Exocytosis of macrophage lysosomes leads to digestion of apoptotic adipocytes and foam cell formation

Journal of Lipid Research

Volumn 57, Issue 6, 2016, Pages 980-992

  Haka, Abigail S ^a   Barbosa Lorenzi, Valéria C ^a   Lee, Hyuek Jong ^a   Falcone, Domenick J ^a   Hudis, Clifford A ^a   Dannenberg, Andrew J ^a   Maxfield, Frederick R ^a  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

Author keywords

Adipose tissue; Crown like structure; Extracellular catabolism; Lipolysis and fatty acid metabolism; Obesity

Indexed keywords

ACTIN;

ADIPOCYTE; ADIPOSE TISSUE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL LABELING; CONTROLLED STUDY; EXOCYTOSIS; FEMALE; FOAM CELL; HOMEOSTASIS; HUMAN; HUMAN TISSUE; HYDROLYSIS; INTRACELLULAR SPACE; LYSOSOME; MACROPHAGE; MALE; METABOLIC CAPACITY; MOUSE; NONHUMAN; OBESITY; POLYMERIZATION; PRIORITY JOURNAL; ANIMAL; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY; PHAGOCYTOSIS; PHYSIOLOGY;

ADIPOCYTES; ADIPOSE TISSUE; ANIMALS; EXOCYTOSIS; FOAM CELLS; HUMANS; LYSOSOMES; MACROPHAGES; MICE; OBESITY; PHAGOCYTOSIS;

EID: 84971571102     PISSN: 00222275     EISSN: 15397262     Source Type: Journal    
DOI: 10.1194/jlr.M064089     Document Type: Article

References (42)

