fructose and glucose: differences in reinforcement potency. Physiol Behav 72: 691-703, 2001.
3. Ackroff K, Yiin YM, Sclafani A. Post-oral infusion sites that support glucose-conditioned flavor preferences in rats. Physiol Behav 99: 402-411, 2010.
4. Ahren B. Sensory nerves contribute to insulin secretion by glucagon-like peptide-1 in mice. Am J Physiol Regul Integr Comp Physiol 286: R269-R272, 2004.
5. Arnold M, Mura A, Langhans W, Geary N. Gut vagal afferents are not necessary for the eating-stimulatory effect of intraperitoneally injected ghrelin in the rat. J Neurosci 26: 11052-11060, 2006.
6. Astrup A, Rossner S, Van Gaal L, Rissanen A, Niskanen L, Al Hakim M, Madsen J, Rasmussen MF, Lean ME. Effects of liraglutide in the treatment of obesity: a randomised, double-blind, placebo-controlled study. Lancet 374: 1606-1616, 2009.
7. Balkan B, Li X. Portal GLP-1 administration in rats augments the insulin response to glucose via neuronal mechanisms. Am J Physiol Regul Integr Comp Physiol 279: R1449-R1454, 2000.
8. Berger T, Ceder L, Hamfelt A, Meurling S. Effect of highly selective vagotomy on gastric emptying. Scand J Gastroenterol 11: 829-832, 1976.
9. Berthoud HR, Kressel M, Neuhuber WL. An anterograde tracing study of the vagal innervation of rat liver, portal vein and biliary system. Anat Embryol (Berl) 186: 431-442, 1992.
10. Berthoud HR, Patterson LM, Willing AE, Mueller K, Neuhuber WL. Capsaicin-resistant vagal afferent fibers in the rat gastrointestinal tract: anatomical identification and functional integrity. Brain Res 746: 195-206, 1997.
11. Blonde L, Klein EJ, Han J, Zhang B, Mac SM, Poon TH, Taylor KL, Trautmann ME, Kim DD, Kendall DM. Interim analysis of the effects of exenatide treatment on A1C, weight and cardiovascular risk factors over 82 weeks in 314 overweight patients with type 2 diabetes. Diabetes Obes Metab 8: 436-447, 2006.
12. Bonacchi KB, Ackroff K, Touzani K, Bodnar RJ, Sclafani A. Opioid mediation of starch and sugar preference in the rat. Pharmacol Biochem Behav 96: 507-514, 2010.
13. Bucinskaite V, Tolessa T, Pedersen J, Rydqvist B, Zerihun L, Holst JJ, Hellstrom PM. Receptor-mediated activation of gastric vagal affer-ents by glucagon-like peptide-1 in the rat. Neurogastroenterol Motil 21: 978-e78, 2009.
14. Data and Statistics Center for Disease Control and Prevention. Overweight and Obesity [http://www.cdc.gov/obesity/data/index.html].
15. De Jonghe BC, Horn CC. Chemotherapy-induced pica and anorexia are reduced by common hepatic branch vagotomy in the rat. Am J Physiol Regul Integr Comp Physiol 294: R756-R765, 2008.
16. Fox EA, Phillips RJ, Martinson FA, Baronowsky EA, Powley TL. Vagal afferent innervation of smooth muscle in the stomach and duodenum of the mouse: morphology and topography. J Comp Neurol 428: 558-576, 2000.
17. Gamse R. Capsaicin and nociception in the rat and mouse. Possible role of substance. P Naunyn Schmiedebergs Arch Pharmacol 320: 205-216, 1982.
18. Gleysteen JJ, Burdeshaw JA, Hallenbeck GA. Gastric emptying of liquids after different vagotomies and pyloroplasty. Surg Gynecol Obstet 142: 41-48, 1976.
19. Hayes MR, De Jonghe BC, Kanoski SE. Role of the glucagon-likepeptide-1 receptor in the control of energy balance. Physiol Behav 100: 503-510, 2010.
20. Hayes MR, Skibicka KP, Grill HJ. Caudal brainstem processing is sufficient for behavioral, sympathetic, and parasympathetic responses driven by peripheral and hindbrain glucagon-like-peptide-1 receptor stimulation. Endocrinology 149: 4059-4068, 2008.
