Egr-1 decreases adipocyte insulin sensitivity by tilting PI3K/Akt and MAPK signal balance in mice

EMBO Journal

Volumn 30, Issue 18, 2011, Pages 3754-3765

  Yu, Xiao ^a,c   Shen, Ning ^a   Zhang, Ming Liang ^d   Pan, Fei Yan ^a   Wang, Chen ^d   Jia, Wei Ping ^d   Liu, Chang ^c   Gao, Qian ^a   Gao, Xiang ^a   Xue, Bin ^a   Li, Chao Jun ^a,b  

^a MEDICAL SCHOOL OF NANJING UNIVERSITY   (China)

^b WENZHOU MEDICAL UNIVERSITY   (China)

^c NANJING NORMAL UNIVERSITY   (China)

^d SHANGHAI JIAO TONG UNIVERSITY AFFILIATED SIXTH PEOPLE S HOSPITAL   (China)

Author keywords

AKT; Egr 1; insulin resistance; MAPK

Indexed keywords

EARLY GROWTH RESPONSE FACTOR 1; FARNESYL TRANS TRANSFERASE; GLUCOSE; INSULIN; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROTEIN KINASE B;

ABDOMINAL FAT; ADIPOCYTE; ADULT; AGED; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DIABETIC PATIENT; ENZYME ACTIVATION; FEMALE; GLUCOSE BLOOD LEVEL; GLUCOSE TOLERANCE TEST; HUMAN; HUMAN TISSUE; HYPERINSULINISM; INSULIN RESISTANCE; INSULIN SENSITIVITY; MALE; MOUSE; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; UPREGULATION;

ADIPOCYTES; ANIMALS; CELL LINE; EARLY GROWTH RESPONSE PROTEIN 1; FARNESYLTRANSTRANSFERASE; GENE EXPRESSION REGULATION; HUMANS; INSULIN; INSULIN RESISTANCE; MICE; MITOGEN-ACTIVATED PROTEIN KINASE KINASES; MULTIENZYME COMPLEXES; PHOSPHATIDYLINOSITOL 3-KINASES; PTEN PHOSPHOHYDROLASE; SIGNAL TRANSDUCTION;

MUS;

EID: 80052775605     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2011.277     Document Type: Article

References (61)

