GLP-1-derived nonapeptide GLP-1(28-36)amide represses hepatic gluconeogenic gene expression and improves pyruvate tolerance in high-fat diet-fed mice

American Journal of Physiology - Endocrinology and Metabolism

Volumn 305, Issue 11, 2013, Pages

  Ip, Wilfred ^a,b   Shao, Weijuan ^a   Chiang, Yu Ting Alex ^a,b   Jin, Tianru ^a,b  

^a UNIVERSITY HEALTH NETWORK   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

Author keywords

Adenosine 3 ,5 cyclic monophosphate; Glucagon like peptide 1; Hepatic glucose production; Protein kinase A; Type 2 diabetes

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 1; BETA CATENIN; CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; GLUCAGON LIKE PEPTIDE 1 [28-36] AMIDE; GLUCAGON LIKE PEPTIDE 1 DERIVATIVE; GLUCOSE; PYRUVIC ACID; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; DIABETES MELLITUS; DRUG MECHANISM; ENZYME INHIBITION; FUNCTION TEST; G6PC GENE; GENE; GENE EXPRESSION; GLUCONEOGENESIS; GLUCOSE METABOLISM; GLUCOSE TOLERANCE TEST; LIPID DIET; LIVER CELL; MALE; METABOLIC DISORDER; MOUSE; NONHUMAN; PCK1 GENE; PPARGC1A GENE; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PYRUVATE TOLERANCE TEST; SIGNAL TRANSDUCTION; WEIGHT REDUCTION;

ADENOSINE 3′,5′-CYCLIC MONOPHOSPHATE; GLUCAGON-LIKE PEPTIDE-1; HEPATIC GLUCOSE PRODUCTION; PROTEIN KINASE A; TYPE 2 DIABETES;

ANIMALS; BODY WEIGHT; CELLS, CULTURED; DIET, HIGH-FAT; DOWN-REGULATION; DRUG-RELATED SIDE EFFECTS AND ADVERSE REACTIONS; GENE EXPRESSION; GLUCAGON-LIKE PEPTIDE 1; GLUCONEOGENESIS; GLUCOSE TOLERANCE TEST; LIVER; MALE; MICE; MICE, INBRED C57BL; PEPTIDE FRAGMENTS; PYRUVIC ACID;

EID: 84888871005     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.00376.2013     Document Type: Article

References (52)