21. Holst JJ. The physiology of glucagon-like peptide 1. Physiol Rev 87: 1409-1439, 2007.
22. Imeryuz N, Yegen BC, Bozkurt A, Coskun T, Villanueva-Penacarrillo ML, Ulusoy NB. Glucagon-like peptide-1 inhibits gastric emptying via vagal afferent-mediated central mechanisms. Am J Physiol Gastrointest Liver Physiol 273: G920-G927, 1997.
23. Kanoski SE, Fortin SM, Arnold M, Grill HJ, Hayes MR. Peripheral and central GLP-1 receptor populations mediate the anorectic effects of peripherally administered GLP-1 receptor agonists, liraglutide and exendin-4. Endocrinology 152: 3103-3112, 2011.
24. Knauf C, Cani PD, Perrin C, Iglesias MA, Maury JF, Bernard E, Benhamed F, Gremeaux T, Drucker DJ, Kahn CR, Girard J, Tanti JF, Delzenne NM, Postic C, Burcelin R. Brain glucagon-like peptide-1 increases insulin secretion and muscle insulin resistance to favor hepatic glycogen storage. J Clin Invest 115: 3554-3563, 2005.
25. Knudsen LB. Liraglutide: the therapeutic promise from animal models. Int J Clin Pract Suppl 64: 4-11, 2010.
26. Kraly FS, Jerome C, Smith GP. Specific postoperative syndromes after total and selective vagotomies in the rat. Appetite 7: 1-17, 1986.
27. Lo CM, Xu M, Yang Q, Zheng S, Carey KM, Tubb MR, Davidson WS, Liu M, Woods SC, Tso P. Effect of intraperitoneal and intravenous administration of cholecystokinin-8 and apolipoprotein AIV on intestinal lymphatic CCK-8 and apo AIV concentration. Am J Physiol Regul Integr Comp Physiol 296: R43-R50, 2009.
28. Lovshin JA, Drucker DJ. Incretin-based therapies for type 2 diabetes mellitus. Nat Rev Endocrinol 5: 262-269, 2009.
29. Lukas G, Brindle SD, Greengard P. The route of absorption of intraperitoneally administered compounds. J Pharmacol Exp Ther 178: 562-564, 1971.
30. Moran TH, Baldessarini AR, Salorio CF, Lowery T, Schwartz GJ. Vagal afferent and efferent contributions to the inhibition of food intake by cholecystokinin. Am J Physiol Regul Integr Comp Physiol 272: R1245-R1251, 1997.
31. Nakabayashi H, Nishizawa M, Nakagawa A, Takeda R, Niijima A. Vagal hepatopancreatic reflex effect evoked by intraportal appearance of tGLP-1. Am J Physiol Endocrinol Metab 271: E808-E813, 1996.
32. Nishizawa M, Nakabayashi H, Kawai K, Ito T, Kawakami S, Nakagawa A, Niijima A, Uchida K. The hepatic vagal reception of intraportal GLP-1 is via receptor different from the pancreatic GLP-1 receptor. J Auton Nerv Syst 80: 14-21, 2000.
33. Nishizawa M, Nakabayashi H, Uchida K, Nakagawa A, Niijima A. The hepatic vagal nerve is receptive to incretin hormone glucagon-like peptide-1, but not to glucose-dependent insulinotropic polypeptide, in the portal vein. J Auton Nerv Syst 61: 149-154, 1996.
34. Norgren R, Smith GP. A method for selective section of vagal afferent or efferent axons in the rat. Am J Physiol Regul Integr Comp Physiol 267: R1136-R1141, 1994.
35. Novin D, Robinson K, Culbreth LA, Tordoff MG. Is there a role for the liver in the control of food intake? Am J Clin Nutr 42: 1050-1062, 1985.
36. Ogden CL, Yanovski SZ, Carroll MD, Flegal KM. The epidemiology of obesity. Gastroenterology 132: 2087-2102, 2007.
37. Peters JH, McKay BM, Simasko SM, Ritter RC. Leptin-induced satiation mediated by abdominal vagal afferents. Am J Physiol Regul Integr Comp Physiol 288: R879-R884, 2005.
