GLP-1 receptor activation modulates appetite- and reward-related brain areas in humans

Diabetes

Volumn 63, Issue 12, 2014, Pages 4186-4196

  Van Bloemendaal, Liselotte ^a   IJzerman, Richard G ^a   Ten Kulve, Jennifer S ^a   Barkhof, Frederik ^a   Konrad, Robert J ^b   Drent, Madeleine L ^a   Veltman, Dick J ^a   Diamant, Michaela ^a  

^a VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^b ELI LILLY AND COMPANY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EXENDIN 4; EXENDIN[9-39]; GLUCAGON LIKE PEPTIDE 1 RECEPTOR; PLACEBO; SOMATOSTATIN; UNCLASSIFIED DRUG; ANTIDIABETIC AGENT; EXENDIN (9-39); GLUCAGON RECEPTOR; GLUCAGON-LIKE PEPTIDE-1 RECEPTOR; PEPTIDE; PEPTIDE FRAGMENT; VENOM;

ADULT; AGED; AMYGDALOID NUCLEUS; APPETITE; ARTICLE; ASSOCIATION; BRAIN REGION; CLINICAL ARTICLE; CONTROLLED STUDY; CROSSOVER PROCEDURE; DRUG EFFECT; EVOKED VISUAL RESPONSE; FEMALE; FOOD INTAKE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; GLUCOSE CLAMP TECHNIQUE; HUMAN; HUNGER; IMAGERY; INSULA; MALE; NEUROMODULATION; NON INSULIN DEPENDENT DIABETES MELLITUS; OBESITY; ORBITAL CORTEX; PUTAMEN; RANDOMIZED CONTROLLED TRIAL; RECEPTOR UPREGULATION; REWARD; SOMATOSTATIN PANCREATIC PITUITARY CLAMP; WEIGHT REDUCTION; AGONISTS; ANTAGONISTS AND INHIBITORS; BRAIN; BRAIN CORTEX; CASE CONTROL STUDY; DRUG EFFECTS; FEEDING BEHAVIOR; FUNCTIONAL NEUROIMAGING; METABOLISM; MIDDLE AGED; NUCLEAR MAGNETIC RESONANCE IMAGING; PHOTOSTIMULATION; PHYSIOLOGY; PREFRONTAL CORTEX;

ADULT; AGED; AMYGDALA; APPETITE; BRAIN; CASE-CONTROL STUDIES; CEREBRAL CORTEX; CROSS-OVER STUDIES; DIABETES MELLITUS, TYPE 2; FEEDING BEHAVIOR; FEMALE; FUNCTIONAL NEUROIMAGING; HUMANS; HYPOGLYCEMIC AGENTS; MAGNETIC RESONANCE IMAGING; MALE; MIDDLE AGED; OBESITY; PEPTIDE FRAGMENTS; PEPTIDES; PHOTIC STIMULATION; PREFRONTAL CORTEX; PUTAMEN; RECEPTORS, GLUCAGON; REWARD; VENOMS;

EID: 84910070505     PISSN: 00121797     EISSN: 1939327X     Source Type: Journal    
DOI: 10.2337/db14-0849     Document Type: Article

References (51)

