Interaction of differentiated human adipocytes with macrophages leads to trogocytosis and selective IL-6 secretion

Cell Death and Disease

Volumn 6, Issue 1, 2015, Pages

  Sarvari A K ^a   Doan Xuan, Q M ^a   Bacso Z ^a   Csomos I ^a   Balajthy, Z ^a   Fesus L ^a  

^a UNIVERSITY OF DEBRECEN   (Hungary)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1BETA; INTERLEUKIN 6; INTERLEUKIN 8; LIPOPOLYSACCHARIDE; MESSENGER RNA; MONOCYTE CHEMOTACTIC PROTEIN 1; TUMOR NECROSIS FACTOR ALPHA; AUTACOID; BREFELDIN A;

ADIPOCYTE; ADIPOSE TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL FUNCTION; CELL INTERACTION; CONTROLLED STUDY; CYTOKINE RELEASE; ENDOPLASMIC RETICULUM; EX VIVO STUDY; FLOW CYTOMETRY; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; HUMAN TISSUE; IN VITRO STUDY; LASER SCANNING CYTOMETRY; LIMIT OF DETECTION; MACROPHAGE; MESENCHYMAL STEM CELL; PHAGOCYTOSIS; PRIORITY JOURNAL; PROADIPOCYTE; PROTEIN FUNCTION; PROTEIN SYNTHESIS; SIGNAL TRANSDUCTION; TIME LAPSE IMAGING; TROGOCYTOSIS; CELL COMMUNICATION; COCULTURE; CYTOLOGY; DRUG EFFECTS; GENE EXPRESSION REGULATION; METABOLISM; SECRETION (PROCESS);

ADIPOCYTES; BREFELDIN A; CELL COMMUNICATION; CELL DIFFERENTIATION; COCULTURE TECHNIQUES; GENE EXPRESSION REGULATION; HUMANS; INFLAMMATION MEDIATORS; INTERLEUKIN-6; LIPOPOLYSACCHARIDES; MACROPHAGES; NF-KAPPA B; PHAGOCYTOSIS;

EID: 84927637590     PISSN: None     EISSN: 20414889     Source Type: Journal    
DOI: 10.1038/cddis.2014.579     Document Type: Article

References (45)

