Depot-specific differences in inflammatory mediators and a role for NK cells and IFN-γ in inflammation in human adipose tissue

International Journal of Obesity

Volumn 33, Issue 9, 2009, Pages 978-990

  O'Rourke, R W ^a   Metcalf, M D ^a   White, A E ^a   Madala, A ^a   Winters, B R ^a   Maizlin, I I ^a   Jobe, B A ^b   Roberts, C T ^c,d   Slifka, M K ^e   Marks, D L ^c  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^b UNIVERSITY OF PITTSBURGH   (United States)

^c OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^d OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^e OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

Adipose tissue; IFN ; Inflammation; NK cells

Indexed keywords

AUTACOID; GAMMA INTERFERON; TUMOR NECROSIS FACTOR ALPHA;

ADIPOSE TISSUE; ARTICLE; BARIATRIC SURGERY; CELL FRACTIONATION; CONTROLLED STUDY; CYTOKINE RELEASE; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; FLOW CYTOMETRY; GENE EXPRESSION PROFILING; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOCYTOCHEMISTRY; IMMUNOMODULATION; IN VITRO STUDY; INTRAABDOMINAL FAT; LEUKOCYTOSIS; LYMPHOCYTE ACTIVATION; MACROPHAGE; NATURAL KILLER CELL; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SOFT TISSUE INFLAMMATION; SUBCUTANEOUS FAT; T LYMPHOCYTE; TRANSCRIPTION REGULATION; ADULT; GENE EXPRESSION REGULATION; GENETICS; IMMUNOHISTOCHEMISTRY; METABOLISM; OBESITY; PANNICULITIS;

ADULT; BARIATRIC SURGERY; FEMALE; GENE EXPRESSION REGULATION; HUMANS; IMMUNOHISTOCHEMISTRY; INFLAMMATION MEDIATORS; INTERFERON-GAMMA; INTRA-ABDOMINAL FAT; KILLER CELLS, NATURAL; OBESITY; PANNICULITIS; SUBCUTANEOUS FAT;

EID: 70349150518     PISSN: 03070565     EISSN: 14765497     Source Type: Journal    
DOI: 10.1038/ijo.2009.133     Document Type: Article

References (44)

