Chronic Exposure to Interleukin-6 Causes Hepatic Insulin Resistance in Mice

Diabetes

Volumn 52, Issue 11, 2003, Pages 2784-2789

  Klover, Peter J ^a   Zimmers, Teresa A ^a   Koniaris, Leonidas G ^a   Mooney, Robert A ^a  

^a UNIVERSITY OF ROCHESTER SCHOOL OF MEDICINE AND DENTISTRY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLUCOKINASE; INSULIN RECEPTOR; INSULIN RECEPTOR SUBSTRATE 1; INSULIN RECEPTOR SUBSTRATE 2; INTERLEUKIN 6; MESSENGER RNA; STAT3 PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOPHOSPHORYLATION; CONTROLLED STUDY; GENE INDUCTION; INSULIN RESISTANCE; INSULIN SENSITIVITY; INSULIN TOLERANCE TEST; LIVER; LONG TERM EXPOSURE; MALE; MOUSE; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OBESITY; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; SKELETAL MUSCLE;

ANIMALS; GLUCOKINASE; INFUSIONS, PARENTERAL; INSULIN ANTAGONISTS; INSULIN RESISTANCE; INTERLEUKIN-6; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LIVER; MICE; MUSCLE, SKELETAL; PHOSPHOPROTEINS; PHOSPHORYLATION; RECEPTOR, INSULIN; RNA, MESSENGER; SIGNAL TRANSDUCTION; TRANSCRIPTION, GENETIC;

EID: 0242268894     PISSN: 00121797     EISSN: None     Source Type: Journal    
DOI: 10.2337/diabetes.52.11.2784     Document Type: Article

References (44)