1. Aguirre V, Uchida T, Yenush L, Davis R, White MF (2000) The c-Jun NH2-terminal kinase promotes insulin resistance during association with insulin receptor substrate-1 and phosphorylation of Ser307. J Biol Chem 275: 9047
2. Benz AH, Shajari M, Peruzki N, Dehghani F, Maronde E (2010) Early growth response-1 induction by fibroblast growth factor-1 viaincrease of mitogen-activated protein kinase and inhibition of protein kinase B in hippocampal neurons. Br J Pharmacol 160: 1621-1630
3. Biddinger SB, Kahn CR. 2006, From mice to men: insights into the insulin resistance syndromes. Annu Rev Physiol, 68, 123-158.
4. Boyle KB, Hadaschik D, Virtue S, Cawthorn WP, Ridley SH, O'Rahilly S, Siddle K (2009) The transcription factors Egr1 and Egr2 have opposing influences on adipocyte differentiation. Cell Death Differ 16: 782-789
5. Burgering BMT, Coffer PJ (1995) Protein kinase B (c-Akt) in phosphatidylinositol-3-OH kinase signal transduction. Nature 376: 599-602
6. Cao XM, Guy GR, Sukhatme VP, Tan YH (1992) Regulation of the Egr-1 gene by tumor necrosis factor and interferons in primary human fibroblasts. J Biol Chem 267: 1345-1349
7. Cavaghan MK, Ehrmann DA, Polonsky KS (2000) Interactions between insulin resistance and insulin secretion in the development of glucose intolerance. J Clin Invest 106: 329-333 (Pubitemid 30655631)
8. Chan TM, Exton JH (1976) A rapid method for the determination of glycogen content and radioactivity in small quantities of tissue or isolated hepatocytes* 1. Anal Biochem 71: 96-105
9. Chavrier P, Zerial M, Lemaire P, Almendral J, Bravo R, Charnay P (1988) A gene encoding a protein with zinc fingers is activated during G0/G1 transition in cultured cells. EMBO J 7: 29-35
10. Elchebly M, Payette P, Michaliszyn E, Cromlish W, Collins S, Loy AL, Normandin D, Cheng A, Himms-Hagen J, Chan CC (1999) Increased insulin sensitivity and obesity resistance in mice lacking the protein tyrosine phosphatase-1B gene. Science 283: 1544
11. Emanuelli B, Eberl D, Suzuki R, Kahn CR (2008) Overexpression of the dual-specificity phosphatase MKP-4/DUSP-9 protects against stress-induced insulin resistance. Proc Natl Acad Sci USA 10 5 : 3545
12. Esma I, Maxenence F, Goran K, Emina S, Jelena V, Branislava D, Pierre M (2008) Insulin regulation of proliferation involves activation of AKT and ERK 1/2 signaling pathways in vascular smooth muscle cells. Exp Clin Endocrinol Diabetes 16: P652
13. Evans JL, Goldfine ID, Maddux BA, Grodsky GM (2003) Are oxidative stress-activated signaling pathways mediators of insulin resistance and b-cell dysfunction? Diabetes 52: 1-8 (Pubitemid 36042100)
14. Franke TF, Yang SI, Chan TO, Datta K, Kazlauskas A, Morrison DK, Kaplan DR, Tsichlis PN (1995) The protein kinase encoded by the Akt proto-oncogene is a target of the PDGF-activated phosphati-dylinositol 3-kinase. Cell 81: 727-736
15. Frayn KN (2007) Adipose tissue and the insulin resistance syndrome. Proc Nutr Soc 60: 375-380
16. Fujishiro M, Gotoh Y, Katagiri H, Sakoda H, Ogihara T, Anai M, Onishi Y, Ono H, Abe M, Shojima N (2003) Three mitogen-activated protein kinases inhibit insulin signaling by different mechanisms in 3T3-L1 adipocytes. Mol Endocrinol 17: 487
17. Fukuhara A, Matsuda M, Nishizawa M, Segawa K, Tanaka M, Kishimoto K, Matsuki Y, Murakami M, Ichisaka T, Murakami H (2005) Visfatin: a protein secreted by visceral fat that mimics the effects of insulin. Science 307: 426
18. Furukawa N, Ongusaha P, Jahng WJ, Araki K, Choi CS, Kim HJ, Lee YH, Kaibuchi K, Kahn BB, Masuzaki H (2005) Role of Rho-kinase in regulation of insulin action and glucose homeostasis. Cell Metab 2: 119-129
19. Gabir MM, Hanson RL, Dabelea D, Imperatore G, Roumain J, Bennett PH, Knowler WC (2000) The 1997 American Diabetes Association and 1999 World Health Organization criteria for hyperglycemia in the diagnosis and prediction of diabetes. Diabetes Care 23: 1108
20. Gashler A, Sukhatme VP (1995) Early growth response protein 1 (Egr-1): prototype of a zinc-finger family of transcription factors. Prog Nucleic Acid Res Mol Biol 50: 191-224
