Hepatic-portal vein infusions of glucagon-like peptide-1 reduce meal size and increase c-fos expression in the nucleus tractus solitarii, area postrema and central nucleus of the amygdala in rats

Journal of Neuroendocrinology

Volumn 22, Issue 6, 2010, Pages 557-563

  Baumgartner, I ^a   Pacheco Lopez G ^a   Ruttimann E B ^a   Arnold, M ^a   Asarian, L ^a   Langhans, W ^a   Geary, N ^a   Hillebrand, J J G ^a  

^a ETH ZURICH   (Switzerland)

Author keywords

Aversion; Eating; Gut peptide; Hindbrain; Satiation

Indexed keywords

GLUCAGON LIKE PEPTIDE 1; PROTEIN C FOS;

AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ARCUATE NUCLEUS; ARTICLE; AVERSION; CONTROLLED STUDY; EATING; FOOD DEPRIVATION; HYPOTHALAMUS NUCLEUS; MALE; NONHUMAN; PORTAL VEIN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SATIETY; SOLITARY TRACT NUCLEUS; ANIMAL; AREA POSTREMA; DRUG EFFECTS; FEEDING BEHAVIOR; IMMUNOHISTOCHEMISTRY; METABOLISM; SPRAGUE DAWLEY RAT;

AMYGDALA; ANIMALS; AREA POSTREMA; FEEDING BEHAVIOR; GLUCAGON-LIKE PEPTIDE 1; IMMUNOHISTOCHEMISTRY; MALE; PORTAL VEIN; PROTO-ONCOGENE PROTEINS C-FOS; RATS; RATS, SPRAGUE-DAWLEY; SOLITARY NUCLEUS;

EID: 77954102250     PISSN: 09538194     EISSN: 13652826     Source Type: Journal    
DOI: 10.1111/j.1365-2826.2010.01995.x     Document Type: Article

References (46)