1. Cancello R, Henegar C, Viguerie N, Taleb S, Poitou C, Rouault C et al. Reduction of macrophage infiltration and chemoattractant gene expression changes in white adipose tissue of morbidly obese subjects after surgery-induced weight loss. Diabetes 2005; 54 : 2277-2286.
2. Lumeng CN, Bodzin JL, Saltiel AR. Obesity induces a phenotypic switch in adipose tissue macrophage polarization. J Clin Invest 2007; 117: 175-184.
3. Weisberg SP, Hunter D, Huber R, Lemieux J, Slaymaker S, Vaddi K et al. CCR2 modulates inflammatory and metabolic effects of high-fat feeding. J Clin Invest 2005; 116: 115-124.
4. Kamei N, Tobe K, Suzuki R, Ohsugi M, Watanabe T, Kubota N et al. Over-expression of MCP-1 in adipose tissues causes macrophage recruitment and insulin resistance. J Biol Chem 2006; 281: 26602-26614.
5. Zeyda M, Farmer D, Todoric J, Aszmann O, Speiser M, Györi G et al. Human adipose tissue macrophages are of an anti-inflammatory phenotype but capable of excessive pro-inflammatory mediator production. Int J Obes (London) 2007; 31: 1420-1428.
6. Carey VJ, Walters EE, Colditz GA, Solomon CG, Willet WC, Rosner BA et al. Body fat distribution and risk of non-insulin-dependent diabetes mellitus in women. Nurses' Health Study. Am J Epidemiol 1997; 145: 614-619.
7. Kissebah AH, Vydelingum N, Murray R, Evans DJ, Hartz AJ, Kalkhoff RK et al. Relation of body fat distribution to metabolic complications of obesity. J Clin Endocrinol Metab 1982; 54: 254-260.
8. Gómez-Ambrosi J, Catalán V, Diez-Caballero A, Martinez-Cruz LA, Gil MJ, García-Foncillas J et al. Gene expression profile of omental adipose tissue in human obesity. FASEB J 2004; 18: 215-217.
9. Vohl MC, Sladek R, Robitaille J, Gurd S, Marceau P, Richard D et al. A survey of genes differentially expressed in subcutaneous and visceral adipose tissue in men. Obes Res 2004; 12: 1217-1222.
10. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001; 25: 402-408.
11. Roederer M. Spectral compensation for flow cytometry: visualization artifacts, limitations, and caveats. Cytometry 2001; 45: 194-205.
12. Mauri DN, Ebner R, Montgomery RI, Kochel KD, Cheung TC, Yu GL et al. LIGHT, a new member of the TNF superfamily, and lymphotoxin-alpha are ligands for herpesvirus entry mediator. Immunity 1998; 8: 21-30.
13. Kim WJ, Kang YJ, Koh EM, Ahn KS, Cha HS, Lee WH. LIGHT is involved in the pathogenesis of rheumatoid arthritis by inducing the expression of pro-inflammatory cytokines and MMP-9 in macrophages. Immunology 2005; 114: 272-279.
14. Wang J, Lo JC, Foster A, Yu P, Chen HM, Wang Y et al. The regulation of T-cell homeostasis and autoimmunity by T cell-derived LIGHT. J Clin Invest 2001; 108: 1771-1780.
15. Cohavy O, Zhou J, Granger SW, Ware CF, Targan SR. LIGHT expression by mucosal T cells may regulate IFN-g expression in the intestine. J Immunol 2004; 173: 251-258.
16. Zhai Y, Guo R, Hsu TL, Yu GL, Ni J, Kwon BS et al. LIGHT, a novel ligand for lymphotoxin beta receptor and TR2/HVEM induces apoptosis and suppresses in-vivo tumor formation via gene transfer. J Clin Invest 1998; 102: 1142-1151.
17. Willis D, Moore AR, Frederick R, Willoughby DA. Haem oxygenase: a novel target for the modulation of the inflammatory response. Nat Med 1996; 2: 87-90.
18. Platt JL, Nath KA. Haem oxygenase: protective gene or Trojan horse. Nat Med 1998; 4: 1364-1365.
19. Otterbein LE, Bach FH, Alam J, Soares M, Tao Lu H, Wysk M et al. Carbon monoxide has anti-inflammatory effects involving the mitogen-activated protein kinase pathway. Nat Med 2000; 6: 422-428.
20. Mantovani A, Sozzani S, Locati M, Allavena P, Sica A. Macrophage polarization: tumor-associated macrophages as a paradigm for polarized M2 mononuclear phagocytes. Trends Immunol 2002; 23: 549-555.
21. Fleetwood AJ, Lawrence T, Hamilton JA, Cook AD. GM-CSF and M-CSF-dependent macrophage phenotypes display differences in cytokine profiles and transcription factor activities: implications for CSF blockade in inflammation. J Immunol 2007; 178: 5245-5252.
22. Makino M, Maeda Y, Fukutomi Y, Mukai T. Contribution of GM-CSF on the enhancement of the T cell-stimulating activity of macrophages. Microbes Infect 2007; 9: 70-77.
23. Ganguly D, Paul K, Bagchi J, Rakshit S, Mandal L, Bandyopadhyay G et al. Granulocyte-macrophage colony-stimulating factor drives monocytes to CD14loCD83+DCSIGN interleukin-10-producing myeloid cells with differential effects on T-cell subsets. Immunology 2007; 121: 499-507.