1. Altarejos JY, Montminy M. CREB and the CRTC co-activators: sensors for hormonal and metabolic signals. Nat Rev Mol Cell Biol 12: 141-151, 2011.
2. Anini Y, Brubaker PL. Muscarinic receptors control glucagon-like peptide 1 secretion by human endocrine L cells. Endocrinology 144: 3244-3250, 2003.
3. Aviv V, Meivar-Levy I, Rachmut IH, Rubinek T, Mor E, Ferber S. Exendin-4 promotes liver cell proliferation and enhances the PDX-1-induced liver to pancreas transdifferentiation process. J Biol Chem 284: 33509-33520, 2009.
4. Baggio LL, Drucker DJ. Biology of incretins: GLP-1 and GIP. Gastroenterology 132: 2131-2157, 2007.
5. Ban K, Kim KH, Cho CK, Sauve M, Diamandis EP, Backx PH, Drucker DJ, Husain M. Glucagon-like peptide (GLP)-1(9-36)amidemediated cytoprotection is blocked by exendin(9-39) yet does not require the known GLP-1 receptor. Endocrinology 151: 1520-1531, 2010.
6. Ban K, Noyan-Ashraf MH, Hoefer J, Bolz SS, Drucker DJ, Husain M. Cardioprotective and vasodilatory actions of glucagon-like peptide 1 receptor are mediated through both glucagon-like peptide 1 receptordependent and-independent pathways. Circulation 117: 2340-2350, 2008.
7. Bullock BP, Heller RS, Habener JF. Tissue distribution of messenger ribonucleic acid encoding the rat glucagon-like peptide-1 receptor. Endocrinology 137: 2968-2978, 1996.
8. Chai W, Dong Z, Wang N, Wang W, Tao L, Cao W, Liu Z. Glucagonlike peptide 1 recruits microvasculature and increases glucose use in muscle via a nitric oxide-dependent mechanism. Diabetes 61: 888-896, 2012.
9. Davidson EP, Coppey LJ, Dake B, Yorek MA. Effect of Treatment of Sprague Dawley Rats with AVE7688, Enalapril, or Candoxatril on Diet-Induced Obesity. J Obes. In press.
10. Davidson EP, Coppey LJ, Holmes A, Yorek MA. Effect of inhibition of angiotensin converting enzyme and/or neutral endopeptidase on vascular and neural complications in high fat fed/low dose streptozotocin-diabetic rats. Eur J Pharmacol 677: 180-187, 2012.
11. Dhanvantari S, Seidah NG, Brubaker PL. Role of prohormone convertases in the tissue-specific processing of proglucagon. Mol Endocrinol 10: 342-355, 1996.
12. Ding X, Saxena NK, Lin S, Gupta NA, Anania FA. Exendin-4, a glucagon-like protein-1 (GLP-1) receptor agonist, reverses hepatic steatosis in ob/ob mice. Hepatology 43: 173-181, 2006.
13. Gupta NA, Mells J, Dunham RM, Grakoui A, Handy J, Saxena NK, Anania FA. Glucagon-like peptide-1 receptor is present on human hepatocytes and has a direct role in decreasing hepatic steatosis in vitro by modulating elements of the insulin signaling pathway. Hepatology 51: 1584-1592, 2010.
14. Herzig S, Long F, Jhala US, Hedrick S, Quinn R, Bauer A, Rudolph D, Schutz G, Yoon C, Puigserver P, Spiegelman B, Montminy M. CREB regulates hepatic gluconeogenesis through the coactivator PGC-1. Nature 413: 179-183, 2001.
15. Hupe-Sodmann K, McGregor GP, Bridenbaugh R, Göke R, Göke B, Thole H, Zimmermann B, Voigt K. Characterisation of the processing by human neutral endopeptidase 24.11 of GLP-1(7-36) amide and comparison of the substrate specificity of the enzyme for other glucagon-like peptides. Regul Pept 58: 149-156, 1995.
16. Hvidberg A, Nielsen MT, Hilsted J, Orskov C, Holst JJ. Effect of glucagon-like peptide-1 (proglucagon 78-107amide) on hepatic glucose production in healthy man. Metabolism 43: 104-108, 1994.
17. Ip W, Shao W, Chiang YT, Jin T. The Wnt signaling pathway effector TCF7L2 is upregulated by insulin and represses hepatic gluconeogenesis. Am J Physiol Endocrinol Metab 303: E1166-E1176, 2012.
18. 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.
19. Larsson H, Holst JJ, Ahren B. Glucagon-like peptide-1 reduces hepatic glucose production indirectly through insulin and glucagon in humans. Acta Physiol Scand 160: 413-422, 1997.
