Glucagon-like peptide-1 production in the GLUTag cell line is impaired by free fatty acids via endoplasmic reticulum stress

Metabolism: Clinical and Experimental

Volumn 63, Issue 6, 2014, Pages 800-811

  Hayashi, Hiroto ^a   Yamada, Ren ^a   Das, Siddhartha Shankar ^a   Sato, Taiki ^a   Takahashi, Aki ^a   Hiratsuka, Masahiro ^a   Hirasawa, Noriyasu ^a  

^a TOHOKU UNIVERSITY   (Japan)

Author keywords

ER stress; GLP 1; GLUTag; PC1 3

Indexed keywords

FURIN; GLUCAGON LIKE PEPTIDE 1; GLUCOSE; OLEIC ACID; PALMITIC ACID; PROGLUCAGON; PROHORMONE CONVERTASE 1; THAPSIGARGIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ATTENUATION; CELL LYSATE; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM STRESS; ENZYME BLOOD LEVEL; ENZYME PHOSPHORYLATION; GLUCOSE BLOOD LEVEL; HYPERINSULINEMIA; IN VIVO STUDY; INSULIN RESISTANCE; INTESTINE; L CELL LINE; LIPID DIET; MALE; MOUSE; MTT ASSAY; NONHUMAN; OBESITY; PRIORITY JOURNAL; SECRETION (PROCESS);

ER STRESS; GLP-1; GLUTAG; PC1/3;

ANIMALS; BLOTTING, WESTERN; DIET, HIGH-FAT; ENDOPLASMIC RETICULUM STRESS; ENZYME INHIBITORS; GLUCAGON-LIKE PEPTIDE 1; L CELLS (CELL LINE); MALE; MICE; MICE, INBRED C57BL; OBESITY; OLEIC ACID; PALMITATES; PROPROTEIN CONVERTASE 1; REAL-TIME POLYMERASE CHAIN REACTION; THAPSIGARGIN;

EID: 84901245909     PISSN: 00260495     EISSN: 15328600     Source Type: Journal    
DOI: 10.1016/j.metabol.2014.02.012     Document Type: Article

References (55)

