Adipocytes modulate the phenotype of human macrophages through secreted lipids

Journal of Immunology

Volumn 191, Issue 3, 2013, Pages 1356-1363

  Klein Wieringa, Inge R ^a   Andersen, Stefan N ^a   Kwekkeboom, Joanneke C ^a   Giera, Martin ^a   De Lange Brokaar, Badelog J E ^a   Van Osch, Gerjo J V M ^b   Zuurmond, Anne Marie ^c   Stojanovic Susulic, Vedrana ^d   Nelissen, Rob G H H ^a   Pijl, Hanno ^a   Huizinga, Tom W J ^a   Kloppenburg, Margreet ^a   Toes, Rene E M ^a   Ioan Facsinay, Andreea ^a  

^a LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^b ERASMUS MEDICAL CENTER   (Netherlands)

^c Erasmus University ^*

^d JANSSEN RESEARCH AND DEVELOPMENT   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

ADIPOCYTOKINE; CYTOKINE; INTERLEUKIN 12P40; LINOLEIC ACID; LIPID; LIPOPOLYSACCHARIDE; OLEIC ACID; PROSTAGLANDIN E2; PROTEIN; TUMOR NECROSIS FACTOR ALPHA;

ADIPOCYTE; ARTICLE; BODY MASS; CELL INTERACTION; CONCENTRATION RESPONSE; CONTROLLED STUDY; CORRELATION ANALYSIS; CULTURE MEDIUM; CYTOKINE PRODUCTION; CYTOKINE RELEASE; DONOR; HUMAN; HUMAN CELL; MACROPHAGE; OBESITY; PHENOTYPE; PRIORITY JOURNAL;

ADIPOCYTES; ADIPOSE TISSUE; BODY MASS INDEX; CELL COMMUNICATION; CULTURE MEDIA, CONDITIONED; DINOPROSTONE; HUMANS; INTERLEUKIN-12 SUBUNIT P40; LINOLEIC ACID; LIPIDS; LIPOPOLYSACCHARIDES; MACROPHAGES; OBESITY; OLEIC ACID; PHENOTYPE; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84880676488     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1203074     Document Type: Article

References (56)

