Influence of TNF-α and IL-6 infusions on insulin sensitivity and expression of IL-18 in humans

American Journal of Physiology - Endocrinology and Metabolism

Volumn 291, Issue 1, 2006, Pages

  Krogh Madsen, Rikke ^a   Plomgaard, Peter ^a   Møller, Kirsten ^a   Mittendorfer, Bettina ^b   Pedersen, Bente K ^a  

^a Rigshospitalet   (Denmark)

^b WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Cytokines; Diabetes; Inflammation; Interleukin 18; Interleukin 6; Tumor necrosis factor

Indexed keywords

GLUCOSE; INSULIN; INTERLEUKIN 18; INTERLEUKIN 1BETA CONVERTING ENZYME; RECOMBINANT INTERLEUKIN 6; RECOMBINANT TUMOR NECROSIS FACTOR ALPHA;

ADIPOSE TISSUE; ADULT; AREA UNDER THE CURVE; ARTICLE; BLOOD SAMPLING; CONTROLLED STUDY; DRUG BLOOD LEVEL; DRUG EFFECT; GENE EXPRESSION; GLUCOSE INFUSION; GLUCOSE TRANSPORT; HUMAN; HUMAN EXPERIMENT; HYPERGLYCEMIA; INSULIN SENSITIVITY; ISOTOPE TRACING; MALE; MUSCLE BIOPSY; MUSCLE TISSUE; NORMAL HUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SKELETAL MUSCLE;

ADIPOSE TISSUE; ADULT; BIOPSY, NEEDLE; BLOOD GLUCOSE; CASPASE 1; GENE EXPRESSION REGULATION; GLUCOSE CLAMP TECHNIQUE; HUMANS; HYDROCORTISONE; INSULIN; INSULIN RESISTANCE; INTERLEUKIN-18; INTERLEUKIN-6; MALE; MUSCLE, SKELETAL; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; TUMOR NECROSIS FACTOR-ALPHA;

EID: 33745819568     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.00471.2005     Document Type: Article

References (75)