1. J.J. Holst The physiology of glucagon-like peptide 1 Physiol Rev 87 4 2007 1409 1439
2. B. Yusta, L.L. Baggio, J.L. Estall, J.A. Koehler, D.P. Holland, and H. Li et al. Glp-1 receptor activation improves beta cell function and survival following induction of endoplasmic reticulum stress Cell Metab 4 5 2006 391 406
3. Y.S. Lee, and H.S. Jun Anti-diabetic actions of glucagon-like peptide-1 on pancreatic beta-cells Metabolism 63 1 2014 9 19
4. G. Xu, D.A. Stoffers, J.F. Habener, and S. Bonner-Weir Exendin-4 stimulates both beta-cell replication and neogenesis, resulting in increased beta-cell mass and improved glucose tolerance in diabetic rats Diabetes 48 12 1999 2270 2276
5. W. Guo, S. Wong, W. Xie, T. Lei, and Z. Luo Palmitate modulates intracellular signaling, induces endoplasmic reticulum stress, and causes apoptosis in mouse 3t3-l1 and rat primary preadipocytes Am J Physiol Endocrinol Metab 293 2 2007 E576 E586
6. J. Lu, Q. Wang, L. Huang, H. Dong, L. Lin, and N. Lin et al. Palmitate causes endoplasmic reticulum stress and apoptosis in human mesenchymal stem cells: Prevention by ampk activator Endocrinology 153 11 2012 5275 5284
7. G. Boden Obesity and free fatty acids Endocrinol Metab Clin North Am 37 3 2008 635 646 [viii-ix]
8. M.A. Charles, E. Eschwege, N. Thibult, J.R. Claude, J.M. Warnet, and G.E. Rosselin et al. The role of non-esterified fatty acids in the deterioration of glucose tolerance in caucasian subjects: Results of the paris prospective study Diabetologia 40 9 1997 1101 1106
9. U. Riserus, W.C. Willett, and F.B. Hu Dietary fats and prevention of type 2 diabetes Prog Lipid Res 48 1 2009 44 51
10. H. Yoshida, T. Matsui, A. Yamamoto, T. Okada, and K. Mori Xbp1 mrna is induced by atf6 and spliced by ire1 in response to er stress to produce a highly active transcription factor Cell 107 7 2001 881 891
11. M. Cnop, F. Foufelle, and L.A. Velloso Endoplasmic reticulum stress, obesity and diabetes Trends Mol Med 18 1 2012 59 68
12. M.B. Toft-Nielsen, M.B. Damholt, S. Madsbad, L.M. Hilsted, T.E. Hughes, and B.K. Michelsen et al. Determinants of the impaired secretion of glucagon-like peptide-1 in type 2 diabetic patients J Clin Endocrinol Metab 86 8 2001 3717 3723
13. L.R. Ranganath, J.M. Beety, L.M. Morgan, J.W. Wright, R. Howland, and V. Marks Attenuated glp-1 secretion in obesity: Cause or consequence? Gut 38 6 1996 916 919
14. T.M. Dao, A. Waget, P. Klopp, M. Serino, C. Vachoux, and L. Pechere et al. Resveratrol increases glucose induced glp-1 secretion in mice: A mechanism which contributes to the glycemic control PLoS One 6 6 2011 e20700
15. D.J. Drucker, T. Jin, S.L. Asa, T.A. Young, and P.L. Brubaker Activation of proglucagon gene transcription by protein kinase-a in a novel mouse enteroendocrine cell line Mol Endocrinol 8 12 1994 1646 1655
16. G.V. Sangle, L.M. Lauffer, A. Grieco, S. Trivedi, R. Iakoubov, and P.L. Brubaker Novel biological action of the dipeptidylpeptidase-iv inhibitor, sitagliptin, as a glucagon-like peptide-1 secretagogue Endocrinology 153 2 2012 564 573
17. G. Tolhurst, H. Heffron, Y.S. Lam, H.E. Parker, A.M. Habib, and E. Diakogiannaki et al. Short-chain fatty acids stimulate glucagon-like peptide-1 secretion via the g-protein-coupled receptor ffar2 Diabetes 61 2 2012 364 371
18. T. Imaizumi, K. Jyonouchi, T. Kato, T. Chikuma, and A. Tanaka Anterograde axonal transport of boc-arg-val-arg-arg-mca hydrolyzing enzyme in rat sciatic nerves: Cleavage occurs between basic residues Biochim Biophys Acta 1476 2 2000 337 349
19. T. Kato, R. Yajima, N. Sato, K. Takahashi, C. Shimizu, and T. Chikuma Axonal transports of boc-gly-arg-arg-mca hydrolysing enzyme in rat sciatic nerves Neurochem Int 32 2 1998 163 170
