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The Intriguing Ultrastructure of Lipid Body Organelles Within Activated Macrophages

Published online by Cambridge University Press:  01 May 2014

Felipe F. Dias ,
Victor C. Zarantonello ,
Gleydes G. Parreira ,
Hélio Chiarini-Garcia  and
Rossana C. N. Melo
Felipe F. Dias
Affiliation:
Laboratory of Cellular Biology, Department of Biology, Federal University of Juiz de Fora (UFJF), Juiz de Fora, MG 36036-900, Brazil
Victor C. Zarantonello
Affiliation:
Laboratory of Cellular Biology, Department of Biology, Federal University of Juiz de Fora (UFJF), Juiz de Fora, MG 36036-900, Brazil
Gleydes G. Parreira
Affiliation:
Laboratory of Structural Biology and Reproduction, Federal University of Minas Gerais (UFMG), Belo Horizonte, MG 31270-901, Brazil
Hélio Chiarini-Garcia
Affiliation:
Laboratory of Structural Biology and Reproduction, Federal University of Minas Gerais (UFMG), Belo Horizonte, MG 31270-901, Brazil
Rossana C. N. Melo*
Affiliation:
Laboratory of Cellular Biology, Department of Biology, Federal University of Juiz de Fora (UFJF), Juiz de Fora, MG 36036-900, Brazil
*
*Corresponding author. rossana.melo@ufjf.edu.br
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Abstract

Macrophages are widely distributed immune system cells with essential functions in tissue homeostasis, apoptotic cell clearance, and first defense in infections. A distinguishing feature of activated macrophages participating in different situations such as inflammatory and metabolic diseases is the presence of increased numbers of lipid-rich organelles, termed lipid bodies (LBs) or lipid droplets, in their cytoplasm. LBs are considered structural markers of activated macrophages and are involved in different functions such as lipid metabolism, intracellular trafficking, and synthesis of inflammatory mediators. In this review, we revisit the distinct morphology of LB organelles actively formed within macrophages in response to infections and cell clearance, taking into account new insights provided by ultrastructural studies. We also discuss the LB interactions within macrophages, revealed by transmission electron microscopy, with a focus on the remarkable LB–phagosome association and discuss potential links between structural aspects and function.

Keywords

lipid dropletscell activationhost-pathogen interactionsinflammationlipid mediators
Type
Biological Applications
Information
Microscopy and Microanalysis , Volume 20 , Issue 3 , June 2014 , pp. 869 - 878
Copyright
© Microscopy Society of America 2014 

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References

Adams, C.W., Abdulla, Y.H. & Bayliss, O.B. (1967). Osmium tetroxide as a histochemical and histological reagent. Histochimie 9(1), 68–77.CrossRefGoogle ScholarPubMed
Araujo-Santos, T., Prates, D.B., Andrade, B.B., Nascimento, D.O., Clarencio, J., Entringer, P.F., Carneiro, A.B., Silva-Neto, M.A., Miranda, J.C., Brodskyn, C.I., Barral, A., Bozza, P.T. & Borges, V.M. (2010). Lutzomyia longipalpis saliva triggers lipid body formation and prostaglandin E production in murine macrophages. PLoS Negl Trop Dis 4(11), e873.CrossRefGoogle ScholarPubMed
Barbu-Tudoran, L., Gavriliuc, O.I., Paunescu, V. & Mic, F.A. (2013). Accumulation of tissue macrophages and depletion of resident macrophages in the diabetic thymus in response to hyperglycemia-induced thymocyte apoptosis. J Diabetes Complications 27(2), 114–122.CrossRefGoogle ScholarPubMed
