Macrophage TNF-α contributes to insulin resistance and hepatic steatosis in diet-induced obesity

American Journal of Physiology - Endocrinology and Metabolism

Volumn 293, Issue 3, 2007, Pages

  De Taeye, Bart M ^a   Novitskaya, Tatiana ^a   McGuinness, Owen P ^b   Gleaves, Linda ^a   Medda, Mousumi ^a   Covington, Joseph W ^a   Vaughan, Douglas E ^a,c  

^a VANDERBILT UNIVERSITY   (United States)

^b VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Cytokine; Hyperinsulinemic euglycemic clamping; Inflammation

Indexed keywords

TUMOR NECROSIS FACTOR ALPHA;

ADIPOSE TISSUE; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BODY COMPOSITION; BODY WEIGHT; CALORIMETRY; CONTROLLED STUDY; GENOTYPE; HISTOLOGY; IMMUNOHISTOCHEMISTRY; INFLAMMATION; INSULIN RESISTANCE; INSULIN SENSITIVITY; LEAN BODY WEIGHT; LIPID DIET; LIPID STORAGE; LIVER WEIGHT; MACROPHAGE; MALE; METABOLIC REGULATION; MORPHOMETRICS; NONALCOHOLIC FATTY LIVER; NONHUMAN; OBESITY; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WEIGHT GAIN;

ANIMALS; DIETARY FATS; FATTY LIVER; INSULIN RESISTANCE; MACROPHAGES; MICE; MICE, KNOCKOUT; OBESITY; TUMOR NECROSIS FACTOR-ALPHA;

EID: 34548395788     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.00194.2007     Document Type: Article

References (50)