1. Hotamisligil, G. S. 2006. Inflammation and metabolic disorders. Nature. 444: 860-867.
2. Olefsky, J. M., and C. K. Glass. 2010. Macrophages, inflammation, and insulin resistance. Annu. Rev. Physiol. 72: 219-246.
3. Lumeng, C. N., and A. R. Saltiel. 2011. Inflammatory links between obesity and metabolic disease. J. Clin. Invest. 121: 2111-2117.
4. Park, J., D. M. Euhus, and P. E. Scherer. 2011. Paracrine and endocrine effects of adipose tissue on cancer development and progression. Endocr. Rev. 32: 550-570.
5. Wernstedt Asterholm, I., C. Tao, T. S. Morley, Q. A. Wang, F. Delgado-Lopez, Z. V. Wang, and P. E. Scherer. 2014. Adipocyte inflammation is essential for healthy adipose tissue expansion and remodeling. Cell Metab. 20: 103-118.
6. Xu, H., G. T. Barnes, Q. Yang, G. Tan, D. Yang, C. J. Chou, J. Sole, A. Nichols, J. S. Ross, L. A. Tartaglia, 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.
7. Nguyen, M. T., S. Favelyukis, A. K. Nguyen, D. Reichart, P. A. Scott, A. Jenn, R. Liu-Bryan, C. K. Glass, J. G. Neels, and J. M. Olefsky. 2007. 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. J. Biol. Chem. 282: 35279-35292.
8. Lumeng, C. N., S. M. Deyoung, J. L. Bodzin, and A. R. Saltiel. 2007. Increased inflammatory properties of adipose tissue macrophages recruited during diet-induced obesity. Diabetes. 56: 16-23.
9. Cancello, R., C. Henegar, N. Viguerie, S. Taleb, C. Poitou, C. Rouault, M. Coupaye, V. Pelloux, D. Hugol, J. L. Bouillot, 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.
10. Cinti, S., G. Mitchell, G. Barbatelli, I. Murano, E. Ceresi, E. Faloia, S. Wang, M. Fortier, A. S. Greenberg, and M. S. Obin. 2005. Adipocyte death defines macrophage localization and function in adipose tissue of obese mice and humans. J. Lipid Res. 46: 2347-2355.
11. Shapiro, H., T. Pecht, R. Shaco-Levy, I. Harman-Boehm, B. Kirshtein, Y. Kuperman, A. Chen, M. Bluher, I. Shai, and A. Rudich. 2013. Adipose tissue foam cells are present in human obesity. J. Clin. Endocrinol. Metab. 98: 1173-1181.
12. Giordano, A., I. Murano, E. Mondini, J. Perugini, A. Smorlesi, I. Severi, R. Barazzoni, P. E. Scherer, and S. Cinti. 2013. Obese adipocytes show ultrastructural features of stressed cells and die of pyroptosis. J. Lipid Res. 54: 2423-2436.
13. Zhang, W. Y., P. M. Gaynor, and H. S. Kruth. 1997. Aggregated low density lipoprotein induces and enters surface-connected compartments of human monocyte-macrophages. Uptake occurs independently of the low density lipoprotein receptor. J. Biol. Chem. 272: 31700-31706.
14. Grosheva, I., A. S. Haka, C. Qin, L. M. Pierini, and F. R. Maxfield. 2009. Aggregated LDL in contact with macrophages induces local increases in free cholesterol levels that regulate local actin polymerization. Arterioscler. Thromb. Vasc. Biol. 29: 1615-1621.
15. Haka, A. S., I. Grosheva, E. Chiang, A. R. Buxbaum, B. A. Baird, L. M. Pierini, and F. R. Maxfield. 2009. Macrophages create an acidic extracellular hydrolytic compartment to digest aggregated lipoproteins. Mol. Biol. Cell. 20: 4932-4940.
16. Baron, R., L. Neff, D. Louvard, and P. J. Courtoy. 1985. Cellmediated extracellular acidification and bone resorption: evidence for a low pH in resorbing lacunae and localization of a 100-kD lysosomal membrane protein at the osteoclast ruffled border. J. Cell Biol. 101: 2210-2222.
17. Stenbeck, G. 2002. Formation and function of the ruffled border in osteoclasts. Semin. Cell Dev. Biol. 13: 285-292.
18. Jurdic, P., F. Saltel, A. Chabadel, and O. Destaing. 2006. Podosome and sealing zone: specificity of the osteoclast model. Eur. J. Cell Biol. 85: 195-202.
19. Moore, K. J., and I. Tabas. 2011. Macrophages in the pathogenesis of atherosclerosis. Cell. 145: 341-355.
20. Hong, J., R. E. Stubbins, R. R. Smith, A. E. Harvey, and N. P. Nunez. 2009. Differential susceptibility to obesity between male, female and ovariectomized female mice. Nutr. J. 8: 11.
21. Motoshima, H., X. Wu, M. K. Sinha, V. E. Hardy, E. L. Rosato, D. J. Barbot, F. E. Rosato, and B. J. Goldstein. 2002. Differential regulation of adiponectin secretion from cultured human omental and subcutaneous adipocytes: effects of insulin and rosiglitazone. J. Clin. Endocrinol. Metab. 87: 5662-5667.
22. Frost, S. C., and M. D. Lane. 1985. Evidence for the involvement of vicinal sulfhydryl groups in insulin-activated hexose transport by 3T3-L1 adipocytes. J. Biol. Chem. 260: 2646-2652.