1. Holst JJ. The physiology of glucagon-like peptide 1. Physiol Rev 2007, 87:1409-1439.
2. Baggio LL, Drucker DJ. Biology of incretins: GLP-1 and GIP. Gastroenterology 2007, 132:2131-2157.
3. Orskov C, Holst JJ, Nielsen OV. Effect of truncated glucagon-like peptide-1 [proglucagon-(78-107) amide] on endocrine secretion from pig pancreas, antrum, and nonantral stomach. Endocrinology 1988, 123:2009-2013.
4. Holst JJ. Enteroglucagon. Annu Rev Physiol 1997, 59:257-271.
5. Rinaman L. A functional role for central glucagon-like peptide-1 receptors in lithium chloride-induced anorexia. Am J Physiol Regul Integr Comp Physiol 1999, 277:R1537-R1540.
6. van Dijk G, Thiele TE. Glucagon-like peptide-1 (7-36) amide: a central regulator of satiety and interoceptive stress. Neuropeptides 1999, 33:406-414.
7. Beglinger C, Degen L. Gastrointestinal satiety signals in humans - physiologic roles for GLP-1 and PYY? Physiol Behav 2006, 89:460-464.
8. Williams DL. Minireview: finding the sweet spot: peripheral versus central glucagon-like peptide 1 action in feeding and glucose homeostasis. Endocrinology 2009, 150:2997-3001.
9. Ruttimann 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 2009, 150:1174-1181.
10. Thiele TE, van Dijk G, Campfield LA, Smith FJ, Burn P, Woods SC, Bernstein IL, Seeley RJ. Central infusion of GLP-1, but not leptin, produces conditioned taste aversions in rats. Am J Physiol Regul Integr Comp Physiol 1997, 272:R726-R730.
11. Williams DL, Baskin DG, Schwartz MW. Evidence that intestinal glucagon-like peptide-1 plays a physiological role in satiety. Endocrinology 2009, 150:1680-1687.
12. Kinzig KP, D'Alessio DA, Seeley RJ. The diverse roles of specific GLP-1 receptors in the control of food intake and the response to visceral illness. J Neurosci 2002, 22:10470-10476.
13. Seeley RJ, Blake K, Rushing PA, Benoit S, Eng J, Woods SC, D'Alessio D. The role of CNS glucagon-like peptide-1 (7-36) amide receptors in mediating the visceral illness effects of lithium chloride. J Neurosci 2000, 20:1616-1621.
14. Thiele TE, Seeley RJ, D'Alessio D, Eng J, Bernstein IL, Woods SC, van Dijk G. Central infusion of glucagon-like peptide-1-(7-36) amide (GLP-1) receptor antagonist attenuates lithium chloride-induced c-Fos induction in rat brainstem. Brain Res 1998, 801:164-170.
15. van Dijk G, Thiele TE, Seeley RJ, Woods SC, Bernstein IL. Glucagon-like peptide-1 and satiety. Nature 1997, 385:214.
16. Verdich C, Flint A, Gutzwiller JP, Naslund E, Beglinger C, Hellstrom PM, Long SJ, Morgan LM, Holst JJ, Astrup A. A meta-analysis of the effect of glucagon-like peptide-1 (7-36) amide on ad libitum energy intake in humans. J Clin Endocrinology Metab 2001, 86:4382-4389.
17. Kim DH, D'Alessio DA, Woods SC, Seeley RJ. The effects of GLP-1 infusion in the hepatic portal region on food intake. Regul Pept 2009, 155:110-114.
18. Pacheco-Lopez G, Espinosa E, Zamorano-Rojas HM, Ramirez-Amaya V, Bermudez-Rattoni F. Peripheral protein immunization induces rapid activation of the CNS, as measured by c-Fos expression. J Neuroimmunol 2002, 131:50-59.
19. Paxinos G, Watson C. The Rat Brain in Stereotaxic Coordinates 1986, 2nd edn, San Diego, CA, Academic Press
20. Holm S. A simple sequentially rejective multiple test procedure. Scand J Stat 1979, 6:65-70.
21. Burke S. Missing Values, Outliers, Robust Statistics & Non-Parameteric Methods. LG-GC Europe Online Supplement http://www.lcgceurope.com/lcgceurope/data/articlestandard/lcgceurope/502001/4509/article.pdf
22. Yamamoto H, Kishi T, Lee CE, Choi BJ, Fang H, Hollenberg AN, Drucker DJ, Elmquist JK. Glucagon-like peptide-1-responsive catecholamine neurons in the area postrema link peripheral glucagon-like peptide-1 with central autonomic control sites. J Neurosci 2003, 23:2939-2946.
23. Rowland NE, Crews EC, Gentry RM. Comparison of Fos induced in rat brain by GLP-1 and amylin. Regul Pept 1997, 71:171-174.
24. Neary NM, Small CJ, Druce MR, Park AJ, Ellis SM, Semjonous NM, Dakin CL, Filipsson K, Wang F, Kent AS, Frost GS, Ghatei MA, Bloom SR. Peptide YY3-36 and glucagon-like peptide-17-36 inhibit food intake additively. Endocrinology 2005, 146:5120-5127.
25. 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 2005, 1044:127-131.
26. Asarian L. Loss of cholecystokinin and glucagon-like peptide-1-induced satiation in mice lacking serotonin 2C receptors. Am J Physiol Regul Integr Comp Physiol 2009, 296:R51-R56.
