Pancreatic GLP-1 receptor activation is sufficient for incretin control of glucose metabolism in mice

Journal of Clinical Investigation

Volumn 122, Issue 1, 2012, Pages 388-402

  Lamont, Benjamin J ^a   Li, Yazhou ^a   Kwan, Edwin ^b   Brown, Theodore J ^a   Gaisano, Herbert ^b   Drucker, Daniel J ^a  

^a MOUNT SINAI HOSPITAL   (Canada)

^b UNIVERSITY HEALTH NETWORK   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC AMP; EXENDIN 4; GLUCAGON LIKE PEPTIDE 1 RECEPTOR; INCRETIN; PROTEIN C FOS; PROTEIN KINASE B;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; FEMALE; GLUCOSE HOMEOSTASIS; GLUCOSE METABOLISM; GLUCOSE TOLERANCE; INSULIN RELEASE; MALE; MOUSE; NERVE TRACT; NONHUMAN; PANCREAS ISLET CELL; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; STOMACH EMPTYING; TRANSGENIC MOUSE;

ANIMALS; GLUCAGON-LIKE PEPTIDE 1; GLUCOSE; GLUCOSE TOLERANCE TEST; HOMEOSTASIS; HUMANS; INCRETINS; INSULIN; INSULIN-SECRETING CELLS; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; NEUROSECRETORY SYSTEMS; PANCREAS; PEPTIDE FRAGMENTS; RECEPTORS, GLUCAGON; RECOMBINANT PROTEINS; SIGNAL TRANSDUCTION;

EID: 84855465547     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI42497     Document Type: Article

References (65)

