Tpl2 kinase is upregulated in adipose tissue in obesity and may mediate interleukin-1β and tumor necrosis factor-α effects on extracellular signal-regulated kinase activation and lipolysis

Diabetes

Volumn 59, Issue 1, 2010, Pages 61-70

  Jager, Jennifer ^a,b   Grémeaux, Thierry ^a,b   Gonzalez, Teresa ^a,b   Bonnafous, Stéphanie ^a,b,c   Debard, Cyrille ^a   Laville, Martine ^a   Vidal, Hubert ^a   Tran, Albert ^a,b,c   Gual, Philippe ^a,b,c   Marchand Brustel, Yannick Le ^a,b,c   Cormont, Mireille ^a,b   Tanti, Jean François ^a,b  

^a INSERM   (France)

^b UNIVERSITÉ CÔTE D'AZUR   (France)

^c UNIVERSITY HOSPITAL OF NICE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

1,4 DIAMINO 1,4 BIS(2 AMINOPHENYLTHIO) 2,3 DICYANOBUTADIENE; GLYCEROL; I KAPPA B KINASE BETA; INSULIN; INSULIN RECEPTOR SUBSTRATE 1; INTERLEUKIN 1BETA; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE KINASE KINASE; SERINE; SMALL INTERFERING RNA; TUMOR NECROSIS FACTOR ALPHA; TUMOR PROGRESSION LOCUS 2; UNCLASSIFIED DRUG; I KAPPA B KINASE; IKBKB PROTEIN, MOUSE; MAP3K8 PROTEIN, MOUSE; ONCOPROTEIN;

ADIPOCYTE; ADIPOSE TISSUE; ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL STRAIN 3T3; CONTROLLED STUDY; DIABETES MELLITUS; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; FEMALE; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN TISSUE; LIPOLYSIS; MALE; MORBID OBESITY; MOUSE; NONHUMAN; OBESITY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; REAL TIME POLYMERASE CHAIN REACTION; UPREGULATION; ANIMAL; BODY WEIGHT; C57BL MOUSE; CELL DIFFERENTIATION; CYTOLOGY; DIET RESTRICTION; DRUG EFFECT; GENETICS; METABOLISM; MOUSE MUTANT; NONOBESE DIABETIC MOUSE; PATHOPHYSIOLOGY; PHYSIOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

3T3-L1 CELLS; ADIPOCYTES; ANIMALS; CELL DIFFERENTIATION; ENZYME ACTIVATION; FASTING; HUMANS; I-KAPPA B KINASE; INTERLEUKIN-1BETA; LIPOLYSIS; MALE; MAP KINASE KINASE KINASES; MICE; MICE, INBRED C57BL; MICE, INBRED NOD; MICE, OBESE; MITOGEN-ACTIVATED PROTEIN KINASE 3; OBESITY, MORBID; PROTO-ONCOGENE PROTEINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; THINNESS; TUMOR NECROSIS FACTOR-ALPHA; UP-REGULATION;

EID: 77449103988     PISSN: 00121797     EISSN: 1939327X     Source Type: Journal    
DOI: 10.2337/db09-0470     Document Type: Article

References (46)

