TNF-α downregulates eNOS expression and mitochondrial biogenesis in fat and muscle of obese rodents

Journal of Clinical Investigation

Volumn 116, Issue 10, 2006, Pages 2791-2798

  Valerio, Alessandra ^a   Cardile, Annalisa ^a,b   Cozzi, Valeria ^a,b   Bracale, Renata ^a,b,c   Tedesco, Laura ^a,b,d   Pisconti, Addolorata ^b,e   Palomba, Letizia ^f   Cantoni, Orazio ^f   Clementi, Emilio ^b,e,g   Moncada, Salvador ^h   Carruba, Michele O ^a,d   Nisoli, Enzo ^a,b,d  

^a UNIVERSITY OF MILAN   (Italy)

^b UNIVERSITY OF MILAN   (Italy)

^c CEINGE BIOTECNOLOGIE AVANZATE   (Italy)

^d ISTITUTO AUXOLOGICO ITALIANO   (Italy)

^e SAN RAFFAELE HOSPITAL   (Italy)

^f UNIVERSITY OF URBINO   (Italy)

^g SCIENTIFIC INSTITUTE   (Italy)

^h UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR RECEPTOR 1;

ADIPOCYTE; ARTICLE; BIOGENESIS; BROWN ADIPOSE TISSUE; DOWN REGULATION; GENE DELETION; OBESITY; PRIORITY JOURNAL; SATELLITE CELL; SOLEUS MUSCLE; WEIGHT GAIN;

ADENOSINE TRIPHOSPHATE; ADIPOSE TISSUE; ANIMALS; CELLS, CULTURED; CYTOCHROMES C; DNA-BINDING PROTEINS; DOWN-REGULATION; ELECTRON TRANSPORT COMPLEX IV; FEMALE; HIGH MOBILITY GROUP PROTEINS; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, OBESE; MITOCHONDRIA; MUSCLE, SKELETAL; NITRIC OXIDE DONORS; NITRIC OXIDE SYNTHASE TYPE III; NUCLEAR RESPIRATORY FACTOR 1; OBESITY; OXYGEN CONSUMPTION; RATS; RATS, ZUCKER; RECEPTORS, TUMOR NECROSIS FACTOR; TUMOR NECROSIS FACTOR-ALPHA;

EID: 33749442351     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI28570     Document Type: Article

References (51)

