Expression of NLRP3 inflammasome and T cell population markers in adipose tissue are associated with insulin resistance and impaired glucose metabolism in humans

Molecular Immunology

Volumn 50, Issue 3, 2012, Pages 142-149

  Goossens, Gijs H ^a   Blaak, Ellen E ^a   Theunissen, Ruud ^b   Duijvestijn, Adriaan M ^b   Clément, Karine ^c,d,e,f   Tervaert, Jan Willem Cohen ^b   Thewissen, Marielle M ^b  

^a MAASTRICHT UNIVERSITY MEDICAL CENTER   (Netherlands)

^b MAASTRICHT UNIVERSITY   (Netherlands)

^c INSERM   (France)

^d CENTRE DE RECHERCHE DES CORDELIERS   (France)

^e Human Nutrition Research Centre   (France)

^f PITIÉ SALPÊTRIÈRE HOSPITAL   (France)

Author keywords

Fat; Glucose metabolism; Human adipose tissue; Inflammation; Insulin resistance

Indexed keywords

CD11B ANTIGEN; CD3 ANTIGEN; CD40 ANTIGEN; CD68 ANTIGEN; CRYOPYRIN; INFLAMMASOME; INTERLEUKIN 18; INTERLEUKIN 1BETA; INTERLEUKIN 1BETA CONVERTING ENZYME; INTERLEUKIN 8; MESSENGER RNA; MONOCYTE CHEMOTACTIC PROTEIN 1; RANTES; TRANSCRIPTION FACTOR FOXP3; TRANSCRIPTION FACTOR GATA 3; TRANSCRIPTION FACTOR T BET; TUMOR NECROSIS FACTOR ALPHA;

ABDOMINAL SUBCUTANEOUS FAT; ADAPTIVE IMMUNITY; ADIPOSE TISSUE; ADULT; ARTICLE; CELL INFILTRATION; CLINICAL ARTICLE; CONTROLLED STUDY; GENE EXPRESSION; GLUCOSE METABOLISM; HUMAN; HUMAN CELL; HUMAN TISSUE; IMPAIRED GLUCOSE TOLERANCE; INSULIN RESISTANCE; MACROPHAGE; MALE; OBESITY; PRIORITY JOURNAL; PROTEIN EXPRESSION; T LYMPHOCYTE; TH1 CELL; TH17 CELL;

ADIPOSE TISSUE; ANIMALS; CARRIER PROTEINS; CASPASE 1; GLUCOSE; HOMEOSTASIS; HUMANS; INFLAMMASOMES; INSULIN RESISTANCE; MALE; MICE; MIDDLE AGED; T-LYMPHOCYTES;

RODENTIA;

EID: 84857364150     PISSN: 01615890     EISSN: 18729142     Source Type: Journal    
DOI: 10.1016/j.molimm.2012.01.005     Document Type: Article

References (27)

