Interleukin-1β mediates macrophage-induced impairment of insulin signaling in human primary adipocytes

American Journal of Physiology - Endocrinology and Metabolism

Volumn 307, Issue 3, 2014, Pages

  Gao, Dan ^a   Madi, Mohamed ^a   Ding, Cherlyn ^a   Fok, Matthew ^a   Steele, Thomas ^a   Ford, Christopher ^a   Hunter, Leif ^a   Bing, Chen ^a  

^a UNIVERSITY OF LIVERPOOL   (United Kingdom)

Author keywords

Cytokines; Human adipocytes; IL 1 ; Insulin signaling; Macrophages

Indexed keywords

CHEMOKINE RECEPTOR CCR5; INSULIN RECEPTOR SUBSTRATE 1; INTERLEUKIN 1BETA; INTERLEUKIN 6; INTERLEUKIN 8; MONOCYTE CHEMOTACTIC PROTEIN 1; PHOSPHATIDYLINOSITOL 3 KINASE;

ADIPOCYTE; ARTICLE; CONTROLLED STUDY; GENE EXPRESSION; GLUCOSE INTAKE; GLUCOSE METABOLISM; HUMAN; HUMAN CELL; INFLAMMATION; INSULIN RESISTANCE; INSULIN SENSITIVITY; LIPID METABOLISM; MACROPHAGE; OBESITY; PRIORITY JOURNAL; PROADIPOCYTE; REAL TIME POLYMERASE CHAIN REACTION; RECEPTOR BINDING; RISK FACTOR; SIGNAL TRANSDUCTION; WESTERN BLOTTING;

CYTOKINES; HUMAN ADIPOCYTES; IL-1Β; INSULIN SIGNALING; MACROPHAGES;

ADIPOCYTES, WHITE; ANTIBODIES, NEUTRALIZING; CASPASE 1; CASPASE INHIBITORS; CELL COMMUNICATION; CELL LINE; CELLS, CULTURED; CULTURE MEDIA, CONDITIONED; GENE EXPRESSION REGULATION; HUMANS; HYPOGLYCEMIC AGENTS; INSULIN; INSULIN RESISTANCE; INTERLEUKIN 1 RECEPTOR ANTAGONIST PROTEIN; INTERLEUKIN-1BETA; LIPOLYSIS; MACROPHAGES; RECEPTORS, INTERLEUKIN-1; RECOMBINANT PROTEINS; SIGNAL TRANSDUCTION;

EID: 84907193701     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.00430.2013     Document Type: Article

References (61)

