Glucose-dependent insulinotropic peptide impairs insulin signaling via inducing adipocyte inflammation in glucose-dependent insulinotropic peptide receptor-overexpressing adipocytes

FASEB Journal

Volumn 26, Issue 6, 2012, Pages 2383-2393

  Nie, Yaohui ^a,b   Ma, Ronald C ^a   Chan, Juliana C N ^a   Xu, Haiyan ^b   Xu, Gang ^a,c  

^a CHINESE UNIVERSITY OF HONG KONG   (Hong Kong)

^b BROWN UNIVERSITY   (United States)

^c CHINESE UNIVERSITY OF HONG KONG   (Hong Kong)

Author keywords

cAMP PKA pathway; G protein coupled receptor; IKK ; Inflammatory cytokines; JNK

Indexed keywords

ADIPONECTIN; ADIPOSE TRIGLYCERIDE LIPASE; CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; GASTRIC INHIBITORY POLYPEPTIDE; GLUCOSE; GLUCOSE TRANSPORTER 4; HORMONE SENSTIVITE LIPASE; I KAPPA B KINASE BETA; INSULIN; INTERLEUKIN 6; LEPTIN; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE P38; MONOCYTE CHEMOTACTIC PROTEIN 1; MONOCYTE CHEMOTACTIC PROTEIN 2; MONOCYTE CHEMOTACTIC PROTEIN 3; PENILIPIN A; PROTEIN; STRESS ACTIVATED PROTEIN KINASE; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ADIPOCYTE; ARTICLE; CYTOKINE RELEASE; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; GENE TRANSFER; GLUCOSE TRANSPORT; LIPOLYSIS; OBESITY; PRIORITY JOURNAL; PROTEIN LOCALIZATION;

3T3-L1 CELLS; ADIPOCYTES; ANIMALS; GASTRIC INHIBITORY POLYPEPTIDE; GENE EXPRESSION; GLUCOSE; I-KAPPA B KINASE; INFLAMMATION; INSULIN; MAP KINASE KINASE 4; MICE; PROTO-ONCOGENE PROTEINS C-AKT; RECEPTORS, GASTROINTESTINAL HORMONE; SIGNAL TRANSDUCTION;

MUS;

EID: 84861782461     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.11-196782     Document Type: Article

References (54)

