Inhibitory cross-talk between the AMPK and ERK pathways mediates endoplasmic reticulum stress-induced insulin resistance in skeletal muscle

British Journal of Pharmacology

Volumn 169, Issue 1, 2013, Pages 69-81

  Hwang, Seung Lark ^a,b   Jeong, Yong Tae ^a   Li, Xian ^a   Kim, Yong Deuk ^b   Lu, Yue ^a   Chang, Young Chae ^c   Lee, In Kyu ^b   Chang, Hyeun Wook ^a  

^a Yeungnam University   (South Korea)

^b Kyungpook National University School of Medicine   (South Korea)

^c Catholic University of Daegu   (South Korea)

Author keywords

AMPK; endoplasmic reticulum; ERK; glucose uptake; insulin resistance

Indexed keywords

1,4 DIAMINO 1,4 BIS(2 AMINOPHENYLTHIO) 2,3 DICYANOBUTADIENE; ADIPONECTIN; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; INSULIN; INSULIN RECEPTOR SUBSTRATE 1; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN KINASE B; ROSIGLITAZONE; SMALL INTERFERING RNA; THAPSIGARGIN; TUNICAMYCIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL METABOLISM; CONCENTRATION RESPONSE; CONTROLLED STUDY; ENDOPLASMIC RETICULUM STRESS; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME REPRESSION; GLUCOSE BLOOD LEVEL; GLUCOSE HOMEOSTASIS; GLUCOSE TRANSPORT; HORMONE ACTION; IMMUNOPRECIPITATION; INSULIN RESISTANCE; INTRACELLULAR SIGNALING; MALE; MOLECULAR INTERACTION; MOUSE; MUSCLE CELL; MUSCLE TISSUE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN PHOSPHORYLATION; PROTEIN TARGETING; REGULATORY MECHANISM; SKELETAL MUSCLE;

AMP-ACTIVATED PROTEIN KINASES; ANIMALS; BLOTTING, WESTERN; DIABETES MELLITUS, EXPERIMENTAL; DIABETES MELLITUS, TYPE 2; ENDOPLASMIC RETICULUM STRESS; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; GENE KNOCKDOWN TECHNIQUES; INSULIN; INSULIN RECEPTOR SUBSTRATE PROTEINS; INSULIN RESISTANCE; MALE; MAP KINASE SIGNALING SYSTEM; MICE; MICE, INBRED C57BL; MUSCLE FIBERS, SKELETAL; MUSCLE, SKELETAL; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-AKT; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; TRANSFECTION;

EID: 84876215872     PISSN: 00071188     EISSN: 14765381     Source Type: Journal    
DOI: 10.1111/bph.12124     Document Type: Article

References (43)

