Inhibition of gastric inhibitory polypeptide receptor signaling in adipose tissue reduces insulin resistance and hepatic steatosis in high-fat diet-fed mice

Diabetes

Volumn 66, Issue 4, 2017, Pages 868-879

  Joo, Erina ^a   Harada, Norio ^a   Yamane, Shunsuke ^a   Fukushima, Toru ^a   Taura, Daisuke ^a   Iwasaki, Kanako ^a   Sankoda, Akiko ^a   Shibue, Kimitaka ^a   Harada, Takanari ^a   Suzuki, Kazuyo ^a   Hamasaki, Akihiro ^a   Inagaki, Nobuya ^a  

^a KYOTO UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYL COENZYME A CARBOXYLASE; ACYL COENZYME A DESATURASE; ADIPONECTIN; BINDING PROTEIN; C PEPTIDE; CARBOHYDRATE RESPONSIVE ELEMENT BINDING PROTEIN; FATTY ACID; GASTRIC INHIBITORY POLYPEPTIDE RECEPTOR; GLUCOSE; HIGH DENSITY LIPOPROTEIN CHOLESTEROL; HORMONE RECEPTOR; INSULIN; INTERLEUKIN 1BETA; INTERLEUKIN 6; INTERLEUKIN 6 RECEPTOR; LEPTIN; LOW DENSITY LIPOPROTEIN CHOLESTEROL; MESSENGER RNA; MONOCYTE CHEMOTACTIC PROTEIN 1; PROTEIN KINASE B; STEROL REGULATORY ELEMENT BINDING PROTEIN 1C; SUPPRESSOR OF CYTOKINE SIGNALING 1; SUPPRESSOR OF CYTOKINE SIGNALING 3; TUMOR NECROSIS FACTOR; UNCLASSIFIED DRUG; INTERLEUKIN-6, MOUSE; SOCS3 PROTEIN, MOUSE;

ADIPOSE TISSUE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD LEVEL; BODY WEIGHT; CONTROLLED STUDY; DIET INDUCED OBESITY; EMBRYO; EPIDIDYMIS FAT; FATTY LIVER; GENE EXPRESSION; GLUCOSE BLOOD LEVEL; GLUCOSE TOLERANCE; IMMUNOHISTOCHEMISTRY; IN VIVO STUDY; INSULIN RESISTANCE; INSULIN SENSITIVITY; INTRAPERITONEAL FAT; LEAN BODY WEIGHT; LIVER TISSUE; LIVER WEIGHT; MESENTERIC FAT; MOUSE; NONHUMAN; ORAL GLUCOSE TOLERANCE TEST; PERIRENAL FAT; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SUBCUTANEOUS FAT; TISSUE SPECIFICITY; 3T3-L1 CELL LINE; ANIMAL; DIAGNOSTIC IMAGING; ENERGY METABOLISM; ENZYME LINKED IMMUNOSORBENT ASSAY; GENETICS; GLUCOSE TOLERANCE TEST; KNOCKOUT MOUSE; LIPID DIET; LIPID METABOLISM; LIVER; LOCOMOTION; METABOLISM; OBESITY; X-RAY COMPUTED TOMOGRAPHY;

3T3-L1 CELLS; ADIPOSE TISSUE; ANIMALS; BODY WEIGHT; DIET, HIGH-FAT; ENERGY METABOLISM; ENZYME-LINKED IMMUNOSORBENT ASSAY; FATTY LIVER; GLUCOSE TOLERANCE TEST; IMMUNOHISTOCHEMISTRY; INSULIN RESISTANCE; INTERLEUKIN-6; LIPID METABOLISM; LIVER; LOCOMOTION; MICE; MICE, KNOCKOUT; OBESITY; RECEPTORS, GASTROINTESTINAL HORMONE; RNA, MESSENGER; SIGNAL TRANSDUCTION; SUPPRESSOR OF CYTOKINE SIGNALING 3 PROTEIN; TOMOGRAPHY, X-RAY COMPUTED;

EID: 85016573357     PISSN: 00121797     EISSN: 1939327X     Source Type: Journal    
DOI: 10.2337/db16-0758     Document Type: Article

References (51)