1. Chung Y., Chang S.H., Martinez G.J., Yang X.O., Nurieva R., Kang H.S., Ma L., Watowich S.S., Jetten A.M., Tian Q., Dong C. Critical regulation of early Th17 cell differentiation by interleukin-1 signaling. Immunity 2009, 30:576-587.
2. DeFronzo R.A., Tobin J.D., Andres R. Glucose clamp technique: a method for quantifying insulin secretion and resistance. Am. J. Physiol. 1979, 237:E214-E223.
3. Dinarello C.A. IL-18: a TH1-inducing, proinflammatory cytokine and new member of the IL-1 family. J. Allergy Clin. Immunol. 1999, 103:11-24.
4. Duffaut C., Galitzky J., Lafontan M., Bouloumie A. Unexpected trafficking of immune cells within the adipose tissue during the onset of obesity. Biochem. Biophys. Res. Commun. 2009, 384:482-485.
5. Feuerer M., Herrero L., Cipolletta D., Naaz A., Wong J., Nayer A., Lee J., Goldfine A.B., Benoist C., Shoelson S., Mathis D. Lean, but not obese, fat is enriched for a unique population of regulatory T cells that affect metabolic parameters. Nat. Med. 2009, 15:930-939.
6. Goossens G.H. The role of adipose tissue dysfunction in the pathogenesis of obesity-related insulin resistance. Physiol. Behav. 2008, 94:206-218.
7. Goossens G.H., Bizzarri A., Venteclef N., Essers Y., Cleutjens J.P., Konings E., Jocken J.W., Cajlakovic M., Ribitsch V., Clement K., Blaak E.E. Increased adipose tissue oxygen tension in obese compared with lean men is accompanied by insulin resistance, impaired adipose tissue capillarization, and inflammation. Circulation 2011, 124:67-76.
8. Kanneganti T.D., Lamkanfi M., Nunez G. Intracellular NOD-like receptors in host defense and disease. Immunity 2007, 27:549-559.
9. Kintscher U., Hartge M., Hess K., Foryst-Ludwig A., Clemenz M., Wabitsch M., Fischer-Posovszky P., Barth T.F., Dragun D., Skurk T., Hauner H., Bluher M., Unger T., Wolf A.M., Knippschild U., Hombach V., Marx N. T-lymphocyte infiltration in visceral adipose tissue: a primary event in adipose tissue inflammation and the development of obesity-mediated insulin resistance. Arterioscler. Thromb. Vasc. Biol. 2008, 28:1304-1310.
10. Koenen T.B., Stienstra R., van Tits L.J., de Graaf J., Stalenhoef A.F., Joosten L.A., Tack C.J., Netea M.G. Hyperglycemia activates caspase-1 and TXNIP-mediated IL-1beta transcription in human adipose tissue. Diabetes 2011, 60:517-524.
11. Lundgren M., Svensson M., Lindmark S., Renstrom F., Ruge T., Eriksson J.W. Fat cell enlargement is an independent marker of insulin resistance and 'hyperleptinaemia'. Diabetologia 2007, 50:625-633.
12. 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. 2009, 15:914-920.
13. Odegaard J.I., Chawla A. Mechanisms of macrophage activation in obesity-induced insulin resistance. Nat. Clin. Pract. Endocrinol. Metab. 2008, 4:619-626.
14. Petrilli V., Dostert C., Muruve D.A., Tschopp J. The inflammasome: a danger sensing complex triggering innate immunity. Curr. Opin. Immunol. 2007, 19:615-622.
15. Rocha V.Z., Folco E.J., Sukhova G., Shimizu K., Gotsman I., Vernon A.H., Libby P. Interferon-gamma, a Th1 cytokine, regulates fat inflammation: a role for adaptive immunity in obesity. Circ. Res. 2008, 103:467-476.
16. Siri W.E. The gross composition of the body. Adv. Biol. Med. Physiol. 1956, 4:239-280.
17. Stienstra R., Joosten L.A., Koenen T., van Tits B., van Diepen J.A., van den Berg S.A., Rensen P.C., Voshol P.J., Fantuzzi G., Hijmans A., Kersten S., Muller M., van den Berg W.B., van Rooijen N., Wabitsch M., Kullberg B.J., van der Meer J.W., Kanneganti T., Tack C.J., Netea M.G. The inflammasome-mediated caspase-1 activation controls adipocyte differentiation and insulin sensitivity. Cell Metab. 2010, 12:593-605.
18. Strissel K.J., DeFuria J., Shaul M.E., Bennett G., Greenberg A.S., Obin M.S. T-cell recruitment and Th1 polarization in adipose tissue during diet-induced obesity in C57BL/6 mice. Obesity (Silver Spring) 2010, 18:1918-1925.
19. Thewissen M.M., Damoiseaux J.G., Duijvestijn A.M., van Greevenbroek M.M., van der Kallen C.J., Feskens E.J., Blaak E.E., Schalkwijk C.G., Stehouwer C.D., Tervaert J.W., Ferreira I. Abdominal fat mass is associated with adaptive immune activation: the CODAM study. Obesity (Silver Spring) 2011, 19:1690-1698.
20. Vandanmagsar B., Youm Y.H., Ravussin A., Galgani J.E., Stadler K., Mynatt R.L., Ravussin E., Stephens J.M., Dixit V.D. The NLRP3 inflammasome instigates obesity-induced inflammation and insulin resistance. Nat. Med. 2011, 17:179-188.
21. Weisberg S.P., McCann D., Desai M., Rosenbaum M., Leibel R.L., Ferrante A.W. Obesity is associated with macrophage accumulation in adipose tissue. J. Clin. Invest. 2003, 112:1796-1808.
22. Wilmanski J.M., Petnicki-Ocwieja T., Kobayashi K.S. NLR proteins: integral members of innate immunity and mediators of inflammatory diseases. J. Leukoc. Biol. 2008, 83:13-30.
23. Winer S., Chan Y., Paltser G., Truong D., Tsui H., Bahrami J., Dorfman R., Wang Y., Zielenski J., Mastronardi F., Maezawa Y., Drucker D.J., Engleman E., Winer D., Dosch H.M. Normalization of obesity-associated insulin resistance through immunotherapy. Nat. Med. 2009, 15:921-929.
24. Wu H., Ghosh S., Perrard X.D., Feng L., Garcia G.E., Perrard J.L., Sweeney J.F., Peterson L.E., Chan L., Smith C.W., Ballantyne C.M. T-cell accumulation and regulated on activation, normal, T cell expressed and secreted upregulation in adipose tissue in obesity. Circulation 2007, 115:1029-1038.
25. Yang H., Youm Y.H., Vandanmagsar B., Ravussin A., Gimble J.M., Greenway F., Stephens J.M., Mynatt R.L., Dixit V.D. Obesity increases the production of proinflammatory mediators from adipose tissue T cells and compromises TCR repertoire diversity: implications for systemic inflammation and insulin resistance. J. Immunol. 2010, 185:1836-1845.
26. Zeyda M., Huber J., Prager G., Stulnig T.M. Inflammation correlates with markers of T-cell subsets including regulatory T cells in adipose tissue from obese patients. Obesity (Silver Spring) 2011, 19:743-748.
27. Zhou R., Tardivel A., Thorens B., Choi I., Tschopp J. Thioredoxin-interacting protein links oxidative stress to inflammasome activation. Nat. Immunol. 2010, 11:136-140.