PPARγ inhibits NF-κB-dependent transcriptional activation in skeletal muscle

American Journal of Physiology - Endocrinology and Metabolism

Volumn 297, Issue 1, 2009, Pages

  Remels, A H V ^a   Langen, R C J ^a   Gosker, H R ^a   Russell, A P ^b   Spaapen, F ^a   Voncken, J W ^a   Schrauwen, P ^a   Schols, A M W J ^a  

^a MAASTRICHT UNIVERSITY   (Netherlands)

^b DEAKIN UNIVERSITY   (Australia)

Author keywords

Inflammation; Nuclear factor B; Peroxisome proliferator activated receptor ; Rosiglitazone; Skeletal muscle atrophy; Type 2 diabetes mellitus

Indexed keywords

[2 METHYL 4 [4 METHYL 2 (4 TRIFLUOROMETHYLPHENYL) 5 THIAZOLYLMETHYLTHIO]PHENOXY]ACETIC ACID; CXCL1 CHEMOKINE; DNA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERCELLULAR ADHESION MOLECULE 1; MESSENGER RNA; N (2 BENZOYLPHENYL) O [2 (METHYL 2 PYRIDINYLAMINO)ETHYL]TYROSINE; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA ANTAGONIST; PIRINIXIC ACID; ROSIGLITAZONE; TRANSCRIPTION FACTOR RELA; TUMOR NECROSIS FACTOR ALPHA; 2,4 THIAZOLIDINEDIONE DERIVATIVE; ANTIDIABETIC AGENT; AUTACOID; CYTOKINE; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PYRIMIDINE DERIVATIVE; THIAZOLE DERIVATIVE;

ADULT; ANIMAL CELL; ANTIINFLAMMATORY ACTIVITY; ARTICLE; CHRONIC INFLAMMATION; CLINICAL ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DOSE TIME EFFECT RELATION; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; INSULIN RESISTANCE; MALE; MOUSE; MUSCLE ATROPHY; MUSCLE BIOPSY; MYOTUBE; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PRIORITY JOURNAL; SKELETAL MUSCLE; TRANSCRIPTION REGULATION; ANIMAL; CELL CULTURE; DOWN REGULATION; DRUG ANTAGONISM; DRUG EFFECT; DRUG POTENTIATION; GENETICS; METABOLISM; MIDDLE AGED; PHYSIOLOGY; TRANSCRIPTION INITIATION;

ANIMALS; CELLS, CULTURED; CYTOKINES; DOWN-REGULATION; HUMANS; HYPOGLYCEMIC AGENTS; INFLAMMATION MEDIATORS; MALE; MICE; MIDDLE AGED; MUSCLE, SKELETAL; NF-KAPPA B; PPAR GAMMA; PYRIMIDINES; THIAZOLES; THIAZOLIDINEDIONES; TRANSCRIPTIONAL ACTIVATION;

EID: 67650034885     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.90632.2008     Document Type: Article

References (48)