1. Hotamisligil GS. Inflammation and metabolic disorders. Nature 2006;444:860-867
2. Wellen KE, Hotamisligil GS. Inflammation, stress, and diabetes. J Clin Invest 2005;115:1111-1119
3. Suganami T, Nishida J, Ogawa Y. A paracrine loop between adipocytes and macrophages aggravates inflammatory changes: role of free fatty acids and tumor necrosis factor alpha. Arterioscler Thromb Vasc Biol 2005;25:2062-2068 (Pubitemid 41416301)
4. Shoelson SE, Herrero L, Naaz A. Obesity, inflammation, and insulin resistance. Gastroenterology 2007;132:2169-2180
5. 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, 2009 [Epub ahead of print]
6. Bouzakri K, Karlsson HK, Vestergaard H, Madsbad S, Christiansen E, Zierath JR. IRS-1 serine phosphorylation and insulin resistance in skeletal muscle from pancreas transplant recipients. Diabetes 2006;55:785-791 (Pubitemid 43343237)
7. Gual P, Le Marchand-Brustel Y, Tanti JF. Positive and negative regulation of insulin signaling through IRS-1 phosphorylation. Biochimie 2005;87:99-109 (Pubitemid 40298772)
8. Jager J, Gremeaux 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 2007;148:241-251 (Pubitemid 46021456)
9. Zick Y. Insulin resistance: a phosphorylation-based uncoupling of insulin signaling. Trends Cell Biol 2001;11:437-441 (Pubitemid 33001425)
10. Souza SC, Palmer HJ, Kang YH, Yamamoto MT, Muliro KV, Paulson KE, Greenberg AS. TNF-alpha induction of lipolysis is mediated through activation of the extracellular signal related kinase pathway in 3T3-L1 adipocytes. J Cell Biochem 2003;89:1077-1086
11. Zhang HH, Halbleib M, Ahmad F, Manganiello VC, Greenberg AS. Tumor necrosis factor-α stimulates lipolysis in differentiated human adipocytes through activation of extracellular signal-related kinase and elevation of intracellular cAMP. Diabetes 2002;51:2929-2935
12. Greenberg AS, Shen WJ, Muliro K, Patel S, Souza SC, Roth RA, Kraemer FB. Stimulation of lipolysis and hormone-sensitive lipase via the extracellular signal-regulated kinase pathway. J Biol Chem 2001;276:45456-45461 (Pubitemid 37391343)
13. Bost F, Aouadi M, Caron L, Even P, Belmonte N, Prot M, Dani C, Hofman P, Pages G, Pouyssegur J, Le Marchand-Brustel Y, Binetruy B. The extracellular signal-regulated kinase isoform ERK1 is specifically required for in vitro and in vivo adipogenesis. Diabetes 2005;54:402-411
14. Emanuelli B, Eberle D, Suzuki R, Kahn CR. Overexpression of the dual-specificity phosphatase MKP-4/DUSP-9 protects against stress-induced insulin resistance. Proc Natl Acad Sci U S A 2008;105:3545-3550 (Pubitemid 351723589)
15. Rodriguez A, Duran A, Selloum M, Champy M-F, Diez-Guerra FJ, Flores JM, Serrano M, Auwerx J, Diaz-Meco MT, Moscat J. Mature-onset obesity and insulin resistance in mice deficient in the signaling adapter p62. Cell Metab 2006;3:211-222 (Pubitemid 43316526)
16. Banerjee A, Gerondakis S. Coordinating TLR-activated signaling pathways in cells of the immune system. Immunol Cell Biol 2007;85:420-424 (Pubitemid 47367508)
17. Raman M, Chen W, Cobb MH. Differential regulation and properties of MAPKs. Oncogene 2007;26:3100-3112
18. Symons A, Beinke S, Ley SC. MAP kinase kinase kinases and innate immunity. Trends Immunol 2006;27:40-48 (Pubitemid 43083563)
19. Ceci JD, Patriotis CP, Tsatsanis C, Makris AM, Kovatch R, Swing DA, Jenkins NA, Tsichlis PN, Copeland NG. Tpl-2 is an oncogenic kinase that is activated by carboxy-terminal truncation. Genes Dev 1997;11:688-700 (Pubitemid 27157158)
20. Hatziapostolou M, Polytarchou C, Panutsopulos D, Covic L, Tsichlis PN. Proteinase-activated receptor-1-triggered activation of tumor progression locus-2 promotes actin cytoskeleton reorganization and cell migration. Cancer Res 2008;68:1851-1861 (Pubitemid 351416571)
21. Gavrin LK, Green N, Hu Y, Janz K, Kaila N, Li HQ, Tam SY, Thomason JR, Gopalsamy A, Ciszewski G, Cuozzo JW, Hall JP, Hsu S, Telliez JB, Lin LL. Inhibition of Tpl2 kinase and TNF-alpha production with 1,7-naphthyridine-3- carbonitriles: synthesis and structure-activity relationships. Bioorg Med Chem Lett 2005;15:5288-5292 (Pubitemid 41463666)
22. Podolin PL, Callahan JF, Bolognese BJ, Li YH, Carlson K, Davis TG, Mellor GW, Evans C, Roshak AK. Attenuation of murine collagen-induced arthritis by a novel, potent, selective small molecule inhibitor of IkappaB kinase 2, TPCA-1 (2-[(aminocarbonyl)amino]-5-(4-fluorophenyl)-3-thiophenecarboxamide), occurs via reduction of proinflammatory cytokines and antigen-induced T cell proliferation. J Pharmacol Exp Ther 2005;312:373-381 (Pubitemid 40096491)
23. Karin M, Yamamoto Y, Wang QM. The IKK NF-kappa B system: a treasure trove for drug development. Nat Rev Drug Discov 2004;3:17-26 (Pubitemid 38088695)