1. Adachi O, Kawai T, Takeda K, Matsumoto M, Tsutsui H, Sakagami M, Nakanishi K, and Akira S. Targeted disruption of the MyD88 gene results in loss of IL-1- and IL-18-mediated function. Immunity 9: 143-150, 1998.
2. Aguirre V, Werner ED, Giraud J, Lee YH, Shoelson SE, and 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.
3. Aso Y, Okumura K, Takebayashi K, Wakabayashi S, and Inukai T. Relationships of plasma interleukin-18 concentrations to hyperhomocysteinemia and carotid intimal-media wall thickness in patients with type 2 diabetes. Diabetes Care 26: 2622-2627, 2003.
4. Baker SJ and Reddy EP. Modulation of life and death by the TNF receptor superfamily. Oncogene 17: 3261-3270, 1998.
5. Borst SE. The role of TNF-alpha in insulin resistance. Endocrine 23: 177-182, 2004.
6. Carey AL and Febbraio MA. Interleukin-6 and insulin sensitivity: friend or foe? Diabetologia 47: 1135-1142, 2004.
7. Carey AL, Lamont B, Andrikopoulos S, Koukoulas I, Proietto J, and Febbraio MA. Interleukin-6 gene expression is increased in insulin-resistant rat skeletal muscle following insulin stimulation. Biochem Biophys Res Commun 302: 837-840, 2003.
8. Chandrasekar B, Colston JT, de la Rosa SD, Rao PP, and Freeman GL. TNF-alpha and H2O2 induce IL-18 and IL-18R beta expression in cardiomyocytes via NF-kappa B activation. Biochem Biophys Res Commun 303: 1152-1158, 2003.
9. Chariot A, Meuwis MA, Bonif M, Leonardi A, Merville MP, Gielen J, Piette J, Siebenlist U, and Bours V. NF-kappaB activating scaffold proteins as signaling molecules and putative therapeutic targets. Curr Med Chem 10: 593-602, 2003.
10. Conti B, Jahng JW, Tinti C, Son JH, and Joh TH. Induction of interferon-gamma inducing factor in the adrenal cortex. J Biol Chem 272: 2035-2037, 1997.
11. Conti B, Park LC, Calingasan NY, Kim Y, Kim H, Bae Y, Gibson GE, and Joh TH. Cultures of astrocytes and microglia express interleukin 18. Brain Res Mol Brain Res 67: 46-52, 1999.
12. Di Gregorio GB, Hensley L, Lu T, Ranganathan G, and Kern PA. 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 287: E182-E187, 2004.
13. Dinarello CA. Interleukin-1 beta, interleukin-18, and the interleukin-1 beta converting enzyme. Ann NY Acad Sci 856: 1-11, 1998.
14. Dinarello CA. IL-18: A TH1-inducing, proinflammatory cytokine and new member of the IL-1 family. J Allergy Clin Immunol 103: 11-24, 1999.
15. Dinarello CA and Fantuzzi G. Interleukin-18 and host defense against infection. J Infect Dis 187, Suppl 2: S370-S384, 2003.
16. Dinarello CA, Novick D, Puren AJ, Fantuzzi G, Shapiro L, Muhl H, Yoon DY, Reznikov LL, Kim SH, and Rubinstein M. Overview of interleukin-18: more than an interferon-gamma inducing factor. J Leukoc Biol 63: 658-664, 1998.
17. Elhage R, Jawien J, Rudling M, Ljunggren HG, Takeda K, Akira S, Bayard F, and Hansson GK. Reduced atherosclerosis in interleukin-18 deficient apolipoprotein E-knockout mice. Cardiovasc Res 59: 234-240, 2003.
18. Escobar-Morreale HF, Botella-Carretero JI, Villuendas G, Sancho J, and San Millan JL. Serum interleukin-18 concentrations are increased in the polycystic ovary syndrome: relationship to insulin resistance and to obesity. J Clin Endocrinol Metab 89: 806-811, 2004.
19. Esposito K, Nappo F, Giugliano F, Di Palo C, Ciotola M, Barbieri M, Paolisso G, and Giugliano D. Cytokine milieu tends toward inflammation in type 2 diabetes. Diabetes Care 26: 1647, 2003.
20. Esposito K, Pontillo A, Ciotola M, Di Palo C, Grella E, Nicoletti G, and Giugliano D. Weight loss reduces interleukin-18 levels in obese women. J Clin Endocrinol Metab 87: 3864-3866, 2002.