21. Gavin JR, Roth J, Neville DM, De Meyts P, Buell DN (1974) Insulin-dependent regulation of insulin receptor concentrations: a direct demonstration in cell culture. Proc Natl Acad Sci USA 71: 84
22. Gregorio F, Ambrosi F, Cristallini S, Filipponi P, Santeusanio F (1996) Effects of glimepiride on insulin and glucagon release from isolated rat pancreas at different glucose concentrations. Acta Diabetol 33: 25-29 (Pubitemid 26096152)
23. Guilherme A, Virbasius JV, Puri V, Czech MP (2008) Adipocyte dysfunctions linking obesity to insulin resistance and type 2 diabetes. Nat Rev Mol Cell Biol 9: 367-377 (Pubitemid 351574198)
24. Hirosumi J, Tuncman G, Chang L, Gorgun CZ, Uysal KT, Maeda K, Karin K, Hotamisligil GS (2002) A central role for JNK in obesity and insulin resistance. Nature 420: 333-336 (Pubitemid 35398190)
25. Hofmann C, Lorenz K, Braithwaite SS, Colca JR, Palazuk BJ, Hotamisligil GS, Spiegelman BM (1994) Altered gene expression for tumor necrosis factor-alpha and its receptors during drug and dietary modulation of insulin resistance. Endocrinology 134: 264
26. Hotamisligil GS (2006) Inflammation and metabolic disorders. Nature 444: 860-867 (Pubitemid 46024993)
27. Hotamisligil GS, Murray DL, Choy LN, Spiegelman BM (1994) Tumor necrosis factor alpha inhibits signaling from the insulin receptor. Proc Natl Acad Sci USA 91 : 4854
28. Hotamisligil GS, Shargill NS, Spiegelman BM (1993) Adipose expression of tumor necrosis factor-alpha: direct role in obesity-linked insulin resistance. Science 259: 87
29. Hug C, Lodish HF (2005) Visfatin: a new adipokine. Science 307: 366-367 (Pubitemid 40139968)
30. Isenovic ER, Kedees MH, Tepavcevic S, Milosavljevic T, Koricanac G, Trpkovic A, Marche P (2009) Role of PI3K/AKT, cPLA2 and ERK1/2 signaling pathways in insulin regulation of vascular smooth muscle cells proliferation. Cardiovasc Haematol Disord Drug Targets 9: 172-180
31. Kammoun HL, Chabanon H, Hainault I, Luquet S, Magnan C, Koike T, Ferr P, Foufelle F (2009) GRP78 expression inhibits insulin and ER stress-induced SREBP-1c activation and reduces hepatic stea-tosis in mice. J Clin Invest 119: 1201
32. Kaneto H, Nakatani Y, Miyatsuka T, Kawamori D, Matsuoka T, Matsuhisa M, Kajimoto Y, Ichijo H, Yamasaki Y, Hori M (2004) Possible novel therapy for diabetes with cell-permeable JNK-inhibitory peptide. Nat Med 10 : 1128-1132 (Pubitemid 39424876)
33. Kershaw EE, Flier JS (2004) Adipose tissue as an endocrine organ. J Clin Endocrinol Metab 89: 2548
34. Kurlawalla-Martinez C, Stiles B, Wang Y, Devaskar SU, Kahn BB, Wu H (2005) Insulin hypersensitivity and resistance to strepto-zotocin-induced diabetes in mice lacking PTEN in adipose tissue. Mol Cell Biol 25: 2498
35. Li CJ, Ning W, Matthay MA, Feghali-Bostwick CA, Choi AMK (2007) MAPK pathway mediates EGR-1-HSP70-dependent cigarette smoke-induced chemokine production. Am J Physiol Lung Cell Mol Physiol 292: L1297
36. Luan B, Zhao J, Wu H, Duan B, Shu G, Wang X, Li D, Jia W, Kang J, Pei G (2009) Deficiency of a beta-arrestin-2 signal complex contributes to insulin resistance. Nature 457: 1146-1149
37. Manning AM, Davis RJ (2003) Targeting JNK for therapeutic benefit: from junk to gold? Nat Rev Drug Discov 2: 554-565 (Pubitemid 37361747)
38. Matsuzawa Y, Shimomura I, Nakamura T, Keno Y, Tokunaga K (1994) Pathophysiology and pathogenesis of visceral fat obesity. Diabetes Res Clin Pract 24: S111-S116
39. Miller WL (2002) Androgen biosynthesis from cholesterol to DHEA. Mol Cell Endocrinol 198: 7-14 (Pubitemid 36169929)
40. Moyers JS, Bilan PJ, Reynet C, Kahn CR (1996) Overexpression of Rad inhibits glucose uptake in cultured muscle and fat cells. J Biol Chem 271: 23111
41. Ning W, Li CJ, Kaminski N, Feghali-Bostwick CA, Alber SM, Di YP, Otterbein SL, Song R, Hayashi S, Zhou Z (2004) Comprehensive gene expression profiles reveal pathways related to the pathogen-esis of chronic obstructive pulmonary disease. Proc Natl Acad Sci USA 101 : 14895