24. Fried SK, Bunkin DA, Greenberg AS. Reciprocal expression of the TNF family receptor herpes virus entry mediator and its ligand LIGHT on activated T cells: LIGHT down-regulates its own receptor. J. Clin Endocrinol Metab 1998; 83: 847-850.
25. van Beek EA, Bakker AH, Kruyt PM, Hofker MH, Saris WH, Keijer J. Intra- and inter-individual variation in gene expression in human adipose tissue. Pflugers Arch 2007; 453: 851-861.
26. Hube F, Birgel M, Lee YM, Hauner H. Expression pattern of tumour necrosis factor receptors in subcutaneous and omental human adipose tissue: role of obesity and non-insulin-dependent diabetes mellitus. Eur J Clin Invest 1999; 29: 672-678.
27. Kintscher U, Hartge M, Hess K, Foryst-Ludwig A, Clemenz M, Wabitsch M et al. 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.
28. Wu H, Ghosh S, Perrard XD, Feng L, Garcia GE, Perrard JL et al. T-cell accumulation and regulated on activation, normal T cell expressed and secreted upregulation in adipose tissue in obesity. Circulation 2007; 115: 1029-1038.
29. Rocha VZ, Folco EJ, Sukhova G, Shimizu K, Gotsman I, Vernon AH et al. Interferon-gamma, a Th1 cytokine, regulates fat inflammation: a role for adaptive immunity in obesity. Circ Res 2008; 103: 467-476.
30. Permana PA, Menge C, Reaven PD. Macrophage-secreted factors induce adipocyte inflammation and insulin resistance. Biochem Biophys Res Commun 2006; 341: 507-514.
31. Xu H, Barnes GT, Yang Q, Tan G, Yang D, Chou CJ et al. Chronic inflammation in fat plays a crucial role in the development of obesity-related insulin resistance. J Clin Invest 2003; 112: 1821-1830.
32. Tamada K, Shimozaki K, Chapoval AI, Zhai Y, Su J, Chen SF et al. LIGHT, a TNF-like molecule, costimulates T cell proliferation and is required for dendritic cell-mediated allogeneic T cell response. J Immunol 2000; 164: 4105-4110.
33. Kosuge H, Suzuki J, Kakuta T, Haraguchi G, Koga N, Futamatsu H et al. Attenuation of graft arterial disease by manipulation of the LIGHT pathway. Arterioscler Thromb Vasc Biol 2004; 24: 1409-1415.
34. Scheu S, Alferink J, Pötzel T, Barchet W, Kalinke U, Pfeffer K. Targeted disruption of LIGHT causes defects in costimulatory T-cell activation and reveals cooperation with lymphotoxin beta in mesenteric lymph node genesis. J Exp Med 2002; 195: 1613-1624.
35. Morel Y, Schiano de Collela JM, Harrop J, Deen KC, Homes SD, Wattam TA et al. Reciprocal expression of the TNF family receptor herpes virus entry mediator and its ligand LIGHT on activated T cells: LIGHT down-regulates its own receptor. J Immunol 2000; 165: 4397-4404.
36. Fan Z, Yu P, Wang Y, Wang Y, Fu ML, Liu W et al. NK-cell activation by LIGHT triggers tumor-specific CD8+T-cell immunity to reject established tumors. Blood 2006; 107: 1342-1351.
37. Lee WH, Kim SH, Lee Y, Lee BB, Kwon B, Song H et al. Tumor necrosis factor receptor superfamily 14 is involved in atherogen-esis by inducing proinflammatory cytokines and matrix metallo-proteinases. Arterioscler Thromb Vasc Biol 2001; 21: 2004-2010. (Pubitemid 34219754)
38. Grage-Griebenow E, Flad HD, Ernst M. Heterogeneity of human peripheral blood monocyte subsets. J Leukocyte Biol 2001; 69: 11-20.
39. Gordon S, Taylor PR. Monocyte and macrophage heterogeneity. Nat Rev Immunol 2005; 5: 953-964.
40. Tchoukalova YD, Koutsari C, Karpyak MV, Votruba SB, Wendland E, Jensen MD. Subcutaneous adipocyte size and body fat distribution. Am J Clin Nutr 2008; 87: 56-63.
41. Klimcakova E, Moro C, Mazzucotelli A, Lolmède K, Viguerie N, Galitzky J et al. Profiling of adipokines secreted from human subcutaneous adipose tissue in response to PPAR agonists. Biochem Biophys Res Commun 2007; 358: 897-902.
42. Nishimura S, Manabe I, Nagasaki M, Hosoya Y, Yamashita H, Fujita H et al. Adipogenesis in obesity requires close interplay between differentiating adipocytes, stromal cells, and blood vessels. Diabetes 2007; 56: 1517-1526.
43. Bourlier V, Zakaroff-Girard A, Miranville A, De Barros S, Maumus M, Sengenes C et al. Remodeling phenotype of human subcutaneous adipose tissue macrophages. Circulation 2008; 117: 806-815.
44. Darwich L, Coma G, Peña R, Bellido R, Blanco EJ, Este JA et al. Secretion of interferon-gamma by human macrophages demonstrated at the single-cell level after costimulation with interleukin IL-12 plus IL-18. Immunology 2009; 126: 386-393.