Mannose-binding lectin is required for the effective clearance of apoptotic cells by adipose tissue macrophages during obesity

Diabetes

Volumn 63, Issue 12, 2014, Pages 4143-4153

  Stienstra, Rinke ^a,b   Dijk, Wieneke ^a   Van Beek, Lianne ^c   Jansen, Henry ^b   Heemskerk, Mattijs ^c   Houtkooper, Riekelt H ^d   Denis, Simone ^d   Van Harmelen, Vanessa ^c   Van Dijk, Ko Willems ^c   Tack, Cees J ^b   Kersten, Sander ^a  

^a WAGENINGEN UNIVERSITY   (Netherlands)

^b RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^c LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^d ACADEMIC MEDICAL CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

FATTY ACID; LEPTIN; MANNOSE BINDING LECTIN;

ADIPOCYTE; ADIPOSE TISSUE; ADULT; AGED; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL COUNT; CELL POLARITY; CELL SIZE; CLEARANCE; GENE EXPRESSION; HUMAN; HUMAN TISSUE; INSULIN RESISTANCE; LIPID DIET; MACROPHAGE; MALE; MOUSE; NONHUMAN; OBESITY; PHAGOCYTOSIS; PHENOTYPE; PROTEIN FUNCTION; ANIMAL; CYTOLOGY; GENETICS; KNOCKOUT MOUSE; LIVER; METABOLISM; OVERWEIGHT;

ADIPOCYTES; ADIPOSE TISSUE; ANIMALS; DIET, HIGH-FAT; HUMANS; INSULIN RESISTANCE; LIVER; MACROPHAGES; MANNOSE-BINDING LECTIN; MICE, KNOCKOUT; OBESITY; OVERWEIGHT; PHAGOCYTOSIS;

EID: 84911935349     PISSN: 00121797     EISSN: 1939327X     Source Type: Journal    
DOI: 10.2337/db14-0256     Document Type: Article

References (44)