42. Nishikawa T, Edelstein D, Du XL, Yamagishi S, Matsumura T, Kaneda Y, Yorek MA, Beebe D, Oates PJ, Hammes HP, Giardino I, Brownlee M (2000) Normalizing mitochondrial superoxide production blocks three pathways of hyperglycaemic damage. Nature 404: 787-790 (Pubitemid 30212409)
43. Olivier LM, Kovacs W, Masuda K, Keller GA, Krisans SK (2000) Identification of peroxisomal targeting signals in cholesterol biosynthetic enzymes: AA-CoA thiolase, HMG-CoA synthase, MPPD, and FPP synthase. J Lipid Res 41: 1921
44. Polonsky KS, Sturis J, Bell GI (1996) Non-insulin-dependent diabetes mellitus-a genetically programmed failure of the beta cell to compensate for insulin resistance. N Engl J Med 334: 777
45. Pou KM, Massaro JM, Hoffmann U, Vasan RS, Maurovich-Horvat P, Larson MG, Keaney Jr JF, Meigs JB, Lipinska I, Kathiresan S (2007) Visceral and subcutaneous adipose tissue volumes are cross-sectionally related to markers of inflammation and oxida-tive stress: the Framingham Heart Study. Circulation 116: 1234
46. Sabio G, Das M, Mora A, Zhang Z, Jun JY, Ko HJ, Barrett T, Kim JK, Davis RJ (2008) A stress signaling pathway in adipose tissue regulates hepatic insulin resistance. Science 322: 1539
47. Samad F, Pandey M, Bell PA, Loskutoff DJ (2000) Insulin continues to induce plasminogen activator inhibitor 1 gene expression in insulin-resistant mice and adipocytes. Mol Med 6: 680
48. Samuelsson AM, Bollano E, Mobini R, Larsson BM, Omerovic E, Fu M, Waagstein F, Holmang A (2006) Hyperinsulinemia: effect on cardiac mass/function, angiotensin II receptor expression, and insulin signaling pathways. Am J Physiol Heart Circ Physiol 291: H787
49. Sartipy P, Loskutoff DJ (2003a) Expression profiling identifies genes that continue to respond to insulin in adipocytes made insulin-resistant by treatment with tumor necrosis factor-a*. J Biol Chem 278: 52298-52306 (Pubitemid 38035818)
50. Sartipy P, Loskutoff DJ (2003b) Monocyte chemoattractant protein 1 in obesity and insulin resistance. Proc Natl Acad Sci USA 100: 7265
51. Shen N, Gong T, Wang JD, Meng FL, Qiao L, Yang RL, Xue B, Pan FY, Zhou XJ, Chen HQ, Ning W, Li CJ (2011a) Cigarette smoke-induced pulmonary inflammatory responses are mediated by Egr-1/GGPPS/MAPK signaling. Am J Pathol 178: 110-118
52. Shen N, Yu X, Pan FY, Gao X, Xue B, Li CJ (2011b) An early response transcription factor, Egr-1, enhances insulin resistance in type 2 diabetes with chronic hyperinsulinism. J Biol Chem 286: 14508-14515
53. Shoelson SE, Lee J, Goldfine AB (2006) Inflammation and insulin resistance. J Clin Invest 116: 1793-1801 (Pubitemid 44033299)
54. Son SW, Min BW, Lim Y, Lee YH, Shin SY (2008) Regulatory mechanism of TNF [alpha] autoregulation in HaCaT cells: the role of the transcription factor EGR-1. Biochem Biophys Res Commun 374: 777-782
55. Steppan CM, Lazar MA (2002) Resistin and obesity-associated insulin resistance. Trends Endocrinol Metab 13: 18-23 (Pubitemid 36734011)
56. Sun XJ, Rothenberg P, Kahn CR, Backer JM, Araki E, Wilden PA, Cahill DA, Goldstein BJ, White MF (1991) Structure of the insulin receptor substrate IRS-1 defines a unique signal transduction protein. Nature 352: 73-77 (Pubitemid 21896701)
57. Uysal KT, Wiesbrock SM, Marino MW, Hotamisligil GS (1997) Protection from obesity-induced insulin resistance in mice lack-́ ing TNF-lA function. Nature 389: 610-614 (Pubitemid 27446179)
58. Virolle T, Adamson ED, Baron V, Birle D, Mercola D, Mustelin T, de Belle I (2001) The Egr-1 transcription factor directly activates PTEN during irradiation-induced signalling. Nat Cell Biol 3: 1124-1128 (Pubitemid 33130464)
59. Wellen KE, Hotamisligil GS (2005) Inflammation, stress, and diabetes. J Clin Invest 115: 1111-1119 (Pubitemid 40629025)
60. Yamada T, Katagiri H, Ishigaki Y, Ogihara T, Imai J, Uno K, Hasegawa Y, Gao J, Ishihara H, Niijima A (2006) Signals from intra-abdominal fat modulate insulin and leptin sensitivity through different mechanisms: neuronal involvement in food-intake regulation. Cell Metab 3: 223-229
61. Yan SF, Pinsky DJ, Mackman N, Stern DM (2000) Egr-1: is it always immediate and early? J Clin Invest 105 : 553