1. Agostini L, Martinon F, Burns K, McDermott MF, Hawkins PN, Tschopp J. NALP3 forms an IL-1beta-processing inflammasome with increased activity in Muckle-Wells autoinflammatory disorder. Immunity 20: 319-325, 2004.
2. Bruun JM, Stallknecht B, Helge JW, Richelsen B. Interleukin-18 in plasma and adipose tissue: effects of obesity, insulin resistance, and weight loss. Eur J Endocrinol 157: 465-471, 2007.
3. Chatterjee P, Seal S, Mukherjee S, Kundu R, Mukherjee S, Ray S, Mukhopadhyay S, Majumdar SS, Bhattacharya S. Adipocyte fetuin-A contributes to macrophage migration into adipose tissue and polarization of macrophages. J Biol Chem 288: 28324-28330, 2013.
4. 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.
5. Constant VA, Gagnon A, Landry A, Sorisky A. Macrophage-conditioned medium inhibits the differentiation of 3T3-L1 and human abdominal preadipocytes. Diabetologia 49: 1402-1411, 2006.
6. Ding C, Wilding JP, Bing C. 1,25-Dihydroxyvitamin D3 protects against macrophage-induced activation of NFkappaB and MAPK signalling and chemokine release in human adipocytes. PLoS ONE 8: e61707, 2013.
7. Ehses JA, Lacraz G, Giroix MH, Schmidlin F, Coulaud J, Kassis N, Irminger JC, Kergoat M, Portha B, Homo-Delarche F, Donath MY. IL-1 antagonism reduces hyperglycemia and tissue inflammation in the type 2 diabetic GK rat. Proc Natl Acad Sci USA 106: 13998-14003, 2009.
8. Fain JN. Release of inflammatory mediators by human adipose tissue is enhanced in obesity and primarily by the nonfat cells: a review. Mediators Inflamm 2010: 513948, 2010.
9. Fain JN. Release of interleukins and other inflammatory cytokines by human adipose tissue is enhanced in obesity and primarily due to the nonfat cells. Vitam Horm 74: 443-477, 2006.
10. Fain JN, Tichansky DS, Madan AK. Most of the interleukin 1 receptor antagonist, cathepsin S, macrophage migration inhibitory factor, nerve growth factor, and interleukin 18 release by explants of human adipose tissue is by the non-fat cells, not by the adipocytes. Metabolism 55: 1113-1121, 2006.
11. Gagnon A, Foster C, Landry A, Sorisky A. The role of interleukin 1beta in the anti-adipogenic action of macrophages on human preadipocytes. J Endocrinol 217: 197-206, 2013.
12. Gao D, Trayhurn P, Bing C. 1,25-Dihydroxyvitamin D3 inhibits the cytokine-induced secretion of MCP-1 and reduces monocyte recruitment by human preadipocytes. Int J Obes (Lond) 37: 357-365, 2013.
13. Gao D, Trayhurn P, Bing C. Macrophage-secreted factors inhibit ZAG expression and secretion by human adipocytes. Mol Cell Endocrinol 325: 135-142, 2010.
14. Heilbronn L, Smith SR, Ravussin E. Failure of fat cell proliferation, mitochondrial function and fat oxidation results in ectopic fat storage, insulin resistance and type II diabetes mellitus. Int J Obes Relat Metab Disord 28, Suppl 4: S12-S21, 2004.
15. Hotamisligil GS. Molecular mechanisms of insulin resistance and the role of the adipocyte. Int J Obes Relat Metab Disord 24, Suppl 4: S23-S27, 2000.
16. 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.
17. Ide J, Gagnon A, Molgat AS, Landry A, Foster C, Sorisky A. Macrophage-conditioned medium inhibits the activation of cyclin-dependent kinase 2 by adipogenic inducers in 3T3-L1 preadipocytes. J Cell Physiol 226: 2297-2306, 2011.
18. Jager J, Gremeaux T, Cormont M, Le Marchand-Brustel Y, Tanti JF. Interleukin-1beta-induced insulin resistance in adipocytes through downregulation of insulin receptor substrate-1 expression. Endocrinology 148: 241-251, 2007.
19. Juge-Aubry CE, Somm E, Chicheportiche R, Burger D, Pernin A, Cuenod-Pittet B, Quinodoz P, Giusti V, Dayer JM, Meier CA. Regulatory effects of interleukin (IL)-1, interferon-beta, and IL-4 on the production of IL-1 receptor antagonist by human adipose tissue. J Clin Endocrinol Metab 89: 2652-2658, 2004.
20. Kamei N, Tobe K, Suzuki R, Ohsugi M, Watanabe T, Kubota N, Ohtsuka-Kowatari N, Kumagai K, Sakamoto K, Kobayashi M, Yamauchi T, Ueki K, Oishi Y, Nishimura S, Manabe I, Hashimoto H, Ohnishi Y, Ogata H, Tokuyama K, Tsunoda M, Ide T, Murakami K, Nagai R, Kadowaki T. Overexpression of monocyte chemoattractant protein-1 in adipose tissues causes macrophage recruitment and insulin resistance. J Biol Chem 281: 26602-26614, 2006.
