Human adipose tissue macrophages are enhanced but changed to an anti-inflammatory profile in obesity

Journal of Immunology Research

Volumn 2014, Issue , 2014, Pages

  Fjeldborg, Karen ^a   Pedersen, Steen B ^a   Møller, Holger J ^a   Christiansen, Tore ^a   Bennetzen, Marianne ^a   Richelsen, Bjørn ^a  

^a AARHUS UNIVERSITY HOSPITAL   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

CD14 ANTIGEN; CD163 ANTIGEN; CD206 ANTIGEN; CD68 ANTIGEN; INTERLEUKIN 10; INTERLEUKIN 6; LOW DENSITY LIPOPROTEIN RECEPTOR RELATED PROTEIN; MANNOSE RECEPTOR; MESSENGER RNA; MONOCYTE CHEMOTACTIC PROTEIN 1; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; BIOLOGICAL MARKER; TRANSCRIPTOME;

ADIPOSE TISSUE; ADULT; ANTIGEN EXPRESSION; ANTIINFLAMMATORY ACTIVITY; ARTICLE; CONTROLLED STUDY; FEMALE; GENE EXPRESSION; HOMEOSTASIS; HOMEOSTASIS MODEL ASSESSMENT INSULIN RESISTANCE INDEX; HUMAN; HUMAN TISSUE; INSULIN RESISTANCE; LEAN BODY WEIGHT; MACROPHAGE; MAJOR CLINICAL STUDY; MALE; OBESITY; PHENOTYPE; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SCORING SYSTEM; SUBCUTANEOUS FAT; CASE CONTROL STUDY; CYTOLOGY; GENE EXPRESSION PROFILING; GENETICS; IMMUNOLOGY; METABOLISM; MIDDLE AGED; PATHOLOGY;

ADIPOSE TISSUE; ADULT; BIOLOGICAL MARKERS; CASE-CONTROL STUDIES; FEMALE; GENE EXPRESSION PROFILING; HUMANS; INSULIN RESISTANCE; MACROPHAGES; MALE; MIDDLE AGED; OBESITY; PHENOTYPE; TRANSCRIPTOME;

EID: 84897502656     PISSN: 23148861     EISSN: 23147156     Source Type: Journal    
DOI: 10.1155/2014/309548     Document Type: Article

References (38)