Bartz, R., Zehmer, J.K., Zhu, M., Chen, Y., Serrero, G., Zhao, Y. & Liu, P. (2007). Dynamic activity of lipid droplets: Protein phosphorylation and GTP-mediated protein translocation. J Proteome Res 6(8), 3256–3265.CrossRefGoogle ScholarPubMed
Bozza, P.T., Bakker-Abreu, I., Navarro-Xavier, R.A. & Bandeira-Melo, C. (2011). Lipid body function in eicosanoid synthesis: An update. Prostaglandins Leukot Essent Fatty Acids 85(5), 205–213.CrossRefGoogle ScholarPubMed
Bozza, P.T., Melo, R.C.N. & Bandeira-Melo, C. (2007). Leukocyte lipid bodies regulation and function: Contribution to allergy and host defense. Pharmacol Ther 113(1), 30–49.CrossRefGoogle ScholarPubMed
Bozza, P.T. & Viola, J.P. (2010). Lipid droplets in inflammation and cancer. Prostaglandins Leukot Essent Fatty Acids 82(4–6), 243–250.CrossRefGoogle ScholarPubMed
Bozza, P.T., Yu, W., Penrose, J.F., Morgan, E.S., Dvorak, A.M. & Weller, P.F. (1997). Eosinophil lipid bodies: Specific, inducible intracellular sites for enhanced eicosanoid formation. J Exp Med 186(6), 909–920.CrossRefGoogle ScholarPubMed
Buja, L.M., Kita, T., Goldstein, J.L., Watanabe, Y. & Brown, M.S. (1983). Cellular pathology of progressive atherosclerosis in the WHHL rabbit. An animal model of familial hypercholesterolemia. Arteriosclerosis 3(1), 87–101.CrossRefGoogle ScholarPubMed
Caceres, N., Tapia, G., Ojanguren, I., Altare, F., Gil, O., Pinto, S., Vilaplana, C. & Cardona, P.J. (2009). Evolution of foamy macrophages in the pulmonary granulomas of experimental tuberculosis models. Tuberculosis (Edinb) 89(2), 175–182.CrossRefGoogle ScholarPubMed
Cao, F., Castrillo, A., Tontonoz, P., Re, F. & Byrne, G.I. (2007). Chlamydia pneumoniae-induced macrophage foam cell formation is mediated by Toll-like receptor 2. Infect Immun 75(2), 753–759.CrossRefGoogle ScholarPubMed
Cardona, P.J., Llatjos, R., Gordillo, S., Diaz, J., Ojanguren, I., Ariza, A. & Ausina, V. (2000). Evolution of granulomas in lungs of mice infected aerogenically with Mycobacterium tuberculosis . Scand J Immunol 52(2), 156–163.CrossRefGoogle ScholarPubMed
Cheng, J., Fujita, A., Ohsaki, Y., Suzuki, M., Shinohara, Y. & Fujimoto, T. (2009). Quantitative electron microscopy shows uniform incorporation of triglycerides into existing lipid droplets. Histochem Cell Biol 132(3), 281–291.CrossRefGoogle ScholarPubMed
Cocchiaro, J.L., Kumar, Y., Fischer, E.R., Hackstadt, T. & Valdivia, R.H. (2008). Cytoplasmic lipid droplets are translocated into the lumen of the Chlamydia trachomatis parasitophorous vacuole. Proc Natl Acad Sci USA 105(27), 9379–9384.CrossRefGoogle ScholarPubMed
D’Avila, H., Freire-de-Lima, C.G., Roque, N.R., Teixeira, L., Barja-Fidalgo, C., Silva, A.R., Melo, R.C.N., Dosreis, G.A., Castro-Faria-Neto, H.C. & Bozza, P.T. (2011). Host cell lipid bodies triggered by Trypanosoma cruzi infection and enhanced by the uptake of apoptotic cells are associated with prostaglandin E generation and increased parasite growth. J Infect Dis 204(6), 951–961.CrossRefGoogle ScholarPubMed
D’Avila, H., Melo, R.C.N., Parreira, G.G., Werneck-Barroso, E., Castro-Faria-Neto, H.C. & Bozza, P.T. (2006). Mycobacterium bovis Bacillus Calmette-Guerin induces TLR2-mediated formation of lipid bodies: Intracellular domains for eicosanoid synthesis in vivo. J Immunol 176(5), 3087–3097.CrossRefGoogle ScholarPubMed
D’Avila, H., Toledo, D.A. & Melo, R.C.N. (2012). Lipid bodies: Inflammatory organelles implicated in host-Trypanosoma cruzi interplay during innate immune responses. Mediators Inflamm 2012, 478601.Google ScholarPubMed
