Pivotal advance: Macrophages become resistant to cholesterol-induced death after phagocytosis of apoptotic cells

Journal of Leukocyte Biology

Volumn 82, Issue 5, 2007, Pages 1040-1050

  Cui, Dongying ^a   Thorp, Edward ^a   Li, Yankun ^a   Wang, Nan ^a   Yvan Charvet, Laurent ^a   Tall, Alan R ^a   Tabas, Ira ^a,b  

^a Och Spine at New York Presbyterian Hospitals   (United States)

^b NewYork Presbyterian Hospital   (United States)

Author keywords

Apoptosis; Atherosclerosis; Cell survival; Efferocytosis

Indexed keywords

ACYL COENZYME A; CHOLESTEROL; CHOLESTEROL ACYLTRANSFERASE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; LIPOPROTEIN; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B;

ANIMAL CELL; APOPTOSIS; ARTICLE; ATHEROSCLEROSIS; ATHEROSCLEROTIC PLAQUE; CELL DEATH; CELL FUNCTION; CELL MIGRATION; CELL SURVIVAL; CELL VIABILITY; CHOLESTEROL ESTERIFICATION; CONTROLLED STUDY; CYTOTOXICITY; DISEASE COURSE; ENDOPLASMIC RETICULUM; ESTERIFICATION; FEMALE; HUMAN; MACROPHAGE; MOUSE; NONHUMAN; PHAGOCYTE; PHAGOCYTOSIS; PRIORITY JOURNAL;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ACETYL-COA C-ACETYLTRANSFERASE; ANIMALS; APOPTOSIS; BLOTTING, WESTERN; CELL COMMUNICATION; CELLS, CULTURED; CHOLESTEROL; ENDOPLASMIC RETICULUM; ESTERIFICATION; FEMALE; MACROPHAGES, PERITONEAL; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NF-KAPPA B; PHAGOCYTES; PHAGOCYTOSIS; PROTO-ONCOGENE PROTEINS C-AKT; ULTRAVIOLET RAYS;

EID: 36249032568     PISSN: 07415400     EISSN: None     Source Type: Journal    
DOI: 10.1189/jlb.0307192     Document Type: Article

References (54)