1. Drucker, D. J. (2006) The biology of incretin hormones. Cell Metab. 3, 153-165
2. Baggio, L. L., and Drucker, D. J. (2007) Biology of incretins: GLP-1 and GIP. Gastroenterology 132, 2131-2157 (Pubitemid 46711096)
3. Xu, G., Stoffers, D. A., Habener, J. F., and Bonner-Weir, S. (1999) Exendin-4 stimulates both beta-cell replication and neogenesis, resulting in increased beta-cell mass and improved glucose tolerance in diabetic rats. Diabetes 48, 2270-2276 (Pubitemid 30395416)
4. Fan, R., Li, X., Gu, X., Chan, J. C., and Xu, G. (2010) Exendin-4 protects pancreatic beta cells from human islet amyloid polypeptide-induced cell damage: potential involvement of AKT and mitochondria biogenesis. Diabetes Obes. Metab. 12, 815-824
5. Iltz, J. L., Baker, D. E., Setter, S. M., and Campbell, K. R. (2006) Exenatide: an incretin mimetic for the treatment of type 2 diabetes mellitus. Clin. Ther. 28, 652-665 (Pubitemid 44067260)
6. Fineman, M. S., Bicsak, T. A., Shen, L. Z., Taylor, K., Gaines, E., Varns, A., Kim, D., and Baron, A. D. (2003) Effect on glycemic control of exenatide (synthetic exendin-4) additive to existing metformin and/or sulfonylurea treatment in patients with type 2 diabetes. Diabetes Care 26, 2370-2377 (Pubitemid 36993328)
7. Kolterman, O. G., Buse, J. B., Fineman, M. S., Gaines, E., Heintz, S., Bicsak, T. A., Taylor, K., Kim, D., Aisporna, M., Wang, Y., and Baron, A. D. (2003) Synthetic exendin-4 (exenatide) significantly reduces postprandial and fasting plasma glucose in subjects with type 2 diabetes. J. Clin. Endocrinol. Metab. 88, 3082-3089 (Pubitemid 36877476)
8. Kendall, D. M., Riddle, M. C., Rosenstock, J., Zhuang, D., Kim, D. D., Fineman, M. S., and Baron, A. D. (2005) Effects of exenatide (exendin-4) on glycemic control over 30 weeks in patients with type 2 diabetes treated with metformin and a sulfonylurea. Diabetes Care 28, 1083-1091 (Pubitemid 40616617)
9. Raz, I., Hanefeld, M., Xu, L., Caria, C., Williams-Herman, D., and Khatami, H. (2006) Efficacy and safety of the dipeptidyl peptidase-4 inhibitor sitagliptin as monotherapy in patients with type 2 diabetes mellitus. Diabetologia 49, 2564-2571
10. Choy, M., and Lam, S. (2007) Sitagliptin: a novel drug for the treatment of type 2 diabetes. Cardiol. Rev. 15, 264-271 (Pubitemid 47282035)
11. Ruiz-Grande, C., Alarcon, C., Merida, E., and Valverde, I. (1992) Lipolytic action of glucagon-like peptides in isolated rat adipocytes. Peptides 13, 13-16
12. Villanueva-Penacarrillo, M. L., Marquez, L., Gonzalez, N., Diaz-Miguel, M., and Valverde, I. (2001) Effect of GLP-1 on lipid metabolism in human adipocytes. Horm. Metab. Res. 33, 73-77 (Pubitemid 32231985)
13. Egan, J. M., Montrose-Rafizadeh, C., Wang, Y., Bernier, M., and Roth, J. (1994) Glucagon-like peptide-1(7-36) amide (GLP-1) enhances insulin-stimulated glucose metabolism in 3T3-L1 adipocytes: one of several potential extrapancreatic sites of GLP-1 action. Endocrinology 135, 2070-2075 (Pubitemid 24363904)
14. Dupre, J., Ross, S. A., Watson, D., and Brown, J. C. (1973) Stimulation of insulin secretion by gastric inhibitory polypeptide in man. J. Clin. Endocrinol. Metab. 37, 826-828
15. Elliott, R. M., Morgan, L. M., Tredger, J. A., Deacon, S., Wright, J., and Marks, V. (1993) Glucagon-like peptide-1 (7-36)amide and glucose-dependent insulinotropic polypeptide secretion in response to nutrient ingestion in man: acute post-prandial and 24-h secretion patterns. J. Endocrinol. 138, 159 -166
16. Raben, A., Andersen, H. B., Christensen, N. J., Madsen, J., Holst, J. J., and Astrup, A. (1994) Evidence for an abnormal postprandial response to a high-fat meal in women predisposed to obesity. Am. J. Physiol. 267, E549-559
17. Wasada, T., McCorkle, K., Harris, V., Kawai, K., Howard, B., and Unger, R. H. (1981) Effect of gastric inhibitory polypeptide on plasma levels of chylomicron triglycerides in dogs. J. Clin. Invest. 68, 1106-1107 (Pubitemid 11023541)
18. Kim, S. J., Nian, C., and McIntosh, C. H. (2007) Resistin is a key mediator of glucose-dependent insulinotropic polypeptide (GIP) stimulation of lipoprotein lipase (LPL) activity in adipocytes. J. Biol. Chem. 282, 34139-34147 (Pubitemid 350159458)
