TWEAK prevents TNF-α-induced insulin resistance through PP2A activation in human adipocytes

American Journal of Physiology - Endocrinology and Metabolism

Volumn 305, Issue 1, 2013, Pages

  Vázquez Carballo, Ana ^a   Ceperuelo Mallafré, Victòria ^b,c   Chacón, Matilde R ^d,e   Maymó Masip, Elsa ^d   Lorenzo, Margarita ^a   Porras, Almudena ^a   Vendrell, Joan ^d,e   Fernández Veledo, Sonia ^d,e  

^a UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

^b HOSPITAL UNIVERSITARIO VIRGEN DE LA VICTORIA   (Spain)

^c Instituto de Salud Carlos III   (Spain)

^d INSTITUTO DE SALUD CARLOS III   (Spain)

^e HOSPITAL UNIVERSITARI JOAN XXIII   (Spain)

Author keywords

Adipose tissue; Glucose uptake; Insulin signaling; Obesity; Phosphatases; TNF

Indexed keywords

GLUCOSE TRANSPORTER 4; JANUS KINASE 1; PROTEIN SERINE THREONINE KINASE; TUMOR NECROSIS FACTOR; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR LIKE WEAK INDUCER OF APOPTOSIS; UNCLASSIFIED DRUG;

ADIPOCYTE; APOPTOSIS; ARTICLE; CATALYSIS; CELL LINE; DEPHOSPHORYLATION; GLUCOSE HOMEOSTASIS; GLUCOSE TRANSPORT; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; INSULIN RESISTANCE; LIPOLYSIS; PRIORITY JOURNAL;

ADIPOSE TISSUE; GLUCOSE UPTAKE; INSULIN SIGNALING; OBESITY; PHOSPHATASES; TNF;

CELL LINE; GLUCOSE; GLUCOSE TRANSPORTER TYPE 4; HUMANS; INSULIN RESISTANCE; INTRA-ABDOMINAL FAT; MAP KINASE SIGNALING SYSTEM; OBESITY; PRIMARY CELL CULTURE; PROTEIN PHOSPHATASE 2; SOLUBILITY; TNF RECEPTOR-ASSOCIATED FACTOR 2; TUMOR NECROSIS FACTOR-ALPHA; TUMOR NECROSIS FACTORS;

EID: 84879569141     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.00589.2012     Document Type: Article

References (49)