21. Fain JN, Madan AK, Hiler ML, Cheema P, and Bahouth SW. Comparison of the release of adipokines by adipose tissue, adipose tissue matrix, and adipocytes from visceral and subcutaneous abdominal adipose tissues of obese humans. Endocrinology 145: 2273-2282, 2004.
22. Fantuzzi G and Dinarello CA. Interleukin-18 and interleukin-1 beta: two cytokine substrates for ICE (caspase-1). J Clin Immunol 19: 1-11, 1999.
23. Fasshauer M, Klein J, Lossner U, and Paschke R. Interleukin (IL)-6 mRNA expression is stimulated by insulin, isoproterenol, tumour necrosis factor alpha, growth hormone, and IL-6 in 3T3-L1 adipocytes. Horm Metab Res 35: 147-152, 2003.
24. Finegood DT, Bergman RN, and Vranic M. Estimation of endogenous glucose production during hyperinsulinemic-euglycemic glucose clamps. Comparison of unlabeled and labeled exogenous glucose infusates. Diabetes 36: 914-924, 1987.
25. Fischer CP, Perstrup LB, Berntsen A, Eskildsen P, and Pedersen BK. Elevated plasma interleukin-18 is a marker of insulin-resistance in type 2 diabetic and non-diabetic humans. Clin Immunol 117: 152-160, 2005.
26. Fried SK, Bunkin DA, and 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.
27. Fukami T, Miyazaki E, Matsumoto T, Kumamoto T, and Tsuda T. Elevated expression of interleukin-18 in the granulomatous lesions of muscular sarcoidosis. Clin Immunol 101: 12-20, 2001.
28. Gracie JA, Robertson SE, and McInnes IB. Interleukin-18. J Leukoc Biol 73: 213-224, 2003.
29. Hirosumi J, Tuncman G, Chang L, Gorgun CZ, Uysal KT, Maeda K, Karin M, and Hotamisligil GS. A central role for JNK in obesity and insulin resistance. Nature 420: 333-336, 2002.
30. Hotamisligil GS, Arner P, Caro JF, Atkinson RL, and Spiegelman BM. Increased adipose tissue expression of tumor necrosis factor-alpha in human obesity and insulin resistance. J Clin Invest 95: 2409-2415, 1995.
31. Hung J, McQuillan BM, Chapman CM, Thompson PL, and Beilby JP. Elevated interleukin-18 levels are associated with the metabolic syndrome independent of obesity and insulin resistance. Arterioscler Thromb Vasc Biol 25: 1268-1273, 2005.
32. Kashiwamura S, Ueda H, and Okamura H. Roles of interleukin-18 in tissue destruction and compensatory reactions. J Immunother 25, Suppl 1: S4-S11, 2002.
33. Katsuki A, Sumida Y, Murashima S, Murata K, Takarada Y, Ito K, Fujii M, Tsuchihashi K, Goto H, Nakatani K, and Yano Y. Serum levels of tumor necrosis factor-alpha are increased in obese patients with noninsulin-dependent diabetes mellitus. J Clin Endocrinol Metab 83: 859-862, 1998.
34. Keller P, Keller C, Carey AL, Jauffred S, Fischer CP, Steensberg A, and Pedersen BK. Interleukin-6 production by contracting human skeletal muscle: autocrine regulation by IL-6. Biochem Biophys Res Commun 310: 550-554, 2003.
35. Keller P, Penkowa M, Keller C, Steensberg A, Fischer CP, Giralt M, Hidalgo J, and Klarlund PB. Interleukin-6 receptor expression in contracting human skeletal muscle: regulating role of IL-6. FASEB J 19: 1181-1183, 2005.
36. Kern PA, Ranganathan S, Li C, Wood L, and 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.
37. Krogh-Madsen R, Plomgaard P, Keller P, Keller C, and Pedersen BK. Insulin stimulates interleukin-6 and tumor necrosis factor-α gene expression in human subcutaneous adipose tissue. Am J Physiol Endocrinol Metab 286: E234-E238, 2004.
38. Lagathu C, Bastard JP, Auclair M, Maachi M, Capeau J, and Caron M. Chronic interleukin-6 (IL-6) treatment increased IL-6 secretion and induced insulin resistance in adipocyte: prevention by rosiglitazone. Biochem Biophys Res Commun 311: 372-379, 2003.