1. Shoelson SE, Herrero L, Naaz A. Obesity, inflammation, and insulin resistance. Gastroenterology 2007; 132: 2169-2180.
2. Wood IS, Wang B, Trayhurn P. IL-33 a recently identified interleukin-1 gene family member, is expressed in human adipocytes. Biochem Biophys Res Commun 2009; 384: 105-109.
3. Spalding KL, Arner E, Westermark PO, Bernard S, Buchholz B a, Bergmann O et al. Dynamics of fat cell turnover in humans. Nature 2008; 453: 783-787.
4. Duvall E, Wyllie a H, Morris RG. Macrophage recognition of cells undergoing programmed cell death (apoptosis). Immunology 1985; 56: 351-358.
5. Keuper M, Blüher M, Schön MR, Möller P, Dzyakanchuk A, Amrein K et al. An inflammatory micro-environment promotes human adipocyte apoptosis. Mol Cell Endocrinol 2011; 339: 105-113.
6. Kerr JFR, Wyllie AH, Currie AR. Apoptosis: a basic biological phenomenon with wide -ranging implications in tissue kinetics. Br J Cancer 1972; 26: 239-257.
7. Cinti S, Mitchell G, Barbatelli G, Murano I, Ceresi E, Faloia E et al. Adipocyte death defines macrophage localization and function in adipose tissue of obese mice and humans. J Lipid Res 2005; 46: 2347-2355.
8. Weisberg SP, Mccann D, Desai M, Rosenbaum M, Leibel RL, Ferrante AW. Obesity is associated with macrophage accumulation. J Clin Invest 2003; 112: 1796-1808.
9. 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.
10. Ortega E, Victoria M De, Xu X, Koska J, Francisco AM, Scalise M et al. Macrophage Content in Subcutaneous Adipose Tissue. Diabetes 2009; 58: 385-393.
11. Kosteli A, Sugaru E, Haemmerle G, Martin JF, Lei J, Zechner R et al. Weight loss and lipolysis promote a dynamic immune response in murine adipose tissue. J Clin Invest 2010; 120: 3466-3479.
12. Keuper M, Dzyakanchuk A, Amrein KE, Wabitsch M, Fischer-Posovszky P. THP-1 Macrophages and SGBS Adipocytes - A New Human in vitro Model System of Inflamed Adipose Tissue. Front Endocrinol (Lausanne) 2011; 2: 89.
13. De Boer A a, Monk JM, Robinson LE. Docosahexaenoic acid decreases pro-inflammatory mediators in an in vitro murine adipocyte macrophage co-culture model. PLoS One 2014; 9: e85037.
14. Xie L, Ortega MT, Mora S, Chapes SK. Interactive changes between macrophages and adipocytes. Clin Vaccine Immunol 2010; 17: 651-659.
15. Lumeng CN, Deyoung SM, Bodzin JL, Saltiel AR. Increased inflammatory properties of adipose tissue macrophages recruited during diet-induced obesity. Diabetes 2007; 56: 16-23.
16. Hill A a, Reid Bolus W, Hasty AH. A decade of progress in adipose tissue macrophage biology. Immunol Rev 2014; 262: 134-152.
17. Mantovani A, Sica A, Sozzani S, Allavena P, Vecchi A, Locati M. The chemokine system in diverse forms of macrophage activation and polarization. Trends Immunol 2004; 25: 677-686.
18. Savill J, Fadok V. Corpse clearance defines the meaning of cell death. Nature 2000; 407: 784-788.
19. Nancy G. Nibbled to death. Nature 2014; 508: 7-8.
20. Joly E, Hudrisier D. What is trogocytosis and what is its purpose? Nat Immunol 2003; 4: 815.
21. Doan-xuan QM, Sarvari AK, Fischer-posovszky P, Wabitsch M, Balajthy Z, Fesus L et al. High content analysis of differentiation and cell death in human adipocytes. Cytom A 2013; 83: 933-943.
22. Toda S, Hanayama R, Nagata S. Two-step engulfment of apoptotic cells. Mol Cell Biol 2012; 32: 118-125.
23. Mukundan L, Odegaard JI, Morel CR, Heredia JE, Mwangi JW, Ricardo-Gonzalez RR et al. PPAR-delta senses and orchestrates clearance of apoptotic cells to promote tolerance. Nat Med 2009; 15: 1266-1272.
24. Henegar C, Tordjman J, Achard V, Lacasa D, Cremer I, Guerre-Millo M et al. Adipose tissue transcriptomic signature highlights the pathological relevance of extracellular matrix in human obesity. Genome Biol 2008; 9: R14.
25. Khalifeh-Soltani A, McKleroy W, Sakuma S, Cheung YY, Tharp K, Qiu Y et al. Mfge8 promotes obesity by mediating the uptake of dietary fats and serum fatty acids. Nat Med 2014; 20: 175-183.
