Obesity induces a phenotypic switch in adipose tissue macrophage polarization

Journal of Clinical Investigation

Volumn 117, Issue 1, 2007, Pages 175-184

  Lumeng, Carey N ^a,b   Bodzin, Jennifer L ^a   Saltiel, Alan R ^a,b,c  

^a UNIVERSITY OF MICHIGAN   (United States)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^c Life Sciences Institute   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARGINASE; CD11 ANTIGEN; CHEMOKINE RECEPTOR CCR2; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 10; MONOCYTE CHEMOTACTIC PROTEIN 1; STAT3 PROTEIN; TUMOR NECROSIS FACTOR ALPHA;

ADIPOSE TISSUE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DRUG INHIBITION; DRUG MECHANISM; GENE DELETION; GENE EXPRESSION; GLUCOSE TRANSPORT; INSULIN RESISTANCE; INSULIN SENSITIVITY; LIPID DIET; MACROPHAGE; MALE; MOUSE; NONHUMAN; OBESITY; PHENOTYPE; POLARIZATION; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION;

3T3 CELLS; ADIPOSE TISSUE; ANIMALS; BASE SEQUENCE; BIOLOGICAL TRANSPORT; DEOXYGLUCOSE; DIETARY FATS; DISEASE MODELS, ANIMAL; DNA PRIMERS; ENERGY INTAKE; MACROPHAGES; MALE; MICE; MICE, INBRED C57BL; MICE, OBESE; OBESITY; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

EID: 33846026712     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI29881     Document Type: Article

References (52)