1. Cherrington AD. Banting Lecture 1997. Control of glucose uptake and release by the liver in vivo. Diabetes. 1999;48(5):1198-1214. (Pubitemid 29226371)
2. Sandoval D, Cota D, Seeley RJ. The integrative role of CNS fuel-sensing mechanisms in energy balance and glucose regulation. Annu Rev Physiol. 2008;70:513-535. (Pubitemid 351738190)
3. Ahima RS, Lazar MA. Adipokines and the peripheral and neural control of energy balance. Mol Endocrinol. 2008;22(5):1023-1031. (Pubitemid 351629604)
4. Scherer PE. Adipose tissue: from lipid storage compartment to endocrine organ. Diabetes. 2006;55(6):1537-1545. (Pubitemid 44324105)
5. Lam TK, Gutierrez-Juarez R, Pocai A, Rossetti L. Regulation of blood glucose by hypothalamic pyruvate metabolism. Science. 2005;309(5736):943-947. (Pubitemid 41099933)
6. Lam TK, et al. Hypothalamic sensing of circulating fatty acids is required for glucose homeostasis. Nat Med. 2005;11(3):320-327. (Pubitemid 40460561)
7. Knauf C, et al. Role of central nervous system glucagon-like peptide-1 receptors in enteric glucose sensing. Diabetes. 2008;57(10):2603-2612.
8. Cheung GW, Kokorovic A, Lam CK, Chari M, Lam TK. Intestinal cholecystokinin controls glucose production through a neuronal network. Cell Metab. 2009;10(2):99-109.
9. Cummings DE, Overduin J. Gastrointestinal regulation of food intake. J Clin Invest. 2007;117(1):13-23. (Pubitemid 46048445)
10. Holst JJ, Gromada J. Role of incretin hormones in the regulation of insulin secretion in diabetic and nondiabetic humans. Am J Physiol Endocrinol Metab. 2004;287(2):E199-E206. (Pubitemid 38943883)
11. Nauck MA. Is glucagon-like peptide 1 an incretin hormone? Diabetologia. 1999;42(3):373-379. (Pubitemid 29111446)
12. Waget A, et al. Physiological and pharmacological mechanisms through which the DPP-4 inhibitor sitagliptin regulates glycemia in mice. Endocrinology. 2011;152(8):3018-3029.
13. Imeryuz N, Yegen BC, Bozkurt A, Coskun T, Villanueva-Pennacarrillo ML, Ulusoy NB. Glucagon-like peptide-1 inhibits gastric emptying via vagal afferent-mediated central mechanisms. Am J Physiol. 1997;273(4 pt 1):G920-G927.
14. 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(9):2492-2500. (Pubitemid 39145610)
15. Baggio LL, Huang Q, Brown TJ, Drucker DJ. Oxyntomodulin and glucagon-like peptide-1 differentially regulate murine food intake and energy expenditure. Gastroenterology. 2004;127(2):546-558. (Pubitemid 39091903)
16. Turton MD, et al. A role for glucagon-like peptide-1 in the central regulation of feeding. Nature. 1996; 379(6560):69-72. (Pubitemid 26008136)
17. Meeran K, et al. Repeated intracerebroventricular administration of glucagon-like peptide-1-(7-36) amide or exendin-(9-39) alters body weight in the rat. Endocrinology. 1999;140(1):244-250. (Pubitemid 29011165)
18. Baggio LL, Huang Q, Cao X, Drucker DJ. The long-acting albumin-exendin-4 GLP-1R agonist CJC-1134 engages central and peripheral mechanisms regulating glucose homeostasis. Gastroenterology. 2008;134(4):1137-1147. (Pubitemid 351451971)
19. Rosenstock J, Reusch J, Bush M, Yang F, Stewart M. Potential of albiglutide, a long-acting GLP-1 receptor agonist, in type 2 diabetes: a randomized controlled trial exploring weekly, biweekly, and monthly dosing. Diabetes Care. 2009;32(10):1880-1886.
20. Williams DL. Minireview: finding the sweet spot: peripheral versus central glucagon-like peptide 1 action in feeding and glucose homeostasis. Endocrinology. 2009;150(7):2997-3001.
21. 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(8):1720-1728. (Pubitemid 33641588)
22. Dardevet D, et al. Insulin secretion-independent effects of glucagon-like peptide 1 (GLP-1) on canine liver glucose metabolism do not involve portal vein GLP-1 receptors. Am J Physiol Gastrointest Liver Physiol. 2005;289(5):G806- G814. (Pubitemid 41532573)
23. Drucker DJ, Brubaker PL. Glucagon biosynthesis in fetal rat intestine. Biomed Res. 1988;9(suppl 3):29-32. (Pubitemid 19237030)
24. Jin S-LC, Han VKM, Simmons JG, Towle AC, Lauder JM, Lund PK. Distribution of glucagonlike peptide 1 (GLP-1), glucagon, and glicentin in the rat brain: An immunocytochemical study. J Comp Neurol. 1988;271(4):519-532.
25. Larsen PJ, Tang-Christensen 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(1):257-270. (Pubitemid 27060323)
26. Knauf C, et al. Brain glucagon-like peptide-1 increases insulin secretion and muscle insulin resistance to favor hepatic glycogen storage. J Clin Invest. 2005;115(12):3554-3563. (Pubitemid 43121843)
27. 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(8):2046-2054.
28. Nakabayashi H, Nishizawa M, Nakagawa A, Takeda R, Niijima A. Vagal hepatopancreatic reflex effect evoked by intraportal appearance of tGLP-1. Am J Physiol. 1996;271(5 Pt 1):E808-E813.
29. Vahl TP, et al. Glucagon-like 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. 2007;148(10):4965-4973. (Pubitemid 47481523)
30. Stoffers DA, Heller RS, Miller CP, Habener JF. Developmental expression of the homeodomain protein IDX-1 in mice transgenic for an IDX-1 promoter/lacZ transcriptional reporter. Endocrinology. 1999;140(11):5374-5381.
31. Drucker DJ, Philippe J, Mojsov S, Chick WL, Habener JF. Glucagon-like peptide I stimulates insulin gene expression and increases cyclic AMP levels in a rat islet cell line. Proc Natl Acad Sci U S A. 1987;84(10):3434-3438. (Pubitemid 17085418)
32. Edwards CM, 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. (Pubitemid 29019356)
33. Scrocchi LA, et al. Glucose intolerance but normal satiety in mice with a null mutation in the glucagon-like peptide receptor gene. Nature Med. 1996;2(11):1254-1258. (Pubitemid 26375413)
34. Ali S, Lamont BJ, Charron MJ, Drucker DJ. Dual elimination of the glucagon and GLP-1 receptors in mice reveals plasticity in the incretin axis. J Clin Invest. 2011;121(5):1917-1929.