39. Lang CH, Silvis C, Deshpande N, Nystrom G, and Frost RA. Endotoxin stimulates in vivo expression of inflammatory cytokines tumor necrosis factor alpha, interleukin-1beta, -6, and high-mobility-group protein-1 in skeletal muscle. Shock 19: 538-546, 2003.
40. Lee YH, Giraud J, Davis RJ, and White MF. c-Jun N-terminal kinase (JNK) mediates feedback inhibition of the insulin signaling cascade. J Biol Chem 278: 2896-2902, 2003.
41. Lindegaard B, Hansen AB, Gerstoft J, and Pedersen BK. High plasma level of interleukin-18 in HIV-infected subjects with lipodystrophy. J Acquir Immune Defic Syndr 36: 588-593, 2004.
42. Lindegaard B, Hansen AB, Pilegaard H, Keller P, Gerstoft J, and Pedersen BK. Adipose tissue expression of IL-18 and HIV-associated lipodystrophy. AIDS 18: 1956-1958, 2004.
43. Mallat Z, Corbaz A, Scoazec A, Besnard S, Leseche G, Chvatchko Y, and Tedgui A. Expression of interleukin-18 in human atherosclerotic plaques and relation to plaque instability. Circulation 104: 1598-1603, 2001.
44. Mishima Y, Kuyama A, Tada A, Takahashi K, Ishioka T, and Kibata M. Relationship between serum tumor necrosis factor-alpha and insulin resistance in obese men with Type 2 diabetes mellitus. Diabetes Res Clin Pract 52: 119-123, 2001.
45. Mohamed-Ali V, Goodrick S, Rawesh A, Katz DR, Miles JM, Yudkin JS, Klein S, and Coppack SW. Subcutaneous adipose tissue releases interleukin-6, but not tumor necrosis factor-alpha, in vivo. J Clin Endocrinol Metab 82: 4196-4200, 1997.
46. Moriwaki Y, Yamamoto T, Shibutani Y, Aoki E, Tsutsumi Z, Takahashi S, Okamura H, Koga M, Fukuchi M, and Hada T. Elevated levels of interleukin-18 and tumor necrosis factor-alpha in serum of patients with type 2 diabetes mellitus: relationship with diabetic nephropathy. Metabolism 52: 605-608, 2003.
47. Muller S, Martin S, Koenig W, Hanifi-Moghaddam P, Rathmann W, Haastert B, Giani G, Illig T, Thorand B, and Kolb H. Impaired glucose tolerance is associated with increased serum concentrations of interleukin 6 and co-regulated acute-phase proteins but not TNF-alpha or its receptors. Diabetologia 45: 805-812, 2002.
48. Nakamura K, Okamura H, Wada M, Nagata K, and Tamura T. Endotoxin-induced serum factor that stimulates gamma interferon production. Infect Immun 57: 590-595, 1989.
49. Nakanishi K, Yoshimoto T, Tsutsui H, and Okamura H. Interleukin-18 is a unique cytokine that stimulates both Th1 and Th2 responses depending on its cytokine milieu. Cytokine Growth Factor Rev 12: 53-72, 2001.
50. Netea MG, Kullberg BJ, Verschueren I, and Van Der Meer JW. Interleukin-18 induces production of proinflammatory cytokines in mice: no intermediate role for the cytokines of the tumor necrosis factor family and interleukin-1beta. Eur J Immunol 30: 3057-3060, 2000.
51. Ofei F, Hurel S, Newkirk J, Sopwith M, and 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.
52. Oikawa Y, Shimada A, Kasuga A, Morimoto J, Osaki T, Tahara H, Miyazaki T, Tashiro F, Yamato E, Miyazaki J, and Saruta T. Systemic administration of IL-18 promotes diabetes development in young nonobese diabetic mice. J Immunol 171: 5865-5875, 2003.
53. Pahl HL. Activators and target genes of Rel/NF-kappaB transcription factors. Oncogene 18: 6853-6866, 1999.
54. Paquot N, Castillo MJ, Lefebvre PJ, and 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.
55. Park HS, Park JY, and Yu R. Relationship of obesity and visceral adiposity with serum concentrations of CRP, TNF-alpha and IL-6. Diabetes Res Clin Pract 69: 29-35, 2005.