1. Dandona P., Aljada A., Bandyopadhyay A., Inflammation: the link between insulin resistance, obesity and diabetes. Trends in Immunology 2004 25 1 4 7 2-s2.0-0348222671 10.1016/j.it.2003.10.013 (Pubitemid 38032801)
2. Weisberg S. P., McCann D., Desai M., Rosenbaum M., Leibel R. L., Ferrante A. W. Jr., Obesity is associated with macrophage accumulation in adipose tissue. Journal of Clinical Investigation 2003 112 12 1796 1808 2-s2.0-0348230958 10.1172/JCI200319246 (Pubitemid 38063703)
3. Cancello R., Henegar C., Viguerie N., Taleb S., Poitou C., Rouault C., Coupaye M., Pelloux V., Hugol D., Bouillot J., Bouloumié A., Barbatelli G., Cinti S., Svensson P., Barsh G. S., Zucker J., Basdevant A., Langin D., Clément K., 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 8 2277 2286 2-s2.0-23644450775 10.2337/diabetes.54.8.2277 (Pubitemid 41134253)
4. Trayhurn P., Hypoxia and adipose tissue function and dysfunction in obesity. Physiological Reviews 2013 93 1 1 21 10.1152/physrev.00017.2012
5. Dalmas E., Clément K., Guerre-Millo M., Defining macrophage phenotype and function in adipose tissue. Trends in Immunology 2011 32 7 307 314 2-s2.0-79959783758 10.1016/j.it.2011.04.008
6. Cinti S., Mitchell G., Barbatelli G., Murano I., Ceresi E., Faloia E., Wang S., Fortier M., Greenberg A. S., Obin M. S., Adipocyte death defines macrophage localization and function in adipose tissue of obese mice and humans. Journal of Lipid Research 2005 46 11 2347 2355 2-s2.0-27444437321 10.1194/jlr.M500294-JLR200 (Pubitemid 41532523)
7. Spencer M., Yao-Borengasser A., Unal R., Rasouli N., Gurley C. M., Zhu B., Peterson C. A., Kern P. A., Adipose tissue macrophages in insulin-resistant subjects are associated with collagen VI and fibrosis and demonstrate alternative activation. The American Journal of Physiology-Endocrinology and Metabolism 2010 299 6 E1016 E1027 2-s2.0-78649652068 10.1152/ajpendo.00329.2010
8. Martinez F. O., Helming L., Gordon S., Alternative activation of macrophages: an immunologic functional perspective. Annual Review of Immunology 2009 27 451 483 2-s2.0-67650485985 10.1146/annurev.immunol.021908.132532
9. Sulahian T. H., Högger P., Wahner A. E., Wardwell K., Goulding N. J., Sorg C., Droste A., Stehling M., Wallace P. K., Morganelli P. M., Guyre P. M., Human monocytes express CD163, which is upregulated by IL-10 and identical to p155. Cytokine 2000 12 9 1312 1321 2-s2.0-0033802512 10.1006/cyto.2000.0720
10. Gratchev A., Schledzewski K., Guillot P., Goerdt S., Alternatively activated antigen-presenting cells: molecular repertoire, immune regulation, and healing. Skin Pharmacology and Applied Skin Physiology 2001 14 5 272 279 2-s2.0-0035741908 10.1159/000056357 (Pubitemid 34701634)
11. Zeyda M., Farmer D., Todoric J., Aszmann O., Speiser M., Györi G., Zlabinger G. J., Stulnig T. M., Human adipose tissue macrophages are of an anti-inflammatory phenotype but capable of excessive pro-inflammatory mediator production. International Journal of Obesity 2007 31 9 1420 1428 2-s2.0-34548354722 10.1038/sj.ijo.0803632 (Pubitemid 47339934)
12. Bourlier V., Zakaroff-Girard A., Miranville A., de Barros S., Maumus M., Sengenes C., Galitzky J., Lafontan M., Karpe F., Frayn K. N., Bouloumié A., Remodeling phenotype of human subcutaneous adipose tissue macrophages. Circulation 2008 117 6 806 815 2-s2.0-39549122799 10.1161/CIRCULATIONAHA.107. 724096 (Pubitemid 351640682)
13. Lumeng C. N., Bodzin J. L., Saltiel A. R., Obesity induces a phenotypic switch in adipose tissue macrophage polarization. Journal of Clinical Investigation 2007 117 1 175 184 2-s2.0-33846026712 10.1172/JCI29881 (Pubitemid 46048464)