1. Barbosa-Tessmann IP, Chen C, Zhong C, Siu F, Schuster SM, Nick HS, et al. (2000). Activation of the human asparagine synthetase gene by the amino acid response and the endoplasmic reticulum stress response pathways occurs by common genomic elements. J Biol Chem 275: 26976-26985.
2. Bashan N, Dorfman K, Tarnovscki T, Harman-Boehm I, Liberty IF, Bluher M, et al. (2007). Mitogen-activated protein kinases, inhibitory-kappaB kinase, and insulin signaling in human omental versus subcutaneous adipose tissue in obesity. Endocrinology 148: 2955-2962.
3. Bost F, Aouadi M, Caron L, Even P, Belmonte N, Prot M, et al. (2005). The extracellular signal-regulated kinase isoform ERK1 is specifically required for in vitro and in vivo adipogenesis. Diabetes 54: 402-411.
4. Bouzakri K, Roques M, Gual P, Espinosa S, Guebre-Egziabher F, Riou JP, et al. (2003). Reduced activation of phosphatidylinositol-3 kinase and increased serine 636 phosphorylation of insulin receptor substrate-1 in primary culture of skeletal muscle cells from patients with type 2 diabetes. Diabetes 52: 1319-1325.
5. Carlson CJ, Koterski S, Sciotti RJ, Poccard GB, Rondinone CM, (2003). Enhanced basal activation of mitogen-activated protein kinases in adipocytes from type 2 diabetes: potential role of p38 in the downregulation of GLUT4 expression. Diabetes 52: 634-641.
6. Chawla A, Chakrabarti S, Ghosh G, Niwa M, (2011). Attenuation of yeast UPR is essential for survival and is mediated by IRE1 kinase. J Cell Biol 193: 41-50.
7. Deivanayagam S, Mohammed BS, Vitola BE, Naguib GH, Keshen TH, Kirk EP, et al. (2008). Nonalcoholic fatty liver disease is associated with hepatic and skeletal muscle insulin resistance in overweight adolescents. Am J Clin Nutr 88: 257-262.
8. Gaster M, Rustan AC, Aas V, Beck-Nielsen H, (2004). Reduced lipid oxidation in skeletal muscle from type 2 diabetic subjects may be of genetic origin: evidence from cultured myotubes. Diabetes 53: 542-548.
9. Gregor MF, Hotamisligil GS, (2007). Thematic review series: adipocyte biology. Adipocyte stress: the endoplasmic reticulum and metabolic disease. J Lipid Res 48: 1905-1914.
10. Harding HP, Zhang Y, Ron D, (1999). Protein translation and folding are coupled by an endoplasmic-reticulum-resident kinase. Nature 397: 271-274.
11. Hayashi T, Hirshman MF, Fujii N, Habinowski SA, Witters LA, Goodyear LJ, (2000). Metabolic stress and altered glucose transport: activation of AMP-activated protein kinase as a unifying coupling mechanism. Diabetes 49: 527-531.
12. Hwang SL, Chang HW, Lee IK, Yang BK, Magae J, Chang YC, (2010). Ascofuranone prevents ER stress-induced insulin resistance via activation of AMP-activated protein kinase in L6 myotube cells. Biochem Biophys Res Commun 396: 967-972.
13. Jager J, Corcelle V, Gremeaux T, Laurent K, Waget A, Pages G, et al. (2011). Deficiency in the extracellular signal-regulated kinase 1 (ERK1) protects leptin-deficient mice from insulin resistance without affecting obesity. Diabetologia 54: 180-189.
14. Jorgensen SB, Nielsen JN, Birk JB, Olsen GS, Viollet B, Andreelli F, et al. (2004). The alpha2-5′AMP-activated protein kinase is a site 2 glycogen synthase kinase in skeletal muscle and is responsive to glucose loading. Diabetes 53: 3074-3081.
15. Kahn SE, Hull RL, Utzschneider KM, (2006). Mechanisms linking obesity to insulin resistance and type 2 diabetes. Nature 444: 840-846.
16. Kelley DE, Simoneau JA, (1994). Impaired free fatty acid utilization by skeletal muscle in non-insulin-dependent diabetes mellitus. J Clin Invest 94: 2349-2356.
17. Kilkenny C, Browne W, Cuthill IC, Emerson M, Altman DG, (2010). NC3Rs Reporting Guidelines Working Group. Br J Pharmacol 160: 1577-1579.
18. Korenblat KM, Fabbrini E, Mohammed BS, Klein S, (2008). Liver, muscle, and adipose tissue insulin action is directly related to intrahepatic triglyceride content in obese subjects. Gastroenterology 134: 1369-1375.
19. Kortum RL, Costanzo DL, Haferbier J, Schreiner SJ, Razidlo GL, Wu MH, et al. (2005). The molecular scaffold kinase suppressor of Ras 1 (KSR1) regulates adipogenesis. Mol Cell Biol 25: 7592-7604.
20. Lee SJ, Pfluger PT, Kim JY, Nogueiras R, Duran A, Pages G, et al. (2010). A functional role for the p62-ERK1 axis in the control of energy homeostasis and adipogenesis. EMBO Rep 11: 226-232.
