Fas (CD95) expression in myeloid cells promotes obesity-induced muscle insulin resistance

EMBO Molecular Medicine

Volumn 6, Issue 1, 2014, Pages 43-56

  Wueest, Stephan ^a   Mueller, Rouven ^b   Blüher, Matthias ^c   Item, Flurin ^a   Chin, Annie S H ^a,d   Wiedemann, Michael S F ^a,d   Takizawa, Hitoshi ^b   Kovtonyuk, Larisa ^b   Chervonsky, Alexander V ^e   Schoenle, Eugen J ^a   Manz, Markus G ^b   Konrad, Daniel ^a,d  

^a UNIVERSITY CHILDREN S HOSPITAL   (Switzerland)

^b UNIVERSITY HOSPITAL ZURICH   (Switzerland)

^c UNIVERSITY OF LEIPZIG   (Germany)

^d UNIVERSITY OF ZURICH   (Switzerland)

^e UNIVERSITY OF CHICAGO   (United States)

Author keywords

Diabetes mellitus; Insulin resistance; Obesity

Indexed keywords

FAS ANTIGEN; GLUCOSE; INTERLEUKIN 6; LIPOPOLYSACCHARIDE; NEUTRALIZING ANTIBODY; TUMOR NECROSIS FACTOR ALPHA;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BARIATRIC SURGERY; BONE MARROW CELL; CELL INFILTRATION; CONTROLLED STUDY; FEMALE; FLOW CYTOMETRY; GENE DELETION; GENE EXPRESSION; GLUCOSE BLOOD LEVEL; GLUCOSE HOMEOSTASIS; GLUCOSE INFUSION; GLUCOSE INTOLERANCE; GLUCOSE METABOLISM; GLUCOSE TOLERANCE; GLUCOSE TRANSPORT; HEMATOPOIETIC CELL; HUMAN; HUMAN CELL; HYPOTHESIS; IMMUNOCOMPETENT CELL; INSULIN RESISTANCE; INSULIN SENSITIVITY; LEAN BODY WEIGHT; LIPID DIET; MACROPHAGE; MAJOR CLINICAL STUDY; MALE; MIDDLE AGED; MONOCYTE; MOUSE; NEUTROPHIL; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OBESITY; POLARIZATION; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; REAL TIME POLYMERASE CHAIN REACTION; SKELETAL MUSCLE; SOLEUS MUSCLE; WESTERN BLOTTING; WILD TYPE;

ADULT; AGED; ANIMALS; ANTIBODIES, NEUTRALIZING; ANTIGENS, CD95; COHORT STUDIES; CROSS-SECTIONAL STUDIES; DIABETES MELLITUS, TYPE 2; FEMALE; GENE EXPRESSION REGULATION; HUMANS; INSULIN RESISTANCE; MALE; MICE; MICE, INBRED C57BL; MICE, OBESE; MIDDLE AGED; MONOCYTES; MUSCLE, SKELETAL; OBESITY;

EID: 84891923662     PISSN: 17574676     EISSN: 17574684     Source Type: Journal    
DOI: 10.1002/emmm.201302962     Document Type: Article

References (55)

