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Am J Physiol Endocrinol Metab 280: E745-E751, 2001;
0193-1849/01 $5.00
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Vol. 280, Issue 5, E745-E751, May 2001

Adipose tissue tumor necrosis factor and interleukin-6 expression in human obesity and insulin resistance

Philip A. Kern, Subramanian Ranganathan, Chunling Li, Linda Wood, and Gouri Ranganathan

Division of Endocrinology, Department of Medicine, University of Arkansas for Medical Sciences and the Central Arkansas Veterans Healthcare System, Little Rock, Arkansas 72205

Adipose tissue expresses tumor necrosis factor (TNF) and interleukin (IL)-6, which may cause obesity-related insulin resistance. We measured TNF and IL-6 expression in the adipose tissue of 50 lean and obese subjects without diabetes. Insulin sensitivity (SI) was determined by an intravenous glucose tolerance test with minimal-model analysis. When lean [body mass index (BMI) <25 kg/m2] and obese (BMI 30-40 kg/m2) subjects were compared, there was a 7.5-fold increase in TNF secretion (P < 0.05) from adipose tissue, and the TNF secretion was inversely related to SI (r = -0.42, P < 0.02). IL-6 was abundantly expressed by adipose tissue. In contrast to TNF, plasma (rather than adipose) IL-6 demonstrated the strongest relationship with obesity and insulin resistance. Plasma IL-6 was significantly higher in obese subjects and demonstrated a highly significant inverse relationship with SI (r = -0.71, P < 0.001). To separate the effects of BMI from SI, subjects who were discordant for SI were matched for BMI, age, and gender. By use of this approach, subjects with low SI demonstrated a 3.0-fold increased level of TNF secretion from adipose tissue and a 2.3-fold higher plasma IL-6 level (P < 0.05) compared with matched subjects with a high SI. Plasma IL-6 was significantly associated with plasma nonesterified fatty acid levels (r = 0.49, P < 0.002). Thus the local expression of TNF and plasma IL-6 are higher in subjects with obesity-related insulin resistance.

type 2 diabetes


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B. Wang, J. R. Jenkins, and P. Trayhurn
Expression and secretion of inflammation-related adipokines by human adipocytes differentiated in culture: integrated response to TNF-{alpha}
Am J Physiol Endocrinol Metab, April 1, 2005; 288(4): E731 - E740.
[Abstract] [Full Text] [PDF]

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 J. Lipid Res.Home page
F. Haugen, N. Zahid, K. T. Dalen, K. Hollung, H. I. Nebb, and C. A. Drevon
Resistin expression in 3T3-L1 adipocytes is reduced by arachidonic acid
J. Lipid Res., January 1, 2005; 46(1): 143 - 153.
[Abstract] [Full Text] [PDF]

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 ANGIOLOGYHome page
J. Okapcova and D. Gabor
The Levels of Soluble Adhesion Molecules in Diabetic and Nondiabetic Patients with Combined Hyperlipoproteinemia and the Effect of Ciprofibrate Therapy
Angiology, November 1, 2004; 55(6): 629 - 639.
[Abstract] [PDF]

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 ANGIOLOGYHome page
J. Okapcova and D. Gabor
The Levels of Soluble Adhesion Molecules in Diabetic and Nondiabetic Patients with Combined Hyperlipoproteinemia and the Effect of Ciprofibrate Therapy
Angiology, November 1, 2004; 55(6): 629 - 639.
[Abstract] [PDF]

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 JPEN J Parenter Enteral NutrHome page
L. Khaodhiar, P.-R. Ling, G. L. Blackburn, and B. R. Bistrian
Serum Levels of Interleukin-6 and C-Reactive Protein Correlate With Body Mass Index Across the Broad Range of Obesity
JPEN J Parenter Enteral Nutr, November 1, 2004; 28(6): 410 - 415.
[Abstract] [Full Text] [PDF]

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 J. Appl. Physiol.Home page
P. Keller, C. Keller, L. E. Robinson, and B. K. Pedersen
Epinephrine infusion increases adipose interleukin-6 gene expression and systemic levels in humans
J Appl Physiol, October 1, 2004; 97(4): 1309 - 1312.
[Abstract] [Full Text] [PDF]

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 J. Appl. Physiol.Home page
J. A. McKenzie, E. P. Weiss, I. A. Ghiu, O. Kulaputana, D. A. Phares, R. E. Ferrell, and J. M. Hagberg
Influence of the interleukin-6 -174 G/C gene polymorphism on exercise training-induced changes in glucose tolerance indexes
J Appl Physiol, October 1, 2004; 97(4): 1338 - 1342.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Endocrinol. Metab.Home page
G. B. Di Gregorio, R. Westergren, S. Enerback, T. Lu, and P. A. Kern
Expression of FOXC2 in adipose and muscle and its association with whole body insulin sensitivity
Am J Physiol Endocrinol Metab, October 1, 2004; 287(4): E799 - E803.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Endocrinol. Metab.Home page
G. B. Di Gregorio, L. Hensley, T. Lu, G. Ranganathan, and P. A. Kern
Lipid and carbohydrate metabolism in mice with a targeted mutation in the IL-6 gene: absence of development of age-related obesity
Am J Physiol Endocrinol Metab, July 1, 2004; 287(1): E182 - E187.
[Abstract] [Full Text] [PDF]

