Glucagon-Like Peptide-1 Receptor in the Brain: Role in Neuroendocrine Control of Energy Metabolism and Treatment Target for Obesity

Journal of Neuroendocrinology

Volumn 25, Issue 7, 2013, Pages 597-604

  Lockie, S H ^a  

^a MONASH UNIVERSITY   (Australia)

Author keywords

Diabetes; Feeding; GLP 1; Metabolism; Obesity; Oxyntomodulin

Indexed keywords

ALOGLIPTIN; EXENDIN 4; FURIN; GLICENTIN; GLUCAGON LIKE PEPTIDE 1; GLUCAGON LIKE PEPTIDE 1 RECEPTOR; GLUCAGON LIKE PEPTIDE 2; LINAGLIPTIN; LIRAGLUTIDE; MESSENGER RNA; OXYNTOMODULIN; PROTEIN FOS; SAXAGLIPTIN; SITAGLIPTIN; STAT3 PROTEIN; VILDAGLIPTIN; GLUCAGON RECEPTOR; GLUCAGON-LIKE PEPTIDE-1 RECEPTOR;

ARTICLE; BLOOD BRAIN BARRIER; CLINICAL TRIAL (TOPIC); DEPOLARIZATION; ENERGY EXPENDITURE; ENERGY METABOLISM; FOOD INTAKE; GASTROINTESTINAL SYMPTOM; HUMAN; IMMUNOREACTIVITY; INSULIN RELEASE; NAUSEA AND VOMITING; NEUROBIOLOGY; NEUROENDOCRINE SYSTEM; NON INSULIN DEPENDENT DIABETES MELLITUS; OBESITY; PRIORITY JOURNAL; RHOMBENCEPHALON; WEIGHT REDUCTION; BRAIN; METABOLISM; PATHOPHYSIOLOGY; PHYSIOLOGY; SIGNAL TRANSDUCTION;

BRAIN; ENERGY METABOLISM; GLUCAGON-LIKE PEPTIDE 1; HUMANS; OBESITY; RECEPTORS, GLUCAGON; SIGNAL TRANSDUCTION;

EID: 84879139320     PISSN: 09538194     EISSN: 13652826     Source Type: Journal    
DOI: 10.1111/jne.12039     Document Type: Article

References (72)