1. Anonymous (2011) Diagnosis and classification of diabetes mellitus. Diabetes Care 34: S62-S69
2. Araujo EP, De Souza CT, Ueno M, Cintra DE, Bertolo MB, Carvalheira JB, Saad MJ, Velloso LA (2007) Infliximab restores glucose homeostasis in an animal model of diet-induced obesity and diabetes. Endocrinology 148: 5991-5997
3. Arkan MC, Hevener AL, Greten FR, Maeda S, Li ZW, Long JM, Wynshaw-Boris A, Poli G, Olefsky J, Karin M (2005) IKK-beta links inflammation to obesity-induced insulin resistance. Nat Med 11: 191-198
4. Cani PD, Amar J, Iglesias MA, Poggi M, Knauf C, Bastelica D, Neyrinck AM, Fava F, Tuohy KM, Chabo C, et al (2007) Metabolic endotoxemia initiates obesity and insulin resistance. Diabetes 56: 1761-1772
5. Clausen BE, Burkhardt C, Reith W, Renkawitz R, Forster I (1999) Conditional gene targeting in macrophages and granulocytes using LysMcre mice. Transgenic Res 8: 265-277
6. Clement K (2011) Bariatric surgery, adipose tissue and gut microbiota. Int J Obes (London) 35: S7-S15
7. DeFronzo RA, Tripathy D (2009) Skeletal muscle insulin resistance is the primary defect in type 2 diabetes. Diabetes Care 32: S157-S163
8. Donath MY, Shoelson SE (2011) Type 2 diabetes as an inflammatory disease. Nat Rev Immunol 11: 98-107
9. Faouzi S, Burckhardt BE, Hanson JC, Campe CB, Schrum LW, Rippe RA, Maher JJ (2001) Anti-Fas induces hepatic chemokines and promotes inflammation by an NF-kappa B-independent, caspase-3-dependent pathway. J Biol Chem 276: 49077-49082
10. Farley SM, Purdy DE, Ryabinina OP, Schneider P, Magun BE, Iordanov MS (2008) Fas ligand-induced proinflammatory transcriptional responses in reconstructed human epidermis. Recruitment of the epidermal growth factor receptor and activation of MAP kinases. J Biol Chem 283: 919-928
11. Fisher SJ, Kahn CR (2003) Insulin signaling is required for insulin's direct and indirect action on hepatic glucose production. J Clin Inves 111: 463-468
12. Furet JP, Kong LC, Tap J, Poitou C, Basdevant A, Bouillot JL, Mariat D, Corthier G, Dore J, Henegar C, et al (2010) Differential adaptation of human gut microbiota to bariatric surgery-induced weight loss: links with metabolic and low-grade inflammation markers. Diabetes 59: 3049-3057
13. Guo Z, Zhang M, Tang H, Cao X (2005) Fas signal links innate and adaptive immunity by promoting dendritic-cell secretion of CC and CXC chemokines. Blood 106: 2033-2041
14. Gupta-Ganguli M, Cox K, Means B, Gerling I, Solomon SS (2011) Does therapy with anti-TNF-alpha improve glucose tolerance and control in patients with type 2 diabetes? Diabetes Care 34: e121
15. Hotamisligil GS, Shargill NS, Spiegelman BM (1993) Adipose expression of tumor necrosis factor-alpha: direct role in obesity-linked insulin resistance. Science 259: 87-91
16. Imamura R, Konaka K, Matsumoto N, Hasegawa M, Fukui M, Mukaida N, Kinoshita T, Suda T (2004) Fas ligand induces cell-autonomous NF-kappaB activation and interleukin-8 production by a mechanism distinct from that of tumor necrosis factor-alpha. J Biol Chem 279: 46415-46423
17. Kim JK, Michael MD, Previs SF, Peroni OD, Mauvais-Jarvis F, Neschen S, Kahn BB, Kahn CR, Shulman GI (2000) Redistribution of substrates to adipose tissue promotes obesity in mice with selective insulin resistance in muscle. J Clin Invest 105: 1791-1797
18. Konrad D, Rudich A, Schoenle EJ (2007) Improved glucose tolerance in mice receiving intraperitoneal transplantation of normal fat tissue. Diabetologia 50: 833-839
19. Lazar MA (2005) How obesity causes diabetes: not a tall tale. Science 307: 373-375
20. Ley RE, Turnbaugh PJ, Klein S, Gordon JI (2006) Microbial ecology: human gut microbes associated with obesity. Nature 444: 1022-1023
