Targeting the ERK signaling pathway as a potential treatment for insulin resistance and type 2 diabetes

American Journal of Physiology - Endocrinology and Metabolism

Volumn 310, Issue 8, 2016, Pages E643-E651

  Ozaki, Kei Ichi ^a   Awazu, Midori ^b   Tamiya, Mayuko ^a   Iwasaki, Yuka ^a   Harada, Aya ^a   Kugisaki, Satomi ^a   Tanimura, Susumu ^a   Kohno, Michiaki ^a  

^a NAGASAKI UNIVERSITY   (Japan)

^b KEIO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

Adipocyte; Adipocytokine; Extracellular signal regulated kinase pathway; MEK inhibitor; Type 2 diabetes

Indexed keywords

2 (2 CHLORO 4 IODOANILINO) N CYCLOPROPYLMETHOXY 3,4 DIFLUOROBENZAMIDE; ADIPOCYTOKINE; FATTY ACID; GLUCOSE; MITOGEN ACTIVATED PROTEIN KINASE; N (2,3 DIHYDROXYPROPOXY) 3,4 DIFLUORO 2 (2 FLUORO 4 IODOANILINO)BENZAMIDE; TRIACYLGLYCEROL; 2-(2-CHLORO-4-IODOPHENYLAMINO)-N-CYCLOPROPYLMETHOXY-3,4-DIFLUOROBENZAMIDE; ADIPONECTIN; BENZAMIDE DERIVATIVE; CCL2 PROTEIN, MOUSE; DIPHENYLAMINE; INSULIN; INTERLEUKIN 6; INTERLEUKIN-6, MOUSE; LEPTIN RECEPTOR; MONOCYTE CHEMOTACTIC PROTEIN 1; PROTEIN KINASE INHIBITOR; TUMOR NECROSIS FACTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; DOWN REGULATION; FATTY ACID BLOOD LEVEL; GLUCOSE BLOOD LEVEL; GLUCOSE TOLERANCE; GLUCOSE TOLERANCE TEST; INSULIN RESISTANCE; INSULIN SENSITIVITY; INTRAPERITONEAL FAT; LIPOLYSIS; MALE; MOUSE; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN TARGETING; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TRIACYLGLYCEROL BLOOD LEVEL; UPREGULATION; 3T3-L1 CELL LINE; ADIPOCYTE; ANALOGS AND DERIVATIVES; ANIMAL; ANTAGONISTS AND INHIBITORS; DEFICIENCY; DISEASE MODEL; DRUG EFFECT; HYPERLIPIDEMIA; IMMUNOBLOTTING; IN VITRO STUDY; LIPID DIET; MAPK SIGNALING; METABOLISM; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

3T3-L1 CELLS; ADIPOCYTES; ADIPOKINES; ADIPONECTIN; ANIMALS; BENZAMIDES; BLOOD GLUCOSE; CHEMOKINE CCL2; DIABETES MELLITUS, TYPE 2; DIET, HIGH-FAT; DIPHENYLAMINE; DISEASE MODELS, ANIMAL; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FATTY ACIDS, NONESTERIFIED; GLUCOSE TOLERANCE TEST; HYPERLIPIDEMIAS; IMMUNOBLOTTING; IN VITRO TECHNIQUES; INSULIN; INSULIN RESISTANCE; INTERLEUKIN-6; LIPOLYSIS; MALE; MAP KINASE SIGNALING SYSTEM; MICE; PROTEIN KINASE INHIBITORS; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTORS, LEPTIN; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TRIGLYCERIDES; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84983761022     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.00445.2015     Document Type: Article

References (41)