20. F. Reimann, and F.M. Gribble Glucose-sensing in glucagon-like peptide-1-secreting cells Diabetes 51 9 2002 2757 2763
21. T. Sato, D. Kotake, M. Hiratsuka, and N. Hirasawa Enhancement of inflammatory protein expression and nuclear factor kappab (nf-kappab) activity by trichostatin a (tsa) in op9 preadipocytes PLoS One 8 3 2013 e59702
22. N. Hirasawa, K. Yashima, and K. Ishihara Enhancement of ligand-dependent down-regulation of glucocorticoid receptor by lipopolysaccharide Life Sci 85 15-16 2009 578 585
23. G. Peng, L. Li, Y. Liu, J. Pu, S. Zhang, and J. Yu et al. Oleate blocks palmitate-induced abnormal lipid distribution, endoplasmic reticulum expansion and stress, and insulin resistance in skeletal muscle Endocrinology 152 6 2011 2206 2218
24. U. Ozcan, Q. Cao, E. Yilmaz, A.H. Lee, N.N. Iwakoshi, and E. Ozdelen et al. Endoplasmic reticulum stress links obesity, insulin action, and type 2 diabetes Science 306 5695 2004 457 461
25. L. Salvado, T. Coll, A.M. Gomez-Foix, E. Salmeron, E. Barroso, and X. Palomer et al. Oleate prevents saturated-fatty-acid-induced er stress, inflammation and insulin resistance in skeletal muscle cells through an ampk-dependent mechanism Diabetologia 56 6 2013 1372 1382
26. K. Ueda, J. Kawano, K. Takeda, T. Yujiri, K. Tanabe, and T. Anno et al. Endoplasmic reticulum stress induces wfs1 gene expression in pancreatic beta-cells via transcriptional activation Eur J Endocrinol 153 1 2005 167 176
27. J. Song, X.J. Zhang, D. Boehning, N.C. Brooks, D.N. Herndon, and M.G. Jeschke Measurement of hepatic protein fractional synthetic rate with stable isotope labeling technique in thapsigargin stressed hepg2 cells Int J Biol Sci 8 2 2012 265 271
28. P. Nickson, A. Toth, and P. Erhardt Puma is critical for neonatal cardiomyocyte apoptosis induced by endoplasmic reticulum stress Cardiovasc Res 73 1 2007 48 56
29. L. Yang, P. Li, S. Fu, E.S. Calay, and G.S. Hotamisligil Defective hepatic autophagy in obesity promotes er stress and causes insulin resistance Cell Metab 11 6 2010 467 478
30. T. Otoda, T. Takamura, H. Misu, T. Ota, S. Murata, and H. Hayashi et al. Proteasome dysfunction mediates obesity-induced endoplasmic reticulum stress and insulin resistance in the liver Diabetes 62 3 2013 811 824
31. E. Bachar-Wikstrom, J.D. Wikstrom, Y. Ariav, B. Tirosh, N. Kaiser, and E. Cerasi et al. Stimulation of autophagy improves endoplasmic reticulum stress-induced diabetes Diabetes 62 4 2013 1227 1237
32. J. Mandl, T. Meszaros, G. Banhegyi, and M. Csala Minireview: Endoplasmic reticulum stress: Control in protein, lipid, and signal homeostasis Mol Endocrinol 27 3 2013 384 393
33. A.L. Goldberg Protein degradation and protection against misfolded or damaged proteins Nature 426 6968 2003 895 899
34. H. Furukawa, R.J. Carroll, H.H. Swift, and D.F. Steiner Long-term elevation of free fatty acids leads to delayed processing of proinsulin and prohormone convertases 2 and 3 in the pancreatic beta-cell line min6 Diabetes 48 7 1999 1395 1401
35. E. Lai, G. Bikopoulos, M.B. Wheeler, M. Rozakis-Adcock, and A. Volchuk Differential activation of er stress and apoptosis in response to chronically elevated free fatty acids in pancreatic beta-cells Am J Physiol Endocrinol Metab 294 3 2008 E540 E550
36. D. Wang, Y. Wei, and M.J. Pagliassotti Saturated fatty acids promote endoplasmic reticulum stress and liver injury in rats with hepatic steatosis Endocrinology 147 2 2006 943 951
37. A.M. Preston, E. Gurisik, C. Bartley, D.R. Laybutt, and T.J. Biden Reduced endoplasmic reticulum (er)-to-golgi protein trafficking contributes to er stress in lipotoxic mouse beta cells by promoting protein overload Diabetologia 52 11 2009 2369 2373