35. Hansotia T, et al. Double incretin receptor knockout (DIRKO) mice reveal an essential role for the enteroinsular axis in transducing the glucoregulatory actions of DPP-IV inhibitors. Diabetes. 2004;53(5):1326-1335. (Pubitemid 38569020)
36. Maida A, Lamont BJ, Cao X, Drucker DJ. Metformin regulates the incretin receptor axis via a pathway dependent on peroxisome proliferator-activated receptor-alpha in mice. Diabetologia. 2011;54(2):339-349.
37. Yamamoto H, et al. 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(7):2939-2946. (Pubitemid 36418630)
38. Yamamoto H, et al. Glucagon-like peptide-1 receptor stimulation increases blood pressure and heart rate and activates autonomic regulatory neurons. J Clin Invest. 2002;110(1):43-52. (Pubitemid 34743464)
39. Rankin MM, Kushner JA. Adaptive beta-cell proliferation is severely restricted with advanced age. Diabetes. 2009;58(6):1365-1372.
40. Xu G, Stoffers DA, Habener JF, Bonner-Weir S. Exendin-4 stimulates both beta-cell replication and neogenesis, resulting in increased beta-cell mass and improved glucose tolerance in diabetic rats. Diabetes. 1999;48(12):2270-2276. (Pubitemid 30395416)
41. Koehler JA, Baggio LL, Lamont BJ, Ali S, Drucker DJ. GLP-1 receptor activation modulates pancreatitis-associated gene expression but does not modify the susceptibility to experimental pancreatitis in mice. Diabetes. 2009;58(9):2148-2161.
42. Simonsen L, et al. Exendin-4, but not dipeptidyl peptidase IV inhibition, increases small intestinal mass in GK rats. Am J Physiol Gastrointest Liver Physiol. 2007;293(1):G288-G295. (Pubitemid 47105178)
43. Tschen SI, Dhawan S, Gurlo T, Bhushan A. Age-dependent decline in beta cell proliferation restricts the capacity of beta cell regeneration in mice. Diabetes. 2009;58(6):1312-1320.
44. Merchenthaler I, Lane M, Shughrue P. Distribution of pre-pro-glucagon and glucagon-like peptide-1 receptor messenger RNAs in the rat central nervous system. J Comp Neurol. 1999;403(2):261-280. (Pubitemid 28566834)
45. Nakagawa A, et al. Receptor gene expression of glucagon-like peptide-1, but not glucose-dependent insulinotropic polypeptide, in rat nodose ganglion cells. Auton Neurosci. 2004;110(1):36-43. (Pubitemid 38180536)
46. Nishizawa M, et al. Effect of intraportal glucagon-like peptide-1 on glucose metabolism in conscious dogs. Am J Physiol Endocrinol Metab. 2003;284(5):E1027-E1036. (Pubitemid 36444040)
47. Ionut V, Hucking K, Liberty IF, Bergman RN. Synergistic effect of portal glucose and glucagon-like peptide-1 to lower systemic glucose and stimulate counter-regulatory hormones. Diabetologia. 2005;48(5):967-975. (Pubitemid 40767991)
48. Ionut V, Zheng D, Stefanovski D, Bergman RN. Exenatide can reduce glucose independent of islet hormones or gastric emptying. Am J Physiol Endocrinol Metab. 2008;295(2):E269-E277.
49. Drucker DJ, Asa S. Glucagon gene expression in vertebrate brain. J Biol Chem. 1988;263(27):13475-13478.
50. Shimizu I, Hirota M, Ohboshi C, Shima K. Identification and localization of glucagon-like peptide-1 and its receptor in rat brain. Endocrinology. 1987;121(3):1076-1082. (Pubitemid 17139162)
51. Kinzig KP, et al. CNS glucagon-like peptide-1 receptors mediate endocrine and anxiety responses to interoceptive and psychogenic stressors. J Neurosci. 2003;23(15):6163-6170. (Pubitemid 36875615)
52. Nogueiras R, et al. Direct control of peripheral lipid deposition by CNS GLP-1 receptor signaling is mediated by the sympathetic nervous system and blunted in diet-induced obesity. J Neurosci. 2009;29(18):5916-5925.
53. Cabou C, et al. Brain glucagon-like peptide-1 regulates arterial blood flow, heart rate, and insulin sensitivity. Diabetes. 2008;57(10):2577-2587.
54. 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(9548):1696-1705. (Pubitemid 46048557)
55. Edvell A, Lindstrom P. Initiation of increased pancreatic islet growth in young normoglycemic mice (Umea +/?). Endocrinology. 1999;140(2):778-783. (Pubitemid 29058212)
56. Buteau J, Roduit R, Susini S, Prentki M. Glucagon-like peptide-1 promotes DNA synthesis, activates phosphatidylinositol 3-kinase and increases transcription factor pancreatic and duodenal homeobox gene 1 (PDX-1) DNA binding activity in beta (INS-1)-cells. Diabetologia. 1999;42(7):856-864. (Pubitemid 29325077)
57. Hansotia T, et al. Extrapancreatic incretin receptors modulate glucose homeostasis, body weight, and energy expenditure. J Clin Invest. 2007;117(1):143-152. (Pubitemid 46048461)
58. Bustin SA. Absolute quantification of mRNA using real-time reverse transcription polymerase chain reaction assays. J Mol Endocrinol. 2000;25(2):169-193.
59. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods. 2001;25(4):402-408. (Pubitemid 34164012)
60. Lamont BJ, Drucker DJ. Differential anti-diabetic efficacy of incretin agonists vs. DPP-4 inhibition in high fat fed mice. Diabetes. 2008;57(1):190-198.
61. Kwan EP, Xie L, Sheu L, Ohtsuka T, Gaisano HY. Interaction between Munc13-1 and RIM is critical for glucagon-like peptide-1 mediated rescue of exocytotic defects in Munc13-1 deficient pancreatic beta-cells. Diabetes. 2007;56(10):2579-2588. (Pubitemid 47523266)
62. Flock G, Holland D, Seino Y, Drucker DJ. GPR119 Regulates Murine Glucose Homeostasis Through Incretin Receptor-Dependent and Independent Mechanisms. Endocrinology. 2011;152(2):374-383.
63. Strommer L, et al. Delayed gastric emptying and intestinal hormones following pancreatoduodenectomy. Pancreatology. 2005;5(6):537-544. (Pubitemid 41407284)
64. Lee J, Martin E, Paulino G, de Lartigue G, Raybould HE. Effect of ghrelin receptor antagonist on meal patterns in cholecystokinin type 1 receptor null mice. Physiol Behav. 2011;103(2):181-187.
65. Franklin K, Paxinos G. The Mouse Brain In Sterotaxic Coordinates. San Diego, California, USA: Academic Press; 1997.