1. Ayala JE, Bracy DP, McGuinness OP, Wasserman DH. Considerations in the design of hyperinsulinemic-euglycemic clamps in the conscious mouse. Diabetes 55: 390-397, 2006.
2. Beutler B, Cerami A. Cachectin (tumor necrosis factor): a macrophage hormone governing cellular metabolism and inflammatory response. Endocr Rev 9: 57-66, 1988.
3. Casteleijn E, Kuiper J, van Rooij HC, Kamps JA, Koster JF, van Berkel TJ. Hormonal control of glycogenolysis in parenchymal liver cells by Kupffer and endothelial liver cells. J Biol Chem 263: 2699-2703, 1988.
4. Chan TM, Exton JH. A rapid method for the determination of glycogen content and radioactivity in small quantities of tissue or isolated hepatocytes. Anal Biochem 71: 96-105, 1976.
5. Chao L, Marcus-Samuels B, Mason MM, Moitra J, Vinson C, Arioglu E, Gavrilova O, Reitman ML. Adipose tissue is required for the antidiabetic, but not for the hypolipidemic, effect of thiazolidinediones. J Clin Invest 106: 1221-1228, 2000.
6. Cinti S, Mitchell G, Barbatelli G, Murano I, Ceresi E, Faloia E, Wang S, Fortier M, Greenberg AS, Obin MS. Adipocyte death defines macrophage localization and function in adipose tissue of obese mice and humans. J Lipid Res 46: 2347-2355, 2005.
7. Clement K, Viguerie N, Poitou C, Carette C, Pelloux V, Curat CA, Sicard A, Rome S, Benis A, Zucker JD, Vidal H, Laville M, Barsh GS, Basdevant A, Stich V, Cancello R, Langin D. Weight loss regulates inflammation-related genes in white adipose tissue of obese subjects. FASEB J 18: 1657-1669, 2004.
8. Crossno JT Jr, Majka SM, Grazia T, Gill RG, Klemm DJ. Rosiglitazone promotes development of a novel adipocyte population from bone marrow-derived circulating progenitor cells. J Clin Invest 116: 3220-3228, 2006.
9. Curat CA, Miranville A, Sengenes C, Diehl M, Tonus C, Busse R, Bouloumie A. From blood monocytes to adipose tissue-resident macrophages: induction of diapedesis by human mature adipocytes. Diabetes 53: 1285-1292, 2004.
10. De Taeye BM, Novitskaya T, Gleaves L, Covington JW, Vaughan DE. Bone marrow plasminogen activator inhibitor-1 influences the development of obesity. J Biol Chem 281: 32796-32805, 2006.
11. Emanuelli B, Peraldi P, Filloux C, Chavey C, Freidinger K, Hilton DJ, Hotamisligil GS, Van Obberghen E. SOCS-3 inhibits insulin signaling and is up-regulated in response to tumor necrosis factor-alpha in the adipose tissue of obese mice. J Biol Chem 276: 47944-47949, 2001.
12. Folch J, Lees M, Sloane Stanley GH. A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem 226: 497-509, 1957.
13. Halseth AE, Bracy DP, Wasserman DH. Overexpression of hexokinase II increases insulinand exercise-stimulated muscle glucose uptake in vivo. Am J Physiol Endocrinol Metab 276: E70-E77, 1999.
14. Hedley AA, Ogden CL, Johnson CL, Carroll MD, Curtin LR, Flegal KM. Prevalence of overweight and obesity among US children, adolescents, and adults, 1999-2002. JAMA 291: 2847-2850, 2004.
15. Hotamisligil GS. Inflammatory pathways and insulin action. Int J Obes Relat Metab Disord 27, Suppl 3: S53-S55, 2003.
16. Hotamisligil GS. The irresistible biology of resistin. J Clin Invest 111: 173-174, 2003.
17. Hotamisligil GS, Arner P, Caro JF, Atkinson RL, Spiegelman BM. Increased adipose tissue expression of tumor necrosis factor-alpha in human obesity and insulin resistance. J Clin Invest 95: 2409-2415, 1995.
18. Hotamisligil GS, Budavari A, Murray D, Spiegelman BM. Reduced tyrosine kinase activity of the insulin receptor in obesity-diabetes. Central role of tumor necrosis factor-alpha. J Clin Invest 94: 1543-1549, 1994.
19. Hotamisligil GS, Peraldi P, Budavari A, Ellis R, White MF, Spiegelman BM. IRS-1-mediated inhibition of insulin receptor tyrosine kinase activity in TNF-alpha- and obesity-induced insulin resistance. Science 271: 665-668, 1996.
20. Hotamisligil GS, Shargill NS, Spiegelman BM. Adipose expression of tumor necrosis factor-alpha: direct role in obesity-linked insulin resistance. Science 259: 87-91, 1993.
21. Hotamisligil GS, Spiegelman BM. Tumor necrosis factor alpha: a key component of the obesity-diabetes link. Diabetes 43: 1271-1278, 1994.
22. Kirchgessner TG, Uysal KT, Wiesbrock SM, Marino MW, Hotamisligil GS. Tumor necrosis factor-alpha contributes to obesity-related hyperleptinemia by regulating leptin release from adipocytes. J Clin Invest 100: 2777-2782, 1997.
23. Kitamura K, Nakamoto Y, Akiyama M, Fujii C, Kondo T, Kobayashi K, Kaneko S, Mukaida N. Pathogenic roles of tumor necrosis factor receptor p55-mediated signals in dimethylnitrosamine-induced murine liver fibrosis. Lab Invest 82: 571-583, 2002.
24. Koistinen HA, Bastard JP, Dusserre E, Ebeling P, Zegari N, Andreelli F, Jardel C, Donner M, Meyer L, Moulin P, Hainque B, Riou JP, Laville M, Koivisto VA, Vidal H. Subcutaneous adipose tissue expression of tumour necrosis factor-alpha is not associated with whole body insulin resistance in obese nondiabetic or in type-2 diabetic subjects. Eur J Clin Invest 30: 302-310, 2000.
25. Kraegen EW, James DE, Jenkins AB, Chisholm DJ. Dose-response curves for in vivo insulin sensitivity in individual tissues in rats. Am J Physiol Endocrinol Metab 248: E353-E362, 1985.