1. Reaven GM. Banting lecture 1988. Role of insulin resistance in human disease. Diabetes 1988;37:1595-1607
2. Kahn BB, Flier JS. Obesity and insulin resistance. J Clin Invest 2000;106: 473-481
3. Lemieux I, Pascot A, Couillard C, et al. Hypertriglyceridemic waist: A marker of the atherogenic metabolic triad (hyperinsulinemia; hyperapolipoprotein B; small, dense LDL) in men? Circulation 2000;102:179-184
4. Creutzfeldt M. Candidate hormones of the gut. XV. Insulin-releasing factors of the gastrointestinal mucosa (Incretin). Gastroenterology 1974;67:748-750
5. Yamane S, Harada N, Inagaki N. Mechanisms of fat-induced gastric inhibitory polypeptide/glucose-dependent insulinotropic polypeptide secretion from K cells. J Diabetes Investig 2016;7(Suppl. 1):20-26
6. Flatt PR, Bailey CJ, Kwasowski P, Page T, Marks V. Plasma immunoreactive gastric inhibitory polypeptide in obese hyperglycaemic (ob/ob) mice. J Endocrinol 1984;101:249-256
7. Pederson RA. Gastric inhibitory polypeptides. In: Gut Peptides: Biochemistry and Physiology. Walsh JH, Dockray GJ, Eds. NY, Raven Press, 1994, p. 217-260
8. Seino Y, Yabe D. Glucose-dependent insulinotropic polypeptide and glucagon-like peptide-1: incretin actions beyond the pancreas. J Diabetes Investig 2013;4:108-130
9. Bailey CJ, Flatt PR, Kwasowski P, Powell CJ, Marks V. Immunoreactive gastric inhibitory polypeptide and K cell hyperplasia in obese hyperglycaemic (ob/ob) mice fed high fat and high carbohydrate cafeteria diets. Acta Endocrinol (Copenh) 1986;112:224-229
10. Suzuki K, Harada N, Yamane S, et al. Transcriptional regulatory factor X6 (Rfx6) increases gastric inhibitory polypeptide (GIP) expression in enteroendocrine K-cells and is involved in GIP hypersecretion in high fat diet-induced obesity. J Biol Chem 2013;288:1929-1938
11. Harada N, Yamada Y, Tsukiyama K, et al. A novel GIP receptor splice variant influences GIP sensitivity of pancreatic beta-cells in obese mice. Am J Physiol Endocrinol Metab 2008;294:E61-E68
12. Usdin TB, Mezey E, Button DC, Brownstein MJ, Bonner TI. Gastric inhibitory polypeptide receptor, a member of the secretin-vasoactive intestinal peptide receptor family, is widely distributed in peripheral organs and the brain. Endocrinology 1993;133:2861-2870
13. Kim SJ, Nian C, McIntosh CH. GIP increases human adipocyte LPL expression through CREB and TORC2-mediated trans-Activation of the LPL gene. J Lipid Res 2010;51:3145-3157
14. Kim SJ, Nian C, McIntosh CH. Activation of lipoprotein lipase by glucosedependent insulinotropic polypeptide in adipocytes. A role for a protein kinase B, LKB1, and AMP-Activated protein kinase cascade. J Biol Chem 2007;282:8557-8567
15. Song DH, Getty-Kaushik L, Tseng E, Simon J, Corkey BE, Wolfe MM. Glucosedependent insulinotropic polypeptide enhances adipocyte development and glucose uptake in part through Akt activation. Gastroenterology 2007;133:1796-1805
16. Kieffer TJ. GIP or not GIP? That is the question. Trends Pharmacol Sci 2003; 24:110-112
17. Miyawaki K, Yamada Y, Ban N, et al. Inhibition of gastric inhibitory polypeptide signaling prevents obesity. Nat Med 2002;8:738-742
18. Naitoh R, Miyawaki K, Harada N, et al. Inhibition of GIP signaling modulates adiponectin levels under high-fat diet in mice. Biochem Biophys Res Commun 2008;376:21-25
19. McClean PL, Irwin N, Cassidy RS, Holst JJ, Gault VA, Flatt PR. GIP receptor antagonism reverses obesity, insulin resistance, and associated metabolic disturbances induced in mice by prolonged consumption of high-fat diet. Am J Physiol Endocrinol Metab 2007;293:E1746-E1755
20. Irwin N, Flatt PR. Therapeutic potential for GIP receptor agonists and antagonists. Best Pract Res Clin Endocrinol Metab 2009;23:499-512
21. Boylan MO, Glazebrook PA, Tatalovic M, Wolfe MM. Gastric inhibitory polypeptide immunoneutralization attenuates development of obesity in mice. Am J Physiol Endocrinol Metab 2015;309:E1008-E1018
22. Tsuneki H, Tokai E, Sugawara C, Wada T, Sakurai T, Sasaoka T. Hypothalamic orexin prevents hepatic insulin resistance induced by social defeat stress in mice. Neuropeptides 2013;47:213-219
23. Folch J, Lees M, Sloane Stanley GH. A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem 1957;226:497-509
24. Nasteska D, Harada N, Suzuki K, et al. Chronic reduction of GIP secretion alleviates obesity and insulin resistance under high-fat diet conditions. Diabetes 2014;63:2332-2343
25. Dahlhoff M, Pfister S, Blutke A, et al. Peri-conceptional obesogenic exposure induces sex-specific programming of disease susceptibilities in adult mouse offspring. Biochim Biophys Acta 2014;1842:304-317