1. Astapova O, Leff T. Adiponectin and PPARγ: cooperative and interdependent actions of two key regulators of metabolism. Vitam Horm 90: 143–162, 2012.
2. Aubert J, Dessolin S, Belmonte N, Li M, McKenzie FR, Staccini L, Villageois P, Barhanin B, Vernallis A, Smith AG, Ailhaud G, Dani C. Leukemia inhibitory factor and its receptor promote adipocyte differentiation via the mitogen-activated protein kinase cascade. J Biol Chem 274: 24965–24972, 1999.
3. Bashan N, Dorfman K, Tarnovscki T, Harman-Boehm I, Liberty IF, Blüher M, Ovadia S, Maymon-Zilberstein T, Potashnik R, Stumvoll M, Avinoach E, Rudich A. Mitogen-activated protein kinases, inhibitorykappaB kinase, and insulin signaling in human omental versus subcutaneous adipose tissue in obesity. Endocrinology 148: 2955–2962, 2007.
4. Belmonte N, Phillips BW, Massiera F, Villageois P, Wdziekonski B, Saint-Marc P, Nichols J, Aubert J, Saeki K, You A, Narumiya S, Ailhaud G, Dani C. Activation of extracellular signal-regulated kinases and CREB/ATF-1 mediate the expression of CCAAT/enhancer binding proteins β and – δ in preadipocytes. Mol Endocrinol 15: 2037–2049, 2001.
5. Black RA. Tumor necrosis factor-α converting enzyme. Int J Biochem Cell Biol 34: 1–5, 2002.
6. Boden G. Effects of free fatty acids on glucose metabolism: significance for insulin resistance and type 2 diabetes. Exp Clin Endocrinol Diabetes 111: 121–124, 2003.
7. Bost F, Aouadi M, Caron L, Binetruy B. The role of MAPKs in adipocyte differentiation and obesity. Biochimie 87: 51–56, 2005.
8. Bost F, Aouadi M, Caron L, Even P, Belmonte N, Prot M, Dani C, Hofman P, Pagés G, Pouysségur J, Marchand-Brustel Y, Binétruy B. The extracellular signal-regulated kinase isoform ERK1 is specifically required for in vitro and in vivo adipogenesis. Diabetes 54: 402–411, 2005.
9. Bouzakri K, Roques M, Gual P, Espinosa S, Guebre-Egziabher F, Riou J, Laville M, Marchand-Brustel YL, Tanti JF, Vidal H. 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, 2003.
10. Cao H. Adipocytokines in obesity and metabolic disease. J Endocrinol 220: T47–T59, 2014.
11. Carlson CJ, Koterski S, Sciotti RJ, Poccard GB, Rondinone CM. 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, 2003.
12. Chen HC, Feener EP. MEK1,2 response element mediates angiotensin II-stimulated plasminogen activator inhibitor-1 promoter activation. Blood 103: 2636–2644, 2004.
13. Chen LF, Greene WC. Shaping the nuclear action of NF-κB. Nat Rev Mol Cell Biol 5: 392–401, 2004.
14. Diaz C, Lee AT, McConkey DJ, Schroit AJ. Phosphatidylserine externalization during differentiation-triggered apoptosis of erythroleukemic cells. Cell Death Differ 6: 218–226, 1999.
15. Farooq A, Zhou MM. Structure and regulation of MAPK phosphatases. Cell Signal 16: 769–779, 2004.
16. Green H, Meuth M. An established pre-adipose cell line and its differentiation in culture. Cell 3: 127–133, 1974.
17. Greenberg AS, Shen WJ, Muliro K, Patel S, Souza SC, Roth RA, Kraemer FB. Stimulating of lipolysis and hormone-sensitive lipase via the extracellular signal-regulated kinase pathway. J Biol Chem 276: 45456–45461, 2001.
18. Hoshino R, Tanimura S, Watanabe K, Kataoka T, Kohno M. Blockade of the extracellular signal-regulated kinase pathway induces marked G1 cell cycle arrest and apoptosis in tumor cells in which the pathway is constitutively activated. J Biol Chem 276: 2686–2692, 2001.
19. Ito A, Suganami T, Miyamoto Y, Yoshimasa Y, Takeya M, Kamei Y, Ogawa Y. Role of MAPK phophatase-1 in the induction of monocyte chemoattractant protein-1 during the course of adipocyte hypertrophy. J Biol Chem 282: 25445–25452, 2007.
20. Jager J, Grémeaux T, Cormont M, Le Marchand-Brustel Y, Tanti JF. Interleukin-1beta-induced insulin resistance in adipocytes through downregulation of insulin receptor substrate-1 expression. Endocrinology 148: 241–251, 2007.
21. Jager J, Corcelle V, Grémeaux T, Laurent K, Waget A, Pegés G, Binétruy B, Marchand-Brustel YL, Burcelin R, Bost F, Tanti JF. Deficiency in the extracellular signal-regulated kinase 1 (ERK1) protects leptin-deficient mice from insulin resistance without affecting obesity. Diabetologia 54: 180–189, 2011.
22. Kajita K, Mori I, Kitada Y, Taguchi K, Kajita T, Hanamoto T, Ikeda T, Fujioka K, Yamauchi M, Okada H, Usui T, Uno Y, Morita H, Ishizuka T. Small proliferative adipocytes: identification of proliferative cell expressing adipocyte markers. Endocr J 60: 931–939, 2013.
