Long-term exposure to a high-fat diet results in the development of glucose intolerance and insulin resistance in interleukin-1 receptor I-deficient mice

American Journal of Physiology - Endocrinology and Metabolism

Volumn 305, Issue 7, 2013, Pages

  McGillicuddy, Fiona C ^a   Reynolds, Clare M ^a   Finucane, Orla ^a   Coleman, Eilish ^a   Harford, Karen A ^a   Grant, Christine ^c   Sergi, Domenico ^c   Williams, Lynda M ^c   Mills, Kingston H G ^b   Roche, Helen M ^a  

^a UNIVERSITY COLLEGE DUBLIN   (Ireland)

^b TRINITY COLLEGE DUBLIN   (Ireland)

^c ROWETT RESEARCH INSTITUTE   (United Kingdom)

Author keywords

Adipose inflammation; Hepatic steatosis

Indexed keywords

CYTOKINE; GLUCOSE; INSULIN; INTERLEUKIN 1 RECEPTOR TYPE I;

ADIPOCYTE; ADIPOGENESIS; ADIPOSE TISSUE; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL STRUCTURE; CONTROLLED STUDY; FATTY LIVER; GLUCOSE HOMEOSTASIS; GLUCOSE INTOLERANCE; HYPERINSULINEMIA; HYPERLEPTINEMIA; HYPERPLASIA; HYPERTROPHY; INSULIN RESISTANCE; INSULIN SENSITIVITY; INSULIN TOLERANCE TEST; LIPID DIET; LIPID LIVER LEVEL; LONG TERM EXPOSURE; LOW FAT DIET; MALE; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROADIPOCYTE; WEIGHT GAIN;

ADIPOSE INFLAMMATION; HEPATIC STEATOSIS;

ADIPOSE TISSUE; ADIPOSITY; ANIMALS; DIET, HIGH-FAT; DIETARY FATS; FATTY LIVER; GLUCOSE INTOLERANCE; GLUCOSE TOLERANCE TEST; INFLAMMATION; INSULIN; INSULIN RESISTANCE; LEPTIN; MALE; MICE; MICE, KNOCKOUT; RECEPTORS, INTERLEUKIN-1 TYPE I;

EID: 84884968464     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.00297.2013     Document Type: Article

References (47)