26. Spooren A, Kooijman R, Lintermans B, et al. Cooperation of NFkappaB and CREB to induce synergistic IL-6 expression in astrocytes. Cell Signal 2010;22: 871-881
27. Mohammad S, Ramos LS, Buck J, Levin LR, Rubino F, McGraw TE. Gastric inhibitory peptide controls adipose insulin sensitivity via activation of cAMPresponse element-binding protein and p110b isoform of phosphatidylinositol 3-kinase. J Biol Chem 2011;286:43062-43070
28. Galic S, Sachithanandan N, Kay TW, Steinberg GR. Suppressor of cytokine signalling (SOCS) proteins as guardians of inflammatory responses critical for regulating insulin sensitivity. Biochem J 2014;461:177-188
29. Trengove MC, Ward AC. SOCS proteins in development and disease. Am J Clin Exp Immunol 2013;2:1-29
30. Ueki K, Kondo T, Tseng YH, Kahn CR. Central role of suppressors of cytokine signaling proteins in hepatic steatosis, insulin resistance, and the metabolic syndrome in the mouse. Proc Natl Acad Sci U S A 2004;101:10422-10427
31. Mehran AE, Templeman NM, Brigidi GS, et al. Hyperinsulinemia drives dietinduced obesity independently of brain insulin production. Cell Metab 2012;16: 723-737
32. Miyawaki K, Yamada Y, Yano H, et al. Glucose intolerance caused by a defect in the entero-insular axis: A study in gastric inhibitory polypeptide receptor knockout mice. Proc Natl Acad Sci U S A 1999;96:14843-14847
33. Ugleholdt R, Pedersen J, Bassi MR, et al. Transgenic rescue of adipocyte glucose-dependent insulinotropic polypeptide receptor expression restores high fat diet-induced body weight gain. J Biol Chem 2011;286:44632-44645
34. Lee YH, Pratley RE. The evolving role of inflammation in obesity and the metabolic syndrome. Curr Diab Rep 2005;5:70-75
35. Bastard JP, Maachi M, Lagathu C, et al. Recent advances in the relationship between obesity, inflammation, and insulin resistance. Eur Cytokine Netw 2006; 17:4-12
36. Hoene M, Weigert C. The role of interleukin-6 in insulin resistance, body fat distribution and energy balance. Obes Rev 2008;9:20-29
37. Moschen AR, Molnar C, Geiger S, et al. Anti-inflammatory effects of excessive weight loss: potent suppression of adipose interleukin 6 and tumour necrosis factor alpha expression. Gut 2010;59:1259-1264
38. Sabio G, Das M, Mora A, et al. A stress signaling pathway in adipose tissue regulates hepatic insulin resistance. Science 2008;322:1539-1543
39. Chen S, Okahara F, Osaki N, Shimotoyodome A. Increased GIP signaling induces adipose inflammation via a HIF-1a-dependent pathway and impairs insulin sensitivity in mice. Am J Physiol Endocrinol Metab 2015;308:E414-E425
40. Timper K, Grisouard J, Sauter NS, et al. Glucose-dependent insulinotropic polypeptide induces cytokine expression, lipolysis, and insulin resistance in human adipocytes. Am J Physiol Endocrinol Metab 2013;304:E1-E13
41. Mauer J, Denson JL, Bröning JC. Versatile functions for IL-6 in metabolism and cancer. Trends Immunol 2015;36:92-101
42. Nogi Y, Nagashima M, Terasaki M, Nohtomi K, Watanabe T, Hirano T. Glucose-dependent insulinotropic polypeptide prevents the progression of macrophage-driven atherosclerosis in diabetic apolipoprotein E-null mice. PLoS One 2012;7:e35683
43. Makowski L, Boord JB, Maeda K, et al. Lack of macrophage fatty-Acidbinding protein aP2 protects mice deficient in apolipoprotein E against atherosclerosis. Nat Med 2001;7:699-705
44. Diehl S, Anguita J, Hoffmeyer A, et al. Inhibition of Th1 differentiation by IL-6 is mediated by SOCS1. Immunity 2000;13:805-815
45. Johnston JA, OShea JJ. Matching SOCS with function. Nat Immunol 2003; 4:507-509
46. Ueki K, Kondo T, Kahn CR. Suppressor of cytokine signaling 1 (SOCS-1) and SOCS-3 cause insulin resistance through inhibition of tyrosine phosphorylation of insulin receptor substrate proteins by discrete mechanisms. Mol Cell Biol 2004; 24:5434-5446
47. Xu X, So JS, Park JG, Lee AH. Transcriptional control of hepatic lipid metabolism by SREBP and ChREBP. Semin Liver Dis 2013;33:301-311
48. Strable MS, Ntambi JM. Genetic control of de novo lipogenesis: role in dietinduced obesity. Crit Rev Biochem Mol Biol 2010;45:199-214
49. Yamane S, Harada N, Hamasaki A, et al. Effects of glucose and meal ingestion on incretin secretion in Japanese subjects with normal glucose tolerance. J Diabetes Investig 2012;3:80-85
50. Vollmer K, Holst JJ, Baller B, et al. Predictors of incretin concentrations in subjects with normal, impaired, and diabetic glucose tolerance. Diabetes 2008; 57:678-687
51. Harada N, Hamasaki A, Yamane S, et al. Plasma gastric inhibitory polypeptide and glucagon-like peptide-1 levels after glucose loading are associated with different factors in Japanese subjects. J Diabetes Investig 2011;2:193-199