21. Kanda H, Tateya S, Tamori Y, Kotani K, Hiasa K, Kitazawa R, Kitazawa S, Miyachi H, Maeda S, Egashira K, Kasuga M. MCP-1 contributes to macrophage infiltration into adipose tissue, insulin resistance, and hepatic steatosis in obesity. J Clin Invest 116: 1494-1505, 2006.
22. Keophiphath M, Rouault C, Divoux A, Clement K, Lacasa D. CCL5 promotes macrophage recruitment and survival in human adipose tissue. Arterioscler Thromb Vasc Biol 30: 39-45, 2010.
23. King D. Foresight report on obesity. Lancet 370: 1754; author reply 1755, 2007.
24. Kitade H, Sawamoto K, Nagashimada M, Inoue H, Yamamoto Y, Sai Y, Takamura T, Yamamoto H, Miyamoto K, Ginsberg HN, Mukaida N, Kaneko S, Ota T. CCR5 plays a critical role in obesity-induced adipose tissue inflammation and insulin resistance by regulating both macrophage recruitment and M1/M2 status. Diabetes 61: 1680-1690, 2012.
25. Koenen TB, Stienstra R, van Tits LJ, Joosten LA, van Velzen JF, Hijmans A, Pol JA, van der Vliet JA, Netea MG, Tack CJ, Stalenhoef AF, de Graaf J. The inflammasome and caspase-1 activation: a new mechanism underlying increased inflammatory activity in human visceral adipose tissue. Endocrinology 152: 3769-3778, 2011.
26. Krebs M, Roden M. Molecular mechanisms of lipid-induced insulin resistance in muscle, liver and vasculature. Diabetes Obes Metab 7: 621-632, 2005.
27. Lacasa D, Taleb S, Keophiphath M, Miranville A, Clement K. Macrophage-secreted factors impair human adipogenesis: involvement of proinflammatory state in preadipocytes. Endocrinology 148: 868-877, 2007.
28. Lagathu C, Yvan-Charvet L, Bastard JP, Maachi M, Quignard-Boulange A, Capeau J, Caron M. Long-term treatment with interleukin-1beta induces insulin resistance in murine and human adipocytes. Diabetologia 49: 2162-2173, 2006.
29. Lumeng CN, Deyoung SM, Bodzin JL, Saltiel AR. Increased inflammatory properties of adipose tissue macrophages recruited during dietinduced obesity. Diabetes 56: 16-23, 2007.
30. Lumeng CN, Deyoung SM, Saltiel AR. Macrophages block insulin action in adipocytes by altering expression of signaling and glucose transport proteins. Am J Physiol Endocrinol Metab 292: E166-E174, 2007.
31. Lumeng CN, Saltiel AR. Inflammatory links between obesity and metabolic disease. J Clin Invest 121: 2111-2117, 2011.
32. Matter CM, Handschin C. RANTES (regulated on activation, normal T cell expressed and secreted), inflammation, obesity, and the metabolic syndrome. Circulation 115: 946-948, 2007.
33. McGillicuddy FC, Harford KA, Reynolds CM, Oliver E, Claessens M, Mills KH, Roche HM. Lack of interleukin-1 receptor I (IL-1RI) protects mice from high-fat diet-induced adipose tissue inflammation coincident with improved glucose homeostasis. Diabetes 60: 1688-1698, 2011.
34. Michaud A, Pelletier M, Noel S, Bouchard C, Tchernof A. Markers of macrophage infiltration and measures of lipolysis in human abdominal adipose tissues. Obesity (Silver Spring) 2013.
35. Neels JG, Badeanlou L, Hester KD, Samad F. Keratinocyte-derived chemokine in obesity: expression, regulation, and role in adipose macrophage infiltration and glucose homeostasis. J Biol Chem 284: 20692-20698, 2009.
36. Nov O, Kohl A, Lewis EC, Bashan N, Dvir I, Ben-Shlomo S, Fishman S, Wueest S, Konrad D, Rudich A. Interleukin-1beta may mediate insulin resistance in liver-derived cells in response to adipocyte inflammation. Endocrinology 151: 4247-4256, 2010.
37. Nov O, Shapiro H, Ovadia H, Tarnovscki T, Dvir I, Shemesh E, Kovsan J, Shelef I, Carmi Y, Voronov E, Apte RN, Lewis E, Haim Y, Konrad D, Bashan N, Rudich A. Interleukin-1beta regulates fat-liver crosstalk in obesity by auto-paracrine modulation of adipose tissue inflammation and expandability. PLoS ONE 8: e53626, 2013.
38. O'Rourke RW, Metcalf MD, White AE, Madala A, Winters BR, Maizlin II, Jobe BA, Roberts CT Jr, Slifka MK, Marks DL. Depotspecific differences in inflammatory mediators and a role for NK cells and IFN-gamma in inflammation in human adipose tissue. Int J Obes (Lond) 33: 978-990, 2009.
39. Odegaard JI, Chawla A. Pleiotropic actions of insulin resistance and inflammation in metabolic homeostasis. Science 339: 172-177, 2013.