38. Phillips RJ, Baronowsky EA, Powley TL. Afferent innervation of gastrointestinal tract smooth muscle by the hepatic branch of the vagus. J Comp Neurol 384: 248-270, 1997.
39. Powley TL, Fox EA, Berthoud HR. Retrograde tracer technique for assessment of selective and total subdiaphragmatic vagotomies. Am J Physiol Regul Integr Comp Physiol 253: R361-R370, 1987.
40. Prechtl JC, Powley TL. The fiber composition of the abdominal vagus of the rat. Anat Embryol (Berl) 181: 101-115, 1990.
41. Raun K, von Voss P, Gotfredsen CF, Golozoubova V, Rolin B, Knudsen LB. Liraglutide, a long-acting glucagon-like peptide-1 analog, reduces body weight and food intake in obese candy-fed rats, whereas a dipeptidyl peptidase-IV inhibitor, vildagliptin, does not. Diabetes 56: 8-15, 2007.
42. Ritter RC. Gastrointestinal mechanisms of satiation for food. Physiol Behav 81: 249-273, 2004.
43. Rocca AS, Brubaker PL. Role of the vagus nerve in mediating proximal nutrient-induced glucagon-like peptide-1 secretion. Endocrinology 140: 1687-1694, 1999.
44. Rüttimann EB, Arnold M, Hillebrand JJ, Geary N, Langhans W. Intrameal hepatic portal and intraperitoneal infusions of glucagon-like peptide-1 reduce spontaneous meal size in the rat via different mechanisms. Endocrinology 150: 1174-1181, 2009.
45. Sclafani A, Ackroff K, Schwartz GJ. Selective effects of vagal deafferentation and celiac-superior mesenteric ganglionectomy on the reinforcing and satiating action of intestinal nutrients. Physiol Behav 78: 285-294, 2003.
46. Scott KA, Moran TH. The GLP-1 agonist exendin-4 reduces food intake in nonhuman primates through changes in meal size. Am J Physiol Regul Integr Comp Physiol 293: R983-R987, 2007.
47. Smith GP, Jerome C, Norgren R. Afferent axons in abdominal vagus mediate satiety effect of cholecystokinin in rats. Am J Physiol Regul Integr Comp Physiol 249: R638-R641, 1985.
48. Steinert RE, Beglinger C. Nutrient sensing in the gut: Interactions between chemosensory cells, visceral afferents and the secretion of satiation peptides. Physiol Behav. In press.
49. Steinert RE, Gerspach AC, Gutmann H, Asarian L, Drewe J, Beglinger C. The functional involvement of gut-expressed sweet taste receptors in glucose-stimulated secretion of glucagon-like peptide-1 (GLP-1) and peptide YY (PYY). Clin Nutr 30: 524-532, 2011.
50. Talsania T, Anini Y, Siu S, Drucker DJ, Brubaker PL. Peripheral exendin-4 and peptide YY(3-36) synergistically reduce food intake through different mechanisms in mice. Endocrinology 146: 3748-3756, 2005.
51. Vahl TP, Tauchi M, Durler TS, Elfers EE, Fernandes TM, Bitner RD, Ellis KS, Woods SC, Seeley RJ, Herman JP, D'Alessio DA. Glucagonlike peptide-1 (GLP-1) receptors expressed on nerve terminals in the portal vein mediate the effects of endogenous GLP-1 on glucose tolerance in rats. Endocrinology 148: 4965-4973, 2007.
52. van de Wall EH, Duffy P, Ritter RC. CCK enhances response to gastric distension by acting on capsaicin insensitive vagal afferents. Am J Physiol Regul Integr Comp Physiol 289: R695-R703, 2005.
53. Wang FB, Powley TL. Vagal innervation of intestines: afferent pathways mapped with new en bloc horseradish peroxidase adaptation. Cell Tissue Res 329: 221-230, 2007.
54. Young RL. Sensing via intestinal sweet taste pathways. Front Neurosci 5: 23, 2011.