26. Li Z, Yang S, Lin H, Huang J, Watkins PA, Moser AB, Desimone C, Song XY, Diehl AM. Probiotics and antibodies to TNF inhibit inflammatory activity and improve nonalcoholic fatty liver disease. Hepatology 37: 343-350, 2003.
27. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2[-Delta Delta C(T)] method. Methods 25: 402-408, 2001.
28. Matsusue K, Haluzik M, Lambert G, Yim SH, Gavrilova O, Ward JM, Brewer B Jr, Reitman ML, Gonzalez FJ. Liver-specific disruption of PPARgamma in leptin-deficient mice improves fatty liver but aggravates diabetic phenotypes. J Clin Invest 111: 737-747, 2003.
29. Moller DE. Potential role of TNF-alpha in the pathogenesis of insulin resistance and type 2 diabetes. Trends Endocrinol Metab 11: 212-217, 2000.
30. Morrison WR, Smith LM. Preparation of fatty acid methyl esters and dimethylacetals from lipids with boron fluoride-methanol. J Lipid Res 5: 600-608, 1964.
31. Nisoli E, Briscini L, Giordano A, Tonello C, Wiesbrock SM, Uysal KT, Cinti S, Carruba MO, Hotamisligil GS. Tumor necrosis factor alpha mediates apoptosis of brown adipocytes and defective brown adipocyte function in obesity. Proc Natl Acad Sci USA 97: 8033-8038, 2000.
32. Permana PA, Menge C, Reaven PD. Macrophage-secreted factors induce adipocyte inflammation and insulin resistance. Biochem Biophys Res Commun 341: 507-514, 2006.
33. Perreault M, Marette A. Targeted disruption of inducible nitric oxide synthase protects against obesity-linked insulin resistance in muscle. Nat Med 7: 1138-1143, 2001.
34. Rajala MW, Scherer PE. Minireview: the adipocyte - at the crossroads of energy homeostasis, inflammation, and atherosclerosis. Endocrinology 144: 3765-3773, 2003.
35. Saghizadeh M, Ong JM, Garvey WT, Henry RR, Kern PA. The expression of TNF alpha by human muscle. Relationship to insulin resistance. J Clin Invest 97: 1111-1116, 1996.
36. Senn JJ, Klover PJ, Nowak IA, Zimmers TA, Koniaris LG, Furlanetto RW, Mooney RA. Suppressor of cytokine signaling-3 (SOCS-3), a potential mediator of interleukin-6-dependent insulin resistance in hepatocytes. J Biol Chem 278: 13740-13746, 2003.
37. Sigmund CD. Viewpoint: are studies in genetically altered mice out of control? Arterioscler Thromb Vasc Biol 20: 1425-1429, 2000.
38. Spolarics Z, Ottlakan A, Lang CH, Spitzer JJ. Kupffer cells play a major role in insulin-mediated hepatic glucose uptake in vivo. Biochem Biophys Res Commun 186: 455-460, 1992.
39. 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.
40. Su GL. Lipopolysaccharides in liver injury: molecular mechanisms of Kupffer cell activation. Am J Physiol Gastrointest Liver Physiol 283: G256-G265, 2002.
41. Tomita K, Tamiya G, Ando S, Ohsumi K, Chiyo T, Mizutani A, Kitamura N, Toda K, Kaneko T, Horie Y, Han JY, Kato S, Shimoda M, Oike Y, Tomizawa M, Makino S, Ohkura T, Saito H, Kumagai N, Nagata H, Ishii H, Hibi T. Tumour necrosis factor alpha signalling through activation of Kupffer cells plays an essential role in liver fibrosis of non-alcoholic steatohepatitis in mice. Gut 55: 415-424, 2006.
42. Torti FM, Dieckmann B, Beutler B, Cerami A, Ringold GM. A macrophage factor inhibits adipocyte gene expression: an in vitro model of cachexia. Science 229: 867-869, 1985.
43. Ueki K, Kondo T, Tseng YH, Kahn CR. Central role of suppressors of cytokine signaling proteins in hepatic steatosis, insulin resistance, and the metabolic syndrome in the mouse. Proc Natl Acad Sci USA 101: 10422-10427, 2004.
44. Uysal KT, Wiesbrock SM, Hotamisligil GS. Functional analysis of tumor necrosis factor (TNF) receptors in TNF-alpha-mediated insulin resistance in genetic obesity. Endocrinology 139: 4832-4838, 1998.
45. Uysal KT, Wiesbrock SM, Marino MW, Hotamisligil GS. Protection from obesity-induced insulin resistance in mice lacking TNF-alpha function. Nature 389: 610-614, 1997.
46. Ventre J, Doebber T, Wu M, MacNaul K, Stevens K, Pasparakis M, Kollias G, Moller DE. Targeted disruption of the tumor necrosis factor-alpha gene: metabolic consequences in obese and nonobese mice. Diabetes 46: 1526-1531, 1997.
47. Weisberg SP, McCann D, Desai M, Rosenbaum M, Leibel RL, Ferrante AW Jr. Obesity is associated with macrophage accumulation in adipose tissue. J Clin Invest 112: 1796-1808, 2003.
48. Xu H, Barnes GT, Yang Q, Tan G, Yang D, Chou CJ, Sole J, Nichols A, Ross JS, Tartaglia LA, Chen H. Chronic inflammation in fat plays a crucial role in the development of obesity-related insulin resistance. J Clin Invest 112: 1821-1830, 2003.
49. You T, Yang R, Lyles MF, Gong D, Nicklas BJ. Abdominal adipose tissue cytokine gene expression: relationship to obesity and metabolic risk factors. Am J Physiol Endocrinol Metab 288: E741-E747, 2005.
50. Yu S, Matsusue K, Kashireddy P, Cao WQ, Yeldandi V, Yeldandi AV, Rao MS, Gonzalez FJ, Reddy JK. Adipocyte-specific gene expression and adipogenic steatosis in the mouse liver due to peroxisome proliferator-activated receptor gamma1 (PPARgamma1) overexpression. J Biol Chem 278: 498-505, 2003.