21. Lee YS, Kim WS, Kim KH, Yoon MJ, Cho HJ, Shen Y, et al. (2006). Berberine, a natural plant product, activates AMP-activated protein kinase with beneficial metabolic effects in diabetic and insulin-resistant states. Diabetes 55: 2256-2264.
22. Lin CL, Lin JK, (2008). Epigallocatechin gallate (EGCG) attenuates high glucose-induced insulin signaling blockade in human hepG2 hepatoma cells. Mol Nutr Food Res 52: 930-939.
23. McGrath J, Drummond G, McLachlan E, Kilkenny C, Wainwright C, (2010). Guidelines for reporting experiments involving animals: the ARRIVE guidelines. Br J Pharmacol 160: 1573-1576.
24. Mu J, Brozinick JT Jr, Valladares O, Bucan M, Birnbaum MJ, (2001). A role for AMP-activated protein kinase in contraction- and hypoxia-regulated glucose transport in skeletal muscle. Mol Cell 7: 1085-1094.
25. Neschen S, Morino K, Hammond LE, Zhang D, Liu ZX, Romanelli AJ, et al. (2005). Prevention of hepatic steatosis and hepatic insulin resistance in mitochondrial acyl-CoA:glycerol-sn-3-phosphate acyltransferase 1 knockout mice. Cell Metab 2: 55-65.
26. Ozcan U, Cao Q, Yilmaz E, Lee AH, Iwakoshi NN, Ozdelen E, et al. (2004). Endoplasmic reticulum stress links obesity, insulin action, and type 2 diabetes. Science 306: 457-461.
27. Ozcan U, Yilmaz E, Ozcan L, Furuhashi M, Vaillancourt E, Smith RO, et al. (2006). Chemical chaperones reduce ER stress and restore glucose homeostasis in a mouse model of type 2 diabetes. Science 313: 1137-1140.
28. Permutt MA, Wasson J, Cox N, (2005). Genetic epidemiology of diabetes. J Clin Invest 115: 1431-1439.
29. Ron D, (2002). Translational control in the endoplasmic reticulum stress response. J Clin Invest 110: 1383-1388.
30. Saltiel AR, Kahn CR, (2001). Insulin signalling and the regulation of glucose and lipid metabolism. Nature 414: 799-806.
31. Savage DB, Choi CS, Samuel VT, Liu ZX, Zhang D, Wang A, et al. (2006). Reversal of diet-induced hepatic steatosis and hepatic insulin resistance by antisense oligonucleotide inhibitors of acetyl-CoA carboxylases 1 and 2. J Clin Invest 116: 817-824.
32. Shen X, Ellis RE, Lee K, Liu CY, Yang K, Solomon A, et al. (2001). Complementary signaling pathways regulate the unfolded protein response and are required for C. elegans development. Cell 107: 893-903.
33. Shi Y, Vattem KM, Sood R, An J, Liang J, Stramm L, et al. (1998). Identification and characterization of pancreatic eukaryotic initiation factor 2 alpha-subunit kinase, PEK, involved in translational control. Mol Cell Biol 18: 7499-7509.
34. Shi Y, Taylor SI, Tan SL, Sonenberg N, (2003). When translation meets metabolism: multiple links to diabetes. Endocr Rev 24: 91-101.
35. Tang X, Shen H, Chen J, Wang X, Zhang Y, Chen LL, et al. (2011). Activating transcription factor 6 protects insulin receptor from ER stress-stimulated desensitization via p42/44 ERK pathway. Acta Pharmacol Sin 32: 1138-1147.
36. Taniguchi CM, Emanuelli B, Kahn CR, (2006). Critical nodes in signaling pathways: insights into insulin action. Nat Rev Mol Cell Biol 7: 85-96.
37. Tanti JF, Jager J, (2009). Cellular mechanisms of insulin resistance: role of stress-regulated serine kinases and insulin receptor substrates (IRS) serine phosphorylation. Curr Opin Pharmacol 9: 753-762.
38. Thirone AC, Huang C, Klip A, (2006). Tissue-specific roles of IRS proteins in insulin signaling and glucose transport. Trends Endocrinol Metab 17: 72-78.
39. Um SH, Frigerio F, Watanabe M, Picard F, Joaquin M, Sticker M, et al. (2004). Absence of S6K1 protects against age- and diet-induced obesity while enhancing insulin sensitivity. Nature 431: 200-205.
40. Vavvas D, Apazidis A, Saha AK, Gamble J, Patel A, Kemp BE, et al. (1997). Contraction-induced changes in acetyl-CoA carboxylase and 5′-AMP- activated kinase in skeletal muscle. J Biol Chem 272: 13255-13261.
41. Viollet B, Andreelli F, Jorgensen SB, Perrin C, Geloen A, Flamez D, et al. (2003). The AMP-activated protein kinase alpha2 catalytic subunit controls whole-body insulin sensitivity. J Clin Invest 111: 91-98.
42. Wojtaszewski JF, Jørgensen SB, Hellsten Y, Hardie DG, Richter EA, (2002). Glycogen-dependent effects of 5-aminoimidazole-4-carboxamide (AICA)-riboside on AMP-activated protein kinase and glycogen synthase activities in rat skeletal muscle. Diabetes 51: 284-292.
43. Zheng Y, Zhang W, Pendleton E, Leng S, Wu J, Chen R, et al. (2009). Improved insulin sensitivity by calorie restriction is associated with reduction of ERK and p70S6K activities in the liver of obese Zucker rats. J Endocrinol 203: 337-347.