21. Ling PR, Bistrian BR, Mendez B, Istfan NW (1994) Effects of systemic infusions of endotoxin, tumor necrosis factor, and interleukin-1 on glucose metabolism in the rat: relationship to endogenous glucose production and peripheral tissue glucose uptake. Metabolism 43: 279-284
22. Ma Y, Liu H, Tu-Rapp H, Thiesen HJ, Ibrahim SM, Cole SM, Pope RM (2004) Fas ligation on macrophages enhances IL-1R1-Toll-like receptor 4 signaling and promotes chronic inflammation. Nat Immunol 5: 380-387
23. Manco M, Putignani L, Bottazzo GF (2010) Gut microbiota, lipopolysaccharides, and innate immunity in the pathogenesis of obesity and cardiovascular risk. Endocr Rev 31: 817-844
24. Mauer J, Chaurasia B, Plum L, Quast T, Hampel B, Bluher M, Kolanus W, Kahn CR, Bruning JC (2010) Myeloid cell-restricted insulin receptor deficiency protects against obesity-induced inflammation and systemic insulin resistance. PLoS Genet 6: e1000938
25. McIlwain DR, Lang PA, Maretzky T, Hamada K, Ohishi K, Maney SK, Berger T, Murthy A, Duncan G, Xu HC, et al (2012) iRhom2 regulation of TACE controls TNF-mediated protection against Listeria and responses to LPS. Science 335: 229-232
26. Miwa K, Asano M, Horai R, Iwakura Y, Nagata S, Suda T (1998) Caspase 1-independent IL-1beta release and inflammation induced by the apoptosis inducer Fas ligand. Nat Med 4: 1287-1292
27. Nguyen MT, Favelyukis S, Nguyen AK, Reichart D, Scott PA, Jenn A, Liu-Bryan R, Glass CK, Neels JG, Olefsky JM (2007) A subpopulation of macrophages infiltrates hypertrophic adipose tissue and is activated by free fatty acids via Toll-like receptors 2 and 4 and JNK-dependent pathways. J Biol Chem 282: 35279-35292
28. Nishimura S, Manabe I, Nagasaki M, Eto K, Yamashita H, Ohsugi M, Otsu M, Hara K, Ueki K, Sugiura S, et al (2009) CD8+ effector T cells contribute to macrophage recruitment and adipose tissue inflammation in obesity. Nat Med 15: 914-920
29. Niu W, Huang C, Nawaz Z, Levy M, Somwar R, Li D, Bilan PJ, Klip A (2003) Maturation of the regulation of GLUT4 activity by p38 MAPK during L6 cell myogenesis. J Biol Chem 278: 17953-17962
30. Nolsoe RL, Hamid YH, Pociot F, Paulsen S, Andersen KM, Borch-Johnsen K, Drivsholm T, Hansen T, Pedersen O, Mandrup-Poulsen T (2006) Association of a microsatellite in FASL to type II diabetes and of the FAS-670G>A genotype to insulin resistance. Genes Immun 7: 316-321
31. Oh DY, Morinaga H, Talukdar S, Bae EJ, Olefsky JM (2012) Increased macrophage migration into adipose tissue in obese mice. Diabete 61: 346-354
32. Olefsky JM, Glass CK (2010) Macrophages, inflammation, and insulin resistance. Annu Rev Physiol 72: 219-246
33. Park DR, Thomsen AR, Frevert CW, Pham U, Skerrett SJ, Kiener PA, Liles WC (2003) Fas (CD95) induces proinflammatory cytokine responses by human monocytes and monocyte-derived macrophages. J Immunol 170: 6209-6216
34. Peter ME, Budd RC, Desbarats J, Hedrick SM, Hueber AO, Newell MK, Owen LB, Pope RM, Tschopp J, Wajant H, et al (2007) The CD95 receptor: apoptosis revisited. Cell 129: 447-450
35. Plomgaard P, Bouzakri K, Krogh-Madsen R, Mittendorfer B, Zierath JR, Pedersen BK (2005) Tumor necrosis factor-alpha induces skeletal muscle insulin resistance in healthy human subjects via inhibition of Akt substrate 160 phosphorylation. Diabetes 54: 2939-2945
36. Qiu W, Wu B, Wang X, Buchanan ME, Regueiro MD, Hartman DJ, Schoen RE, Yu J, Zhang L (2011) PUMA-mediated intestinal epithelial apoptosis contributes to ulcerative colitis in humans and mice. J Clin Invest 121: 1722-1732
37. Rudich A, Konrad D, Török D, Ben-Romano R, Huang C, Niu W, Garg RR, Wijesekara N, Germinario RJ, Bilan PJ, et al (2003) Indinavir uncovers different contributions of GLUT4 and GLUT1 towards glucose uptake in muscle and fat cells and tissues. Diabetologia 46: 649-658
38. Rytka JM, Wueest S, Schoenle EJ, Konrad D (2011) The portal theory supported by venous drainage-selective fat transplantation. Diabetes 60: 56-63