24. Kaddai V, Jager J, Gonzalez T, Najem-Lendom R, Bonnafous S, Tran A, Le Marchand-Brustel Y, Gual P, Tanti JF, Cormont M. Involvement of TNF-alpha in abnormal adipocyte and muscle sortilin expression in obese mice and humans. Diabetologia 2009;52:932-940
25. Kennedy A, Martinez K, Chuang CC, LaPoint K, McIntosh M. Saturated fatty acid-mediated inflammation and insulin resistance in adipose tissue: mechanisms of action and implications. J Nutr 2009;139:1-4
26. Cohen P. Targeting protein kinases for the development of anti-inflammatory drugs. Curr Opin Cell Biol 2009;21:317-324
27. Waterfield M, Jin W, Reiley W, Zhang M, Sun SC. IkappaB kinase is an essential component of the Tpl2 signaling pathway. Mol Cell Biol 2004;24:6040-6048 (Pubitemid 38787986)
28. Aoki M, Hamada F, Sugimoto T, Sumida S, Akiyama T, Toyoshima K. The human cot proto-oncogene encodes two protein serine/threonine kinases with different transforming activities by alternative initiation of translation. J Biol Chem 1993;268:22723-22732 (Pubitemid 23318331)
29. Waterfield MR, Zhang M, Norman LP, Sun SC. NF-kappaB1/p105 regulates lipopolysaccharide-stimulated MAP kinase signaling by governing the stability and function of the Tpl2 kinase. Mol Cell 2003;11:685-694 (Pubitemid 36385122)
30. Beinke S, Robinson MJ, Hugunin M, Ley SC. Lipopolysaccharide activation of the TPL-2/MEK/extracellular signal-regulated kinase mitogen-activated protein kinase cascade is regulated by IkappaB kinase-induced proteolysis of NF-kappaB1 p105. Mol Cell Biol 2004;24:9658-9667 (Pubitemid 39391700)
31. Gual P, Gremeaux T, Gonzalez T, Le Marchand-Brustel Y, Tanti JF. MAP kinases and mTOR mediate insulin-induced phosphorylation of insulin receptor substrate-1 on serine residues 307, 612 and 632. Diabetologia 2003;46:1532-1542 (Pubitemid 37518574)
32. Salmeron A, Ahmad TB, Carlile GW, Pappin D, Narsimhan RP, Ley SC. Activation of MEK-1 and SEK-1 by Tpl-2 proto-oncoprotein, a novel MAP kinase kinase kinase. EMBO J 1996;15:817-826 (Pubitemid 26064288)
33. Ohara R, Miyoshi J, Aoki M, Toyoshima K. The murine cot proto-oncogene: genome structure and tissue-specific expression. Jpn J Cancer Res 1993;84:518-525 (Pubitemid 23193810)
34. Dumitru CD, Ceci JD, Tsatsanis C, Kontoyiannis D, Stamatakis K, Lin JH, Patriotis C, Jenkins NA, Copeland NG, Kollias G, Tsichlis PN. TNF-alpha induction by LPS is regulated posttranscriptionally via a Tpl2/ERK-dependent pathway. Cell 2000;103:1071-1083 (Pubitemid 32040907)
35. Eliopoulos AG, Wang CC, Dumitru CD, Tsichlis PN. Tpl2 transduces CD40 and TNF signals that activate ERK and regulates IgE induction by CD40. EMBO J 2003;22:3855-3864
36. Chan H, Reed JC. TRAF-dependent association of protein kinase Tpl2/COT1 (MAP3K8) with CD40. Biochem Biophys Res Commun 2005;328:198-205 (Pubitemid 40164655)
37. Stafford MJ, Morrice NA, Peggie MW, Cohen P. Interleukin-1 stimulated activation of the COT catalytic subunit through the phosphorylation of Thr290 and Ser62. FEBS Lett 2006;580:4010-4014 (Pubitemid 43946869)
38. Tilg H, Moschen AR. Adipocytokines: mediators linking adipose tissue, inflammation and immunity. Nat Rev Immunol 2006;6:772-783 (Pubitemid 44453463)
39. Das S, Cho J, Lambertz I, Kelliher MA, Eliopoulos AG, Du K, Tsichlis PN. Tpl2/cot signals activate ERK, JNK, and NF-kappaB in a cell-type and stimulus-specific manner. J Biol Chem 2005;280:23748-23757 (Pubitemid 40884858)
40. Laurencikiene J, van Harmelen V, Arvidsson Nordstrom E, Dicker A, Blomqvist L, Naslund E, Langin D, Arner P, Ryden M. NF-kappaB is important for TNF-alpha-induced lipolysis in human adipocytes. J Lipid Res 2007;48:1069-1077 (Pubitemid 46708674)
41. Ryden M, Arvidsson E, Blomqvist L, Perbeck L, Dicker A, Arner P. Targets for TNF-alpha-induced lipolysis in human adipocytes. Biochem Biophys Res Commun 2004;318:168-175
42. Ruan H, Hacohen N, Golub TR, Van Parijs L, Lodish HF. Tumor necrosis factor-α suppresses adipocyte-specific genes and activates expression of preadipocyte genes in 3T3-L1 adipocytes: nuclear factor-κB activation by TNF-α is obligatory. Diabetes 2002;51:1319-1336
43. Nordstrom EA, Ryden M, Backlund EC, Dahlman I, Kaaman M, Blomqvist L, Cannon B, Nedergaard J, Arner P. A human-specific role of cell death-inducing DFFA (DNA fragmentation factor-α)-like effector A (CIDEA) in adipocyte lipolysis and obesity. Diabetes 2005;54:1726-1734
44. Guilherme A, Virbasius JV, Puri V, Czech MP. Adipocyte dysfunctions linking obesity to insulin resistance and type 2 diabetes. Nat Rev Mol Cell Biol 2008;9:367-377
45. Bouzakri K, Roques M, Gual P, Espinosa S, Guebre-Egziabher F, Riou JP, Laville M, Le Marchand-Brustel Y, 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 2003;52:1319-1325
46. Mothe I, Van Obberghen E. Phosphorylation of the insulin receptor substrate-1 on multiple serine residues, 612, 632, 662 and 731, modulates insulin action. J Biol Chem 1996;271:11222-11227