38. Y. Kijima, E. Ogunbunmi, and S. Fleischer Drug action of thapsigargin on the ca2 + pump protein of sarcoplasmic reticulum J Biol Chem 266 34 1991 22912 22918
39. M.T. Nguyen, S. Favelyukis, A.K. Nguyen, D. Reichart, P.A. Scott, and A. Jenn et al. A subpopulation of macrophages infiltrates hypertrophic adipose tissue and is activated by free fatty acids via toll-like receptors 2 and 4 and jnk-dependent pathways J Biol Chem 282 48 2007 35279 35292
40. H. Shi, M.V. Kokoeva, K. Inouye, I. Tzameli, H. Yin, and J.S. Flier Tlr4 links innate immunity and fatty acid-induced insulin resistance J Clin Invest 116 11 2006 3015 3025
41. N. Lin, H. Chen, H. Zhang, X. Wan, and Q. Su Mitochondrial reactive oxygen species (ros) inhibition ameliorates palmitate-induced ins-1 beta cell death Endocrine 42 1 2012 107 117
42. R.A. Egnatchik, A.K. Leamy, Y. Noguchi, M. Shiota, and J.D. Young Palmitate-induced activation of mitochondrial metabolism promotes oxidative stress and apoptosis in h4iiec3 rat hepatocytes Metabolism 63 2 2014 283 295
43. A. Berdichevsky, L. Guarente, and A. Bose Acute oxidative stress can reverse insulin resistance by inactivation of cytoplasmic jnk J Biol Chem 285 28 2010 21581 21589
44. E. Takimoto, and D.A. Kass Role of oxidative stress in cardiac hypertrophy and remodeling Hypertension 49 2 2007 241 248
45. C. Kappe, J.J. Holst, Q. Zhang, and A. Sjoholm Molecular mechanisms of lipoapoptosis and metformin protection in glp-1 secreting cells Biochem Biophys Res Commun 427 1 2012 91 95
46. J.F. Chase, and P.K. Tubbs Specific inhibition of mitochondrial fatty acid oxidation by 2-bromopalmitate and its coenzyme a and carnitine esters Biochem J 129 1 1972 55 65
47. A.C. Nicholson, S. Frieda, A. Pearce, and R.L. Silverstein Oxidized ldl binds to cd36 on human monocyte-derived macrophages and transfected cell lines. Evidence implicating the lipid moiety of the lipoprotein as the binding site Arterioscler Thromb Vasc Biol 15 2 1995 269 275
48. R. Iakoubov, A. Ahmed, L.M. Lauffer, R.P. Bazinet, and P.L. Brubaker Essential role for protein kinase czeta in oleic acid-induced glucagon-like peptide-1 secretion in vivo in the rat Endocrinology 152 4 2011 1244 1252
49. V. Koshkin, F.F. Dai, C.A. Robson-Doucette, C.B. Chan, and M.B. Wheeler Limited mitochondrial permeabilization is an early manifestation of palmitate-induced lipotoxicity in pancreatic beta-cells J Biol Chem 283 12 2008 7936 7948
50. Y. Kanda, M. Shimoda, S. Hamamoto, K. Tawaramoto, F. Kawasaki, and M. Hashiramoto et al. Molecular mechanism by which pioglitazone preserves pancreatic beta-cells in obese diabetic mice: Evidence for acute and chronic actions as a ppargamma agonist Am J Physiol Endocrinol Metab 298 2 2010 E278 E286
51. K. Eguchi, I. Manabe, Y. Oishi-Tanaka, M. Ohsugi, N. Kono, and F. Ogata et al. Saturated fatty acid and tlr signaling link beta cell dysfunction and islet inflammation Cell Metab 15 4 2012 518 533
52. R.S. Jackson, J.W. Creemers, S. Ohagi, M.L. Raffin-Sanson, L. Sanders, and C.T. Montague et al. Obesity and impaired prohormone processing associated with mutations in the human prohormone convertase 1 gene Nat Genet 16 3 1997 303 306
53. R.S. Jackson, J.W. Creemers, I.S. Farooqi, M.L. Raffin-Sanson, A. Varro, and G.J. Dockray et al. Small-intestinal dysfunction accompanies the complex endocrinopathy of human proprotein convertase 1 deficiency J Clin Invest 112 10 2003 1550 1560
54. M. Benzinou, J.W. Creemers, H. Choquet, S. Lobbens, C. Dina, and E. Durand et al. Common nonsynonymous variants in pcsk1 confer risk of obesity Nat Genet 40 8 2008 943 945
55. M.A. Nauck, I. Vardarli, C.F. Deacon, J.J. Holst, and J.J. Meier Secretion of glucagon-like peptide-1 (glp-1) in type 2 diabetes: What is up, what is down? Diabetologia 54 1 2011 10 18