Daniel, J., Maamar, H., Deb, C., Sirakova, T.D. & Kolattukudy, P.E. (2011). Mycobacterium tuberculosis uses host triacylglycerol to accumulate lipid droplets and acquires a dormancy-like phenotype in lipid-loaded macrophages. PLoS Pathog 7(6), e1002093.CrossRefGoogle ScholarPubMed
de Assis, E.F., Silva, A.R., Caiado, L.F., Marathe, G.K., Zimmerman, G.A., Prescott, S.M., McIntyre, T.M., Bozza, P.T. & de Castro-Faria-Neto, H.C. (2003). Synergism between platelet-activating factor-like phospholipids and peroxisome proliferator-activated receptor gamma agonists generated during low density lipoprotein oxidation that induces lipid body formation in leukocytes. J Immunol 171(4), 2090–2098.CrossRefGoogle ScholarPubMed
Dias, F.F., Chiarini-Garcia, H., Parreira, G.G. & Melo, R.C.N. (2011). Mice spermatogonial stem cells transplantation induces macrophage migration into the seminiferous epithelium and lipid body formation: High-resolution light microscopy and ultrastructural studies. Microsc Microanal 17(6), 1–13.CrossRefGoogle ScholarPubMed
Dong, H. & Czaja, M.J. (2011). Regulation of lipid droplets by autophagy. Trends Endocrinol Metab 22(6), 234–240.CrossRefGoogle ScholarPubMed
Dvorak, A.M., Morgan, E., Schleimer, R.P., Ryeom, S.W., Lichtenstein, L.M. & Weller, P.F. (1992). Ultrastructural immunogold localization of prostaglandin endoperoxide synthase (cyclooxygenase) to non-membrane-bound cytoplasmic lipid bodies in human lung mast cells, alveolar macrophages, type II pneumocytes, and neutrophils. J Histochem Cytochem 40(6), 759–769.CrossRefGoogle ScholarPubMed
Dvorak, A.M., Morgan, E.S., Tzizik, D.M. & Weller, P.F. (1994). Prostaglandin endoperoxide synthase (cyclooxygenase): Ultrastructural localization to nonmembrane-bound cytoplasmic lipid bodies in human eosinophils and 3T3 fibroblasts. Int Arch Allergy Immunol 105(3), 245–250.CrossRefGoogle ScholarPubMed
Fan, J., Shimokama, T., Tokunaga, O. & Watanabe, T. (1994). Activation and cholesterol accumulation of macrophages induced by hypercholesterolemia. A study using a rat peritoneal macrophage model for extravascular in vivo generation of foam cells. Pathobiology 62(1), 1–7.CrossRefGoogle ScholarPubMed
Feng, X., Yuan, Y., Wang, C., Feng, J., Yuan, Z., Zhang, X., Sui, W., Hu, P., Zheng, P. & Ye, J. (2014). Autophagy involved in lipopolysaccharide-induced foam cell formation is mediated by adipose differentiation-related protein. Lipids Health Dis 13, 10.CrossRefGoogle ScholarPubMed
Freire-de-Lima, C.G., Nascimento, D.O., Soares, M.B., Bozza, P.T., Castro-Faria-Neto, H.C., de Mello, F.G., DosReis, G.A. & Lopes, M.F. (2000). Uptake of apoptotic cells drives the growth of a pathogenic trypanosome in macrophages. Nature 403(6766), 199–203.CrossRefGoogle ScholarPubMed
Geissmann, F., Manz, M.G., Jung, S., Sieweke, M.H., Merad, M. & Ley, K. (2010). Development of monocytes, macrophages, and dendritic cells. Science 327(5966), 656–661.CrossRefGoogle ScholarPubMed
Giannotti, K.C., Leiguez, E., Moreira, V., Nascimento, N.G., Lomonte, B., Gutierrez, J.M., Lopes de Melo, R., Teixeira, C. (2013). A Lys49 phospholipase A2, isolated from Bothrops asper snake venom, induces lipid droplet formation in macrophages which depends on distinct signaling pathways and the C-terminal region. Biomed Res Int 2013, 807982.Google ScholarPubMed
Gold, E.S., Ramsey, S.A., Sartain, M.J., Selinummi, J., Podolsky, I., Rodriguez, D.J., Moritz, R.L. & Aderem, A. (2012). ATF3 protects against atherosclerosis by suppressing 25-hydroxycholesterol-induced lipid body formation. J Exp Med 209(4), 807–817.CrossRefGoogle ScholarPubMed