40. Owyang AM, Maedler K, Gross L, Yin J, Esposito L, Shu L, Jadhav J, Domsgen E, Bergemann J, Lee S, Kantak S. XOMA 052, an anti-IL-1beta monoclonal antibody, improves glucose control and betacell function in the diet-induced obesity mouse model. Endocrinology 151: 2515-2527, 2010.
41. Rotter V, Nagaev I, Smith U. Interleukin-6 (IL-6) induces insulin resistance in 3T3-L1 adipocytes and is, like IL-8 and tumor necrosis factor-alpha, overexpressed in human fat cells from insulin-resistant subjects. J Biol Chem 278: 45777-45784, 2003.
42. Sauter NS, Schulthess FT, Galasso R, Castellani LW, Maedler K. The antiinflammatory cytokine interleukin-1 receptor antagonist protects from high-fat diet-induced hyperglycemia. Endocrinology 149: 2208-2218, 2008.
43. Smith U. Impaired ("diabetic") insulin signaling and action occur in fat cells long before glucose intolerance-is insulin resistance initiated in the adipose tissue? Int J Obes Relat Metab Disord 26: 897-904, 2002.
44. Spranger J, Kroke A, Mohlig M, Hoffmann K, Bergmann MM, Ristow M, Boeing H, Pfeiffer AF. Inflammatory cytokines and the risk to develop type 2 diabetes: results of the prospective population-based European Prospective Investigation into Cancer and Nutrition (EPIC)-Potsdam Study. Diabetes 52: 812-817, 2003.
45. Stephens JM, Lee J, Pilch PF. Tumor necrosis factor-alpha-induced insulin resistance in 3T3-L1 adipocytes is accompanied by a loss of insulin receptor substrate-1 and GLUT4 expression without a loss of insulin receptor-mediated signal transduction. J Biol Chem 272: 971-976, 1997.
46. Stienstra R, Joosten LA, Koenen T, van Tits B, van Diepen JA, van den Berg SA, Rensen PC, Voshol PJ, Fantuzzi G, Hijmans A, Kersten S, Muller M, van den Berg WB, van Rooijen N, Wabitsch M, Kullberg BJ, van der Meer JW, Kanneganti T, Tack CJ, Netea MG. The inflammasome-mediated caspase-1 activation controls adipocyte differentiation and insulin sensitivity. Cell Metab 12: 593-605, 2010.
47. Suganami T, Tanaka M, Ogawa Y. Adipose tissue inflammation and ectopic lipid accumulation. Endocr J 59: 849-857, 2012.
48. Sun X, Casbas-Hernandez P, Bigelow C, Makowski L, Joseph Jerry D, Smith Schneider S, Troester MA. Normal breast tissue of obese women is enriched for macrophage markers and macrophage-associated gene expression. Breast Cancer Res Treat 131: 1003-1012, 2012.
49. Tack CJ, Stienstra R, Joosten LA, Netea MG. Inflammation links excess fat to insulin resistance: the role of the interleukin-1 family. Immunol Rev 249: 239-252, 2012.
50. Taniguchi CM, Emanuelli B, Kahn CR. Critical nodes in signalling pathways: insights into insulin action. Nat Rev Mol Cell Biol 7: 85-96, 2006.
51. Tsou CL, Peters W, Si Y, Slaymaker S, Aslanian AM, Weisberg SP, Mack M, Charo IF. Critical roles for CCR2 and MCP-3 in monocyte mobilization from bone marrow and recruitment to inflammatory sites. J Clin Invest 117: 902-909, 2007.
52. 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.
53. Vandanmagsar B, Youm YH, Ravussin A, Galgani JE, Stadler K, Mynatt RL, Ravussin E, Stephens JM, Dixit VD. The NLRP3 inflammasome instigates obesity-induced inflammation and insulin resistance. Nat Med 17: 179-188, 2011.
54. Vozarova B, Weyer C, Hanson K, Tataranni PA, Bogardus C, Pratley RE. Circulating interleukin-6 in relation to adiposity, insulin action, and insulin secretion. Obes Res 9: 414-417, 2001.
55. Waugh DJ, Wilson C. The interleukin-8 pathway in cancer. Clin Cancer Res 14: 6735-6741, 2008.
56. 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.
57. Wen H, Gris D, Lei Y, Jha S, Zhang L, Huang MT, Brickey WJ, Ting JP. Fatty acid-induced NLRP3-ASC inflammasome activation interferes with insulin signaling. Nat Immunol 12: 408-415, 2011.
58. Xie L, Ortega MT, Mora S, Chapes SK. Interactive changes between macrophages and adipocytes. Clin Vaccine Immunol 17: 651-659, 2010.
59. 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.
60. Yang YS, Li XY, Hong J, Gu WQ, Zhang YF, Yang J, Song HD, Chen JL, Ning G. Interleukin-18 enhances glucose uptake in 3T3-L1 adipocytes. Endocrine 32: 297-302, 2007.
61. Yin J, Hu R, Chen M, Tang J, Li F, Yang Y, Chen J. Effects of berberine on glucose metabolism in vitro. Metabolism 51: 1439-1443, 2002.