23. Lin, J., K. A. Page, M. A. Della-Fera, and C. A. Baile. 2004. Evaluation of adipocyte apoptosis by laser scanning cytometry. Int. J. Obes. Relat. Metab. Disord. 28: 1535-1540.
24. Sagulenko, V., S. J. Thygesen, D. P. Sester, A. Idris, J. A. Cridland, P. R. Vajjhala, T. L. Roberts, K. Schroder, J. E. Vince, J. M. Hill, et al. 2013. AIM2 and NLRP3 inflammasomes activate both apoptotic and pyroptotic death pathways via ASC. Cell Death Differ. 20: 1149-1160.
25. Huynh, K. K., E. L. Eskelinen, C. C. Scott, A. Malevanets, P. Saftig, and S. Grinstein. 2007. LAMP proteins are required for fusion of lysosomes with phagosomes. EMBO J. 26: 313-324.
26. Harter, C., and I. Mellman. 1992. Transport of the lysosomal membrane glycoprotein lgp120 (lgp-A) to lysosomes does not require appearance on the plasma membrane. J. Cell Biol. 117: 311-325.
27. Colvin, R. A., T. K. Means, T. J. Diefenbach, L. F. Moita, R. P. Friday, S. Sever, G. S. Campanella, T. Abrazinski, L. A. Manice, C. Moita, et al. 2010. Synaptotagmin-mediated vesicle fusion regulates cell migration. Nat. Immunol. 11: 495-502.
28. Xu, X., A. Grijalva, A. Skowronski, M. van Eijk, M. J. Serlie, and A. W. Ferrante, Jr. 2013. Obesity activates a program of lysosomaldependent lipid metabolism in adipose tissue macrophages independently of classic activation. Cell Metab. 18: 816-830.
29. Hotamisligil, G. S., N. S. Shargill, and B. M. Spiegelman. 1993. Adipose expression of tumor necrosis factor-alpha: direct role in obesity-linked insulin resistance. Science. 259: 87-91.
30. Zhang, Y., and C. Huang. 2012. Targeting adipocyte apoptosis: a novel strategy for obesity therapy. Biochem. Biophys. Res. Commun. 417: 1-4.
31. Bennett, G., K. J. Strissel, J. DeFuria, J. Wang, D. Wu, L. C. Burkly, and M. S. Obin. 2014. Deletion of TNF-like weak inducer of apoptosis (TWEAK) protects mice from adipose and systemic impacts of severe obesity. Obesity (Silver Spring). 22: 1485-1494.
32. Singh, R. K., V. C. Barbosa-Lorenzi, F. W. Lund, I. Grosheva, F. R. Maxfield, and A. S. Haka. 2016. Degradation of aggregated LDL occurs in complex extracellular sub-compartments of the lysosomal synapse. J. Cell Sci. 129: 1072-1082.
33. Mayor, S., K. G. Rothberg, and F. R. Maxfield. 1994. Sequestration of GPI-anchored proteins in caveolae triggered by cross-linking. Science. 264: 1948-1951.
34. Beletskii, A., M. Cooper, P. Sriraman, C. Chiriac, L. Zhao, S. Abbot, and L. Yu. 2005. High-throughput phagocytosis assay utilizing a pH-sensitive fluorescent dye. Biotechniques. 39: 894-897.
35. Grinstein, S., A. Nanda, G. Lukacs, and O. Rotstein. 1992. V-ATPases in phagocytic cells. J. Exp. Biol. 172: 179-192.
36. Bowman, B. J., and E. J. Bowman. 2002. Mutations in subunit C of the vacuolar ATPase confer resistance to bafilomycin and identify a conserved antibiotic binding site. J. Biol. Chem. 277: 3965-3972.
37. Labrousse, A. M., E. Meunier, J. Record, A. Labernadie, A. Beduer, C. Vieu, T. Ben Safta, and I. Maridonneau-Parini. 2011. Frustrated phagocytosis on micro-patterned immune complexes to characterize lysosome movements in live macrophages. Front. Immunol. 2: 51.
38. Singh, A. V., M. Batuwangala, R. Mundra, K. Mehta, S. Patke, E. Falletta, R. Patil, and W. N. Gade. 2014. Biomineralized anisotropic gold microplate-macrophage interactions reveal frustrated phagocytosis-like phenomenon: a novel paclitaxel drug delivery vehicle. ACS Appl. Mater. Interfaces. 6: 14679-14689.
39. Lee, J. Y., J. Ye, Z. Gao, H. S. Youn, W. H. Lee, L. Zhao, N. Sizemore, and D. H. Hwang. 2003. Reciprocal modulation of Toll-like receptor-4 signaling pathways involving MyD88 and phosphatidylinositol 3-kinase/AKT by saturated and polyunsaturated fatty acids. J. Biol. Chem. 278: 37041-37051.
40. Lee, J. Y. K. H. Sohn S. H. Rhee D. Hwang2001Saturated fatty acids, but not unsaturated fatty acids, induce the expression of cyclooxygenase-2 mediated through Toll-like receptorJ. Biol. Chem.27616683-16689
41. Huang, S. C., B. Everts, Y. Ivanova, D. O'Sullivan, M. Nascimento, A. M. Smith, W. Beatty, L. Love-Gregory, W. Y. Lam, C. M. O'Neill, et al. 2014. Cell-intrinsic lysosomal lipolysis is essential for alternative activation of macrophages. Nat. Immunol. 15: 846-855.
42. Spann, N. J., L. X. Garmire, J. G. McDonald, D. S. Myers, S. B. Milne, N. Shibata, D. Reichart, J. N. Fox, I. Shaked, D. Heudobler, et al. 2012. Regulated accumulation of desmosterol integrates macrophage lipid metabolism and inflammatory responses. Cell. 151: 138-152.