Goodman, J.M. (2009). Demonstrated and inferred metabolism associated with cytosolic lipid droplets. J Lipid Res 50(11), 2148–2156.CrossRefGoogle ScholarPubMed
Hayes, T.L., Lindgren, F.T. & Gofman, J.W. (1963). A quantitative determination of the osmium tetroxide-lipoprotein interaction. J Cell Biol 19, 251–255.CrossRefGoogle ScholarPubMed
Hodges, B.D. & Wu, C.C. (2010). Proteomic insights into an expanded cellular role for cytoplasmic lipid droplets. J Lipid Res 51(2), 262–273.CrossRefGoogle ScholarPubMed
Jaakkola, O., Yla-Herttuala, S., Sarkioja, T. & Nikkari, T. (1989). Macrophage foam cells from human aortic fatty streaks take up beta-VLDL and acetylated LDL in primary culture. Atherosclerosis 79(2–3), 173–182.CrossRefGoogle ScholarPubMed
Katabuchi, H., Yih, S., Ohba, T., Matsui, K., Takahashi, K., Takeya, M. & Okamura, H. (2003). Characterization of macrophages in the decidual atherotic spiral artery with special reference to the cytology of foam cells. Med Electron Microsc 36(4), 253–262.CrossRefGoogle Scholar
Kiss, E., Kranzlin, B., Wagenblabeta, K., Bonrouhi, M., Thiery, J., Grone, E., Nordstrom, V., Teupser, D., Gretz, N., Malle, E. & Grone, H.J. (2013). Lipid droplet accumulation is associated with an increase in hyperglycemia-induced renal damage: Prevention by liver X receptors. Am J Pathol 182(3), 727–741.CrossRefGoogle ScholarPubMed
Kondo, H., Iwasa, H. & Saino-Saito, S. (2008). First disclosure of lipid droplet substructure and myelin translucency in embedment-free section electron microscopy. Tohoku J Exp Med 214(3), 167–174.CrossRefGoogle ScholarPubMed
Koster, A.J., Grimm, R., Typke, D., Hegerl, R., Stoschek, A., Walz, J. & Baumeister, W. (1997). Perspectives of molecular and cellular electron tomography. J Struct Biol 120(3), 276–308.CrossRefGoogle ScholarPubMed
Kumar, Y., Cocchiaro, J. & Valdivia, R.H. (2006). The obligate intracellular pathogen Chlamydia trachomatis targets host lipid droplets. Curr Biol 16(16), 1646–1651.CrossRefGoogle ScholarPubMed
Luo, M., Fadeev, E.A. & Groves, J.T. (2005). Mycobactin-mediated iron acquisition within macrophages. Nat Chem Biol 1(3), 149–153.CrossRefGoogle Scholar
Lupu, F., Danaricu, I. & Simionescu, N. (1987). Development of intracellular lipid deposits in the lipid-laden cells of atherosclerotic lesions. A cytochemical and ultrastructural study. Atherosclerosis 67(2–3), 127–142.CrossRefGoogle ScholarPubMed
Martin, S., Driessen, K., Nixon, S.J., Zerial, M. & Parton, R.G. (2005). Regulated localization of Rab18 to lipid droplets: Effects of lipolytic stimulation and inhibition of lipid droplet catabolism. J Biol Chem 280(51), 42325–42335.CrossRefGoogle ScholarPubMed
Mattos, K.A., D’Avila, H., Rodrigues, L.S., Oliveira, V.G., Sarno, E.N., Atella, G.C., Pereira, G.M., Bozza, P.T. & Pessolani, M.C. (2010). Lipid droplet formation in leprosy: Toll-like receptor-regulated organelles involved in eicosanoid formation and Mycobacterium leprae pathogenesis. J Leukoc Biol 87(3), 371–384.CrossRefGoogle ScholarPubMed
Mattos, K.A., Lara, F.A., Oliveira, V.G., Rodrigues, L.S., D’Avila, H., Melo, R.C.N., Manso, P.P., Sarno, E.N., Bozza, P.T. & Pessolani, M.C. (2011). Modulation of lipid droplets by Mycobacterium leprae in Schwann cells: A putative mechanism for host lipid acquisition and bacterial survival in phagosomes. Cell Microbiol 13(2), 259–273.CrossRefGoogle ScholarPubMed