1. Walls HL, Magliano DJ, Stevenson CE, Backholer K, Mannan HR, Shaw JE, Peeters A. Projected progression of the prevalence of obesity in Australia. Obesity (Silver Spring) 2012; 20: 872-878.
2. Nejat EJ, Polotsky AJ, Pal L. Predictors of chronic disease at midlife and beyond - the health risks of obesity. Maturitas 2010; 65: 106-111.
3. Hammond RA, Levine R. The economic impact of obesity in the United States. Diabetes Metab Syndr Obes 2010; 3: 285-295.
4. Sikorski C, Luppa M, Kaiser M, Glaesmer H, Schomerus G, Konig HH, Riedel-Heller SG. The stigma of obesity in the general public and its implications for public health - a systematic review. BMC Public Health 2011; 11: 661.
5. Fettich KC, Chen EY. Coping with obesity stigma affects depressed mood in African-American and Caucasian candidates for bariatric surgery. Obesity (Silver Spring) 2012; 20: 1118-1121.
6. Dansinger ML, Tatsioni A, Wong JB, Chung M, Balk EM. Meta-analysis: the effect of dietary counseling for weight loss. Ann Intern Med 2007; 147: 41-50.
7. Cooke D, Bloom S. The obesity pipeline: current strategies in the development of anti-obesity drugs. Nat Rev Drug Discov 2006; 5: 919-931.
8. Gadde KM, Allison DB, Ryan DH, Peterson CA, Troupin B, Schwiers ML, Day WW. Effects of low-dose, controlled-release, phentermine plus topiramate combination on weight and associated comorbidities in overweight and obese adults (CONQUER): a randomised, placebo-controlled, phase 3 trial. Lancet 2011; 377: 1341-1352.
9. Smith SR, Weissman NJ, Anderson CM, Sanchez M, Chuang E, Stubbe S, Bays H, Shanahan WR, Behav M, Lorcaserin O. Multicenter, placebo-controlled trial of lorcaserin for weight management. N Engl J Med 2010; 363: 245-256.
10. O'Brien PE, McPhail T, Chaston TB, Dixon JB. Systematic review of medium-term weight loss after bariatric operations. Obes Surg 2006; 16: 1032-1040.
11. Dixon JB, le Roux CW, Rubino F, Zimmet P. Bariatric surgery for type 2 diabetes. Lancet 2012; 379: 2300-2311.
12. Buchwald H, Estok R, Fahrbach K, Banel D, Sledge I. Trends in mortality in bariatric surgery: a systematic review and meta-analysis. Surgery 2007; 142: 621-632.
13. Mentlein R, Gallwitz B, Schmidt WE. Dipeptidylpeptidase-IV hydrolyzes gastric-inhibitory polypeptide, glucagon-like peptide-1(7-36)amide, peptide histidine methionine and is responsible for their Degradation in human serum. Eur J Biochem 1993; 214: 829-835.
14. Bataille D. Pro-protein convertases in intermediary metabolism: islet hormones, brain/gut hormones and integrated physiology. J Mol Med 2007; 85: 673-684.
15. Mineo I, Matsumura T, Shingu R, Namba M, Kuwajima M, Matsuzawa Y. THE ROLe of prohormone convertases PC1 (PC3) and PC2 in the cell-specific processing of proglucagon. Biochem Biophys Res Commun 1995; 207: 646-651.
16. Drucker DJ, Asa S. GLUCAGON gene-expression in vertebrate brain. J Biol Chem 1988; 263: 13475-13478.
17. Baggio LL, Huang QL, Brown TJ, Drucker DJ. Oxyntomodulin and glucagon-like peptide-1 differentially regulate murine food intake and energy expenditure. Gastroenterology 2004; 127: 546-558.
18. Larsen PJ, TangChristensen M, Holst JJ, Orskov C. Distribution of glucagon-like peptide-1 and other preproglucagon-derived peptides in the rat hypothalamus and brainstem. Neuroscience 1997; 77: 257-270.
19. Goke R, Larsen PJ, Mikkelsen JD, Sheikh SP. Distribution of GLP-1 binding-sites in the rat-brain - evidence that exendin-4 is A ligand of brain GLP-1 binding-sites. Eur J Neurosci 1995; 7: 2294-2300.