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 Arterioscler. Thromb. Vasc. Bio.Home page
T. Skurk, V. van Harmelen, and H. Hauner
Angiotensin II Stimulates the Release of Interleukin-6 and Interleukin-8 From Cultured Human Adipocytes by Activation of NF-{kappa}B
Arterioscler Thromb Vasc Biol, July 1, 2004; 24(7): 1199 - 1203.
[Abstract] [Full Text] [PDF]

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 NEJMHome page
S. Klein, L. Fontana, V. L. Young, A. R. Coggan, C. Kilo, B. W. Patterson, and B. S. Mohammed
Absence of an Effect of Liposuction on Insulin Action and Risk Factors for Coronary Heart Disease
N. Engl. J. Med., June 17, 2004; 350(25): 2549 - 2557.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
C. Weigert, K. Brodbeck, H. Staiger, C. Kausch, F. Machicao, H. U. Haring, and E. D. Schleicher
Palmitate, but Not Unsaturated Fatty Acids, Induces the Expression of Interleukin-6 in Human Myotubes through Proteasome-dependent Activation of Nuclear Factor-{kappa}B
J. Biol. Chem., June 4, 2004; 279(23): 23942 - 23952.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Renal Physiol.Home page
J. T. Lane
Microalbuminuria as a marker of cardiovascular and renal risk in type 2 diabetes mellitus: a temporal perspective
Am J Physiol Renal Physiol, March 1, 2004; 286(3): F442 - F450.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Regul. Integr. Comp. Physiol.Home page
K. M. Ajuwon, S. K. Jacobi, J. L. Kuske, and M. E. Spurlock
Interleukin-6 and interleukin-15 are selectively regulated by lipopolysaccharide and interferon-{gamma} in primary pig adipocytes
Am J Physiol Regulatory Integrative Comp Physiol, March 1, 2004; 286(3): R547 - R553.
[Abstract] [Full Text] [PDF]

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 NEJMHome page
K. F. Petersen, S. Dufour, D. Befroy, R. Garcia, and G. I. Shulman
Impaired Mitochondrial Activity in the Insulin-Resistant Offspring of Patients with Type 2 Diabetes
N. Engl. J. Med., February 12, 2004; 350(7): 664 - 671.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Endocrinol. Metab.Home page
R. Krogh-Madsen, P. Plomgaard, P. Keller, C. Keller, and B. K. Pedersen
Insulin stimulates interleukin-6 and tumor necrosis factor-{alpha} gene expression in human subcutaneous adipose tissue
Am J Physiol Endocrinol Metab, February 1, 2004; 286(2): E234 - E238.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Endocrinol. Metab.Home page
J. A. Johnson, J. B. Albu, E. S. Engelson, S. K. Fried, Y. Inada, G. Ionescu, and D. P. Kotler
Increased systemic and adipose tissue cytokines in patients with HIV-associated lipodystrophy
Am J Physiol Endocrinol Metab, February 1, 2004; 286(2): E261 - E271.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Endocrinol. Metab.Home page
H. Wang, W. S. Chu, T. Lu, S. J. Hasstedt, P. A. Kern, and S. C. Elbein
Uncoupling protein-2 polymorphisms in type 2 diabetes, obesity, and insulin secretion
Am J Physiol Endocrinol Metab, January 1, 2004; 286(1): E1 - E7.
[Abstract] [Full Text]

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 CirculationHome page
T. Mazurek, L. Zhang, A. Zalewski, J. D. Mannion, J. T. Diehl, H. Arafat, L. Sarov-Blat, S. O'Brien, E. A. Keiper, A. G. Johnson, et al.
Human Epicardial Adipose Tissue Is a Source of Inflammatory Mediators
Circulation, November 18, 2003; 108(20): 2460 - 2466.
[Abstract] [Full Text] [PDF]

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 DiabetesHome page
P. J. Klover, T. A. Zimmers, L. G. Koniaris, and R. A. Mooney
Chronic Exposure to Interleukin-6 Causes Hepatic Insulin Resistance in Mice
Diabetes, November 1, 2003; 52(11): 2784 - 2789.
[Abstract] [Full Text] [PDF]

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 CirculationHome page
C. Rask-Madsen, H. Dominguez, N. Ihlemann, T. Hermann, L. Kober, and C. Torp-Pedersen
Tumor Necrosis Factor-{alpha} Inhibits Insulin's Stimulating Effect on Glucose Uptake and Endothelium-Dependent Vasodilation in Humans
Circulation, October 14, 2003; 108(15): 1815 - 1821.
[Abstract] [Full Text] [PDF]

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 DiabetesHome page
S. P. Kim, M. Ellmerer, G. W. Van Citters, and R. N. Bergman
Primacy of Hepatic Insulin Resistance in the Development of the Metabolic Syndrome Induced by an Isocaloric Moderate-Fat Diet in the Dog
Diabetes, October 1, 2003; 52(10): 2453 - 2460.
[Abstract] [Full Text] [PDF]