1. Pickup JC, Mattock MB, Chusney GD, Burt D: NIDDM as a disease of the innate immune system: association of acute-phase reactants and interleukin-6 with metabolic syndrome X. Diabetologia 40:1286-1292, 1997
2. Nelson KA, Walsh D, Sheehan FA: The cancer anorexia-cachexia syndrome. J Clin Oncol 12:213-225, 1994
3. Kern PA, Ranganathan S, Li C, Wood L, Ranganathan G: Adipose tissue tumor necrosis factor and interleukin-6 expression in human obesity and insulin resistance. Am J Physiol Endocrinol Metab 280: E745-E751, 2001
4. Shiba T, Higashi N, Nishimura Y: Hyperglycaemia due to insulin resistance caused by interferon-gamma. Diabet Med 15:435-436, 1998
5. Pickup JC, Crook MA: Is type II diabetes mellitus a disease of the innate immune system? Diabetologia 41:1241-1248, 1998
6. Pradhan AD, Manson JE, Rifai N, Buring JE, Ridker PM: C-reactive protein, interleukin 6, and risk of developing type 2 diabetes mellitus. JAMA 286:327-334, 2001
7. Bastard JP, Maachi M, Van Nhieu JT, Jardel C, Bruckert E, Grimaldi A, Robert JJ, Capeau J, Hainque B: Adipose tissue IL-6 content correlates with resistance to insulin activation of glucose uptake both in vivo and in vitro. J Clin Endocrinol Metab 87:2084-2089, 2002
8. Carey DG, Jenkins AB, Campbell LV, Freund J, Chisholm DJ: Abdominal fat and insulin resistance in normal and overweight women: direct measurements reveal a strong relationship in subjects at both low and high risk of NIDDM. Diabetes 45:633-638, 1996
9. Fried SK, Bunkin DA, Greenberg AS: Omental and subcutaneous adipose tissues of obese subjects release interleukin-6: depot difference and regulation by glucocorticoid. J Clin Endocrinol Metab 83:847-850, 1998
10. Senn JJ, Igover PJ, Nowak IA, Mooney RA: Interleukin-6 induces cellular insulin resistance in hepatocytes. Diabetes 51:3391-3399, 2002
11. Stith RD, Luo J: Endocrine and carbohydrate responses to interleukin-6 in vivo. Circ Shock 44:210-215, 1994
12. Tsigos C, Papanicolaou DA, Kyrou I, Defensor R, Mitsiadis CS, Chrousos GP: Dose-dependent effects of recombinant human interleukin-6 on glucose regulation. J Clin Endocrinol Metab 82:4167-4170, 1997
13. Senn JJ, Igover 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
14. Bradford MM: A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248-254, 1976
15. Saltiel AR, Kahn CR: Insulin signalling and the regulation of glucose and lipid metabolism. Nature 414:799-806, 2001
16. Dhahbi JM, Mote PL, Wingo J, Rowley BC, Cao SX, Walford RL, Spindler SR: Caloric restriction alters the feeding response of key metabolic enzyme genes. Mech Ageing Dev 122:1033-1048, 2001
17. Caro JF, Sinha MK, Raju SM, Ittoop O, Pories WJ, Flickinger EG, Meelheim D, Dohm GL: Insulin receptor kinase in human skeletal muscle from obese subjects with and without noninsulin dependent diabetes. J Clin Invest 79:1330-1337, 1987
18. Caro JF, Ittoop O, Pories WJ, Meelheim D, Flickinger EG, Thomas F, Jenquin M, Silverman JF, Khazanie PG, Sinha MK: Studies on the mechanism of insulin resistance in the liver from humans with noninsulin-dependent diabetes: insulin action and binding in isolated hepatocytes, insulin receptor structure, and kinase activity. J Clin Invest 78:249-258, 1986
19. Freidenberg GR, Henry RR, Klein HH, Reichart DR, Olefsky JM: Decreased kinase activity of insulin receptors from adipocytes of non-insulin-dependent diabetic subjects. J Clin Invest 79:240-250, 1987
20. Goodyear LJ, Giorgino F, Sherman LA, Carey J, Smith RJ, Dohm GL: Insulin receptor phosphorylation, insulin receptor substrate-1 phosphorylation, and phosphatidylinositol 3-kinase activity are decreased in intact skeletal muscle strips from obese subjects. J Clin Invest 95:2195-2204, 1995
21. Bjornholm M, Kawano Y, Lehtihet M, Zierath JR: Insulin receptor substrate-1 phosphorylation and phosphatidylinositol 3-kinase activity in skeletal muscle from NIDDM subjects after in vivo insulin stimulation. Diabetes 46:524-527, 1997
22. Hotamisligil GS, Murray DL, Choy LN, Spiegelman BM: Tumor necrosis factor alpha inhibits signaling from the insulin receptor. Proc Natl Acad Sci U S A 91:4854-4858, 1994
23. Feinstein R, Kanety H, Papa MZ, Lunenfeld B, Karasik A: Tumor necrosis factor-alpha suppresses insulin-induced tyrosine phosphorylation of insulin receptor and its substrates. J Biol Chem 268:26055-26058, 1993
24. Kanety H, Feinstein R, Papa MZ, Hemi R, Karasik A: Tumor necrosis factor alpha-induced phosphorylation of insulin receptor substrate-1 (IRS-1): possible mechanism for suppression of insulin-stimulated tyrosine phosphorylation of 1RS-1. J Biol Chem 270:23780-23784, 1995
25. 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
26. 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
27. Kern PA, Saghizadeh M, Ong JM, Bosch RJ, Deem R, Simsolo RB: The expression of tumor necrosis factor in human adipose tissue: regulation by obesity, weight loss, and relationship to lipoprotein lipase. J Clin Invest 95:2111-2119, 1995
28. 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
29. Ofei F, Hurel S, Newkirk J, Sopwith M, Taylor R: Effects of an engineered human anti-TNF-alpha antibody (CDP571) on insulin sensitivity and glycemic control in patients with NIDDM. Diabetes 45:881-885, 1996
30. Paquot N, Castillo MJ, Lefebvre PJ, Scheen AJ: No increased insulin sensitivity after a single intravenous administration of a recombinant human tumor necrosis factor receptor: Fc fusion protein in obese insulin-resistant patients. J Clin Endocrinol Metab 85:1316-1319, 2000
31. Cheung AT, Ree D, Kolls JK, Fuselier J, Coy DH, Bryer-Ash M: An in vivo model for elucidation of the mechanism of tumor necrosis factor-alpha (TNF-alpha)-induced insulin resistance: evidence for differential regulation of insulin signaling by TNF-alpha. Endocrinology 139:4928-4935, 1998
32. 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
33. Engeli S, Feldpausch M, Gorzelniak K, Hartwig F, Heintze U, Janke J, Mohlig M, Pfeiffer AF, Luft FC, Sharma AM: Association between adiponectin and mediators of inflammation in obese women. Diabetes 52:942-947, 2003
34. Greenberg AS, Nordan RP, McIntosh J, Calvo JC, Scow RO, Jablons D: Interleukin 6 reduces lipoprotein lipase activity in adipose tissue of mice in vivo and in 3T3-L1 adipocytes: a possible role for interleukin 6 in cancer cachexia. Cancer Res 52:4113-4116, 1992
35. Campbell JS, Prichard L, Schaper F, Schmitz J, Stephenson-Famy A, Rosenfeld ME, Argast GM, Heinrich PC, Fausto N: Expression of suppressors of cytokine signaling during liver regeneration. J Clin Invest 107: 1285-1292, 2001
36. Zhang Y, Pilon G, Marette A, Baracos VE: Cytokines and endotoxin induce cytokine receptors in skeletal muscle. Am J Physiol Endocrinol Metab 279: E196-E205, 2000
37. Kami K, Morikawa Y, Sekimoto M, Senba E: Gene expression of receptors for IL-6, LIF, and CNTF in regenerating skeletal muscles. J Histochem Cytochem 48:1203-1213, 2000
38. Fujita J, Tsujinaka T, Ebisui C, Yano M, Shiozaki H, Katsume A, Ohsugi Y, Monden M: Role of interleukin-6 in skeletal muscle protein breakdown and cathepsin activity in vivo. Eur Surg Res 28:361-366, 1996
39. Tsujinaka T, Fujita J, Ebisui C, Yano M, Kominami E, Suzuki K, Tanaka K, Katsume A, Ohsugi Y, Shiozaki H, Monden M: Interleukin 6 receptor antibody inhibits muscle atrophy and modulates proteolytic systems in interleukin 6 transgenic mice. J Clin Invest 97:244-249, 1996
40. Gao Z, Zuberi A, Quon MJ, Dong Z, Ye J: Aspirin inhibits serine phosphorylation of IRS-1 in TNF-treated cells through targeting multiple serine kinases. J Biol Chem 2003
41. Tanti JF, Gremeaux T, van Obberghen E, Marchand-Brustel Y: Serine/threonine phosphorylation of insulin receptor substrate 1 modulates insulin receptor signaling. J Biol Chem 269:6051-6057, 1994
42. Rui L, Fisher TL, Thomas J, White MF: Regulation of insulin/insulin-like growth factor-1 signaling by proteasome-mediated degradation of insulin receptor substrate-2. J Biol Chem 276:40362-40367, 2001
43. Aguirre V, Werner ED, Giraud J, Lee YH, Shoelson SE, White MF: Phosphorylation of Ser307 in insulin receptor substrate-1 blocks interactions with the insulin receptor and inhibits insulin action. J Biol Chem 277:1531-1537, 2002
44. Pederson TM, Kramer DL, Rondinone CM: Serine/threonine phosphorylation of IRS-1 triggers its degradation: possible regulation by tyrosine phosphorylation. Diabetes 50:24-31, 2001