39. Saberi M, Bjelica D, Schenk S, Imamura T, Bandyopadhyay G, Li P, Vargeese C, Wang W, Bowman K, Zhang Y, et al (2009a) Novel liver-specific TORC2 siRNA corrects hyperglycemia in rodent models of type 2 diabetes. Am J Physiol Endocrinol Metab 297: E1137-E1146
40. Saberi M, Woods NB, de Luca C, Schenk S, Lu JC, Bandyopadhyay G, Verma IM, Olefsky JM (2009b) Hematopoietic cell-specific deletion of toll-like receptor 4 ameliorates hepatic and adipose tissue insulin resistance in high-fat-fed mice. Cell Metab 10: 419-429
41. Samokhvalov V, Bilan PJ, Schertzer JD, Antonescu CN, Klip A (2009) Palmitate- and lipopolysaccharide-activated macrophages evoke contrasting insulin responses in muscle cells. Am J Physiol Endocrinol Metab 296: E37-E46
42. Schaub FJ, Liles WC, Ferri N, Sayson K, Seifert RA, Bowen-Pope DF (2003) Fas and Fas-associated death domain protein regulate monocyte chemoattractant protein-1 expression by human smooth muscle cells through caspase- and calpain-dependent release of interleukin-1alpha. Circ Res 93: 515-522
43. Schumann DM, Maedler K, Franklin I, Konrad D, Storling J, Boni-Schnetzler M, Gjinovci A, Kurrer MO, Gauthier BR, Bosco D, et al (2007) The Fas pathway is involved in pancreatic beta cell secretory function. Proc Natl Acad Sci USA 104: 2861-2866
44. Shi H, Kokoeva MV, Inouye K, Tzameli I, Yin H, Flier JS (2006) TLR4 links innate immunity and fatty acid-induced insulin resistance. J Clin Invest 116: 3015-3025
45. Stranges PB, Watson J, Cooper CJ, Choisy-Rossi CM, Stonebraker AC, Beighton RA, Hartig H, Sundberg JP, Servick S, Kaufmann G, et al (2007) Elimination of antigen-presenting cells and autoreactive T cells by Fas contributes to prevention of autoimmunity. Immunit 26: 629-641
46. Strissel KJ, Stancheva Z, Miyoshi H, Perfield JW II, DeFuria J, Jick Z, Greenberg AS, Obin MS (2007) Adipocyte death, adipose tissue remodeling, and obesity complications. Diabetes 56: 2910-2918
47. Wajant H, Pfizenmaier K, Scheurich P (2003) Non-apoptotic Fas signaling. Cytokine Growth Factor Rev 14: 53-66
48. Wang F, Lu Z, Hawkes M, Yang H, Kain KC, Liles WC (2010) Fas (CD95) induces rapid, TLR4/IRAK4-dependent release of pro-inflammatory HMGB1 from macrophages. J Inflamm (Lond) 7: 30
49. Weisberg SP, McCann D, Desai M, Rosenbaum M, Leibel RL, Ferrante AW Jr (2003) Obesity is associated with macrophage accumulation in adipose tissue. J Clin Invest 112: 1796-1808
50. Winer DA, Winer S, Shen L, Wadia PP, Yantha J, Paltser G, Tsui H, Wu P, Davidson MG, Alonso MN, et al (2011) B cells promote insulin resistance through modulation of T cells and production of pathogenic IgG antibodies. Nat Med 17: 610-617
51. Winer S, Chan Y, Paltser G, Truong D, Tsui H, Bahrami J, Dorfman R, Wang Y, Zielenski J, Mastronardi F, et al (2009) Normalization of obesity-associated insulin resistance through immunotherapy. Nat Med 15: 921-929
52. Wueest S, Rapold RA, Schoenle EJ, Konrad D (2010a) Fas activation in adipocytes impairs insulin-stimulated glucose uptake by reducing Akt. FEBS Lett 584: 4187-4192
53. Wueest S, Rapold RA, Schumann DM, Rytka JM, Schildknecht A, Nov O, Chervonsky AV, Rudich A, Schoenle EJ, Donath MY, et al (2010b) Deletion of Fas in adipocytes relieves adipose tissue inflammation and hepatic manifestations of obesity in mice. J Clin Inves 120: 191-202
54. Xu H, Barnes GT, Yang Q, Tan G, Yang D, Chou CJ, Sole J, Nichols A, Ross JS, Tartaglia LA, et al (2003) Chronic inflammation in fat plays a crucial role in the development of obesity-related insulin resistance. J Clin Invest 112: 1821-1830
55. Yuan M, Konstantopoulos N, Lee J, Hansen L, Li ZW, Karin M, Shoelson SE (2001) Reversal of obesity- and diet-induced insulin resistance with salicylates or targeted disruption of Ikkbeta. Science 293: 1673-1677