1. Greenberg, A.S., and Obin, M.S. 2006. Obesity and the role of adipose tissue in inflammation and metabolism. Am. J. Clin. Nutr. 83:461S-465S.
2. Shoelson, S.E., Lee, J., and Goldfine, A.B. 2006. Inflammation and insulin resistance. J. Clin. Invest. 116:1793-1801. doi:10.1172/JCI29069.
3. Neels, J.G., and Olefsky, J.M. 2006. Inflamed fat: what starts the fire? J. Clin. Invest. 116:33-35. doi:10.1172/JCI27280.
4. Cancello, R., et al. 2005. Reduction of macrophage infiltration and chemoattractant gene expression changes in white adipose tissue of morbidly obese subjects after surgery-induced weight loss. Diabetes. 54:2277-2286.
5. Weisberg, S.P., et al. 2003. Obesity is associated with macrophage accumulation in adipose tissue. J. Clin. Invest. 112:1796-1808. doi:10.1172/JCI200319246.
6. Xu, H., 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. doi:10.1172/JCI200319451.
7. Cancello, R., et al. 2006. Increased infiltration of macrophages in omental adipose tissue is associated with marked hepatic lesions in morbid human obesity. Diabetes. 55:1554-1561.
8. Harkins, J.M., et al. 2004. Expression of interleukin-6 is greater in preadipocytes than in adipocytes of 3T3-L1 cells and C57BL/6J and ob/ob mice. J. Nutr. 134:2673-2677.
9. Kanda, H., et al. 2006. MCP-1 contributes to macrophage infiltration into adipose tissue, insulin resistance, and hepatic steatosis in obesity. J. Clin. Invest. 116:1494-1505. doi:10.1172/JCI26498.
10. Weisberg, S.P., et al. 2005. CCR2 modulates inflammatory and metabolic effects of high-fat feeding. J. Clin. Invest. 116:115-124. doi:10.1172/JCI24335.
11. Kamei, N., et al. 2006. Overexpression of MCP-1 in adipose tissues causes macrophage recruitment and insulin resistance. J. Biol. Chem. 281:26602-26614.
12. Arkan, M.C., et al. 2005. IKK-beta links inflammation to obesity-induced insulin resistance. Nat. Med. 11:191-198.
13. Gordon, S., and Taylor, P.R. 2005. Monocyte and macrophage heterogeneity. Nat. Rev. Immunol. 5:953-964.
14. Mantovani, A., et al. 2004. The chemokine system in diverse forms of macrophage activation and polarization. Trends Immunol. 25:677-686.
15. Gordon, S. 2003. Alternative activation of macrophages. Nat. Rev. Immunol. 3:23-35.
16. Bronte, V., and Zanovello, P. 2005. Regulation of immune responses by L-arginine metabolism. Nat. Rev. Immunol. 5:641-654.
17. Dupasquier, M., et al. 2006. The dermal microenvironment induces the expression of the alternative activation marker CD301/mMGL in mononuclear phagocytes, independent of IL-4/IL-13 signaling. J. Leukoc. Biol. 80:838-849.
18. Vats, D., et al. 2006. Oxidative metabolism and PGC-1beta attenuate macrophage-mediated inflammation. Cell Metab. 4:13-24.
19. Tacke, F., and Randolph, G.J. 2006. Migratory fate and differentiation of blood monocyte subsets. Immunobiology. 211:609-618.
20. Geissmann, F., Jung, S., and Littman, D.R. 2003. Blood monocytes consist of two principal subsets with distinct migratory properties. Immunity. 19:71-82.
21. Sunderkotter, C., et al. 2004. Subpopulations of mouse blood monocytes differ in maturation stage and inflammatory response. J. Immunol. 172:4410-4417.
22. Barzilai, N., et al. 1999. Decreased visceral adiposity accounts for leptin effect on hepatic but not peripheral insulin action. Am. J. Physiol. 277:E291-E298.
23. Raes, G., et al. 2005. Macrophage galactose-type C-type lectins as novel markers for alternatively activated macrophages elicited by parasitic infections and allergic airway inflammation. J. Leukoc. Biol. 77:321-327.
24. Williams, L., Bradley, L., Smith, A., and Foxwell, B. 2004. Signal transducer and activator of transcription 3 is the dominant mediator of the anti-inflammatory effects of IL-10 in human macrophages. J. Immunol. 172:567-576.
25. Zhou, J.H., et al. 2001. IL-10 inhibits apoptosis of promyeloid cells by activating insulin receptor substrate-2 and phosphatidylinositol 3′-kinase. J. Immunol. 167:4436-4442.
26. Williams, L.M., Ricchetti, G., Sarma, U., Smallie, T., and Foxwell, B.M. 2004. Interleukin-10 suppression of myeloid cell activation - a continuing puzzle. Immunology. 113:281-292.
27. Dahlman, I., et al. 2005. A unique role of monocyte chemoattractant protein 1 among chemokines in adipose tissue of obese subjects. J. Clin. Endocrinol. Metab. 90:5834-5840.
28. Schottelius, A.J., Mayo, M.W., Sartor, R.B., and Baldwin, A.S., Jr. 1999. Interleukin-10 signaling blocks inhibitor of kappaB kinase activity and nuclear factor kappaB DNA binding. J. Biol. Chem. 274:31868-31874.