1. Whiting DR, Guariguata L, Weil C, Shaw J. IDF diabetes atlas: global estimates of the prevalence of diabetes for 2011 and 2030. Diabetes Res Clin Pract 2011;94:311-321
2. Flegal KM, Carroll MD, Kit BK, Ogden CL. Prevalence of obesity and trends in the distribution of body mass index among US adults, 1999-2010. JAMA 2012; 307:491-497
3. Volkow ND, Wang GJ, Tomasi D, Baler RD. Obesity and addiction: neurobiological overlaps. Obes Rev 2013;14:2-18
4. Tang DW, Fellows LK, Small DM, Dagher A. Food and drug cues activate similar brain regions: a meta-analysis of functional MRI studies. Physiol Behav 2012;106:317-324
5. Rothemund Y, Preuschhof C, Bohner G, et al. Differential activation of the dorsal striatum by high-calorie visual food stimuli in obese individuals. Neuroimage 2007;37:410-421
6. Stoeckel LE, Weller RE, Cook EW 3rd, Twieg DB, Knowlton RC, Cox JE. Widespread reward-system activation in obese women in response to pictures of high-calorie foods. Neuroimage 2008;41:636-647
7. Murdaugh DL, Cox JE, Cook EW 3rd, Weller RE. fMRI reactivity to highcalorie food pictures predicts short- and long-term outcome in a weight-loss program. Neuroimage 2012;59:2709-2721
8. Karra E, O'Daly OG, Choudhury AI, et al. A link between FTO, ghrelin, and impaired brain food-cue responsivity. J Clin Invest 2013;123:3539-3551
9. Rosenbaum M, Sy M, Pavlovich K, Leibel RL, Hirsch J. Leptin reverses weight loss-induced changes in regional neural activity responses to visual food stimuli. J Clin Invest 2008;118:2583-2591
10. Schloegl H, Percik R, Horstmann A, Villringer A, Stumvoll M. Peptide hormones regulating appetite-focus on neuroimaging studies in humans. Diabetes Metab Res Rev 2011;27:104-112
11. Drucker DJ, Nauck MA. The incretin system: glucagon-like peptide-1 receptor agonists and dipeptidyl peptidase-4 inhibitors in type 2 diabetes. Lancet 2006;368:1696-1705
12. Verdich C, Flint A, Gutzwiller JP, et al. A meta-analysis of the effect of glucagon-like peptide-1 (7-36) amide on ad libitum energy intake in humans. J Clin Endocrinol Metab 2001;86:4382-4389
13. Williams DL, Baskin DG, Schwartz MW. Evidence that intestinal glucagonlike peptide-1 plays a physiological role in satiety. Endocrinology 2009;150: 1680-1687
14. Vilsbøll T, Christensen M, Junker AE, Knop FK, Gluud LL. Effects of glucagon-like peptide-1 receptor agonists on weight loss: systematic review and meta-analyses of randomised controlled trials. BMJ 2012;344:d7771
15. van Bloemendaal L, Ten Kulve JS, la Fleur SE, Ijzerman RG, Diamant M. Effects of glucagon-like peptide 1 on appetite and body weight: focus on the CNS. J Endocrinol 2014;221:T1-T16
16. Sisley S, Gutierrez-Aguilar R, Scott M, D'Alessio DA, Sandoval DA, Seeley RJ. Neuronal GLP1R mediates liraglutide's anorectic but not glucose-lowering effect. J Clin Invest 2014;124:2456-2463
17. Pannacciulli N, Le DS, Salbe AD, et al. Postprandial glucagon-like peptide-1 (GLP-1) response is positively associated with changes in neuronal activity of brain areas implicated in satiety and food intake regulation in humans. Neuroimage 2007;35:511-517
18. Garner DM, Olmsted MP. Scoring the eating disorder inventory. Am J Psychiatry 1986;143:680-681
19. Schroevers MJ, Sanderman R, van Sonderen E, Ranchor AV. The evaluation of the Center for Epidemiologic Studies Depression (CES-D) scale: depressed and positive affect in cancer patients and healthy reference subjects. Qual Life Res 2000;9:1015-1029
20. Lerche S, Brock B, Rungby J, et al. Glucagon-like peptide-1 inhibits bloodbrain glucose transfer in humans. Diabetes 2008;57:325-331
21. Salehi M, Vahl TP, D'Alessio DA. Regulation of islet hormone release and gastric emptying by endogenous glucagon-like peptide 1 after glucose ingestion. J Clin Endocrinol Metab 2008;93:4909-4916
22. Fehse F, Trautmann M, Holst JJ, et al. Exenatide augments first- and second-phase insulin secretion in response to intravenous glucose in subjects with type 2 diabetes. J Clin Endocrinol Metab 2005;90:5991-5997
23. Hill AJ, Rogers PJ, Blundell JE. Techniques for the experimental measurement of human eating behaviour and food intake: a practical guide. Int J Obes Relat Metab Disord 1995;19:361-375
24. Wald FDM, Mellenbergh GJ. The shortened version of the Dutch translation of the Profile of Mood States (POMS). Ned Tijdschr Psychol 1990;45:86-90 [in Dutch]
25. Killgore WD, Young AD, Femia LA, Bogorodzki P, Rogowska J, Yurgelun- Todd DA. Cortical and limbic activation during viewing of high- versus low-calorie foods. Neuroimage 2003;19:1381-1394