Maya-Monteiro, C.M., Almeida, P.E., D’Avila, H., Martins, A.S., Rezende, A.P., Castro-Faria-Neto, H. & Bozza, P.T. (2008). Leptin induces macrophage lipid body formation by a phosphatidylinositol 3-kinase- and mammalian target of rapamycin-dependent mechanism. J Biol Chem 283(4), 2203–2210.CrossRefGoogle ScholarPubMed
Mei, C.L., He, P., Cheng, B., Liu, W., Wang, Y.F. & Wan, J.J. (2009). Chlamydia pneumoniae induces macrophage-derived foam cell formation via PPAR alpha and PPAR gamma-dependent pathways. Cell Biol Int 33(3), 301–308.CrossRefGoogle ScholarPubMed
Melo, R.C.N. (2009). Acute heart inflammation: Ultrastructural and functional aspects of macrophages elicited by Trypanosoma cruzi infection. J Cell Mol Med 13(2), 279–294.CrossRefGoogle ScholarPubMed
Melo, R.C.N., D’Avila, H., Fabrino, D.L., Almeida, P.E. & Bozza, P.T. (2003). Macrophage lipid body induction by Chagas disease in vivo: Putative intracellular domains for eicosanoid formation during infection. Tissue Cell 35(1), 59–67.CrossRefGoogle ScholarPubMed
Melo, R.C.N., D’Avila, H., Wan, H.C., Bozza, P.T., Dvorak, A.M. & Weller, P.F. (2011). Lipid bodies in inflammatory cells: Structure, function, and current imaging techniques. J Histochem Cytochem 59(5), 540–556.CrossRefGoogle ScholarPubMed
Melo, R.C.N. & Dvorak, A.M. (2012). Lipid body-phagosome interaction in macrophages during infectious diseases: Host defense or pathogen survival strategy? PLoS Pathog 8(7), e1002729.CrossRefGoogle ScholarPubMed
Melo, R.C.N., Fabrino, D.L., Dias, F.F. & Parreira, G.G. (2006). Lipid bodies: Structural markers of inflammatory macrophages in innate immunity. Inflamm Res 55(8), 342–348.CrossRefGoogle ScholarPubMed
Melo, R.C.N. & Machado, C.R.S. (2001). Trypanosoma cruzi: Peripheral blood monocytes and heart macrophages in the resistance to acute experimental infection in rats. Exp Parasitol 97(1), 15–23.CrossRefGoogle ScholarPubMed
Melo, R.C.N., Paganoti, G.F., Dvorak, A.M. & Weller, P.F. (2013). The internal architecture of leukocyte lipid body organelles captured by three-dimensional electron microscopy tomography. PLoS One 8(3), e59578.CrossRefGoogle ScholarPubMed
Murphy, D.J. (2012). The dynamic roles of intracellular lipid droplets: From archaea to mammals. Protoplasma 249(3), 541–585.CrossRefGoogle ScholarPubMed
Ozeki, S., Cheng, J., Tauchi-Sato, K., Hatano, N., Taniguchi, H. & Fujimoto, T. (2005). Rab18 localizes to lipid droplets and induces their close apposition to the endoplasmic reticulum-derived membrane. J Cell Sci 118(Pt 12), 2601–2611.CrossRefGoogle Scholar
Pacheco, P., Bozza, F.A., Gomes, R.N., Bozza, M., Weller, P.F., Castro-Faria-Neto, H.C. & Bozza, P.T. (2002). Lipopolysaccharide-induced leukocyte lipid body formation in vivo: Innate immunity elicited intracellular loci involved in eicosanoid metabolism. J Immunol 169(11), 6498–6506.CrossRefGoogle ScholarPubMed
Pacheco, P., Vieira-de-Abreu, A., Gomes, R.N., Barbosa-Lima, G., Wermelinger, L.B., Maya-Monteiro, C.M., Silva, A.R., Bozza, M.T., Castro-Faria-Neto, H.C., Bandeira-Melo, C. & Bozza, P.T. (2007). Monocyte chemoattractant protein-1/CC chemokine ligand 2 controls microtubule-driven biogenesis and leukotriene B4-synthesizing function of macrophage lipid bodies elicited by innate immune response. J Immunol 179(12), 8500–8508.CrossRefGoogle ScholarPubMed
Paraje, M.G., Correa, S.G., Renna, M.S., Theumer, M. & Sotomayor, C.E. (2008). Candida albicans-secreted lipase induces injury and steatosis in immune and parenchymal cells. Can J Microbiol 54(8), 647–659.CrossRefGoogle ScholarPubMed