1. Blouin CM, Prado C, Takane KK, Lasnier F, Garcia-Ocana A, Ferre P, Dugail I, Hajduch E. Plasma membrane subdomain compartmentalization contributes to distinct mechanisms of ceramide action on insulin signaling. Diabetes 59: 600-610, 2010.
2. Brown SA, Ghosh A, Winkles JA. Full-length, membrane-anchored TWEAK can function as a juxtacrine signaling molecule and activate the NF-kappaB pathway. J Biol Chem 285: 17432-17441, 2010.
3. Brown SA, Richards CM, Hanscom HN, Feng SL, Winkles JA. The Fn14 cytoplasmic tail binds tumour-necrosis-factor-receptor-associated factors 1, 2, 3 and 5 and mediates nuclear factor-kappaB activation. Biochem J 371: 395-403, 2003.
4. Cabal-Hierro L, Lazo PS. Signal transduction by tumor necrosis factor receptors. Cell Signal 24: 1297-1305, 2012.
5. Carlson CJ, White MF, Rondinone CM. Mammalian target of rapamycin regulates IRS-1 serine 307 phosphorylation. Biochem Biophys Res Commun 316: 533-539, 2004.
6. Cawthorn WP, Sethi JK. TNF-alpha and adipocyte biology. FEBS Lett 582: 117-131, 2008.
7. Chacon MR, Richart C, Gomez JM, Megia A, Vilarrasa N, Fernandez-Real JM, Garcia-Espana A, Miranda M, Masdevall C, Ricard W, Caubet E, Soler J, Vendrell J. Expression of TWEAK and its receptor Fn14 in human subcutaneous adipose tissue. Relationship with other inflammatory cytokines in obesity. Cytokine 33: 129-137, 2006.
8. Deepa SS, Zhou L, Ryu J, Wang C, Mao X, Li C, Zhang N, Musi N, DeFronzo RA, Liu F, Dong LQ. APPL1 mediates adiponectin-induced LKB1 cytosolic localization through the PP2A-PKCzeta signaling pathway. Mol Endocrinol 25: 1773-1785, 2011.
9. Dogra C, Changotra H, Wedhas N, Qin X, Wergedal JE, Kumar A. TNF-related weak inducer of apoptosis (TWEAK) is a potent skeletal muscle-wasting cytokine. FASEB J 21: 1857-1869, 2007.
10. Feng F, Wang L, Albanese N, Holmes A, Xia P. Tumor necrosis factor-like weak inducer of apoptosis attenuates the action of insulin in hepatocytes. Endocrinology 149: 1505-1513, 2008.
11. Fernandez-Veledo S, Nieto-Vazquez I, de CJ, Ramos MP, Bruderlein S, Moller P, Lorenzo M. Hyperinsulinemia induces insulin resistance on glucose and lipid metabolism in a human adipocytic cell line: paracrine interaction with myocytes. J Clin Endocrinol Metab 93: 2866-2876, 2008.
12. Fernandez-Veledo S, Nieto-Vazquez I, Vila-Bedmar R, Garcia-Guerra L, onso-Chamorro M, Lorenzo M. Molecular mechanisms involved in obesity-associated insulin resistance: therapeutical approach. Arch Physiol Biochem 115: 227-239, 2009.
13. Fernandez-Veledo S, Vila-Bedmar R, Nieto-Vazquez I, Lorenzo M. c-Jun N-terminal kinase 1/2 activation by tumor necrosis factor-alpha induces insulin resistance in human visceral but not subcutaneous adipocytes: reversal by liver X receptor agonists. J Clin Endocrinol Metab 94: 3583-3593, 2009.
14. Gregor MF, Hotamisligil GS. Inflammatory mechanisms in obesity. Annu Rev Immunol 29: 415-445, 2011.
15. Gutierrez-Uzquiza A, Arechederra M, Bragado P, Aguirre-Ghiso JA, Porras A. p38Alpha mediates cell survival in response to oxidative stress via induction of antioxidant genes: effect on the p70S6K pathway. J Biol Chem 287: 2632-2642, 2012.
16. Hahn K, Miranda M, Francis VA, Vendrell J, Zorzano A, Teleman AA. PP2A regulatory subunit PP2A-B= counteracts S6K phosphorylation. Cell Metab 11: 438-444, 2010.
17. Han S, Yoon K, Lee K, Kim K, Jang H, Lee NK, Hwang K, Young Lee S. TNF-related weak inducer of apoptosis receptor, a TNF receptor superfamily member, activates NF-kappa B through TNF receptor-associated factors. Biochem Biophys Res Commun 305: 789-796, 2003.
18. Houdali B, Nguyen V, Ammon HP, Haap M, Schechinger W, Machicao F, Rett K, Haring HU, Schleicher ED. Prolonged glucose infusion into conscious rats inhibits early steps in insulin signalling and induces translocation of GLUT4 and protein kinase C in skeletal muscle. Diabetologia 45: 356-368, 2002.