27. Yamamoto H, Lee CE, Marcus JN, Williams TD, Overton JM, Lopez ME, Hollenberg AN, Baggio L, Saper CB, Drucker DJ, Elmquist JK. Glucagon-like peptide-1 receptor stimulation increases blood pressure and heart rate and activates autonomic regulatory neurons. J Clin Invest 2002, 110:43-52.
28. Baggio LL, Huang Q, Brown TJ, Drucker DJ. A recombinant human glucagon-like peptide (GLP)-1-albumin protein (albugon) mimics peptidergic activation of GLP-1 receptor-dependent pathways coupled with satiety, gastrointestinal motility, and glucose homeostasis. Diabetes 2004, 53:2492-2500.
29. Parkes DG, Pittner R, Jodka C, Smith P, Young A. Insulinotropic actions of exendin-4 and glucagon-like peptide-1 in vivo and in vitro. Metabolism 2001, 50:583-589.
30. Kim W, Egan JM. The role of incretins in glucose homeostasis and diabetes treatment. Pharmacol Rev 2008, 60:470-512.
31. Young AA, Gedulin BR, Bhavsar S, Bodkin N, Jodka C, Hansen B, Denaro M. Glucose-lowering and insulin-sensitizing actions of exendin-4: studies in obese diabetic (ob/ob, db/db) mice, diabetic fatty Zucker rats, and diabetic rhesus monkeys (Macaca mulatta). Diabetes 1999, 48:1026-1034.
32. Parkinson JR, Chaudhri OB, Kuo YT, Field BC, Herlihy AH, Dhillo WS, Ghatei MA, Bloom SR, Bell JD. Differential patterns of neuronal activation in the brainstem and hypothalamus following peripheral injection of GLP-1, oxyntomodulin and lithium chloride in mice detected by manganese-enhanced magnetic resonance imaging (MEMRI). Neuroimage 2009, 44:1022-1031.
33. Eckel LA, Geary N. Estradiol treatment increases feeding-induced c-Fos expression in the brains of ovariectomized rats. Am J Physiol Regul Integr Comp Physiol 2001, 281:R738-R746.
34. Fraser KA, Davison JS. Meal-induced c-fos expression in brain stem is not dependent on cholecystokinin release. Am J Physiol Regul Integr Comp Physiol 1993, 265:R235-R239.
35. Smith GP. Cholecystokinin: A Molecular Negative-Feedback Control of Eating. Hormones, Brain and Behavior 2009, 2527-2540. Pfaff DWArnold APEtgen AMFahrbach SERubin RT. In, eds, San Diego, CA, Academic Press
36. Zittel TT, Glatzle J, Kreis ME, Starlinger M, Eichner M, Raybould HE, Becker HD, Jehle EC. C-fos protein expression in the nucleus of the solitary tract correlates with cholecystokinin dose injected and food intake in rats. Brain Res 1999, 846:1-11.
37. Rinaman L, Baker EA, Hoffman GE, Stricker EM, Verbalis JG. Medullary c-Fos activation in rats after ingestion of a satiating meal. Am J Physiol Regul Integr Comp Physiol 1998, 275:R262-R268.
38. Emond M, Schwartz GJ, Moran TH. Meal-related stimuli differentially induce c-Fos activation in the nucleus of the solitary tract. Am J Physiol Regul Integr Comp Physiol 2001, 280:R1315-R1321.
39. Verbalis JG, McCann MJ, McHale CM, Stricker EM. Oxytocin secretion in response to cholecystokinin and food: differentiation of nausea from satiety. Science 1986, 232:1417-1419.
40. Michel S, Becskei C, Erguven E, Lutz TA, Riediger T. Diet-derived nutrients modulate the effects of amylin on c-Fos expression in the area postrema and on food intake. Neuroendocrinology 2007, 86:124-135.
41. Rinaman L. Interoceptive stress activates glucagon-like peptide-1 neurons that project to the hypothalamus. Am J Physiol Regul Integr Comp Physiol 1999, 277:R582-R590.
42. Hayes MR, Bradley L, Grill HJ. Endogenous hindbrain glucagon-like peptide-1 receptor activation contributes to the control of food intake by mediating gastric satiation signaling. Endocrinology 2009, 150:2654-2659.
43. Vrang N, Phifer CB, Corkern MM, Berthoud HR. Gastric distension induces c-Fos in medullary GLP-1/2 containing neurons. Am J Physiol Regul Integr Comp Physiol 2003, 285:R470-R478.
44. Gaykema RP, Daniels TE, Shapiro NJ, Thacker GC, Park SM, Goehler LE. Immune challenge and satiety-related activation of both distinct and overlapping neuronal populations in the brainstem indicate parallel pathways for viscerosensory signaling. Brain Res 2009, 1294:61-79.
45. 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 2000, 279:R1449-R1454.
46. Burcelin R, Da Costa A, Drucker D, Thorens B. Glucose competence of the hepatoportal vein sensor requires the presence of an activated glucagon-like peptide-1 receptor. Diabetes 2001, 50:1720-1728.