1. Adams V, Spate U, Krankel N, Schulze PC, Linke A, Schuler G, Hambrecht R. Nuclear factor-kappa B activation in skeletal muscle of patients with chronic heart failure: correlation with the expression of inducible nitric oxide synthase. Eur J Cardiovasc Prev Rehabil 10: 273-277, 2003.
2. Agusti A, Morla M, Sauleda J, Saus C, Busquets X. NF-kappaB activation and iNOS upregulation in skeletal muscle of patients with COPD and low body weight. Thorax 59: 483-487, 2004.
3. Altman DG, Gore SM, Gardner MJ, Pocock SJ. Statistical guidelines for contributors to medical journals. Br Med J (Clin Res Ed) 286: 1489-1493, 1983.
4. Anandharajan R, Jaiganesh S, Shankernarayanan NP, Viswakarma RA, Balakrishnan A. In vitro glucose uptake activity of Aegles marmelos and Syzygium cumini by activation of Glut-4, PI3 kinase and PPAR-gamma in L6 myotubes. Phytomedicine 13: 434-441, 2006.
5. Arnold R, Neumann M, Konig W. Peroxisome proliferator-activated receptor-gamma agonists inhibit respiratory syncytial virus-induced expression of intercellular adhesion molecule-1 in human lung epithelial cells. Immunology 121: 71-81, 2007.
6. Bai YP, Liu YH, Chen J, Song T, You Y, Tang ZY, Li YJ, Zhang GG. Rosiglitazone attenuates NF-kappaB-dependent ICAM-1 and TNF-alpha production caused by homocysteine via inhibiting ERK1/2/p38MAPK activation. Biochem Biophys Res Commun 360: 20-26, 2007.
7. Bendinelli P, Piccoletti R, Maroni P. Leptin rapidly activates PPARs in C2C12 muscle cells. Biochem Biophys Res Commun 332: 719-725, 2005.
8. Bjorndal B, Helleland C, Boe SO, Gudbrandsen OA, Kalland KH, Bohov P, Berge RK, Lillehaug JR. Nuclear import of factors involved in signaling is inhibited in C3H/10T1/2 cells treated with tetradecylthioacetic acid. J Lipid Res 43: 1630-1640, 2002.
9. Bragt MC, Popeijus HE. Peroxisome proliferator-activated receptors and the metabolic syndrome. Physiol Behav 94: 187-197, 2007.
10. Cai D, Frantz JD, Tawa NE Jr, Melendez PA, Oh BC, Lidov HG, Hasselgren PO, Frontera WR, Lee J, Glass DJ, Shoelson SE. IKKbeta/NF-kappaB activation causes severe muscle wasting in mice. Cell 119: 285-298, 2004.
11. Castrillo A, Diaz-Guerra MJ, Hortelano S, Martin-Sanz P, Bosca L. Inhibition of IkappaB kinase and IkappaB phosphorylation by 15-deoxy-Delta(12, 14)-prostaglandin J(2) in activated murine macrophages. Mol Cell Biol 20: 1692-1698, 2000.
12. Chawla A, Barak Y, Nagy L, Liao D, Tontonoz P, Evans RM. PPARgamma dependent and independent effects on macrophage-gene expression in lipid metabolism and inflammation. Nat Med 7: 48-52, 2001.
13. Daynes RA, Jones DC. Emerging roles of PPARs in inflammation and immunity. Nat Rev Immunol 2: 748-759, 2002.
14. Delerive P, De Bosscher K, Besnard S, Vanden Berghe W, Peters JM, Gonzalez FJ, Fruchart JC, Tedgui A, Haegeman G, Staels B. Peroxisome proliferator-activated receptor alpha negatively regulates the vascular inflammatory gene response by negative cross-talk with transcription factors NF-kappaB and AP-1. J Biol Chem 274: 32048-32054, 1999.
15. Dyroy E, Yndestad A, Ueland T, Halvorsen B, Damas JK, Aukrust P, Berge RK. Antiinflammatory effects of tetradecylthioacetic acid involve both peroxisome proliferator-activated receptor alpha-dependent and -independent pathways. Arterioscler Thromb Vasc Biol 25: 1364-1369, 2005.
16. Francis GA, Fayard E, Picard F, Auwerx J. Nuclear receptors and the control of metabolism. Annu Rev Physiol 65: 261-311, 2003.