56. Pedersen M, Bruunsgaard H, Weis N, Hendel HW, Andreassen BU, Eldrup E, Dela F, and Pedersen BK. Circulating levels of TNF-alpha and IL-6-relation to truncal fat mass and muscle mass in healthy elderly individuals and in patients with type-2 diabetes. Mech Ageing Dev 124: 495-502, 2003.
57. Petersen AM and Pedersen BK. The anti-inflammatory effect of exercise. J Appl Physiol 98: 1154-1162, 2005.
58. Pickup JC, Chusney GD, Thomas SM, and Burt D. Plasma interleukin-6, tumour necrosis factor alpha and blood cytokine production in type 2 diabetes. Life Sci 67: 291-300, 2000.
59. Pickup JC, Mattock MB, Chusney GD, and 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.
60. Plomgaard P, Bouzakri K, Krogh-Madsen R, Mittendorfer B, Zierath JR, and Pedersen BK. Tumor necrosis factor-alpha induces skeletal muscle insulin resistance in healthy human subjects via inhibition of Akt substrate 160 phosphorylation. Diabetes 54: 2939-2945, 2005.
61. Puren AJ, Fantuzzi G, Gu Y, Su MS, and Dinarello CA. Interleukin-18 (IFNgamma-inducing factor) induces IL-8 and IL-1beta via TNFalpha production from non-CD14+ human blood mononuclear cells. J Clin Invest 101: 711-721, 1998.
62. Rask-Madsen C, Dominguez H, Ihlemann N, Hermann T, Kober L, and Torp-Pedersen C. Tumor necrosis factor-alpha inhibits insulin's stimulating effect on glucose uptake and endothelium-dependent vasodilation in humans. Circulation 108: 1815-1821, 2003.
63. Reddy P. Interleukin-18: recent advances. Curr Opin Hematol 11: 405-410, 2004.
64. Rose RM, Kreuz LE, Holaday JW, Sulak KJ, and Johnson CE. Diurnal variation of plasma testosterone and cortisol. J Endocrinol 54: 177-178, 1972.
65. Saghizadeh M, Ong JM, Garvey WT, Henry RR, and Kern PA. The expression of TNF alpha by human muscle. Relationship to insulin resistance. J Clin Invest 97: 1111-1116, 1996.
66. Starkie RL, Arkinstall MJ, Koukoulas I, Hawley JA, and Febbraio MA. Carbohydrate ingestion attenuates the increase in plasma interleukin-6, but not skeletal muscle interleukin-6 mRNA, during exercise in humans. J Physiol 533: 585-591, 2001.
67. Steele R. Influences of glucose loading and of injected insulin on hepatic glucose output. Ann NY Acad Sci 82: 420-430, 1959.
68. Steensberg A, Fischer CP, Sacchetti M, Keller C, Osada T, Schjerling P, van Hall G, Febbraio MA, and Pedersen BK. Acute interleukin-6 administration does not impair muscle glucose uptake or whole-body glucose disposal in healthy humans. J Physiol 548: 631-638, 2003.
69. Vozarova B, Weyer C, Hanson K, Tataranni PA, Bogardus C, and Pratley RE. Circulating interleukin-6 in relation to adiposity, insulin action, and insulin secretion. Obes Res 9: 414-417, 2001.
70. Wald D, Commane M, Stark GR, and Li X. IRAK and TAK1 are required for IL-18-mediated signaling. Eur J Immunol 31: 3747-3754, 2001.
71. Wallenius V, Wallenius K, Ahren B, Rudling M, Carlsten H, Dickson SL, Ohlsson C, and Jansson JO. Interleukin-6-deficient mice develop mature-onset obesity. Nat Med 8: 75-79, 2002.
72. Wang B, Jenkins JR, and Trayhurn P. Expression and secretion of inflammation-related adipokines by human adipocytes differentiated in culture: integrated response to TNF-α. Am J Physiol Endocrinol Metab 288: E731-E740, 2005.
73. Weisberg SP, McCann D, Desai M, Rosenbaum M, Leibel RL, and Ferrante AW Jr. Obesity is associated with macrophage accumulation in adipose tissue. J Clin Invest 112: 1796-1808, 2003.
74. Wellen KE and Hotamisligil GS. Inflammation, stress, and diabetes. J Clin Invest 115: 1111-1119, 2005.
75. Xu H, Barnes GT, Yang Q, Tan G, Yang D, Chou CJ, Sole J, Nichols A, Ross JS, Tartaglia LA, and 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.