20. Deacon CF, Nauck MA, Toftnielsen M, Pridal L, Willms B, Holst JJ. Both subcutaneously and intravenously administered glucagon-like Peptide-I are rapidly degraded from the NH2-terminus in type-II diabetic-patients and in healthy-subjects. Diabetes 1995; 44: 1126-1131.
21. Turton MD, Oshea D, Gunn I, Beak SA, Edwards CMB, Meeran K, Choi SJ, Taylor GM, Heath MM, Lambert PD, Wilding JPH, Smith DM, Ghatei MA, Herbert J, Bloom SR. A role for glucagon-like peptide-1 in the central regulation of feeding. Nature 1996; 379: 69-72.
22. vanDijk G, Thiele TE, Donahey JCK, Campfield LA, Smith FJ, Burn P, Bernstein IL, Woods SC, Seeley RJ. Central infusions of leptin and GLP-1-(7-36) amide differentially stimulate c-FLI in the rat brain. Am J Physiol-Regul Integr Comp Physiol 1996; 271: R1096-R1100.
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. 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.
25. 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.
26. Dakin CL, Small CJ, Batterham RL, Neary NM, Cohen MA, Patterson M, Ghatei MA, Bloom SR. Peripheral oxyntomodulin reduces food intake and body weight gain in rats. Endocrinology 2004; 145: 2687-2695.
27. Lockie SH, Heppner KM, Chaudhary N, Chabenne JR, Morgan DA, Veyrat-Durebex C, Ananthakrishnan G, Rohner-Jeanrenaud F, Drucker DJ, Dimarchi R, Rahmouni K, Oldfield BJ, Tschop MH, Perez-Tilve D. Direct control of brown adipose tissue thermogenesis by central nervous system glucagon-like peptide-1 receptor signaling. Diabetes 2012; 61: 2753-2762.
28. Tang-Christensen M, Larsen PJ, Goke R, FinkJensen A, Jessop DS, Moller M, Sheikh SP. Central administration of GLP-1-(7-36) amide inhibits food and water intake in rats. Am J Physiol-Regul Integr Comp Physiol 1996; 271: R848-R856.
29. Gao Q, Horvath TL. Neuronal control of energy homeostasis. FEBS Lett 2008; 582: 132-141.
30. Seo S, Ju S, Chung H, Lee D, Park S. Acute effects of glucagon-like peptide-1 on hypothalamic neuropeptide and amp activated kinase expression in fasted rats. Endocr J 2008; 55: 867-874.
31. Sandoval DA, Bagnol D, Woods SC, D'Alessio DA, Seeley RJ. Arcuate glucagon-like peptide 1 receptors regulate glucose homeostasis but not food intake. Diabetes 2008; 57: 2046-2054.
32. McMahon LR, Wellman PJ. PVN infusion of GLP-1-(7-36) amide suppresses feeding but does not induce aversion or alter locomotion in rats. Am J Physiol-Regul Integr Comp Physiol 1998; 274: R23-R29.
33. Tang-Christensen M, Vrang N, Larsen PJ. Glucagon-like peptide 1(7-36) amide's central inhibition of feeding and peripheral inhibition of drinking are abolished by neonatal monosodium glutamate treatment. Diabetes 1998; 47: 530-537.
34. Poleni PE, Akieda-Asai S, Koda S, Sakurai M, Bae CR, Senba K, Cha YS, Furuya M, Date Y. Possible involvement of melanocortin-4-receptor and AMP-activated protein kinase in the interaction of glucagon-like peptide-1 and leptin on feeding in rats. Biochem Biophys Res Commun 2012; 420: 36-41.
35. Knauf C, Cani PD, Kim DH, Iglesias MA, Chabo C, Waget A, Colom A, Rastrelli S, Delzenne NM, Drucker DJ, Seeley RJ, Burcelin R. Role of central nervous system glueagon-like peptide-1 reeeptors in enteric glueose sensing. Diabetes 2008; 57: 2603-2612.
36. 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.
37. Hisadome K, Reimann F, Gribble FM, Trapp S. CCK Stimulation of GLP-1 neurons involves alpha(1)-adrenoceptor-mediated increase in glutamatergic synaptic inputs. Diabetes 2011; 60: 2701-2709.
38. Renner E, Puskas N, Dobolyi A, Palkovits M. Glucagon-like peptide-1 of brainstem origin activates dorsomedial hypothalamic neurons in satiated rats. Peptides 2012; 35: 14-22.
39. 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.
40. 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 2008; 149: 4059-4068.