1. Dandona, P., A. Aljada, and A. Bandyopadhyay. 2004. Inflammation: the link between insulin resistance, obesity and diabetes. Trends Immunol. 25: 4-7.
2. Hotamisligil, G. S. 2006. Inflammation and metabolic disorders. Nature 444: 860-867.
3. Lolméde, K., C. Duffaut, A. Zakaroff-Girard, and A. Bouloumié. 2011. Immune cells in adipose tissue: key players in metabolic disorders. Diabetes Metab. 37: 283-290.
4. Wozniak, S. E., L. L. Gee, M. S. Wachtel, and E. E. Frezza. 2009. Adipose tissue: the new endocrine organ? A review article. Dig. Dis. Sci. 54: 1847-1856.
5. Anderson, E. K., D. A. Gutierrez, and A. H. Hasty. 2010. Adipose tissue recruitment of leukocytes. Curr. Opin. Lipidol. 21: 172-177.
6. Morris, D. L., K. Singer, and C. N. Lumeng. 2011. Adipose tissue macrophages: phenotypic plasticity and diversity in lean and obese states. Curr. Opin. Clin. Nutr. Metab. Care 14: 341-346.
7. Gordon, S. 2003. Alternative activation of macrophages. Nat. Rev. Immunol. 3: 23-35.
8. Mantovani, A., A. Sica, S. Sozzani, P. Allavena, A. Vecchi, and M. Locati. 2004. The chemokine system in diverse forms of macrophage activation and polarization. Trends Immunol. 25: 677-686.
9. Cinti, S., G. Mitchell, G. Barbatelli, I. Murano, E. Ceresi, E. Faloia, S. Wang, M. Fortier, A. S. Greenberg, and M. S. Obin. 2005. Adipocyte death defines macrophage localization and function in adipose tissue of obese mice and humans. J. Lipid Res. 46: 2347-2355.
10. Lumeng, C. N., J. B. DelProposto, D. J. Westcott, and A. R. Saltiel. 2008. Phenotypic switching of adipose tissue macrophages with obesity is generated by spatiotemporal differences in macrophage subtypes. Diabetes 57: 3239-3246.
11. Lumeng, C. N., J. L. Bodzin, and A. R. Saltiel. 2007. Obesity induces a phenotypic switch in adipose tissue macrophage polarization. J. Clin. Invest. 117: 175-184.
12. Bourlier, V., A. Zakaroff-Girard, A. Miranville, S. De Barros, M. Maumus, C. Sengenes, J. Galitzky, M. Lafontan, F. Karpe, K. N. Frayn, and A. Bouloumié. 2008. Remodeling phenotype of human subcutaneous adipose tissue macrophages. Circulation 117: 806-815.
13. Zeyda, M., D. Farmer, J. Todoric, O. Aszmann, M. Speiser, G. Gyö ri, G. J. Zlabinger, and T. M. Stulnig. 2007. Human adipose tissue macrophages are of an anti-inflammatory phenotype but capable of excessive pro-inflammatory mediator production. Int. J. Obes. 31: 1420-1428.
14. Wentworth, J. M., G. Naselli, W. A. Brown, L. Doyle, B. Phipson, G. K. Smyth, M. Wabitsch, P. E. O'Brien, and L. C. Harrison. 2010. Pro-inflammatory CD11c +CD206+ adipose tissue macrophages are associated with insulin resistance in human obesity. Diabetes 59: 1648-1656.
15. Kanda, H., S. Tateya, Y. Tamori, K. Kotani, K. Hiasa, R. Kitazawa, S. Kitazawa, H. Miyachi, S. Maeda, K. Egashira, and M. Kasuga. 2006. MCP-1 contributes to macrophage infiltration into adipose tissue, insulin resistance, and hepatic steatosis in obesity. J. Clin. Invest. 116: 1494-1505.
16. Kamei, N., K. Tobe, R. Suzuki, M. Ohsugi, T.Watanabe, N. Kubota, N. Ohtsuka-Kowatari, K. Kumagai, K. Sakamoto, M. Kobayashi, et al. 2006. Overexpression of monocyte chemoattractant protein-1 in adipose tissues causes macrophage recruitment and insulin resistance. J. Biol. Chem. 281: 26602-26614.
17. Sartipy, P., and D. J. Loskutoff. 2003. Monocyte chemoattractant protein 1 in obesity and insulin resistance. Proc. Natl. Acad. Sci. USA 100: 7265-7270.
18. Sun, K., C. M. Kusminski, and P. E. Scherer. 2011. Adipose tissue remodeling and obesity. J. Clin. Invest. 121: 2094-2101.
19. Suganami, T., J. Nishida, and Y. Ogawa. 2005. A paracrine loop between adipocytes and macrophages aggravates inflammatory changes: role of free fatty acids and tumor necrosis factor alpha. Arterioscler. Thromb. Vasc. Biol. 25: 2062-2068.
20. Keuper, M., A. Dzyakanchuk, K. E. Amrein, M. Wabitsch, and P. Fischer-Posovszky. 2011. THP-1 macrophages and SGBS adipocytes: a new human in vitro model system of inflamed adipose tissue. Front. Endocrinol. 2: 89.