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 J ANIM SCIHome page
J. A. Daniel, T. H. Elsasser, C. D. Morrison, D. H. Keisler, B. K. Whitlock, B. Steele, D. Pugh, and J. L. Sartin
Leptin, tumor necrosis factor-{alpha} (TNF), and CD14 in ovine adipose tissue and changes in circulating TNF in lean and fat sheep
J Anim Sci, October 1, 2003; 81(10): 2590 - 2599.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Endocrinol. Metab.Home page
J. M. Bruun, A. S. Lihn, C. Verdich, S. B. Pedersen, S. Toubro, A. Astrup, and B. Richelsen
Regulation of adiponectin by adipose tissue-derived cytokines: in vivo and in vitro investigations in humans
Am J Physiol Endocrinol Metab, September 1, 2003; 285(3): E527 - E533.
[Abstract] [Full Text] [PDF]

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 CirculationHome page
N. Varo, D. Vicent, P. Libby, R. Nuzzo, A. L. Calle-Pascual, M. R. Bernal, A. Fernandez-Cruz, A. Veves, P. Jarolim, J. J. Varo, et al.
Elevated Plasma Levels of the Atherogenic Mediator Soluble CD40 Ligand in Diabetic Patients: A Novel Target of Thiazolidinediones
Circulation, June 3, 2003; 107(21): 2664 - 2669.
[Abstract] [Full Text] [PDF]

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 Arterioscler. Thromb. Vasc. Bio.Home page
H.P. Kopp, C.W. Kopp, A. Festa, K. Krzyzanowska, S. Kriwanek, E. Minar, R. Roka, and G. Schernthaner
Impact of Weight Loss on Inflammatory Proteins and Their Association With the Insulin Resistance Syndrome in Morbidly Obese Patients
Arterioscler Thromb Vasc Biol, June 1, 2003; 23(6): 1042 - 1047.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Endocrinol. Metab.Home page
T.-B. Nguyen-Duy, M. Z. Nichaman, T. S. Church, S. N. Blair, and R. Ross
Visceral fat and liver fat are independent predictors of metabolic risk factors in men
Am J Physiol Endocrinol Metab, June 1, 2003; 284(6): E1065 - E1071.
[Abstract] [Full Text] [PDF]

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 J. Lipid Res.Home page
A. Abderrahim-Ferkoune, O. Bezy, C. Chiellini, M. Maffei, P. Grimaldi, F. Bonino, N. Moustaid-Moussa, F. Pasqualini, A. Mantovani, G. Ailhaud, et al.
Characterization of the long pentraxin PTX3 as a TNF{alpha}-induced secreted protein of adipose cells
J. Lipid Res., May 1, 2003; 44(5): 994 - 1000.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
J. J. Senn, P. J. Klover, I. A. Nowak, T. A. Zimmers, L. G. Koniaris, R. W. Furlanetto, and R. A. Mooney
Suppressor of Cytokine Signaling-3 (SOCS-3), a Potential Mediator of Interleukin-6-dependent Insulin Resistance in Hepatocytes
J. Biol. Chem., April 11, 2003; 278(16): 13740 - 13746.
[Abstract] [Full Text] [PDF]

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 DiabetesHome page
S. Engeli, M. Feldpausch, K. Gorzelniak, F. Hartwig, U. Heintze, J. Janke, M. Mohlig, A. F.H. Pfeiffer, F. C. Luft, and A. M. Sharma
Association Between Adiponectin and Mediators of Inflammation in Obese Women
Diabetes, April 1, 2003; 52(4): 942 - 947.
[Abstract] [Full Text] [PDF]

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 Diabetes CareHome page
M. Wolf, L. Sandler, K. Hsu, K. Vossen-Smirnakis, J. L. Ecker, and R. Thadhani
First-Trimester C-Reactive Protein and Subsequent Gestational Diabetes
Diabetes Care, March 1, 2003; 26(3): 819 - 824.
[Abstract] [Full Text] [PDF]

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 DiabetesHome page
H. Lan, M. E. Rabaglia, J. P. Stoehr, S. T. Nadler, K. L. Schueler, F. Zou, B. S. Yandell, and A. D. Attie
Gene Expression Profiles of Nondiabetic and Diabetic Obese Mice Suggest a Role of Hepatic Lipogenic Capacity in Diabetes Susceptibility
Diabetes, March 1, 2003; 52(3): 688 - 700.
[Abstract] [Full Text] [PDF]

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 DiabetesHome page
J. J. Senn, P. J. Klover, I. A. Nowak, and R. A. Mooney
Interleukin-6 Induces Cellular Insulin Resistance in Hepatocytes
Diabetes, December 1, 2002; 51(12): 3391 - 3399.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Endocrinol. Metab.Home page
A. Steensberg, C. Keller, R. L. Starkie, T. Osada, M. A. Febbraio, and B. K. Pedersen
IL-6 and TNF-alpha expression in, and release from, contracting human skeletal muscle
Am J Physiol Endocrinol Metab, December 1, 2002; 283(6): E1272 - E1278.
[Abstract] [Full Text] [PDF]


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