19. Hu P, Han Z, Couvillon AD, Kaufman RJ, Exton JH. Autocrine tumor necrosis factor alpha links endoplasmic reticulum stress to the membrane death receptor pathway through IRE1alpha-mediated NF-kappaB activation and down-regulation of TRAF2 expression. Mol Cell Biol 26: 3071-3084, 2006.
20. Hube F, Hauner H. The role of TNF-alpha in human adipose tissue: prevention of weight gain at the expense of insulin resistance? Horm Metab Res 31: 626-631, 1999.
21. Hube F, Hauner H. The two tumor necrosis factor receptors mediate opposite effects on differentiation and glucose metabolism in human adipocytes in primary culture. Endocrinology 141: 2582-2588, 2000.
22. Janssens V, Goris J. Protein phosphatase 2A: a highly regulated family of serine/threonine phosphatases implicated in cell growth and signalling. Biochem J 353: 417-439, 2001.
23. Jupp OJ, McFarlane SM, Anderson HM, Littlejohn AF, Mohamed AA, MacKay RH, Vandenabeele P, MacEwan DJ. Type II tumour necrosis factor-alpha receptor (TNFR2) activates c-Jun N-terminal kinase (JNK) but not mitogen-activated protein kinase (MAPK) or p38 MAPK pathways. Biochem J 359: 525-535, 2001.
24. Kralisch S, Ziegelmeier M, Bachmann A, Seeger J, Lossner U, Bluher M, Stumvoll M, Fasshauer M. Serum levels of the atherosclerosis biomarker sTWEAK are decreased in type 2 diabetes and end-stage renal disease. Atherosclerosis 199: 440-444, 2008.
25. Kumar M, Makonchuk DY, Li H, Mittal A, Kumar A. TNF-like weak inducer of apoptosis (TWEAK) activates proinflammatory signaling pathways and gene expression through the activation of TGF-beta-activated kinase 1. J Immunol 182: 2439-2448, 2009.
26. Lansey MN, Walker NN, Hargett SR, Stevens JR, Keller SR. Deletion of Rab GAP AS160 modifies glucose uptake and GLUT4 translocation in primary skeletal muscles and adipocytes and impairs glucose homeostasis. Am J Physiol Endocrinol Metab 303: E1273-E1286, 2012.
27. Li W, Chen Z, Gong FR, Zong Y, Chen K, Li DM, Yin H, Duan WM, Miao Y, Tao M, Han X, Xu ZK. Growth of the pancreatic cancer cell line PANC-1 is inhibited by protein phosphatase 2A inhibitors through overactivation of the c-Jun N-terminal kinase pathway. Eur J Cancer 47: 2654-2664, 2011.
28. Llaurado G, Gonzalez-Clemente JM, Maymo-Masip E, Subias D, Vendrell J, Chacon MR. Serum levels of TWEAK and scavenger receptor CD163 in type 1 diabetes mellitus: relationship with cardiovascular risk factors. A case-control study. PLoS One 7: e43919, 2012.
29. Maecker H, Varfolomeev E, Kischkel F, Lawrence D, LeBlanc H, Lee W, Hurst S, Danilenko D, Li J, Filvaroff E, Yang B, Daniel D, Ashkenazi A. TWEAK attenuates the transition from innate to adaptive immunity. Cell 123: 931-944, 2005.
30. Nieto-Vazquez I, Fernandez-Veledo S, Kramer DK, Vila-Bedmar R, Garcia-Guerra L, Lorenzo M. Insulin resistance associated to obesity: the link TNF-alpha. Arch Physiol Biochem 114: 183-194, 2008.
31. Nishimura M, Shin MS, Singhirunnusorn P, Suzuki S, Kawanishi M, Koizumi K, Saiki I, Sakurai H. TAK1-mediated serine/threonine phosphorylation of epidermal growth factor receptor via p38/extracellular signal-regulated kinase: NF-(kappa)B-independent survival pathways in tumor necrosis factor alpha signaling. Mol Cell Biol 29: 5529-5539, 2009.
32. Peraldi P, Hotamisligil GS, Buurman WA, White MF, Spiegelman BM. Tumor necrosis factor (TNF)-alpha inhibits insulin signaling through stimulation of the p55 TNF receptor and activation of sphingomyelinase. J Biol Chem 271: 13018-13022, 1996.
33. Roos C, Wicovsky A, Muller N, Salzmann S, Rosenthal T, Kalthoff H, Trauzold A, Seher A, Henkler F, Kneitz C, Wajant H. Soluble and transmembrane TNF-like weak inducer of apoptosis differentially activate the classical and noncanonical NF-kappa B pathway. J Immunol 185: 1593-1605, 2010.