41. Goldstone AP, Mercer JG, Gunn I, Moar KM, Edwards CMB, Rossi M, Howard JK, Rasheed S, Turton MD, Small C, Heath MM, Oshea D, Steere J, Meeran K, Ghatei MA, Hoggard N, Bloom SR. Leptin interacts with glucagon-like peptide-1 neurons to reduce food intake and body weight in rodents. FEBS Lett 1997; 415: 134-138.
42. Hisadome K, Reimann F, Gribble FM, Trapp S. Leptin directly depolarizes preproglucagon neurons in the nucleus tractus solitarius electrical properties of glucagon-like peptide 1 neurons. Diabetes 2010; 59: 1890-1898.
43. Scott MM, Williams KW, Rossi J, Lee CE, Elmquist JK. Leptin receptor expression in hindbrain Glp-1 neurons regulates food intake and energy balance in mice. J Clin Invest 2011; 121: 2413-2421.
44. Abbott CR, Monteiro M, Small CJ, Sajedi A, Smith KL, Parkinson JRC, Ghatei MA, Bloom SR. The inhibitory effects of peripheral administration of peptide YY3-36 and glucagon-like peptide-1 on food intake are attenuated by ablation of the vagal-brainstem-hypothalamic pathway. Brain Res 2005; 1044: 127-131.
45. Nakagawa A, Satake H, Nakabayashi H, Nishizawa M, Furuya K, Nakano S, Kigoshi T, Nakayama K, Uchida K. Receptor gene expression of glucagon-like peptide-1, but not glucose-dependent insulinotropic polypeptide, in rat nodose ganglion cells. Auton Neurosci-Basic Clin 2004; 110: 36-43.
46. Fujiwara K, Gotoh K, Chiba S, Masaki T, Katsuragi I, Kakuma T, Yoshimatsu H. 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: 66-76.
47. Kelley AE, Berridge KC. The neuroscience of natural rewards: relevance to addictive drugs. J Neurosci 2002; 22: 3306-3311.
48. Alhadeff AL, Rupprecht LE, Hayes MR. GLP-1 neurons in the nucleus of the solitary tract project directly to the ventral tegmental area and nucleus accumbens to control for food intake. Endocrinology 2012; 153: 647-658.
49. Dossat AM, Lilly N, Kay K, Williams DL. Glucagon-like peptide 1 receptors in nucleus accumbens affect food intake. J Neurosci 2011; 31: 14453-14457.
50. 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.
51. Miras AD, le Roux CW. Bariatric surgery and taste: novel mechanisms of weight loss. Curr Opin Gastroenterol 2010; 26: 140-145.
52. Deacon CF, Mannucci E, Ahren B. Glycaemic efficacy of glucagon-like peptide-1 receptor agonists and dipeptidyl peptidase-4 inhibitors as add-on therapy to metformin in subjects with type 2 diabetes-a review and meta analysis. Diabetes Obes Metab 2012; 14: 762-767.
53. Aroda VR, Henry RR, Han J, Huang WY, DeYoung MB, Darsow T, Hoogwerf BJ. Efficacy of GLP-1 receptor agonists and DPP-4 inhibitors: meta-analysis and systematic review. Clin Ther 2012; 34: 1247-1258.
54. Singh S, Chang HY, Richards TM, Weiner JP, Clark JM, Segal JB. Glucagonlike peptide 1-based therapies and risk of hospitalization for acute pancreatitis in type 2 diabetes mellitus: a population-based matched case-control study. JAMA Intern Med 2013; 173: 534-539.
55. Osaka T, Endo M, Yamakawa M, Inoue S. Energy expenditure by intravenous administration of glucagon-like peptide-1 mediated by the lower brainstem and sympathoadrenal system. Peptides 2005; 26: 1623-1631.
56. Pannacciulli N, Bunt JC, Koska J, Bogardus C, Krakoff J. Higher fasting plasma concentrations of glucagon-like peptide 1 are associated with higher resting energy expenditure and fat oxidation rates in humans. Am J Clin Nutr 2006; 84: 556-560.
57. Lockie SH, Czyzyk TA, Chaudhary N, Perez-Tilve D, Woods SC, Oldfield BJ, Statnick MA, Tschop MH. CNS opioid signaling separates cannabinoid receptor 1-mediated effects on body weight and mood-related behavior in mice. Endocrinology 2011; 152: 3661-3667.