20. Liu H, Fergusson MM, Wu JJ, Rovira II, Liu J, Gavrilova O, Lu T, Bao J, Han D, Sack MN, Finkel T. Wnt signaling regulates hepatic metabolism. Sci Signal 4: ra6, 2011.
21. Liu Z, Stanojevic V, Brindamour LJ, Habener JF. GLP1-derived nonapeptide GLP1(28-36)amide protects pancreatic beta-cells from glucolipotoxicity. J Endocrinol 213: 143-154, 2012.
22. Ma T, Du X, Pick JE, Sui G, Brownlee M, Klann E. Glucagon-like peptide-1 cleavage product GLP-1(9-36) amide rescues synaptic plasticity and memory deficits in Alzheimer's disease model mice. J Neurosci 32: 13701-13708, 2012.
23. Matsumoto M, Accili D. The tangled path to glucose production. Nat Med 12: 33-34; discussion 34, 2006.
24. Meier JJ, Gallwitz B, Salmen S, Goetze O, Holst JJ, Schmidt WE, Nauck MA. 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 88: 2719-2725, 2003.
25. Mojsov S, Weir GC, Habener JF. Insulinotropin: glucagon-like peptide I (7-37) co-encoded in the glucagon gene is a potent stimulator of insulin release in the perfused rat pancreas. J Clin Invest 79: 616-619, 1987.
26. Nikolaidis LA, Elahi D, Hentosz T, Doverspike A, Huerbin R, Zourelias L, Stolarski C, Shen YT, Shannon RP. Recombinant glucagon-like peptide-1 increases myocardial glucose uptake and improves left ventricular performance in conscious dogs with pacing-induced dilated cardiomyopathy. Circulation 110: 955-961, 2004.
27. Nikolaidis LA, Elahi D, Shen YT, Shannon RP. Active metabolite of GLP-1 mediates myocardial glucose uptake and improves left ventricular performance in conscious dogs with dilated cardiomyopathy. Am J Physiol Heart Circ Physiol 289: H2401-H2408, 2005.
28. Norton L, Fourcaudot M, Abdul-Ghani MA, Winnier D, Mehta FF, Jenkinson CP, Defronzo RA. Chromatin occupancy of transcription factor 7-like 2 (TCF7L2) and its role in hepatic glucose metabolism. Diabetologia 54: 3132-3142, 2011.
29. Oh KJ, Park J, Kim SS, Oh H, Choi CS, Koo SH. TCF7L2 modulates glucose homeostasis by regulating CREB-and FoxO1-dependent transcriptional pathway in the liver. PLoS Genet 8: e1002986, 2012.
30. Oltman CL, Davidson EP, Coppey LJ, Kleinschmidt TL, Dake B, Yorek MA. Role of the effect of inhibition of neutral endopeptidase on vascular and neural complications in streptozotocin-induced diabetic rats. Eur J Pharmacol 650: 556-562, 2011.
31. Orskov C, Wettergren A, Holst JJ. Biological effects and metabolic rates of glucagonlike peptide-1 7-36 amide and glucagonlike peptide-1 7-37 in healthy subjects are indistinguishable. Diabetes 42: 658-661, 1993.
32. Panjwani N, Mulvihill EE, Longuet C, Yusta B, Campbell JE, Brown TJ, Streutker C, Holland D, Cao X, Baggio LL, Drucker DJ. GLP-1 receptor activation indirectly reduces hepatic lipid accumulation but does not attenuate development of atherosclerosis in diabetic male ApoE(-/-) mice. Endocrinology 154: 127-139, 2013.
33. Plamboeck A, Holst JJ, Carr RD, Deacon CF. Neutral endopeptidase 24.11 and dipeptidyl peptidase IV are both mediators of the degradation of glucagon-like peptide 1 in the anaesthetised pig. Diabetologia 48: 1882-1890, 2005.
34. Prigeon RL, Quddusi S, Paty B, D'Alessio DA. Suppression of glucose production by GLP-1 independent of islet hormones: a novel extrapancreatic effect. Am J Physiol Endocrinol Metab 285: E701-E707, 2003.
35. Ryu H, Lee J, Impey S, Ratan RR, Ferrante RJ. Antioxidants modulate mitochondrial PKA and increase CREB binding to D-loop DNA of the mitochondrial genome in neurons. Proc Natl Acad Sci USA 102: 13915-13920, 2005.
36. Seghieri M, Rebelos E, Gastaldelli A, Astiarraga BD, Casolaro A, Barsotti E, Pocai A, Nauck M, Muscelli E, Ferrannini E. Direct effect of GLP-1 infusion on endogenous glucose production in humans. Diabetologia 56: 156-161, 2013.