17. Friedman JE, Kirwan JP, Jing M, Presley L, Catalano PM. Increased skeletal muscle tumor necrosis factor-alpha and impaired insulin signaling persist in obese women with gestational diabetes mellitus 1 year postpartum. Diabetes 57: 606-613, 2008.
18. Guttridge DC, Mayo MW, Madrid LV, Wang CY, Baldwin AS Jr. NF-kappaB-induced loss of MyoD messenger RNA: possible role in muscle decay and cachexia. Science 289: 2363-2366, 2000.
19. Haffner SM, Greenberg AS, Weston WM, Chen H, Williams K, Freed MI. Effect of rosiglitazone treatment on nontraditional markers of cardiovascular disease in patients with type 2 diabetes mellitus. Circulation 106: 679-684, 2002.
20. Jagoe RT, Engelen MP. Muscle wasting and changes in muscle protein metabolism in chronic obstructive pulmonary disease. Eur Respir J Suppl 46: 52s- 63s, 2003.
21. Kersten S, Desvergne B, Wahli W. Roles of PPARs in health and disease. Nature 405: 421-424, 2000.
22. Kim EK, Kwon KB, Koo BS, Han MJ, Song MY, Song EK, Han MK, Park JW, Ryu DG, Park BH. Activation of peroxisome proliferator-activated receptor-gamma protects pancreatic beta-cells from cytokine-induced cytotoxicity via NF kappaB pathway. Int J Biochem Cell Biol 39: 1260-1275, 2007.
23. Kumar N, Dey CS. Development of insulin resistance and reversal by thiazolidinediones in C2C12 skeletal muscle cells. Biochem Pharmacol 65: 249-257, 2003.
24. Ladner KJ, Caligiuri MA, Guttridge DC. Tumor necrosis factor-regulated biphasic activation of NF-kappa B is required for cytokine-induced loss of skeletal muscle gene products. J Biol Chem 278: 2294-2303, 2003.
25. Langen RC, Schols AM, Kelders MC, Wouters EF, Janssen-Heininger YM. Enhanced myogenic differentiation by extracellular matrix is regulated at the early stages of myogenesis. In Vitro Cell Dev Biol Anim 39: 163-169, 2003.
26. Langen RC, Schols AM, Kelders MC, Wouters EF, Janssen-Heininger YM. Inflammatory cytokines inhibit myogenic differentiation through activation of nuclear factor-kappaB. FASEB J 15: 1169-1180, 2001.
27. Lappas M, Permezel M, Rice GE. Release of proinflammatory cytokines and 8-isoprostane from placenta, adipose tissue, and skeletal muscle from normal pregnant women and women with gestational diabetes mellitus. J Clin Endocrinol Metab 89: 5627-5633, 2004.
28. Li M, Pascual G, Glass CK. Peroxisome proliferator-activated receptor gamma-dependent repression of the inducible nitric oxide synthase gene. Mol Cell Biol 20: 4699-4707, 2000.
29. Lo YT, Tzeng TF, Liu IM. Role of tumor suppressor PTEN in tumor necrosis factor alpha-induced inhibition of insulin signaling in murine skeletal muscle C2C12 cells. Horm Metab Res 39: 173-178, 2007.
30. McNamara MJ, Alexander HR, Norton JA. Cytokines and their role in the pathophysiology of cancer cachexia. J Parenter Enteral Nutr 16: 50S-55S, 1992.
31. Mensink M, Hesselink MK, Russell AP, Schaart G, Sels JP, Schrauwen P. Improved skeletal muscle oxidative enzyme activity and restoration of PGC-1 alpha and PPAR beta/delta gene expression upon rosiglitazone treatment in obese patients with type 2 diabetes mellitus. Int J Obes (Lond) 31: 1302-1310, 2007.
32. Pahl HL. Activators and target genes of Rel/NF-kappaB transcription factors. Oncogene 18: 6853-6866, 1999.
