Abstract
OBJECTIVE AND DESIGN: We recently reported that white preadipocytes phagocyte and kill micro-organisms, suggesting an active involvement of fat cells in host defence. Since characteristics of adipose tissues vary according to their localization, we measured the phagocytic capacity of stromal–vascular fraction (SVF) cells from different pads of white and brown adipose tissue in primary culture.
RESULTS: The microbicidal activities of SVF cells in inguinal and epididymal white depots were similar, but much higher than in brown fat pad. Considering the whole pad, the highest cytotoxic potential was found in inguinal white adipose tissue (WAT) depot, whereas interscapular brown adipose tissue (BAT) showed an extremely low ability to kill micro-organisms. These differences might be mainly attributed to preadipocyte activities, with regard to the low content in resident macrophages identified by their expression of F4/80 antigen.
CONCLUSIONS: Taken together these results suggest that the role as macrophage-like cells for cells of the fat stroma-vascular fraction, among which preadipocytes, is not negligible. This emphasizes the relationship existing between inflammatory and adipose cells. A differential responsiveness of adipose pads to infections and inflammatory situations due to the specific phagocytic ability of their SVF cells was thus proposed.
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References
Mohamed-Ali V, Pinkney JH, Coppack SW . Adipose tissue as an endocrine and paracrine organ Int J Obes Relat Metab Disord 1998 22: 1145–1158.
Friedman JM, Halaas JL . Leptin and the regulation of body weight in mammals Nature 1998 395: 763–770.
White RT, Damm D, Hancock N, Rosen BS, Lowell BB, Usher P, Flier JS, Spiegelman BM . Human adipsin is identical to complement factor D and is expressed at high levels in adipose tissue J Biol Chem 1992 267: 9210–9213.
Cianflone K, Maslowska M . Differentiation-induced production of ASP in human adipocytes Eur J Clin Invest 1995 25: 817–825.
Choy LN, Rosen BS, Spiegelman BM . Adipsin and an endogenous pathway of complement from adipose cells J Biol Chem 1992 267: 12736–12741.
Hotamisligil GS, Shargill NS, Spiegelman BM . Adipose expression of tumor necrosis factor-alpha: direct role in obesity-linked insulin resistance Science 1993 259: 87–91.
Hotamisligil GS, Arner P, Caro JF, Atkinson RL, Spiegelman BM . Increased adipose tissue expression of tumor necrosis factor-alpha in human obesity and insulin resistance J Clin Invest 1995 95: 2409–2415.
Levine JA, Jensen MD, Eberhardt NL, O'Brien T . Adipocyte macrophage colony-stimulating factor is a mediator of adipose tissue growth J Clin Invest 1998 101: 1557–1564.
Hirokawa J, Sakaue S, Furuya Y, Ishii J, Hasegawa A, Tagami S, Kawakami Y, Sakai M, Nishi S, Nishihira J . Tumor necrosis factor-alpha regulates the gene expression of macrophage migration inhibitory factor through tyrosine kinase-dependent pathway in 3T3-L1 adipocytes J Biochem 1998 123: 733–739.
Loffreda S, Yang SQ, Lin HZ, Karp CL, Brengman ML, Wang DJ, Klein AS, Bulkley GB, Bao C, Noble PW, Lane MD, Diehl AM . Leptin regulates proinflammatory immune responses FASEB J 1998 12: 57–65.
Lord GM, Matarese G, Howard JK, Baker RJ, Bloom SR, Lechler RI . Leptin modulates the T-cell immune response and reverses starvation-induced immunosuppression Nature 1998 394: 897–901.
Soukas A, Cohen P, Socci DN, Friedman JM . Leptin-specific patterns of gene expression in white adipose tissue Genes & Devl 2000 14: 963–980.
Cousin B, Munoz O, Andre M, Fontanilles AM, Dani C, Cousin JL, Laharrague P, Casteilla L, Penicaud L . A role for preadipocytes as macrophage-like cells FASEB J 1999 13: 305–312.
Martin ML, Jensen MD . Effects of body fat distribution on regional lipolysis in obesity J Clin Invest 1991 88: 609–613.
Prunet-Marcassus B, Moulin K, Carmona MC, Villarroya F, Penicaud L, Casteilla L . Inverse distribution of uncoupling proteins expression and oxidative capacity in mature adipocytes and stromal–vascular fractions of rat white and brown adipose tissues FEBS Lett 1999 464: 184–188.