34. Ryden M, Dicker A, van Harmelen V, Hauner H, Brunnberg M, Perbeck L, Lonnqvist F, Arner P. Mapping of early signaling events in tumor necrosis factor-alpha-mediated lipolysis in human fat cells. J Biol Chem 277: 1085-1091, 2002.
35. Saitoh T, Nakayama M, Nakano H, Yagita H, Yamamoto N, Yamaoka S. TWEAK induces NF-kappaB2 p100 processing and long lasting NFkappaB activation. J Biol Chem 278: 36005-36012, 2003.
36. Steinberg GR, Michell BJ, van Denderen BJ, Watt MJ, Carey AL, Fam BC, Andrikopoulos S, Proietto J, Gorgun CZ, Carling D, Hotamisligil GS, Febbraio MA, Kay TW, Kemp BE. Tumor necrosis factor alpha-induced skeletal muscle insulin resistance involves suppression of AMP-kinase signaling. Cell Metab 4: 465-474, 2006.
37. Sun SC. Non-canonical NF-kappaB signaling pathway. Cell Res 21: 71-85, 2011.
38. Talior I, Yarkoni M, Bashan N, Eldar-Finkelman H. Increased glucose uptake promotes oxidative stress and PKC activation in adipocytes of obese, insulin-resistant mice. Am J Physiol Endocrinol Metab 285: E295-E302, 2003.
39. Teruel T, Hernandez R, Lorenzo M. Ceramide mediates insulin resistance by tumor necrosis factor-alpha in brown adipocytes by maintaining Akt in an inactive dephosphorylated state. Diabetes 50: 2563-2571, 2001.
40. Tiller G, Fischer-Posovszky P, Laumen H, Finck A, Skurk T, Keuper M, Brinkmann U, Wabitsch M, Link D, Hauner H. Effects of TWEAK (TNF superfamily member 12) on differentiation, metabolism, and secretory function of human primary preadipocytes and adipocytes. Endocrinology 150: 5373-5383, 2009.
41. van Beek EA, Bakker AH, Kruyt PM, Vink C, Saris WH, Franssenvan Hal NL, Keijer J. Comparative expression analysis of isolated human adipocytes and the human adipose cell lines LiSa-2 and PAZ6. Int J Obes (Lond) 32: 912-921, 2008.
42. Vendrell J, Maymo-Masip E, Tinahones F, Garcia-Espana A, Megia A, Caubet E, Garcia-Fuentes E, Chacon MR. Tumor necrosis-like weak inducer of apoptosis as a proinflammatory cytokine in human adipocyte cells: up-regulation in severe obesity is mediated by inflammation but not hypoxia. J Clin Endocrinol Metab 95: 2983-2992, 2010.
43. Vince JE, Chau D, Callus B, Wong WW, Hawkins CJ, Schneider P, McKinlay M, Benetatos CA, Condon SM, Chunduru SK, Yeoh G, Brink R, Vaux DL, Silke J. TWEAK-FN14 signaling induces lysosomal degradation of a cIAP1-TRAF2 complex to sensitize tumor cells to TNFalpha. J Cell Biol 182: 171-184, 2008.
44. Wabitsch M, Bruderlein S, Melzner I, Braun M, Mechtersheimer G, Moller P. LiSa-2, a novel human liposarcoma cell line with a high capacity for terminal adipose differentiation. Int J Cancer 88: 889-894, 2000.
45. Wadgaonkar R, Pierce JW, Somnay K, Damico RL, Crow MT, Collins T, Garcia JG. Regulation of c-Jun N-terminal kinase and p38 kinase pathways in endothelial cells. Am J Respir Cell Mol Biol 31: 423-431, 2004.
46. Wicovsky A, Salzmann S, Roos C, Ehrenschwender M, Rosenthal T, Siegmund D, Henkler F, Gohlke F, Kneitz C, Wajant H. TNF-like weak inducer of apoptosis inhibits proinflammatory TNF receptor-1 signaling. Cell Death Differ 16: 1445-1459, 2009.
47. Wiley SR, Winkles JA. TWEAK, a member of the TNF superfamily, is a multifunctional cytokine that binds the TweakR/Fn14 receptor. Cytokine Growth Factor Rev 14: 241-249, 2003.
48. Williams LM, Lali F, Willetts K, Balague C, Godessart N, Brennan F, Feldmann M, Foxwell BM. Rac mediates TNF-induced cytokine production via modulation of NF-kappaB. Mol Immunol 45: 2446-2454, 2008.
49. Zhou G, Mihindukulasuriya KA, Corkle-Chosnek RA, Van HA, Hu MC, Brinkley BR, Tan TH. Protein phosphatase 4 is involved in tumor necrosis factor-alpha-induced activation of c-Jun N-terminal kinase. J Biol Chem 277: 6391-6398, 2002.