21. Kang, K., S. M. Reilly, V. Karabacak, M. R. Gangl, K. Fitzgerald, B. Hatano, and C. H. Lee. 2008. Adipocyte-derived Th2 cytokines and myeloid PPARdelta regulate macrophage polarization and insulin sensitivity. Cell Metab. 7: 485-495.
22. Lovren, F., Y. Pan, A. Quan, P. E. Szmitko, K. K. Singh, P. C. Shukla, M. Gupta, L. Chan, M. Al-Omran, H. Teoh, and S. Verma. 2010. Adiponectin primes human monocytes into alternative anti-inflammatory M2 macrophages. Am. J. Physiol. Heart Circ. Physiol. 299: H656-H663.
23. Ohashi, K., J. L. Parker, N. Ouchi, A. Higuchi, J. A. Vita, N. Gokce, A. A. Pedersen, C. Kalthoff, S. Tullin, A. Sams, et al. 2010. Adiponectin promotes macrophage polarization toward an anti-inflammatory phenotype. J. Biol. Chem. 285: 6153-6160.
24. Vaughan, T., and L. Li. 2010. Molecular mechanism underlying the inflammatory complication of leptin in macrophages. Mol. Immunol. 47: 2515-2518.
25. Santos-Alvarez, J., R. Goberna, and V. Sánchez-Margalet. 1999. Human leptin stimulates proliferation and activation of human circulating monocytes. Cell. Immunol. 194: 6-11.
26. Klein-Wieringa, I. R., M. Kloppenburg, Y. M. Bastiaansen-Jenniskens, E. Yusuf J. C. Kwekkeboom, H. El-Bannoudi, R. G. Nelissen, A. Zuurmond, V. Stojanovic-Susulic, G. J. Van Osch, et al. 2011. The infrapatellar fat pad of patients with osteoarthritis has an inflammatory phenotype. Ann. Rheum. Dis. 70: 851-857.
27. Giera, M., A. Ioan-Facsinay, R. Toes, F. Gao, J. Dalli, A. M. Deelder, C. N. Serhan, and O. A. Mayboroda. 2012. Lipid and lipid mediator profiling of human synovial fluid in rheumatoid arthritis patients by means of LC-MS/MS. Biochim. Biophys. Acta 1821: 1415-1424.
28. Yang, R., N. Chiang, S. F. Oh, and C. N. Serhan. 2011. Metabolomics-lipidomics of eicosanoids and docosanoids generated by phagocytes. Curr. Protoc. Immunol. Chapter 14: Unit 14.26.
29. Serhan, C. N., N. Chiang, and T. E. Van Dyke. 2008. Resolving inflammation: dual anti-inflammatory and pro-resolution lipid mediators. Nat. Rev. Immunol. 8: 349-361.
30. van der Pouw Kraan, T. C., L. C. Boeije, R. J. Smeenk, J. Wijdenes, and L. A. Aarden. 1995. Prostaglandin-E2 is a potent inhibitor of human interleukin 12 production. J. Exp. Med. 181: 775-779.
31. Handel-Fernandez, M. E., X. Cheng, L. M. Herbert, and D. M. Lopez. 1997. Down-regulation of IL-12, not a shift from a T helper-1 to a T helper-2 phenotype, is responsible for impaired IFN-gamma production in mammary tumorbearing mice. J. Immunol. 158: 280-286.
32. Chinen, T., K. Komai, G. Muto, R. Morita, N. Inoue, H. Yoshida, T. Sekiya, R. Yoshida, K. Nakamura, R. Takayanagi, and A. Yoshimura. 2011. Prostaglandin E2 and SOCS1 have a role in intestinal immune tolerance. Nat. Commun. 2: 190.
33. Shiraishi, H., H. Yoshida, K. Saeki, Y. Miura, S. Watanabe, T. Ishizaki, M. Hashimoto, G. Takaesu, T. Kobayashi, and A. Yoshimura. 2008. Prostaglandin E2 is a major soluble factor produced by stromal cells for preventing inflammatory cytokine production from dendritic cells. Int. Immunol. 20: 1219-1229.
34. Haversen, L., K. N. Danielsson, L. Fogelstrand, and O.Wiklund. 2009. Induction of proinflammatory cytokines by long-chain saturated fatty acids in human macrophages. Atherosclerosis 202: 382-393.
35. Wang,S., D.Wu, S. Lamon-Fava, N. R.Matthan,K. L. Honda, andA. H. Lichtenstein. 2009. In vitro fatty acid enrichment of macrophages alters inflammatory response and net cholesterol accumulation. Br. J. Nutr. 102: 497-501.
36. Lee, J. Y., K. H. Sohn, S. H. Rhee, and D. Hwang. 2001. Saturated fatty acids, but not unsaturated fatty acids, induce the expression of cyclooxygenase-2 mediated through Toll-like receptor 4. J. Biol. Chem. 276: 16683-16689.
37. de Lima-Salgado, T. M., T. C. Alba-Loureiro, C. S. do Nascimento, M. T. Nunes, and R. Curi. 2011. Molecular mechanisms by which saturated fatty acids modulate TNF-A expression in mouse macrophage lineage. Cell Biochem. Biophys. 59: 89-97.
38. Cao, H., K. Gerhold, J. R. Mayers, M. M. Wiest, S. M. Watkins, and G. S. Hotamisligil. 2008. Identification of a lipokine, a lipid hormone linking adipose tissue to systemic metabolism. Cell 134: 933-944.