Cousin B, Casteilla L, Dani C, Muzzin P, Revelli JP, Penicaud L . Adipose tissues from various anatomical sites are characterized by different patterns of gene expression and regulation Biochem J 1993 292: 873–876.
Montague CT, Prins JB, Sanders L, Digby JE, O'Rahilly S . Depot- and sex-specific differences in human leptin mRNA expression: implications for the control of regional fat distribution Diabetes 1997 46: 342–347.
Lefebvre AM, Laville M, Vega N, Riou JP, van Gaal L, Auwerx J, Vidal H . Depot-specific differences in adipose tissue gene expression in lean and obese subjects Diabetes 1998 47: 98–103.
Takao S, Smith EH, Wang D, Chan CK, Bulkley GB, Klein AS . Role of reactive oxygen metabolites in murine peritoneal macrophage phagocytosis and phagocytic killing Am J Physiol 1996 271: C1278–1284.
Ibrahimi A, Bonino F, Bardon S, Ailhaud G, Dani C . Essential role of collagens for terminal differentiation of preadipocytes Biochem Biophys Res Commun 1992 187: 1314–1322.
Kras KM, Hausman DB, Hausman J, Martin RJ . Adipocyte development is dependent upon stem cell recruitment and proliferation of preadipocytes Obes Res 1999 7: 491–497.
Geloen A, Roy PE, Bukowiecki LJ . Regression of white adipose tissue in diabetic rats Am J Physiol 1989 257: E547–553.
Morris L, Graham CF, Gordon S . Macrophages in haemopoietic and other tissues of the developing mouse detected by the monoclonal antibody F4/80 Development 1991 112: 517–526.
Gordon S . Macrophage-restricted molecules: role in differentiation and activation Immunol Lett 1999 65: 5–8.
Leenen PJ, de Bruijn MF, Voerman JS, Campbell PA, van Ewijk W . Markers of mouse macrophage development detected by monoclonal antibodies J Immunol Meth 1994 174: 5–19.
Ailhaud G, Grimaldi P, Negrel R . Cellular and molecular aspects of adipose tissue development A Rev Nutr 1992 12: 207–233.
Brummer E, Stevens DA . Candidacidal mechanisms of peritoneal macrophages activated with lymphokines or gamma-interferon J Med Microbiol 1989 28: 173–181.
Kern PA, Saghizadeh M, Ong JM, Bosch RJ, Deem R, Simsolo RB . The expression of tumor necrosis factor in human adipose tissue. Regulation by obesity, weight loss, and relationship to lipoprotein lipase J Clin Invest 1995 95: 2111–2119.
Grunfeld C, Zhao C, Fuller J, Pollack A, Moser A, Friedman J, Feingold KR . Endotoxin and cytokines induce expression of leptin, the ob gene product, in hamsters J Clin Invest 1996 97: 2152–2157.
Sarraf P, Frederich RC, Turner EM, Ma G, Jaskowiak NT, Rivet DJ III, Flier JS, Lowell BB, Fraker DL, Alexander HR . Multiple cytokines and acute inflammation raise mouse leptin levels: potential role in inflammatory anorexia J Exp Med 1997 185: 171–175.
Kapur S, Marcotte B, Marette A . Mechanism of adipose tissue iNOS induction in endotoxemia Am J Physiol 1999 276: E635–641.
Moncada S, Palmer RM, Higgs EA . Nitric oxide: physiology, pathophysiology, and pharmacology Pharmac Rev 1991 43: 109–142.
Acknowledgements
Authors would like to thank the technical staff from the zootechnical department, M André for technical advice and assistance, C Dani and R Martin for the gift of antibodies against A2COL6 and AD3 respectively and V Planat for linguistic revision of the text. JA Villena was a Research Scientist Fellow of the Centre National de la Recherche Scientifique.
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Villena, J., Cousin, B., Pénicaud, L. et al. Adipose tissues display differential phagocytic and microbicidal activities depending on their localization. Int J Obes 25, 1275–1280 (2001). https://doi.org/10.1038/sj.ijo.0801680
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DOI: https://doi.org/10.1038/sj.ijo.0801680
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