19. Knapper, J. M., Puddicombe, S. M., Morgan, L. M., and Fletcher, J. M. (1995) Investigations into the actions of glucose-dependent insulinotropic polypeptide and glucagon-like peptide- 1(7-36)amide on lipoprotein lipase activity in explants of rat adipose tissue. J. Nutr. 125, 183-188
20. Bailey, C. J., Flatt, P. R., Kwasowski, P., Powell, C. J., and Marks, V. (1986) 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.) 112, 224-229 (Pubitemid 16062608)
21. Morgan, L. M., Tredger, J. A., Hampton, S. M., French, A. P., Peake, J. C., and Marks, V. (1988) The effect of dietary modification and hyperglycaemia on gastric emptying and gastric inhibitory polypeptide (GIP) secretion. Br. J. Nutr. 60, 29 -37
22. Flatt, P. R., Bailey, C. J., Kwasowski, P., Page, T., and Marks, V. (1984) Plasma immunoreactive gastric inhibitory polypeptide in obese hyperglycaemic (ob/ob) mice. J. Endocrinol. 101, 249 -256
23. Speliotes, E. K., Ingelsson, E., Loos, R. J. et al., 2010) Association analyses of 249,796 individuals reveal 18 new loci associated with body mass index. Nat. Genet. 42, 937-948
24. Miyawaki, K., Yamada, Y., Ban, N., Ihara, Y., Tsukiyama, K., Zhou, H., Fujimoto, S., Oku, A., Tsuda, K., Toyokuni, S., Hiai, H., Mizunoya, W., Fushiki, T., Holst, J. J., Makino, M., Tashita, A., Kobara, Y., Tsubamoto, Y., Jinnouchi, T., Jomori, T., and Seino, Y. (2002) Inhibition of gastric inhibitory polypeptide signaling prevents obesity. Nat. Med. 8, 738-742 (Pubitemid 34778728)
25. McClean, P. L., Irwin, N., Cassidy, R. S., Holst, J. J., Gault, V. A., and Flatt, P. R. (2007) 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. 293, E1746-1755 (Pubitemid 350255128)
26. Yip, R. G., Boylan, M. O., Kieffer, T. J., and Wolfe, M. M. (1998) Functional GIP receptors are present on adipocytes. Endocrinology 139, 4004-4007 (Pubitemid 28512285)
27. McIntosh, C. H., Bremsak, I., Lynn, F. C., Gill, R., Hinke, S. A., Gelling, R., Nian, C., McKnight, G., Jaspers, S., and Pederson, R. A. (1999) Glucose-dependent insulinotropic polypeptide stimulation of lipolysis in differentiated 3T3-L1 cells: wortmannin-sensitive inhibition by insulin. Endocrinology 140, 398 -404
28. Dupre, J., Greenidge, N., McDonald, T. J., Ross, S. A., and Rubinstein, D. (1976) Inhibition of actions of glucagon in adipocytes by gastric inhibitory polypeptide. Metabolism 25, 1197-1199
29. Eckel, R. H., Fujimoto, W. Y., and Brunzell, J. D. (1979) Gastric inhibitory polypeptide enhanced lipoprotein lipase activity in cultured preadipocytes. Diabetes 28, 1141-1142 (Pubitemid 10215022)
30. Weaver, R. E., Donnelly, D., Wabitsch, M., Grant, P. J., and Balmforth, A. J. (2008) Functional expression of glucose-dependent insulinotropic polypeptide receptors is coupled to differentiation in a human adipocyte model. Int. J. Obes. (Lond.) 32, 1705-1711
31. Song, D. H., Getty-Kaushik, L., Tseng, E., Simon, J., Corkey, B. E., and Wolfe, M. M. (2007) Glucose-dependent insulinotropic polypeptide enhances adipocyte development and glucose uptake in part through Akt activation. Gastroenterology 133, 1796-1805 (Pubitemid 350180808)
32. Orlicky, D. J., DeGregori, J., and Schaack, J. (2001) Construction of stable coxsackievirus and adenovirus receptor-expressing 3T3-L1 cells. J. Lipid Res. 42, 910-915
33. Kaneto, H., Xu, G., Fujii, N., Kim, S., Bonner-Weir, S., and Weir, G. C. (2002) Involvement of c-Jun N-terminal kinase in oxidative stress-mediated suppression of insulin gene expression. J. Biol. Chem. 277, 30010-30018
34. Jiao, P., Chen, Q., Shah, S., Du, J., Tao, B., Tzameli, I., Yan, W., and Xu, H. (2009) Obesity-related upregulation of monocyte chemotactic factors in adipocytes: involvement of nuclear factor- kappaB and c-Jun NH2-terminal kinase pathways. Diabetes 58, 104-115
35. Nie, Y., and Wong, C. (2009) Suppressing the activity of ERRalpha in 3T3-L1 adipocytes reduces mitochondrial biogenesis but enhances glycolysis and basal glucose uptake. J. Cell. Mol. Med. 13, 3051-3060
36. Hotamisligil, G. S., and Spiegelman, B. M. (1994) Tumor necrosis factor alpha: a key component of the obesity-diabetes link. Diabetes 43, 1271-1278