39. Strissel, K. J., J. DeFuria, M. E. Shaul, G. Bennett, A. S. Greenberg, and M. S. Obin. 2010. T-cell recruitment and Th1 polarization in adipose tissue during diet-induced obesity in C57BL/6 mice. Obesity 18: 1918-1925.
40. Mestas, J., and C. C. Hughes. 2004. Of mice and not men: differences between mouse and human immunology. J. Immunol. 172: 2731-2738.
41. Kosteli, A., E. Sugaru, G. Haemmerle, J. F. Martin, J. Lei, R. Zechner, and A. W. Ferrante, Jr. 2010. Weight loss and lipolysis promote a dynamic immune response in murine adipose tissue. J. Clin. Invest. 120: 3466-3479.
42. Schuetze, N., S. Schoeneberger, U. Mueller, M. A. Freudenberg, G. Alber, and R. K. Straubinger. 2005. IL-12 family members: differential kinetics of their TLR4-mediated induction by Salmonella enteritidis and the impact of IL-10 in bone marrow-derived macrophages. Int. Immunol. 17: 649-659.
43. D'Andrea, A., M. Rengaraju, N. M. Valiante, J. Chehimi, M. Kubin, M. Aste, S. H. Chan, M. Kobayashi, D. Young, E. Nickbarg, et al. 1992. Production of natural killer cell stimulatory factor (interleukin 12) by peripheral blood mononuclear cells. J. Exp. Med. 176: 1387-1398.
44. Cooper, A. M., and S. A. Khader. 2007. IL-12p40: an inherently agonistic cytokine. Trends Immunol. 28: 33-38.
45. Mikols, C. L., L. Yan, J. Y. Norris, T. D. Russell, A. P. Khalifah, R. R. Hachem, M. M. Chakinala, R. D. Yusen, M. Castro, E. Kuo, et al. 2006. IL-12 p80 is an innate epithelial cell effector that mediates chronic allograft dysfunction. Am. J. Respir. Crit. Care Med. 174: 461-470.
46. Walter, M. J., N. Kajiwara, P. Karanja, M. Castro, and M. J. Holtzman. 2001. Interleukin 12 p40 production by barrier epithelial cells during airway inflammation. J. Exp. Med. 193: 339-351.
47. Stallmach, A., T. Marth, B. Weiss, B. M. Wittig, A. Hombach, C. Schmidt, M. Neurath, M. Zeitz, S. Zeuzem, and H. Abken. 2004. An interleukin 12 p40-IgG2b fusion protein abrogates T cell mediated inflammation: anti-inflammatory activity in Crohn's disease and experimental colitis in vivo. Gut 53: 339-345.
48. Nishimura, S., I. Manabe, M. Nagasaki, K. Eto, H. Yamashita, M. Ohsugi, M. Otsu, K. Hara, K. Ueki, S. Sugiura, et al. 2009. CD8+ effector T cells contribute to macrophage recruitment and adipose tissue inflammation in obesity. Nat. Med. 15: 914-920.
49. Gillessen, S., D. Carvajal, P. Ling, F. J. Podlaski, D. L. Stremlo, P. C. Familletti, U. Gubler, D. H. Presky, A. S. Stern, and M. K. Gately. 1995. Mouse interleukin-12 (IL-12) p40 homodimer: a potent IL-12 antagonist. Eur. J. Immunol. 25: 200-206.
50. Ling, P., M. K. Gately, U. Gubler, A. S. Stern, P. Lin, K. Hollfelder, C. Su, Y. C. Pan, and J. Hakimi. 1995. Human IL-12 p40 homodimer binds to the IL-12 receptor but does not mediate biologic activity. J. Immunol. 154: 116-127.
51. Wegner, M., H. Winiarska, T. Bobkiewicz-Kozlowska, and M. Dworacka. 2008. IL-12 serum levels in patients with type 2 diabetes treated with sulphonylureas. Cytokine 42: 312-316.
52. Winkler, G., O. Dworak, F. Salamon, D. Salamon, G. Speer, and K. Cseh. 1998. Increased interleukin-12 plasma concentrations in both, insulin-dependent and non-insulin-dependent diabetes mellitus. Diabetologia 41: 488.
53. Prieur, X., C. Y. Mok, V. R. Velagapudi, V. Núnez, L. Fuentes, D. Montaner, K. Ishikawa, A. Camacho, N. Barbarroja, S. O'Rahilly, et al. 2011. Differential lipid partitioning between adipocytes and tissue macrophages modulates macrophage lipotoxicity and M2/M1 polarization in obese mice. Diabetes 60: 797-809.
54. Fain, J. N., A. K. Madan, M. L. Hiler, P. Cheema, and S. W. Bahouth. 2004. Comparison of the release of adipokines by adipose tissue, adipose tissue matrix, and adipocytes from visceral and subcutaneous abdominal adipose tissues of obese humans. Endocrinology 145: 2273-2282.
55. Clária, J., J. Dalli, S. Yacoubian, F. Gao, and C. N. Serhan. 2012. Resolvin D1 and resolvin D2 govern local inflammatory tone in obese fat. J. Immunol. 189: 2597-2605.
56. Hellmann, J., Y. Tang, M. Kosuri, A. Bhatnagar, and M. Spite. 2011. Resolvin D1 decreases adipose tissue macrophage accumulation and improves insulin sensitivity in obese-diabetic mice. FASEB J. 25: 2399-2407.