1. Haslam, D.W., and James, W.P. 2005. Obesity. Lancet. 366:1197-1209.
2. Wellen, K.E., and Hotamisligil, G.S. 2005. Inflammation, stress, and diabetes. J. Clin. Invest. 115:1111-1119. doi:10.1172/JCI200525102.
3. Hotamisligil, G.S., Shargill, N.S., and Spiegelman, B.M. 1993. Adipose expression of tumor necrosis factor-α: direct role in obesity-linked insulin resistance. Science. 259:87-91.
4. Hotamisligil, G.S., Arner, P., Caro, J.F., Atkinson, R.L., and Spiegelman, B.M. 1995. Increased adipose tissue expression of tumor necrosis factor-α in human obesity and insulin resistance. J. Clin. Invest. 95:2409-2415.
5. Perreault, M., and Marette, A. 2001. Targeted disruption of inducible nitric oxide synthase protects against obesity-linked insulin resistance in muscle. Nat. Med. 7:1138-1143.
6. Wlodek, D., and Gonzales, M. 2003. Decreased energy levels can cause and sustain obesity. J. Theor. Biol. 225:33-44.
7. Boudina, S., et al. 2005. Reduced mitochondrial oxidative capacity and increased mitochondrial uncoupling impair myocardial energetics in obesity. Circulation. 112:2686-2695.
8. Munzberg, H., and Myers, M.G., Jr. 2005. Molecular and anatomical determinants of central leptin resistance. Nat. Neurosci. 8:566-570.
9. Nisoli, E., et al. 2003. Mitochondrial biogenesis in mammals: the role of endogenous nitric oxide. Science. 299:896-899.
10. Nisoli, E., et al. 2004. Mitochondrial biogenesis by NO yields functionally active mitochondria in mammals. Proc. Natl. Acad. Sci. U. S. A. 101:16507-16512.
11. Kelly, D.P., and Scarpulla, R.C. 2004. Transcriptional regulatory circuits controlling mitochondrial biogenesis and function. Genes Dev. 18:357-368.
12. Larrouy, D., Vidal, H., Andreelli, F., Laville, M., and Langin, D. 1999. Cloning and mRNA tissue distribution of human PPARγ coactivator-1. Int. J. Obes. Relat. Metab. Disord. 23:1327-1332.
13. Higami, y., et al. 2004. Adipose tissue energy metabolism: altered gene expression profile of mice subjected to long-term caloric restriction. FASEB J. 18:415-417.
14. Levin, B.E., Finnegan, M., Triscari, J., and Sullivan, A.C. 1985. Brown adipose and metabolic features of chronic diet-induced obesity. Am. J. Physiol. 248:R717-R723.
15. Nicholls, D.G., Cunningham, S.A., and Rial, E. 1986. The bioenergetic mechanisms of brown adipose tissue thermogenesis. In Brown adipose tissue. P. Trayhurn and D.G. Nicholls, editors. Edward Arnold. London, United Kingdom. 52-85.
16. Uysal, K.T., Wiesbrock, S.M., Marino, M.W., and Hotamisligil, G.S. 1997. Protection from obesity-induced insulin resistance in mice lacking TNF-α function. Nature. 389:610-614.
17. Charge, S.B., and Rudnicki, M.A. 2004. Cellular and molecular regulation of muscle regeneration. Physiol. Rev. 84:209-238.
18. Jezek, P. 2002. Possible physiological roles of mitochondrial uncoupling proteins - UCPn. Int. J. Biochem. Cell Biol. 34:1190-1206.
19. Sparks, L.M., et al. 2005. A high-fat diet coordinately downregulates genes required for mitochondrial oxidative phosphorylation in skeletal muscle. Diabetes. 54:1926-1933.
20. Wisloff, U., et al. 2005. Cardiovascular risk factors emerge after artificial selection for low aerobic capacity. Science. 307:418-420.
21. Kim, J.y., Hickner, R.C., Cortright, R.L., Dohm, G.L., and Houmard, J.A. 2000. Lipid oxidation is reduced in obese human skeletal muscle. Am. J. Physiol. Endocrinol. Metab. 279:E1039-E1044.
22. Cook, S., et al. 2003. Clustering of cardiovascular risk factors mimicking the human metabolic syndrome X in eNOS null mice. Swiss Med. Wkly. 133:360-363.
23. Moraes, R.C., et al. 2003. Study of the alteration of gene expression in adipose tissue of diet-induced obese mice by microarray and reverse transcription-polymerase chain reaction analyses. Endocrinology. 144:4773-4782.
24. Hickner, R.C., Kemeny, G., Stallings, H.W., Manning, S.M., and McIver, K.L. 2006. Relationship between body composition and skeletal muscle eNOS. Int. J. Obes. (Lond). 30:308-312.
25. Fu, W.J., et al. 2005. Dietary l-arginine supplementation reduces fat mass in Zucker diabetic fatty rats. J. Nutr. 135:714-721.
26. Xu, H., et al. 2003. Chronic inflammation in fat plays a crucial role in the development of obesity-related insulin resistance. J. Clin. Invest. 112:1821-1830. doi:10.1172/JCI200319451.
27. Weisberg, S.P., et al. 2003. Obesity is associated with macrophage accumulation in adipose tissue. J. Clin. Invest. 112:1796-1808. doi:10.1172/JCI200319246.
28. Patti, M.E., et al. 2003. Coordinated reduction of genes of oxidative metabolism in humans with insulin resistance and diabetes: potential role of PGC1 and NRF1. Proc. Natl. Acad. Sci. U. S. A. 100:8466-8471.