33. Pascual G, Fong AL, Ogawa S, Gamliel A, Li AC, Perissi V, Rose DW, Willson TM, Rosenfeld MG, Glass CK. A SUMOylation-dependent pathway mediates transrepression of inflammatory response genes by PPARgamma. Nature 437: 759-763, 2005.
34. Poynter ME, Daynes RA. Peroxisome proliferator-activated receptor alpha activation modulates cellular redox status, represses nuclear factor-kappaB signaling, and reduces inflammatory cytokine production in aging. J Biol Chem 273: 32833-32841, 1998.
35. Reid MB, Li YP. Tumor necrosis factor-alpha and muscle wasting: a cellular perspective. Respir Res 2: 269-272, 2001.
36. Rossi A, Kapahi P, Natoli G, Takahashi T, Chen Y, Karin M, Santoro MG. Anti-inflammatory cyclopentenone prostaglandins are direct inhibitors of IkappaB kinase. Nature 403: 103-108, 2000.
37. Schrauwen P, Mensink M, Schaart G, Moonen-Kornips E, Sels JP, Blaak EE, Russell AP, Hesselink MK. Reduced skeletal muscle uncoupling protein-3 content in prediabetic subjects and type 2 diabetic patients: restoration by rosiglitazone treatment. J Clin Endocrinol Metab 91: 1520-1525, 2006.
38. Sparatore A, Godio C, Perrino E, Romeo S, Staels B, Fruchart JC, Crestani M. [4-(2H-1,2,3-benzotriazol-2-yl)phenoxy]alkanoic acids as agonists of peroxisome proliferator-activated receptors (PPARs). Chem Biodivers 3: 385-395, 2006.
39. Sriwijitkamol A, Christ-Roberts C, Berria R, Eagan P, Pratipanawatr T, DeFronzo RA, Mandarino LJ, Musi N. Reduced skeletal muscle inhibitor of kappaB beta content is associated with insulin resistance in subjects with type 2 diabetes: reversal by exercise training. Diabetes 55: 760-767, 2006.
40. Staels B, Koenig W, Habib A, Merval R, Lebret M, Torra IP, Delerive P, Fadel A, Chinetti G, Fruchart JC, Najib J, Maclouf J, Tedgui A. Activation of human aortic smooth-muscle cells is inhibited by PPARalpha but not by PPARgamma activators. Nature 393: 790-793, 1998.
41. Stienstra R, Duval C, M ML, Kersten S. PPARs, obesity, and inflammation. PPAR Res 2007: 95974, 2006.
42. Straus DS, Glass CK. Anti-inflammatory actions of PPAR ligands: new insights on cellular and molecular mechanisms. Trends Immunol 28: 551-558, 2007.
43. Sznaidman ML, Haffner CD, Maloney PR, Fivush A, Chao E, Goreham D, Sierra ML, LeGrumelec C, Xu HE, Montana VG, Lambert MH, Willson TM, Oliver WR Jr, Sternbach DD. Novel selective small molecule agonists for peroxisome proliferator-activated receptor delta (PPARdelta) - synthesis and biological activity. Bioorg Med Chem Lett 13: 1517-1521, 2003.
44. Tisdale MJ. Biomedicine. Protein loss in cancer cachexia. Science 289: 2293-2294, 2000.
45. van der Velden JL, Schols AM, Willems J, Kelders MC, Langen RC. Glycogen synthase kinase 3 suppresses myogenic differentiation through negative regulation of NFATc3. J Biol Chem 283: 358-366, 2008.
46. Verges B. Clinical interest of PPARs ligands. Diabetes Metab 30: 7-12, 2004.
47. Woo CH, Massett MP, Shishido T, Itoh S, Ding B, McClain C, Che W, Vulapalli SR, Yan C, Abe J. ERK5 activation inhibits inflammatory responses via peroxisome proliferator-activated receptor delta (PPARdelta) stimulation. J Biol Chem 281: 32164-32174, 2006.
48. Yoon MJ, Lee GY, Chung JJ, Ahn YH, Hong SH, Kim JB. Adiponectin increases fatty acid oxidation in skeletal muscle cells by sequential activation of AMP-activated protein kinase, p38 mitogen-activated protein kinase, and peroxisome proliferator-activated receptor alpha. Diabetes 55: 2562-2570, 2006.