37. Shao W, Wang Z, Ip W, Chiang YT, Xiong X, Chai T, Xu C, Wang Q, Jin T. GLP-1(28-36) improves β-cell mass and glucose disposal in streptozotocin-induced diabetic mice and activates cAMP/PKA/α-catenin signaling in β-cells in vitro. Am J Physiol Endocrinol Metab 304: E1263-E1272, 2013.
38. Skoglund G, Hussain MA, Holz GG. Glucagon-like peptide 1 stimulates insulin gene promoter activity by protein kinase A-independent activation of the rat insulin I gene cAMP response element. Diabetes 49: 1156-1164, 2000.
39. Svegliati-Baroni G, Saccomanno S, Rychlicki C, Agostinelli L, De Minicis S, Candelaresi C, Faraci G, Pacetti D, Vivarelli M, Nicolini D, Garelli P, Casini A, Manco M, Mingrone G, Risaliti A, Frega GN, Benedetti A, Gastaldelli A. Glucagon-like peptide-1 receptor activation stimulates hepatic lipid oxidation and restores hepatic signalling alteration induced by a high-fat diet in nonalcoholic steatohepatitis. Liver Int 31: 1285-1297, 2011.
40. Thomson DM, Herway ST, Fillmore N, Kim H, Brown JD, Barrow JR, Winder WW. AMP-activated protein kinase phosphorylates transcription factors of the CREB family. J Appl Physiol 104: 429-438, 2008.
41. Toft-Nielson M, Madsbad S, Holst JJ. The effect of glucagon-like peptide I (GLP-I) on glucose elimination in healthy subjects depends on the pancreatic glucoregulatory hormones. Diabetes 45: 552-556, 1996.
42. Tomas E, Stanojevic V, Habener JF. GLP-1-derived nonapeptide GLP-1(28-36)amide targets to mitochondria and suppresses glucose production and oxidative stress in isolated mouse hepatocytes. Regul Pept 167: 177-184, 2011.
43. Tomas E, Stanojevic V, Habener JF. GLP-1 (9-36) amide metabolite suppression of glucose production in isolated mouse hepatocytes. Horm Metab Res 42: 657-662, 2010.
44. Tomas E, Stanojevic V, Laudone R, Habener JF. GLP-1-Derived Pentapeptide GLP-1(32-36)amide Attenuates the Development of Obesity, Diabetes, Hepatic Steatosis and Increases Energy Expenditure in Diet-Induced Obese Mice (Abstract). Diabetes 61, Suppl 1: 1915-P, 2012.
45. Tomas E, Wood JA, Stanojevic V, Habener JF. GLP-1-derived nonapeptide GLP-1(28-36)amide inhibits weight gain and attenuates diabetes and hepatic steatosis in diet-induced obese mice. Regul Pept 169: 43-48, 2011.
46. Tomas E, Wood JA, Stanojevic V, Habener JF. Glucagon-like peptide-1(9-36)amide metabolite inhibits weight gain and attenuates diabetes and hepatic steatosis in diet-induced obese mice. Diabetes Obes Metab 13: 26-33, 2011.
47. Turton MD, O'Shea D, Gunn I, Beak SA, Edwards CM, Meeran K, Choi SJ, Taylor GM, Heath MM, Lambert PD, Wilding JP, Smith DM, Ghatei MA, Herbert J, Bloom SR. A role for glucagon-like peptide-1 in the central regulation of feeding. Nature 379: 69-72, 1996.
48. Wideman RD, Kieffer TJ. Mining incretin hormone pathways for novel therapies. Trends Endocrinol Metab 20: 280-286, 2009.
49. Yi F, Brubaker PL, Jin T. TCF-4 mediates cell type-specific regulation of proglucagon gene expression by beta-catenin and glycogen synthase kinase-3beta. J Biol Chem 280: 1457-1464, 2005.
50. Yoon JC, Puigserver P, Chen G, Donovan J, Wu Z, Rhee J, Adelmant G, Stafford J, Kahn CR, Granner DK, Newgard CB, Spiegelman BM. Control of hepatic gluconeogenesis through the transcriptional coactivator PGC-1. Nature 413: 131-138, 2001.
51. Yu Z, Shao W, Chiang Y, Foltz W, Zhang Z, Ling W, Fantus IG, Jin T. Oltipraz upregulates the nuclear factor (erythroid-derived 2)-like 2 [corrected](NRF2) antioxidant system and prevents insulin resistance and obesity induced by a high-fat diet in C57BL/6J mice. Diabetologia 54: 922-934, 2011.
52. Zhande R, Zhang W, Zheng Y, Pendleton E, Li Y, Polakiewicz RD, Sun XJ. Dephosphorylation by default, a potential mechanism for regulation of insulin receptor substrate-1/2, Akt, and ERK1/2. J Biol Chem 281: 39071-39080, 2006.