26. A-Gonzalez N, Bensinger SJ, Hong C, Beceiro S, Bradley MN, Zelcer N et al. Apoptotic cells promote their own clearance and immune tolerance through activation of the nuclear receptor LXR. Immunity 2009; 31: 245-258.
27. Mohamed-Ali V, Goodrick S, Rawesh a, Katz DR, Miles JM, Yudkin JS et al. Subcutaneous adipose tissue releases interleukin-6, but not tumor necrosis factor-alpha, in vivo. J Clin Endocrinol Metab 1997; 82: 4196-4200.
28. Kranendonk MEG, Visseren FLJ, van Balkom BWM, Nolte-'t Hoen ENM, van Herwaarden J a, de Jager W et al. Human adipocyte extracellular vesicles in reciprocal signaling between adipocytes and macrophages. Obesity (Silver Spring) 2014; 22: 1296-1308.
29. Phoonsawat W, Aoki-Yoshida A, Tsuruta T, Sonoyama K. Adiponectin is partially associated with exosomes in mouse serum. Biochem Biophys Res Commun 2014; 448: 261-266.
30. Deng Z, Poliakov A, Hardy RW, Clements R, Liu C, Liu Y et al. Adipose tissue exosome-like vesicles mediate activation of macrophage-induced insulin resistance. Diabetes 2009; 58: 2498-2505.
31. Lee JY, Sohn KH, Rhee SH, Hwang D. Saturated fatty acids, but not unsaturated fatty acids, induce the expression of cyclooxygenase-2 mediated through Toll-like receptor 4. J Biol Chem 2001; 276: 16683-16689.
32. Alexopoulou L, Thomas V, Schnare M, Lobet Y, Anguita J, Schoen RT et al. Hyporesponsiveness to vaccination with Borrelia burgdorferi OspA in humans and in TLR1- and TLR2-deficient mice. Nat Med 2002; 8: 878-884.
33. Takeuchi O, Sato S, Horiuchi T, Hoshino K, Takeda K, Dong Z et al. Cutting edge: role of Tolllike receptor 1 in mediating immune response to microbial lipoproteins. J Immunol 2002; 169: 10-14.
34. Lumeng CN, Bodzin JL, Saltiel AR. Obesity induces a phenotypic switch in adipose tissue macrophage polarization. J Clin Invest 2007; 117: 175-184.
35. Lee JY, Plakidas A, Lee WH, Heikkinen A, Chanmugam P, Bray G et al. Differential modulation of Toll-like receptors by fatty acids: preferential inhibition by n-3 polyunsaturated fatty acids. J Lipid Res 2003; 44: 479-486.
36. Suganami T, Tanimoto-Koyama K, Nishida J, Itoh M, Yuan X, Mizuarai S et al. Role of the Toll-like receptor 4/NF-kappaB pathway in saturated fatty acid-induced inflammatory changes in the interaction between adipocytes and macrophages. Arterioscler Thromb Vasc Biol 2007; 27: 84-91.
37. Tartaglia L a, Dembski M, Weng X, Deng N, Culpepper J, Devos R et al. Identification and expression cloning of a leptin receptor, OB-R. Cell 1995; 83: 1263-1271.
38. Tilg H, Trehu E, Atkins MB, Dinarello C a, Mier JW. Interleukin-6 (IL-6) as an antiinflammatory cytokine: induction of circulating IL-1 receptor antagonist and soluble tumor necrosis factor receptor p55. Blood 1994; 83: 113-118.
39. Mauer J, Chaurasia B, Goldau J, Vogt MC, Ruud J, Nguyen KD et al. Signaling by IL-6 promotes alternative activation of macrophages to limit endotoxemia and obesity-associated resistance to insulin. Nat Immunol 2014; 15: 423-430.
40. Aderka DAN, Le J, Vilcek J. IL-6 inhibits lipopolysacharide-induced tumor necrosis factor production in cultured human monocyte, U937 cells, and in mice. J Immunol 1989; 143: 3517-3523.
41. Fischer-Posovszky P, Newell FS, Wabitsch M, Tornqvist HE. Human SGBS cells - a unique tool for studies of human fat cell biology. Obes Facts 2008; 1: 184-189.
42. Sárvári AK, Veréb Z, Uray IP, Fésüs L, Balajthy Z. Atypical antipsychotics induce both proinflammatory and adipogenic gene expression in human adipocytes in vitro. Biochem Biophys Res Commun 2014; 450: 1383-1389.
43. Schneider CA, Rasband WS, Eliceiri KW. HISTORICAL commentary NIH Image to ImageJ : 225 years of image analysis 2012; 9: 671-676.
44. Carpenter AE, Jones TR, Lamprecht MR, Clarke C, Kang IH, Friman O et al. CellProfiler: image analysis software for identifying and quantifying cell phenotypes. Genome Biol 2006; 7: R100.
45. Kamentsky L, Jones TR, Fraser A, Bray M-A, Logan DJ, Madden KL et al. Improved structure, function and compatibility for CellProfiler: modular high-throughput image analysis software. Bioinformatics 2011; 27: 1179-1180.