23. Kotzka J, Müller-Wieland D, Roth G, Kremer L, Munck M, Schürmann S, Knebel B, Krone W. Sterol regulatory element binding proteins (SREBP)-1a and SREBP-2 are linked to the MAP-kinase cascade. Lipid Res 41: 99–108, 2000.
24. Leonard M, Ryan MP, Watson AJ, Schramek H, Healy E. Role of MAP kinase pathways in mediating IL-6 production in human primary mesangial and proximal tubular cells. Kidney Int 56: 1366–1377, 1999.
25. Lindsay RS, Funahashi T, Hanson RL, Matsuzawa Y, Tanaka S, Tataranni PA, Knowler WC, Krakoff J. Adiponectin and development of type 2 diabetes in the Pima Indian population. Lancet 360: 57–58, 2002.
26. Ozaki KI, Kishikawa F, Tanaka M, Sakamoto T, Tanimura S, Kohno M. Histone deacetylase inhibitors enhance the chemosensitivity of tumor cells with cross-resistance to a wide range of DNA-damaging agent. Cancer Sci 99: 376–384, 2008.
27. Ozaki K, Kosugi M, Baba N, Fujio K, Sakamoto T, Kimura S, Tanimura S, Kohno M. Blockade of the ERK or PI3K-Akt signaling pathway enhances the cytotoxicity of the histone deacetylase inhibitor in tumor cells resistant to gefitinib or imatinib. Biochem Biophys Res Commun 391: 1610–1615, 2010.
28. Prusty D, Park BH, Davis KE, Farmer SR. Activation of MEK/ERK signaling promotes adipogenesis by enhancing peroxisome proliferatoractivated receptor γ (PPARγ) and C/EBPα gene expression during the differentiation of 3T3-L1 preadipocytes. J Biol Chem 277: 46226–46232, 2002.
29. Qatanani M, Lazar MA. Mechanisms of obesity-associated insulin resistance: many choices on the menu. Genes Dev 21: 1443–1455, 2007.
30. Ramirez-Zacarias JL, Castro-Munozledo F, Kuri-Harcuch W. Quantitation of adipose conversion and triglycerides by staining intracytoplasmic lipids with Oil red O. Histochemistry 97: 493–497, 1992.
31. Roth G, Kotzka J, Kremer L, Lehr S, Lohaus C, Meyer HE, Krone W, Müller-Wieland D. MAP kinase Erk1/2 phosphorylate sterol regulatory element-binding protein (SREBP)-1a at serine 117 in vitro. J Biol Chem 275: 33302–33307, 2000.
32. Sakamoto T, Ozaki KI, Fujio K, Kajikawa S, Uesato S, Watanabe K, Tanimura S, Koji T, Kohno M. Blockade of the ERK pathway enhances the therapeutic efficacy of the histone deacetylase inhibitor MS-275 in human tumor xenograft models. Biochem Biophys Res Commun 433: 456–462, 2013.
33. Savage DB, Petersen KF, Shulman GI. Disordered lipid metabolism and the pathogenesis of insulin resistance. Physiol Rev 87: 507–520, 2007.
34. Shao D, Rangwala SM, Bailey ST, Krakow SL, Reginato MJ, Lazar MA. Interdomain communication regulating ligand binding by PPAR-γ. Nature 396: 377–380, 1998.
35. Shi H, Kokoeva MV, Inouye K, Tzameli I, Yin H, Flier JS. TLR4 links innate immunity and fatty acid-induced insulin resistance. J Clin Invest 116: 3015–3025, 2006.
36. Suzawa M, Takada I, Yanagisawa J, Ohtake F, Ogawa S, Yamauchi T, Kadowaki T, Takeuchi Y, Shibuya H, Gotoh Y, Matsumoto K, Kato S. Cytokines suppress adipogenesis and PPAR-γ function through the TAK1/TAB1/NIK cascade. Nat Cell Biol 5: 224–230, 2003.
37. Tanimura S, Asato K, Fujishiro S, Kohno M. Specific blockade of the ERK pathway inhibits the invasiveness of tumor cells: down-regulation of matrix metalloproteinase-3/-9/-14 and CD44. Biochem Biophys Res Commun 304: 801–803, 2003.
38. Tanti JF, Jager J. Cellular mechanisms of insulin resistance: role of stress-regulated serine kinases and insulin receptor substrates (IRS) serine phosphorylation. Curr Opin Pharmacol 9: 753–762, 2009.
39. Tsuchida A, Yamauchi T, Takekawa S, Hada Y, Ito Y, Maki T, Kadowaki T. Peroxisome proliferator-activated receptor (PPAR) α activation increases adiponectin receptors and reduces obesity-related inflammation in adipose tissue. Diabetes 54: 3358–3370, 2005.
40. Watanabe K, Tanimura S, Uchiyama A, Sakamoto S, Kawabata T, Ozaki KI, Kohno M. Blockade of the extracellular signal-regulated kinase pathway enhances the therapeutic efficacy of microtubule-destabilizing agents in human tumor xenograft models. Clin Cancer Res 16: 1170–1178, 2010.
41. Weisberg SP, McCann D, Desai M, Rosenbaum M, Leibel RL, Ferrante AW Jr.. Obesity is associated with macrophage accumulation in adipose tissue. J Clin Invest 112: 1796–1808, 2003.