26. Yokum S, Ng J, Stice E. Attentional bias to food images associated with elevated weight and future weight gain: an fMRI study. Obesity (Silver Spring) 2011;19:1775-1783
27. Small DM, Gregory MD, Mak YE, Gitelman D, Mesulam MM, Parrish T. Dissociation of neural representation of intensity and affective valuation in human gustation. Neuron 2003;39:701-711
28. Feltrin KL, Little TJ, Meyer JH, et al. Effects of intraduodenal fatty acids on appetite, antropyloroduodenal motility, and plasma CCK and GLP-1 in humans vary with their chain length. Am J Physiol Regul Integr Comp Physiol 2004;287: R524-R533
29. Fineman M, Flanagan S, Taylor K, et al. Pharmacokinetics and pharmacodynamics of exenatide extended-release after single and multiple dosing. Clin Pharmacokinet 2011;50:65-74
30. Drucker DJ, Buse JB, Taylor K, et al.; DURATION-1 Study Group. Exenatide once weekly versus twice daily for the treatment of type 2 diabetes: a randomised, open-label, non-inferiority study. Lancet 2008;372:1240-1250
31. Pelchat ML, Johnson A, Chan R, Valdez J, Ragland JD. Images of desire: food-craving activation during fMRI. Neuroimage 2004;23:1486-1493
32. Small DM, Zatorre RJ, Dagher A, Evans AC, Jones-Gotman M. Changes in brain activity related to eating chocolate: from pleasure to aversion. Brain 2001; 124:1720-1733
33. Baxter MG, Murray EA. The amygdala and reward. Nat Rev Neurosci 2002; 3:563-573
34. Everitt BJ, Cardinal RN, Parkinson JA, Robbins TW. Appetitive behavior: impact of amygdala-dependent mechanisms of emotional learning. Ann N Y Acad Sci 2003;985:233-250
35. Hare TA, O'Doherty J, Camerer CF, Schultz W, Rangel A. Dissociating the role of the orbitofrontal cortex and the striatum in the computation of goal values and prediction errors. J Neurosci 2008;28:5623-5630
36. Wallis JD. Orbitofrontal cortex and its contribution to decision-making. Annu Rev Neurosci 2007;30:31-56
37. Malik S, McGlone F, Bedrossian D, Dagher A. Ghrelin modulates brain activity in areas that control appetitive behavior. Cell Metab 2008;7:400-409
38. De Silva A, Salem V, Long CJ, et al. The gut hormones PYY 3-36 and GLP-1 7-36 amide reduce food intake and modulate brain activity in appetite centers in humans. Cell Metab 2011;14:700-706
39. Hussain SS, Bloom SR. The regulation of food intake by the gut-brain axis: implications for obesity. Int J Obes (Lond) 2013;37:625-633
40. Kastin AJ, Akerstrom V. Entry of exendin-4 into brain is rapid but may be limited at high doses. Int J Obes Relat Metab Disord 2003;27:313-318
41. Dickson SL, Shirazi RH, Hansson C, Bergquist F, Nissbrandt H, Skibicka KP. The glucagon-like peptide 1 (GLP-1) analogue, exendin-4, decreases the rewarding value of food: a new role for mesolimbic GLP-1 receptors. J Neurosci 2012;32:4812-4820
42. Abbott CR, Monteiro M, Small CJ, et al. 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
43. 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
44. Banks WA, During MJ, Niehoff ML. Brain uptake of the glucagon-like peptide-1 antagonist exendin(9-39) after intranasal administration. J Pharmacol Exp Ther 2004;309:469-475
45. Meier JJ, Gallwitz B, Salmen S, et al. Normalization of glucose concentrations and deceleration of gastric emptying after solid meals during intravenous glucagon-like peptide 1 in patients with type 2 diabetes. J Clin Endocrinol Metab 2003;88:2719-2725
46. Gutzwiller JP, Drewe J, Göke B, et al. Glucagon-like peptide-1 promotes satiety and reduces food intake in patients with diabetes mellitus type 2. Am J Physiol 1999;276:R1541-R1544
47. DeFronzo RA, Ratner RE, Han J, Kim DD, Fineman MS, Baron AD. Effects of exenatide (exendin-4) on glycemic control and weight over 30 weeks in metformin-treated patients with type 2 diabetes. Diabetes Care 2005;28:1092-1100
48. Nauck MA, Kemmeries G, Holst JJ, Meier JJ. Rapid tachyphylaxis of the glucagon-like peptide 1-induced deceleration of gastric emptying in humans. Diabetes 2011;60:1561-1565
49. Diamant M, Van Gaal L, Guerci B, et al. Exenatide once weekly versus insulin glargine for type 2 diabetes (DURATION-3): 3-year results of an open-label randomised trial. Lancet Diabetes Endocrinol 2014;2:464-473
50. Flint A, Raben A, Astrup A, Holst JJ. Glucagon-like peptide 1 promotes satiety and suppresses energy intake in humans. J Clin Invest 1998;101:515-520
51. Stubbs RJ, Hughes DA, Johnstone AM, et al. The use of visual analogue scales to assess motivation to eat in human subjects: a review of their reliability and validity with an evaluation of new hand-held computerized systems for temporal tracking of appetite ratings. Br J Nutr 2000;84:405-415