58. Verty AN, Lockie SH, Stefanidis A, Oldfield BJ. Anti-obesity effects of the combined administration of CB1 receptor antagonist rimonabant and melanin-concentrating hormone antagonist SNAP-94847 in diet-inudced obese mice. Int J Obes (Lond) 2013; 37: 279-287.
59. Ravussin E, Smith SR, Mitchell JA, Shringarpure R, Shan K, Maier H, Koda JE, Weyer C. Enhanced weight loss with pramlintide/metreleptin: an integrated neurohormonal approach to obesity pharmacotherapy. Obesity 2009; 17: 1736-1743.
60. Greenway FL, Whitehouse MJ, Guttadauria M, Anderson JW, Atkinson RL, Fujioka K, Gadde KM, Gupta AK, O'Neil P, Schumacher D, Smith D, Dunayevich E, Tollefson GD, Weber E, Cowley MA. Rational design of a combination medication for the treatment of obesity. Obesity 2009; 17: 30-39.
61. Wynne K, Park AJ, Small CJ, Meeran K, Ghatei MA, Frost GS, Bloom SR. Oxyntomodulin increases energy expenditure in addition to decreasing energy intake in overweight and obese humans: a randomised controlled trial. Int J Obes 2006; 30: 1729-1736.
62. Dakin CL, Small CJ, Park AJ, Seth A, Ghatei MA, Bloom SR. Repeated ICV administration of oxyntomodulin causes a greater reduction in body weight gain than in pair-fed rats. Am J Physiol-Endocrinol Metab 2002; 283: E1173-E1177.
63. Maida A, Lovshin JA, Baggio LL, Drucker DJ. The Glucagon-like peptide-1 receptor agonist oxyntomodulin enhances beta-cell function but does not inhibit gastric emptying in mice. Endocrinology 2008; 149: 5670-5678.
64. Parkinson JRC, Chaudhri OB, Kuo YT, Field BCT, 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.
65. Pocai A, Carrington PE, Adams JR, Wright M, Eiermann G, Zhu L, Du XB, Petrov A, Lassman ME, Jiang GQ, Liu F, Miller C, Tota LM, Zhou GC, Zhang XP, Sountis MM, Santoprete A, Capito E, Chicchi GG, Thornberry N, Bianchi E, Pessi A, Marsh DJ, SinhaRoy R. Glucagon-like peptide 1/glucagon receptor dual agonism reverses obesity in mice. Diabetes 2009; 58: 2258-2266.
66. Du XB, Kosinski JR, Lao JL, Shen XL, Petrov A, Chicchi GG, Eiermann GJ, Pocai A. Differential effects of oxyntomodulin and GLP-1 on glucose metabolism. Am J Physiol-Endocrinol Metab 2012; 303: E265-E271.
67. Holloway SA, Stevenson JA. Effect of glucagon on oxygen consumption in cold-adapted rat. Can J Physiol Pharmacol 1964; 42: 860-&.
68. Davidson IWF, Salter JM, Best CH. The effect of glucagon on the metabolic rate of rats. Am J Clin Nutr 1960; 8: 540-546.
69. Habegger KM, Heppner KM, Geary N, Bartness TJ, DiMarchi R, Tschop MH. The metabolic actions of glucagon revisited. Nat Rev Endocrinol 2010; 6: 689-697.
70. Day JW, Ottaway N, Patterson JT, Gelfanov V, Smiley D, Gidda J, Findeisen H, Bruemmer D, Drucker DJ, Chaudhary N, Holland J, Hembree J, Abplanalp W, Grant E, Ruehl J, Wilson H, Kirchner H, Lockie SH, Hofmann S, Woods SC, Nogueiras R, Pfluger PT, Perez-Tilve D, DiMarchi R, Tschop MH. A new glucagon and GLP-1 co-agonist eliminates obesity in rodents. Nat Chem Biol 2009; 5: 749-757.
71. Day JW, Gelfanov V, Smiley D, Carrington PE, Eiermann G, Chicchi G, Erion MD, Gidda J, Thornberry NA, Tschop MH, Marsh DJ, SinhaRoy R, DiMarchi R, Pocai A. Optimization of co-agonism at GLP-1 and glucagon receptors to safely maximize weight reduction in DIO-rodents. Biopolymers 2012; 98: 443-450.
72. Tan TM, Field BC, McCullough KA, Troke RC, Chambers ES, Salem V, Gonzalez MJ, Baynes KC, De Silva A, Viardot A, Alsafi A, Frost GS, Ghatei MA, Bloom SR. Coadministration of glucagon-like Peptide-1 during glucagon infusion in humans results in increased energy expenditure and amelioration of hyperglycemia. Diabetes 2013; 62: 1131-1138.