1. Brown MS, Goldstein JL. Selective versus total insulin resistance: a pathogenic paradox. Cell Metab 7: 95-96, 2008.
2. Chida D, Osaka T, Hashimoto O, Iwakura Y. Combined interleukin-6 and interleukin-1 deficiency causes obesity in young mice. Diabetes 55: 971-977, 2006.
3. Csak T, Ganz M, Pespisa J, Kodys K, Dolganiuc A, Szabo G. Fatty acid and endotoxin activate inflammasomes in mouse hepatocytes that release danger signals to stimulate immune cells. Hepatology 54: 133-144, 2011.
4. Duewell P, Kono H, Rayner KJ, Sirois CM, Vladimer G, Bauernfeind FG, Abela GS, Franchi L, Nunez G, Schnurr M, Espevik T, Lien E, Fitzgerald KA, Rock KL, Moore KJ, Wright SD, Hornung V, Latz E. NLRP3 inflammasomes are required for atherogenesis and activated by cholesterol crystals. Nature 464: 1357-1361.
5. Febbraio MA, Rose-John S, Pedersen BK. Is interleukin-6 receptor blockade the Holy Grail for inflammatory diseases? Clin Pharmacol Ther 87: 396-398, 2010.
6. Gao Q, Wolfgang MJ, Neschen S, Morino K, Horvath TL, Shulman GI, Fu XY. Disruption of neural signal transducer and activator of transcription 3 causes obesity, diabetes, infertility, and thermal dysregulation. Proc Natl Acad Sci USA 101: 4661-4666, 2004.
7. Garcia MC, Wernstedt I, Berndtsson A, Enge M, Bell M, Hultgren O, Horn M, Ahren B, Enerback S, Ohlsson C, Wallenius V, Jansson JO. Mature-onset obesity in interleukin-1 receptor I knockout mice. Diabetes 55: 1205-1213, 2006.
8. Glass CK, Olefsky JM. Inflammation and lipid signaling in the etiology of insulin resistance. Cell Metab 15: 635-645, 2012.
9. Harford KA, Reynolds CM, McGillicuddy FC, Roche HM. Fats, inflammation and insulin resistance: insights to the role of macrophage and T-cell accumulation in adipose tissue. Proc Nutr Soc 70: 408-417, 2011.
10. Henao-Mejia J, Elinav E, Jin C, Hao L, Mehal WZ, Strowig T, Thaiss CA, Kau AL, Eisenbarth SC, Jurczak MJ, Camporez JP, Shulman GI, Gordon JI, Hoffman HM, Flavell RA. Inflammasome-mediated dysbiosis regulates progression of NAFLD and obesity. Nature 482: 179-185, 2012.
11. Holland WL, Bikman BT, Wang LP, Yuguang G, Sargent KM, Bulchand S, Knotts TA, Shui G, Clegg DJ, Wenk MR, Pagliassotti MJ, Scherer PE, Summers SA. Lipid-induced insulin resistance mediated by the proinflammatory receptor TLR4 requires saturated fatty acidinduced ceramide biosynthesis in mice. J Clin Invest 121: 1858-1870, 2011.
12. Hotamisligil GS. Inflammation and metabolic disorders. Nature 444: 860-867, 2006.
13. Hotta K, Bodkin NL, Gustafson TA, Yoshioka S, Ortmeyer HK, Hansen BC. Age-related adipose tissue mRNA expression of ADD1/ SREBP1, PPARgamma, lipoprotein lipase, and GLUT4 glucose transporter in rhesus monkeys. J Gerontol 54: B183-B188, 1999.
14. Karagiannides I, Tchkonia T, Dobson DE, Steppan CM, Cummins P, Chan G, Salvatori K, Hadzopoulou-Cladaras M, Kirkland JL. Altered expression of C/EBP family members results in decreased adipogenesis with aging. Am J Physiol Regul Integr Comp Physiol 280: R1772-R1780, 2001.
15. Kintscher U, Hartge M, Hess K, Foryst-Ludwig A, Clemenz M, Wabitsch M, Fischer-Posovszky P, Barth TF, Dragun D, Skurk T, Hauner H, Bluher M, Unger T, Wolf AM, Knippschild U, Hombach V, Marx N. T-lymphocyte infiltration in visceral adipose tissue: a primary event in adipose tissue inflammation and the development of obesitymediated insulin resistance. Arterioscler Thromb Vasc Biol 28: 1304-1310, 2008.
16. Kozak W, Zheng H, Conn CA, Soszynski D, van der Ploeg LH, Kluger MJ. Thermal and behavioral effects of lipopolysaccharide and influenza in interleukin-1 beta-deficient mice. Am J Physiol Regul Integr Comp Physiol 269: R969-R977, 1995.
17. Kuilman T, Michaloglou C, Vredeveld LC, Douma S, van Doorn R, Desmet CJ, Aarden LA, Mooi WJ, Peeper DS. Oncogene-induced senescence relayed by an interleukin-dependent inflammatory network. Cell 133: 1019-1031, 2008.
18. 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.
19. Lelliott C, Vidal-Puig AJ. Lipotoxicity, an imbalance between lipogenesis de novo and fatty acid oxidation. Int J Obesity Related Metab Disorders 28, Suppl 4: S22-S28, 2004.
20. Lumeng CN, Bodzin JL, Saltiel AR. Obesity induces a phenotypic switch in adipose tissue macrophage polarization. J Clin Invest 117: 175-184, 2007.
21. Lumeng CN, Deyoung SM, Bodzin JL, Saltiel AR. Increased inflammatory properties of adipose tissue macrophages recruited during dietinduced obesity. Diabetes 56: 16-23, 2007.