14. Nguyen M. T. A., Favelyukis S., Nguyen A., Reichart D., Scott P. A., Jenn A., Liu-Bryan R., Glass C. K., Neels J. G., Olefsky J. M., 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. The Journal of Biological Chemistry 2007 282 48 35279 35292 2-s2.0-36849005372 10.1074/jbc.M706762200 (Pubitemid 350232441)
15. Aron-Wisnewsky J., Tordjman J., Poitou C., Darakhshan F., Hugol D., Basdevant A., Aissat A., Guerre-Millo M., Clément K., Human adipose tissue macrophages: M1 and M2 cell surface markers in subcutaneous and omental depots and after weight loss. Journal of Clinical Endocrinology and Metabolism 2009 94 11 4619 4623 2-s2.0-70449113184 10.1210/jc.2009-0925
16. Clément K., Viguerie N., Poitou C., Carette C., Pelloux V., Curat C. A., Sicard A., Rome S., Benis A., Zucker J., Vidal H., Laville M., Barsh G. S., Basdevant A., Stich V., Cancello R., Langin D., Weight loss regulates inflammation-related genes in white adipose tissue of obese subjects. FASEB Journal 2004 18 14 1657 1669 2-s2.0-7744226149 10.1096/fj.04-2204com (Pubitemid 39463705)
17. Wentworth J. M., Naselli G., Brown W. A., Doyle L., Phipson B., Smyth G. K., Wabitsch M., O'Brien P. E., Harrison L. C., Pro-inflammatory CD11c+CD206+ adipose tissue macrophages are associated with insulin resistance in human obesity. Diabetes 2010 59 7 1648 1656 2-s2.0-77954249680 10.2337/db09-0287
18. Christiansen T., Richelsen B., Bruun J. M., Monocyte chemoattractant protein-1 is produced in isolated adipocytes, associated with adiposity and reduced after weight loss in morbid obese subjects. International Journal of Obesity 2005 29 1 146 150 2-s2.0-11244302456 10.1038/sj.ijo.0802839 (Pubitemid 40065478)
19. Koppaka S., Kehlenbrink S., Carey M., Li W., Sanchez E., Lee D. E., Lee H., Chen J., Carrasco E., Kishore P., Zhang K., Hawkins M., Reduced adipose tissue macrophage content is associated with improved insulin sensitivity in thiazolidinedione-treated diabetic humans. Diabetes 2013 62 6 1843 1854 10.2337/db12-0868
20. Bouhlel M. A., Derudas B., Rigamonti E., Dièvart R., Brozek J., Haulon S., Zawadzki C., Jude B., Torpier G., Marx N., Staels B., Chinetti-Gbaguidi G., PPAR γ activation primes human monocytes into alternative M2 macrophages with anti-inflammatory properties. Cell Metabolism 2007 6 2 137 143 2-s2.0-34547492488 10.1016/j.cmet.2007.06.010 (Pubitemid 47189091)
21. Møller H. J., Peterslund N. A., Graversen J. H., Moestrup S. K., Identification of the hemoglobin scavenger receptor/CD163 as a natural soluble protein in plasma. Blood 2002 99 1 378 380 2-s2.0-0005136199 10.1182/blood.V99.1.378 (Pubitemid 34533008)
22. Moestrup S. K., Moller H. J., CD163: a regulated hemoglobin scavenger receptor with a role in the anti-inflammatory response. Annals of Medicine 2004 36 5 347 354 2-s2.0-4544246612 10.1080/07853890410033171 (Pubitemid 39233102)
23. Fjeldborg K., Christiansen T., Bennetzen M., Moller H. J., Pedersen S. B., Richelsen B., The macrophage specific serum marker, soluble CD163, is increased in obesity and reduced after dietary induced weight loss. Obesity 2013 21 12 2437 2443 10.1002/oby.20376
24. Møller H. J., Aerts H., Grønbæk H., Peterslund N. A., Petersen P. H., Hornung N., Rejnmark L., Jabbarpour E., Moestrup S. K., Soluble CD163: a marker molecule for monocyte/macrophage activity in disease. Scandinavian Journal of Clinical and Laboratory Investigation, Supplement 2002 62 237 29 33 2-s2.0-0038487124
25. Moller H. J., Nielsen A. R., Pedersen B. K., Parkner T., Increased plasma levels of macrophage specifc sCD163 in type 2 diabetes and obesity. Diabetes 2009 58 article LB27