29. Murray, P.J. 2005. The primary mechanism of the IL-10-regulated antiinflammatory response is to selectively inhibit transcription. Proc. Natl. Acad. Sci. U. S. A. 102:8686-8691.
30. Stephens, J.M., Lee, J., and Pilch, P.F. 1997. Tumor necrosis factor-alpha-induced insulin resistance in 3T3-L1 adipocytes is accompanied by a loss of insulin receptor substrate-1 and GLUT4 expression without a loss of insulin receptor-mediated signal transduction. J. Biol. Chem. 272:971-976.
31. Lumeng, C.N., DeYoung, S.M., and Saltiel, A.R. 2006. Macrophages block insulin action in adipocytes by altering expression of signaling and glucose transport proteins. Am. J. Physiol. Endocrinol. Metab. doi:10.1152/ajpendo.00284.2006.
32. Bruun, J.M., Helge, J.W., Richelsen, B., and Stallknecht, B. 2006. Diet and exercise reduce low-grade inflammation and macrophage infiltration in adipose tissue but not in skeletal muscle in severely obese subjects. Am. J. Physiol. Endocrinol. Metab. 290:E961-E967.
33. Stout, R.D., and Suttles, J. 2004. Functional plasticity of macrophages: reversible adaptation to changing microenvironments. J. Leukoc. Biol. 76:509-513.
34. Mantovani, A., Sozzani, S., Locati, M., Allavena, P., and Sica, A. 2002. Macrophage polarization: tumor-associated macrophages as a paradigm for polarized M2 mononuclear phagocytes. Trends Immunol. 23:549-555.
35. Kim, H.J., et al. 2004. Differential effects of interleukin-6 and -10 on skeletal muscle and liver insulin action in vivo. Diabetes. 53:1060-1067.
36. Bluher, M., et al. 2005. Association of interleukin-6, C-reactive protein, interleukin-10 and adiponectin plasma concentrations with measures of obesity, insulin sensitivity and glucose metabolism. Exp. Clin. Endocrinol. Diabetes. 113:534-537.
37. Oberbach, A., et al. 2006. Effect of a 4 week physical training program on plasma concentrations of inflammatory markers in patients with abnormal glucose tolerance. Eur. J. Endocrinol. 154:577-585.
38. Scarpelli, D., et al. 2006. Variants of the interleukin-10 promoter gene are associated with obesity and insulin resistance but not type 2 diabetes in Caucasian Italian subjects. Diabetes. 55:1529-1533.
39. Wolf, A.M., Wolf, D., Rumpold, H., Enrich, B., and Tilg, H. 2004. Adiponectin induces the anti-inflammatory cytokines IL-10 and IL-1RA in human leukocytes. Biochem. Biophys. Res. Commun. 323:630-635.
40. Juge-Aubry, C.E., et al. 2005. Adipose tissue is a regulated source of interleukin-10. Cytokine. 29:270-274.
41. Soos, T.J., et al. 2006. CX3CR1+ interstitial dendritic cells form a contiguous network throughout the entire kidney. Kidney Int. 70:591-596.
42. Lumeng, C.N., Bodzin, J.L., Deyoung, S.M., and Saltiel, A.R. 2006. Increased inflammatory properties of adipose tissue macrophages recruited during diet induced obesity. Diabetes. In press.
43. Van Ginderachter, J.A., et al. 2006. Peroxisome proliferator-activated receptor gamma (PPARgamma) ligands reverse CTL suppression by alternatively activated (M2) macrophages in cancer. Blood. 108:525-535.
44. Katakura, T., Miyazaki, M., Kobayashi, M., Herndon, D.N., and Suzuki, F. 2004. CCL17 and IL-10 as effectors that enable alternatively activated macrophages to inhibit the generation of classically activated macrophages. J. Immunol. 172:1407-1413.
45. Lee, J.Y., Sohn, K.H., Rhee, S.H., and Hwang, D. 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.
46. Boschmann, M., et al. 2005. Adipose tissue metabolism and CD11b expression on monocytes in obese hypertensives. Hypertension. 46:130-136.
47. Ghanim, H., et al. 2004. Circulating mononuclear cells in the obese are in a proinflammatory state. Circulation. 110:1564-1571.
48. Stout, R.D., et al. 2005. Macrophages sequentially change their functional phenotype in response to changes in microenvironmental influences. J. Immunol. 175:342-349.
49. Park-Min, K.H., Antoniv, T.T., and Ivashkiv, L.B. 2005. Regulation of macrophage phenotype by long-term exposure to IL-10. Immunobiology. 210:77-86.
50. Baumann, C.A., et al. 2000. CAP defines a second signalling pathway required for insulin-stimulated glucose transport. Nature. 407:202-207.
51. Inoue, M., Chiang, S.H., Chang, L., Chen, X.W., and Saltiel, A.R. 2006. Compartmentalization of the exocyst complex in lipid rafts controls Glut4 vesicle tethering. Mol. Biol. Cell. 17:2303-2311.
52. Munder, M., et al. 1999. Th1/Th2-regulated expression of arginase isoforms in murine macrophages and dendritic cells. J. Immunol. 163:3771-3777.