22. Matsuki T, Horai R, Sudo K, Iwakura Y. IL-1 plays an important role in lipid metabolism by regulating insulin levels under physiological conditions. J Exp Med 198: 877-888, 2003.
23. Matthews VB, Allen TL, Risis S, Chan MH, Henstridge DC, Watson N, Zaffino LA, Babb JR, Boon J, Meikle PJ, Jowett JB, Watt MJ, Jansson JO, Bruce CR, Febbraio MA. Interleukin-6-deficient mice develop hepatic inflammation and systemic insulin resistance. Diabetologia 53: 2431-2441, 2010.
24. 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.
25. Mills KH, Dunne A. Immune modulation: IL-1, master mediator or initiator of inflammation. Nat Med 15: 1363-1364, 2009.
26. Netea MG, Joosten LA, Lewis E, Jensen DR, Voshol PJ, Kullberg BJ, Tack CJ, van Krieken H, Kim SH, Stalenhoef AF, van de Loo FA, Verschueren I, Pulawa L, Akira S, Eckel RH, Dinarello CA, van den Berg W, van der Meer JW. Deficiency of interleukin-18 in mice leads to hyperphagia, obesity and insulin resistance. Nat Med 12: 650-656, 2006.
27. Nishimura S, Manabe I, Nagasaki M, Eto K, Yamashita H, Ohsugi M, Otsu M, Hara K, Ueki K, Sugiura S, Yoshimura K, Kadowaki T, Nagai R. CD8+ effector T cells contribute to macrophage recruitment and adipose tissue inflammation in obesity. Nat Med 15: 914-920, 2009.
28. Osborn O, Olefsky JM. The cellular and signaling networks linking the immune system and metabolism in disease. Nat Med 18: 363-374, 2012.
29. Patsouris D, Li PP, Thapar D, Chapman J, Olefsky JM, Neels JG. Ablation of CD11c-positive cells normalizes insulin sensitivity in obese insulin resistant animals. Cell Metab 8: 301-309, 2008.
30. Poggi M, Bastelica D, Gual P, Iglesias MA, Gremeaux T, Knauf C, Peiretti F, Verdier M, Juhan-Vague I, Tanti JF, Burcelin R, Alessi MC. C3H/HeJ mice carrying a toll-like receptor 4 mutation are protected against the development of insulin resistance in white adipose tissue in response to a high-fat diet. Diabetologia 50: 1267-1276, 2007.
31. Rausch ME, Weisberg S, Vardhana P, Tortoriello DV. Obesity in C57BL/6J mice is characterized by adipose tissue hypoxia and cytotoxic T-cell infiltration. Int J Obesity 32: 451-463, 2008.
32. Reynolds CM, McGillicuddy FC, Harford KA, Finucane OM, Mills KH, Roche HM. Dietary saturated fatty acids prime the NLRP3 inflammasome via TLR4 in dendritic cells-implications for diet-induced insulin resistance. Mol Nutr Food Res 56: 1212-1222, 2012.
33. Roy AK, Oh T, Rivera O, Mubiru J, Song CS, Chatterjee B. Impacts of transcriptional regulation on aging and senescence. Ageing Res Rev 1: 367-380, 2002.
34. Schroder K, Tschopp J. The inflammasomes. Cell 140: 821-832, 2010.
35. Semple RK, Sleigh A, Murgatroyd PR, Adams CA, Bluck L, Jackson S, Vottero A, Kanabar D, Charlton-Menys V, Durrington P, Soos MA, Carpenter TA, Lomas DJ, Cochran EK, Gorden P, O'Rahilly S, Savage DB. Postreceptor insulin resistance contributes to human dyslipidemia and hepatic steatosis. J Clin Invest 119: 315-322, 2009.
36. Shi H, Kokoeva MV, Inouye K, Tzameli I, Yin H, Flier JS. TLR4 links innate immunity and fatty acid-induced insulin resistance. J Clin Invest 116: 3015-3025, 2006.
37. Shoelson SE, Lee J, Goldfine AB. Inflammation and insulin resistance. J Clin Invest 116: 1793-1801, 2006.
38. Somm E, Henrichot E, Pernin A, Juge-Aubry CE, Muzzin P, Dayer JM, Nicklin MJ, Meier CA. Decreased fat mass in interleukin-1 receptor antagonist-deficient mice: impact on adipogenesis, food intake, and energy expenditure. Diabetes 54: 3503-3509, 2005.
39. 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.
40. Tchkonia T, Morbeck DE, Von Zglinicki T, Van Deursen J, Lustgarten J, Scrable H, Khosla S, Jensen MD, Kirkland JL. Fat tissue, aging, and cellular senescence. Aging Cell 9: 667-684, 2010.
41. 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.
42. 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.
43. Wallenius V, Wallenius K, Ahren B, Rudling M, Carlsten H, Dickson SL, Ohlsson C, Jansson JO. Interleukin-6-deficient mice develop mature-onset obesity. Nat Med 8: 75-79, 2002.
44. 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.
45. 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.
46. Winer S, Chan Y, Paltser G, Truong D, Tsui H, Bahrami J, Dorfman R, Wang Y, Zielenski J, Mastronardi F, Maezawa Y, Drucker DJ, Engleman E, Winer D, Dosch HM. Normalization of obesity-associated insulin resistance through immunotherapy. Nat Med 15: 921-929, 2009.
47. Zhou R, Tardivel A, Thorens B, Choi I, Tschopp J. Thioredoxininteracting protein links oxidative stress to inflammasome activation. Nat Immunol 11: 136-140, 2010.