26. Zanni M. V., Burdo T. H., Makimura H., Williams K. C., Grinspoon S. K., Relationship between monocyte/macrophage activation marker soluble CD163 and insulin resistance in obese and normal-weight subjects. Clinical Endocrinology 2012 77 3 385 390 10.1111/j.1365-2265.2011.04284.x
27. Bennetzen M. F., Wellner N., Ahmed S. S., Ahmed S. M., Diep T. A., Hansen H. S., Richelsen B., Pedersen S. B., Investigations of the human endocannabinoid system in two subcutaneous adipose tissue depots in lean subjects and in obese subjects before and after weight loss. International Journal of Obesity 2011 35 11 1377 1384 2-s2.0-81155134826 10.1038/ijo.2011.8
28. Christiansen T., Paulsen S. K., Bruun J. M., Overgaard K., Ringgaard S., Pedersen S. B., Positano V., Richelsen B., Comparable reduction of the visceral adipose tissue depot after a diet-induced weight loss with or without aerobic exercise in obese subjects: a 12-week randomized intervention study. European Journal of Endocrinology 2009 160 5 759 767 2-s2.0-65549110195 10.1530/EJE-08-1009
29. Matthews D. R., Hosker J. P., Rudenski A. S., Naylor B. A., Treacher D. F., Turner R. C., Homeostasis model assessment: insulin resistance and β -cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia 1985 28 7 412 419 2-s2.0-0021813187 (Pubitemid 15018832)
30. Volund A., Conversion of insulin units to SI units. The American Journal of Clinical Nutrition 1993 58 5 714 715 2-s2.0-0027432272
31. Møller H. J., Hald K., Moestrup S. K., Characterization of an enzyme-linked immunosorbent assay for soluble CD163. Scandinavian Journal of Clinical and Laboratory Investigation 2002 62 4 293 299 2-s2.0-1842836478 10.1080/003655102760145852 (Pubitemid 34816231)
32. Arvidsson S., Kwasniewski M., Riaño-Pachón D. M., Mueller-Roeber B., QuantPrime-a flexible tool for reliable high-throughput primer design for quantitative PCR. BMC Bioinformatics 2008 9 article 465 2-s2.0-58149307466 10.1186/1471-2105-9-465
33. Michaud A., Drolet R., Noël S., Paris G., Tchernof A., Visceral fat accumulation is an indicator of adipose tissue macrophage infiltration in women. Metabolism 2012 61 5 689 698 2-s2.0-84860250440 10.1016/j.metabol.2011.10.004
34. Harman-Boehm I., Blüher M., Redel H., Sion-Vardy N., Ovadia S., Avinoach E., Shai I., Klöting N., Stumvoll M., Bashan N., Rudich A., Macrophage infiltration into omental versus subcutaneous fat across different populations: effect of regional adiposity and the comorbidities of obesity. Journal of Clinical Endocrinology and Metabolism 2007 92 6 2240 2247 2-s2.0-34347249246 10.1210/jc.2006-1811 (Pubitemid 46997129)
35. Shaul M. E., Bennett G., Strissel K. J., Greenberg A. S., Obin M. S., Dynamic, M2-like remodeling phenotypes of CD11c+ adipose tissue macrophages during high-fat diet-induced obesity in mice. Diabetes 2010 59 5 1171 1181 2-s2.0-77951822653 10.2337/db09-1402
36. Shakeri-Manesch S., Zeyda M., Huber J., Ludvik B., Prager G., Stulnig T. M., Diminished upregulation of visceral adipose heme oxygenase-1 correlates with waist-to-hip ratio and insulin resistance. International Journal of Obesity 2009 33 11 1257 1264 2-s2.0-70450270702 10.1038/ijo.2009.160
37. Parkner T., Sørensen L. P., Nielsen A. R., Fischer C. P., Bibby B. M., Nielsen S., Pedersen B. K., Møller H. J., Soluble CD163: a biomarker linking macrophages and insulin resistance. Diabetologia 2012 55 6 1856 1862 2-s2.0-84858729457 10.1007/s00125-012-2533-1
38. de Victoria E. O. M., Xu X., Koska J., Francisco A. M., Scalise M., Ferrante A. W. Jr., Krakoff J., Macrophage content in subcutaneous adipose tissue: associations with adiposity, age, inflammatory markers, and whole-body insulin action in healthy pima Indians. Diabetes 2009 58 2 385 393 2-s2.0-63249106129 10.2337/db08-0536