37. Weisberg, S. P., McCann, D., Desai, M., Rosenbaum, M., Leibel, R. L., and Ferrante, A. W., Jr. (2003) Obesity is associated with macrophage accumulation in adipose tissue. J. Clin. Invest. 112, 1796-1808 (Pubitemid 38063703)
38. Xu, H., Barnes, G. T., Yang, Q., Tan, G., Yang, D., Chou, C. J., Sole, J., Nichols, A., Ross, J. S., Tartaglia, L. A., and Chen, H. (2003) Chronic inflammation in fat plays a crucial role in the development of obesity-related insulin resistance. J. Clin. Invest. 112, 1821-1830 (Pubitemid 38063705)
39. Shoelson, S. E., Lee, J., and Goldfine, A. B. (2006) Inflammation and insulin resistance. J. Clin. Invest. 116, 1793-1801 (Pubitemid 44033299)
40. Green, B. D., Gault, V. A., O'Harte F, P., and Flatt, P. R. (2004) Structurally modified analogues of glucagon-like peptide-1 (GLP-1) and glucose-dependent insulinotropic polypeptide (GIP) as future antidiabetic agents. Curr. Pharm. Des. 10, 3651-3662 (Pubitemid 39386580)
41. Irwin, N., McClean, P. L., Cassidy, R. S., O'Harte, F., P., Green, B. D., Gault, V. A., Harriott, P., and Flatt, P. R. (2007) Comparison of the anti-diabetic effects of GIP- and GLP-1-receptor activation in obese diabetic (ob/ob) mice: studies with DPP IV resistant N-AcGIP and exendin(1-39)amide. Diabetes Metab. Res. Rev. 23, 572-579 (Pubitemid 350018032)
42. Kim, S. J., Nian, C., and McIntosh, C. H. (2010) GIP increases human adipocyte LPL expression through CREB and TORC2-mediated trans-activation of the LPL gene. J. Lipid Res. 51, 3145-3157
43. Kim, S. J., Nian, C., and McIntosh, C. H. (2007) Activation of lipoprotein lipase by glucose-dependent insulinotropic polypeptide in adipocytes. A role for a protein kinase B, LKB1, and AMP-activated protein kinase cascade. J. Biol. Chem. 282, 8557-8567 (Pubitemid 47093503)
44. Semb, H., Peterson, J., Tavernier, J., and Olivecrona, T. (1987) Multiple effects of tumor necrosis factor on lipoprotein lipase in vivo. J. Biol. Chem. 262, 8390-8394 (Pubitemid 17104269)
45. Cornelius, P., Enerback, S., Bjursell, G., Olivecrona, T., and Pekala, P. H. (1988) Regulation of lipoprotein lipase mRNA content in 3T3-L1 cells by tumour necrosis factor. Biochem. J. 249, 765-769 (Pubitemid 18042796)
46. Kawakami, M., Murase, T., Ogawa, H., Ishibashi, S., Mori, N., Takaku, F., and Shibata, S. (1987) Human recombinant TNF suppresses lipoprotein lipase activity and stimulates lipolysis in 3T3-L1 cells. J. Biochem. 101, 331-338 (Pubitemid 17004304)
47. Mohammad, S., Ramos, L. S., Buck, J., Levin, L. R., Rubino, F., and McGraw, T. E. (2011) Gastric inhibitory peptide controls adipose insulin sensitivity via activation of CREB and p110beta isoform of PI3 kinase. J. Biol. Chem. 286, 43062-43070
48. Gloerich, M., and Bos, J. L. (2010) Epac: defining a new mechanism for cAMP action. Annu. Rev. Pharmacol. Toxicol. 50, 355-375
49. Tchivileva, I. E., Tan, K. S., Gambarian, M., Nackley, A. G., Medvedev, A. V., Romanov, S., Flood, P. M., Maixner, W., Makarov, S. S., and Diatchenko, L. (2009) Signaling pathways mediating beta3-adrenergic receptor-induced production of interleukin-6 in adipocytes. Mol. Immunol. 46, 2256-2266
50. Ruan, H., Zarnowski, M. J., Cushman, S. W., and Lodish, H. F. (2003) Standard isolation of primary adipose cells from mouse epididymal fat pads induces inflammatory mediators and down-regulates adipocyte genes. J. Biol. Chem. 278, 47585-47593 (Pubitemid 37523202)
51. Siegel, E. G., and Creutzfeldt, W. (1985) Stimulation of insulin release in isolated rat islets by GIP in physiological concentrations and its relation to islet cyclic AMP content. Diabetologia 28, 857-861 (Pubitemid 16176057)
52. Mottillo, E. P., Shen, X. J., and Granneman, J. G. beta3- adrenergic receptor induction of adipocyte inflammation requires lipolytic activation of stress kinases p38 and JNK. Biochim Biophys Acta 1801, 1048-1055
53. Qi, L., Saberi, M., Zmuda, E., Wang, Y., Altarejos, J., Zhang, X., Dentin, R., Hedrick, S., Bandyopadhyay, G., Hai, T., Olefsky, J., and Montminy, M. (2009) Adipocyte CREB promotes insulin resistance in obesity. Cell Metab. 9, 277-286
54. Roust, L. R., Stesin, M., Go, V. L., O'Brien, P. C., Rizza, R. A., and Service, F. J. (1988) Role of gastric inhibitory polypeptide in postprandial hyperinsulinemia of obesity. Am. J. Physiol. 254, E767-774