29. Mootha, V.K., et al. 2003. PGC-1α-responsive genes involved in oxidative phosphorylation are coordinately downregulated in human diabetes. Nat. Genet. 34:267-273.
30. Wilson-Fritch, L., et al. 2004. Mitochondrial remodeling in adipose tissue associated with obesity and treatment with rosiglitazone. J. Clin. Invest. 114:1281-1289. doi:10.1172/JCI200421752.
31. Vartanian, V., et al. 2006. The metabolic syndrome resulting from a knockout of the NEIL1 DNA glycosylase. Proc. Natl. Acad. Sci. U. S. A. 103:1864-1869.
32. Lennmarken, C., Sandstedt, S., von Schenck, H., and Larsson, J. 1986. Skeletal muscle function and metabolism in obese women. JPEN J. Parenter. Enteral Nutr. 10:583-587.
33. Green, H.J. 1997. Mechanisms of muscle fatigue in intense exercise. J. Sports Sci. 15:247-256.
34. Bach, D., et al. 2003. Mitofusin-2 determines mitochondrial network architecture and mitochondrial metabolism. A novel regulatory mechanism altered in obesity. J. Biol. Chem. 278:17190-17197.
35. Cinti, S., et al. 2005. Adipocyte death defines macrophage localization and function in adipose tissue of obese mice and humans. J. Lipid Res. 46:2347-2355.
36. Bojunga, J., Dresar-Mayert, B., Usadel, K.H., Kusterer, K., and Zeuzem, S. 2004. Antioxidative treatment reverses imbalances of nitric oxide synthase isoform expression and attenuates tissue-cGMP activation in diabetic rats. Biochem. Biophys. Res. Commun. 316:771-780.
37. Munoz-Fernandez, M.A., and Fresno, M. 1998. The role of tumour necrosis factor, interleukin 6, interferon-gamma and inducible nitric oxide synthase in the development and pathology of the nervous system. Prog. Neurobiol. 56:307-340.
38. Anderson, H.D., Rahmutula, D., and Gardner, D.G. 2004. Tumor necrosis factor-α inhibits endothelial nitric-oxide synthase gene promoter activity in bovine aortic endothelial cells. J. Biol. Chem. 279:963-969.
39. Schulze-Osthoff, K., et al. 1992. Cytotoxic activity of tumor necrosis factor is mediated by early damage of mitochondrial functions. Evidence for the involvement of mitochondrial radical generation. J. Biol. Chem. 267:5317-5323.
40. Tatsumi, T., et al. 2000. Cytokine-induced nitric oxide production inhibits mitochondrial energy production and impairs contractile function in rat cardiac myocytes. J. Am. Coll. Cardiol. 35:1338-1346.
41. Neels, J.G., Pandey, M., Hotamisligil, G.S., and Samad, F. 2006. Autoamplification of tumor necrosis factor-α: a potential mechanism for the maintenance of elevated tumor necrosis factor-α in male but not female obese mice. Am. J. Pathol. 168:435-444.
42. Visser, M., Bouter, L.M., McQuillan, G.M., Wener, M.H., and Harris, T.B. 1999. Elevated C-reactive protein levels in overweight and obese adults. JAMA. 282:2131-2135.
43. Nair, S.P., Chacko, V., Arnold, C., and Diehl, A.M. 2003. Hepatic ATP reserve and efficiency of replenishing: comparison between obese and nonobese normal individuals. Am. J. Gastroenterol. 98:466-470.
44. Woods, S.C., Benoit, S.C., Clegg, D.J., and Seeley, R.J. 2004. Clinical endocrinology and metabolism. Regulation of energy homeostasis by peripheral signals. Best Pract. Res. Clin. Endocrinol. Metab. 18:497-515.
45. Selman, C., et al. 2005. Energy expenditure of calorically restricted rats is higher than predicted from their altered body composition. Mech. Ageing Dev. 126:783-793.
46. Nisoli, E., et al. 2005. Calorie restriction promotes mitochondrial biogenesis by inducing the expression of eNOS. Science. 310:314-317.
47. Kempen, K.P., Saris, W.H., Kuipers, H., Glatz, J.F., and Van Der Vusse, G.J. 1998. Skeletal muscle metabolic characteristics before and after energy restriction in human obesity: fibre type, enzymatic beta-oxidative capacity and fatty acid-binding protein content. Eur. J. Clin. Invest. 28:1030-1037.
48. Rodbell, M. 1964. Metabolism of isolated fat cells. I. Effects of hormones on glucose metabolism and lipolysis. J. Biol. Chem. 239:375-380.
49. Cossu, G., et al. 1980. In vitro differentiation of satellite cells isolated from normal and dystrophic mammalian muscles. A comparison with embryonic myogenic cells. Cell Differ. 9:357-368.
50. Clementi, E., Brown, G.C., Feelisch, M., and Moncada, S. 1998. Persistent inhibition of cell respiration by nitric oxide: crucial role of S-nitrosylation of mitochondrial complex I and protective action of glutathione. Proc. Natl. Acad. Sci. U. S. A. 95:7631-7636.
51. Stocchi, V., et al. 1985. Simultaneous extraction and reverse-phase high-performance liquid chromatographic determination of adenine and pyridine nucleotides in human red blood cells. Anal. Biochem. 146:118-124.