Parreira, G.G., Ogawa, T., Avarbock, M.R., Franca, L.R., Hausler, C.L., Brinster, R.L. & Russell, L.D. (1999). Development of germ cell transplants: Morphometric and ultrastructural studies. Tissue Cell 31(3), 242–254.CrossRefGoogle ScholarPubMed
Peyron, P., Vaubourgeix, J., Poquet, Y., Levillain, F., Botanch, C., Bardou, F., Daffe, M., Emile, J.F., Marchou, B., Cardona, P.J., de Chastellier, C. & Altare, F. (2008). Foamy macrophages from tuberculous patients’ granulomas constitute a nutrient-rich reservoir for M. tuberculosis persistence. PLoS Pathog 4(11), e1000204.CrossRefGoogle ScholarPubMed
Pinheiro, R.O., Nunes, M.P., Pinheiro, C.S., D’Avila, H., Bozza, P.T., Takiya, C.M., Corte-Real, S., Freire-de-Lima, C.G. & DosReis, G.A. (2009). Induction of autophagy correlates with increased parasite load of Leishmania amazonensis in BALB/c but not C57BL/6 macrophages. Microbes Infect 11(2), 181–190.CrossRefGoogle ScholarPubMed
Rank, R.G., Whittimore, J., Bowlin, A.K. & Wyrick, P.B. (2011). In vivo ultrastructural analysis of the intimate relationship between polymorphonuclear leukocytes and the chlamydial developmental cycle. Infect Immun 79(8), 3291–3301.CrossRefGoogle ScholarPubMed
Renz, H., Gong, J.H., Schmidt, A., Nain, M. & Gemsa, D. (1988). Release of tumor necrosis factor-alpha from macrophages. Enhancement and suppression are dose-dependently regulated by prostaglandin E2 and cyclic nucleotides. J Immunol 141(7), 2388–2393.CrossRefGoogle ScholarPubMed
Robenek, H., Robenek, M.J. & Troyer, D. (2005). PAT family proteins pervade lipid droplet cores. J Lipid Res 46(6), 1331–1338.CrossRefGoogle ScholarPubMed
Robenek, M.J., Severs, N.J., Schlattmann, K., Plenz, G., Zimmer, K.P., Troyer, D. & Robenek, H. (2004). Lipids partition caveolin-1 from ER membranes into lipid droplets: Updating the model of lipid droplet biogenesis. FASEB J 18(7), 866–868.CrossRefGoogle ScholarPubMed
Saka, H.A. & Valdivia, R. (2012). Emerging roles for lipid droplets in immunity and host-pathogen interactions. Annu Rev Cell Dev Biol 28, 411–437.CrossRefGoogle ScholarPubMed
Schmitz, G. & Grandl, M. (2008). Lipid homeostasis in macrophages—implications for atherosclerosis. Rev Physiol Biochem Pharmacol 160, 93–125.Google Scholar
Singh, R. & Cuervo, A.M. (2012). Lipophagy: Connecting autophagy and lipid metabolism. Int J Cell Biol 2012, 282041.CrossRefGoogle ScholarPubMed
Singh, R., Kaushik, S., Wang, Y., Xiang, Y., Novak, I., Komatsu, M., Tanaka, K., Cuervo, A.M. & Czaja, M.J. (2009). Autophagy regulates lipid metabolism. Nature 458(7242), 1131–1135.CrossRefGoogle ScholarPubMed
Walther, T.C. & Farese, R.V. Jr. (2009). The life of lipid droplets. Biochim Biophys Acta 1791(6), 459–466.CrossRefGoogle ScholarPubMed
Wan, H.C., Melo, R.C.N., Jin, Z., Dvorak, A.M. & Weller, P.F. (2007). Roles and origins of leukocyte lipid bodies: Proteomic and ultrastructural studies. FASEB J 21(1), 167–178.CrossRefGoogle ScholarPubMed
Wynn, T.A., Chawla, A. & Pollard, J.W. (2013). Macrophage biology in development, homeostasis and disease. Nature 496(7446), 445–455.CrossRefGoogle ScholarPubMed
Xu, W., Yu, L., Zhou, W. & Luo, M. (2006). Resistin increases lipid accumulation and CD36 expression in human macrophages. Biochem Biophys Res Commun 351(2), 376–382.CrossRefGoogle ScholarPubMed
Yang, L., Ding, Y., Chen, Y., Zhang, S., Huo, C., Wang, Y., Yu, J., Zhang, P., Na, H., Zhang, H., Ma, Y. & Liu, P. (2012). The proteomics of lipid droplets: Structure, dynamics, and functions of the organelle conserved from bacteria to humans. J Lipid Res 53(7), 1245–1253.CrossRefGoogle ScholarPubMed