1. Hotamisligil GS, Erbay E. Nutrient sensing and in flammation in metabolic diseases. Nat Rev Immunol 2008;8:923-934
2. Steinberg GR. Inflammation in obesity is the common link between defects in fatty acid metabolism and insulin resistance. Cell Cycle 2007;6:888-894
3. Anderson EK, Gutierrez DA, Hasty AH. Adipose tissue recruitment of leukocytes. Curr Opin Lipidol 2010;21:172-177
4. Lumeng CN, Maillard I, Saltiel AR. T-ing up inflammation in fat. Nat Med 2009;15:846-847
5. Weisberg SP, McCann D, Desai M, Rosenbaum M, Leibel RL, Ferrante AW Jr. Obesity is associated with macrophage accumulation in adipose tissue. J Clin Invest 2003;112:1796-1808
6. Kaminski DA, Randall TD. Adaptive immunity and adipose tissue biology. Trends Immunol 2010;31:384-390
7. Kanda H, Tateya S, Tamori Y, et al. MCP-1 contributes to macrophage infiltration into adipose tissue, insulin resistance, and hepatic steatosis in obesity. J Clin Invest 2006;116:1494-1505
8. Bourlier V, Bouloumie A. Role of macrophage tissue infiltration in obesity and insulin resistance. Diabetes Metab 2009;35:251-260
9. Cinti S, Mitchell G, Barbatelli G, et al. Adipocyte death defines macrophage localization and function in adipose tissue of obese mice and humans. J Lipid Res 2005;46:2347-2355
10. Alkhouri N, Gornicka A, Berk MP, et al. Adipocyte apoptosis, a link between obesity, insulin resistance, and hepatic steatosis. J Biol Chem 2010;285:3428-3438
11. Fischer-Posovszky P, Wang QA, Asterholm IW, Rutkowski JM, Scherer PE. Targeted deletion of adipocytes by apoptosis leads to adipose tissue recruitment of alternatively activated M2 macrophages. Endocrinology 2011;152:3074-3081
12. Lumeng CN, Bodzin JL, Saltiel AR. Obesity induces a phenotypic switch in adipose tissue macrophage polarization. J Clin Invest 2007;117:175-184
13. Li P, Lu M, Nguyen MT, et al. Functional heterogeneity of CD11c-positive adipose tissue macrophages in diet-induced obese mice. J Biol Chem 2010;285:15333-15345
14. Morris DL, Singer K, Lumeng CN. Adipose tissue macrophages: phenotypic plasticity and diversity in lean and obese states. Curr Opin Clin Nutr Metab Care 2011;14:341-346
15. Murray PJ, Wynn TA. Protective and pathogenic functions of macrophage subsets. Nat Rev Immunol 2011;11:723-737
16. Epstein J, Eichbaum Q, Sheriff S, Ezekowitz RA. The collectins in innate immunity. Curr Opin Immunol 1996;8:29-35
17. Shi L, Takahashi K, Dundee J, et al. Mannose-binding lectin-deficient mice are susceptible to infection with Staphylococcus aureus. J Exp Med 2004;199:1379-1390
18. Kilpatrick DC. Mannan-binding lectin: clinical significance and applications. Biochim Biophys Acta 2002;1572:401-413
19. Stuart LM, Takahashi K, Shi L, Savill J, Ezekowitz RA. Mannose-binding lectin-deficient mice display defective apoptotic cell clearance but no autoimmune phenotype. J Immunol 2005;174:3220-3226
20. Thiel S, Holmskov U, Hviid L, Laursen SB, Jensenius JC. The concentration of the C-type lectin, mannan-binding protein, in human plasma increases during an acute phase response. Clin Exp Immunol 1992;90:31-35
21. Ogden CA, deCathelineau A, Hoffmann PR, et al. C1q and mannose binding lectin engagement of cell surface calreticulin and CD91 initiates macropinocytosis and uptake of apoptotic cells. J Exp Med 2001;194:781-795
22. Nauta AJ, Raaschou-Jensen N, Roos A, et al. Mannose-binding lectin engagement with late apoptotic and necrotic cells. Eur J Immunol 2003;33:2853-2863
23. Shimizu T, Nishitani C, Mitsuzawa H, et al. Mannose binding lectin and lung collectins interact with Toll-like receptor 4 and MD-2 by different mechanisms. Biochim Biophys Acta 2009;1790:1705-1710
24. Koneti A, Linke MJ, Brummer E, Stevens DA. Evasion of innate immune responses: evidence for mannose binding lectin inhibition of tumor necrosis factor alpha production by macrophages in response to Blastomyces dermatitidis. Infect Immun 2008;76:994-1002
25. Fraser DA, Bohlson SS, Jasinskiene N, et al. C1q and MBL, components of the innate immune system, influence monocyte cytokine expression. J Leukoc Biol 2006;80:107-116
26. Matsushita M, Endo Y, Nonaka M, Fujita T. Complement-related serine proteases in tunicates and vertebrates. Curr Opin Immunol 1998;10:29-35
27. Madsen HO, Garred P, Thiel S, et al. Interplay between promoter and structural gene variants control basal serum level of mannan-binding protein. J Immunol 1995;155:3013-3020
28. Megia A, Gallart L, Fernández-Real JM, et al. Mannose-binding lectin gene polymorphisms are associated with gestational diabetes mellitus. J Clin Endocrinol Metab 2004;89:5081-5087
29. Garred P, Madsen HO, Marquart H, et al. Two edged role of mannose binding lectin in rheumatoid arthritis: a cross sectional study. J Rheumatol 2000;27:26-34
30. Best LG, Davidson M, North KE, et al. Prospective analysis of mannose-binding lectin genotypes and coronary artery disease in American Indians: the Strong Heart Study. Circulation 2004;109:471-475
31. Fernández-Real JM, Stracz M, Vendrell J, et al. Protection from inflammatory disease in insulin resistance: the role of mannan-binding lectin. Diabetologia 2006;49:2402-2411
32. Kowalska I, Fernandez-Real JM, Straczkowski M, et al. Insulin resistance is associated with decreased circulating mannan-binding lectin concentrations in women with polycystic ovary syndrome. Diabetes Care 2008;31:e20
33. Muller YL, Hanson RL, Bian L, et al. Functional variants in MBL2 are associated with type 2 diabetes and pre-diabetes traits in Pima Indians and the old order Amish. Diabetes 2010;59:2080-2085
34. Péronnet F, Massicotte D. Table of nonprotein respiratory quotient: an update. Can J Sport Sci 1991;16:23-29
35. Clark AM, Sousa KM, Jennings C, MacDougald OA, Kennedy RT. Continuous-flow enzyme assay on a microfluidic chip for monitoring glycerol secretion from cultured adipocytes. Anal Chem 2009;81:2350-2356
36. Villena JA, Cousin B, Pénicaud L, Casteilla L. Adipose tissues display differential phagocytic and microbicidal activities depending on their localization. Int J Obes Relat Metab Disord 2001;25:1275-1280
37. Lucas M, Stuart LM, Savill J, Lacy-Hulbert A. Apoptotic cells and innate immune stimuli combine to regulate macrophage cytokine secretion. J Immunol 2003;171:2610-2615
38. Soell M, Lett E, Holveck F, Schöller M, Wachsmann D, Klein JP. Activation of human monocytes by streptococcal rhamnose glucose polymers is mediated by CD14 antigen, and mannan binding protein inhibits TNF-alpha release. J Immunol 1995;154:851-860
39. Dean MM, Flower RL, Eisen DP, Minchinton RM, Hart DN, Vuckovic S. Mannose-binding lectin deficiency influences innate and antigen-presenting functions of blood myeloid dendritic cells. Immunology 2011;132:296-305
40. Wang M, Chen Y, Zhang Y, Zhang L, Lu X, Chen Z. Mannan-binding lectin directly interacts with Toll-like receptor 4 and suppresses lipopolysaccharide-induced inflammatory cytokine secretion from THP-1 cells. Cell Mol Immunol 2011;8:265-275
41. Chaka W, Verheul AF, Vaishnav VV, et al. Induction of TNF-alpha in human peripheral blood mononuclear cells by the mannoprotein of Cryptococcus neoformans involves human mannose binding protein. J Immunol 1997;159:2979-2985
42. Jack DL, Read RC, Tenner AJ, Frosch M, Turner MW, Klein NJ. Mannose-binding lectin regulates the inflammatory response of human professional phagocytes to Neisseria meningitidis serogroup B. J Infect Dis 2001;184:1152-1162
43. MacDonald SL, Downing I, Atkinson AP, Gallagher RC, Turner ML, Kilpatrick DC. Dendritic cells previously exposed to mannan-binding lectin enhance cytokine production in allogeneic mononuclear cell cultures. Hum Immunol 2010;71:1077-1083
44. Ip WK, Takahashi K, Moore KJ, Stuart LM, Ezekowitz RA. Mannose-binding lectin enhances Toll-like receptors 2 and 6 signaling from the phagosome. J Exp Med 2008;205:169-181