1. Savill, J. (1997) Recognition and phagocytosis of cells undergoing apoptosis. Br. Med. Bull. 53, 491-508.
2. Henson, P. M., Bratton, D. L., Fadok, V. A. (2001) Apoptotic cell removal. Curr. Biol. 11, R795-R805.
3. Warner, G. J., Stoudt, G., Bamberger, M., Johnson, W. J., Rothblat, G. H. (1995) Cell toxicity induced by inhibition of acyl coenzyme A: cholesterol acyltransferase and accumulation of unesterified cholesterol. J. Biol. Chem. 270, 5772-5778.
4. Yao, P. M., Tabas, I. (2000) Free cholesterol loading of macrophages induces apoptosis involving the fas pathway. J. Biol. Chem. 275, 23807-23813.
5. Yao, P. M., Tabas, I. (2001) Free cholesterol loading of macrophages is associated with widespread mitochondrial dysfunction and activation of the mitochondrial apoptosis pathway. J. Biol. Chem. 276, 42468-42476.
6. Feng, B., Yao, P. M., Li, Y., Devlin, C. M., Zhang, D., Harding, H. P., Sweeney, M., Rong, J. X., Kuriakose, G., Fisher, E. A., et al. (2003) The endoplasmic reticulum is the site of cholesterol-induced cytotoxicity in macrophages. Nat. Cell Biol. 5, 781-792.
7. Ross, R. (1995) Cell biology of atherosclerosis. Annu. Rev. Physiol. 57, 791-804.
8. Glass, C. K., Witztum, J. L. (2001) Atherosclerosis: the road ahead. Cell 104, 503-516.
9. Lusis, A. J. (2000) Atherosclerosis. Nature 407, 233-241.
10. Kockx, M. M. (1998) Apoptosis in the atherosclerotic plaque: quantitative and qualitative aspects. Arterioscler. Thromb. Vasc. Biol. 18, 1519-1522.
11. Tabas, I. (2002) Consequences of cellular cholesterol accumulation: basic concepts and physiological implications. J. Clin. Invest. 110, 905-911.
12. Schaefer, H. E. (1981) The role of macrophages in atherosclerosis. Haematol. Blood Transfus. 27, 137-142.
13. Ball, R. Y., Stowers, E. C., Burton, J. H., Cary, N. R., Skepper, J. N., Mitchinson, M. J. (1995) Evidence that the death of macrophage foam cells contributes to the lipid core of atheroma. Atherosclerosis 114, 45-54.
14. Libby, P., Clinton, S. K. (1993) The role of macrophages in atherogenesis. Curr. Opin. Lipidol. 4, 355-363.
15. Hegyi, L., Skepper, J. N., Cary, N. R. B., Mitchinson, M. J. (1996) Foam cell apoptosis and the development of the lipid core of human atherosclerosis. J. Pathol. 180, 423-429.
16. Burke, A. P., Virmani, R., Galis, Z., Haudenschild, C. C., Muller, J. E. (2003) 34th Bethesda Conference: Task force #2-What is the pathologic basis for new atherosclerosis imaging techniques? J. Am. Coll. Cardiol. 41, 1874-1886.
17. Naghavi, M., Libby, P., Falk, E., Casscells, S. W., Litovsky, S., Rumberger, J., Badimon, J. J., Stefanadis, C., Moreno, P., Pasterkamp, G., et al. (2003) From vulnerable plaque to vulnerable patient: a call for new definitions and risk assessment strategies: Part I. Circulation 108, 1664-1672.
18. Tabas, I. (2005) Consequences and therapeutic implications of macrophage apoptosis in atherosclerosis: the importance of lesion stage and phagocytic efficiency. Arterioscler. Thromb. Vasc. Biol. 25, 2255-2264.
19. Schrijvers, D. M., De Meyer, G. R., Herman, A. G., Martinet, W. (2007) Phagocytosis in atherosclerosis: Molecular mechanisms and implications for plaque progression and stability. Cardiovasc. Res. 73, 470-480.
20. Havel, R. J., Eder, H., Bragdon, J. (1955) The distribution and chemical composition of ultracentrifugally reported lipoproteins in human serum. J. Clin. Invest. 34, 1345-1353.
21. Basu, S. K., Goldstein, J. L., Anderson, R. G. W., Brown, M. S. (1976) Degradation of cationized low density lipoprotein and regulation of cholesterol metabolism in homozygous familial hypercholesterolemia fibroblasts. Proc. Natl. Acad. Sci. USA 73, 3178-3182.
22. Pitas, R. E., Innerarity, T. L., Weinstein, J. N., Mahley, R. W. (1981) Acetoacetylated lipoproteins used to distinguish fibroblasts from macrophages in vitro by fluorescence microscopy. Arteriosclerosis 1, 177-185.
23. Ross, A. C., Go, K. J., Heider, J. G., Rothblat, G. H. (1984) Selective inhibition of acyl coenzyme A:cholesterol acyltransferase by compound 58-035. J. Biol. Chem. 259, 815-819.
24. Hideshima, T., Chauhan, D., Richardson, P., Mitsiades, C., Mitsiades, N., Hayashi, T., Munshi, N., Dang, L., Castro, A., Palombella, V., et al. (2002) NF-kappa B as a therapeutic target in multiple myeloma. J. Biol. Chem. 277, 16639-16647.
25. Cho, J., Melnick, M., Solidakis, G. P., Tsichlis, P. N. (2005) Tpl2 (tumor progression locus 2) phosphorylation at Thr290 is induced by lipopolysaccharide via an Ikappa-B Kinase-beta-dependent pathway and is required for Tpl2 activation by external signals. J. Biol. Chem. 280, 20442-20448.
26. Li, Y., Gerbod-Giannone, M. C., Seitz, H., Cui, D., Thorp, E., Tall, A. R., Matsushima, G. K., Tabas, I. (2006) Cholesterol-induced apoptotic macrophages elicit an inflammatory response in phagocytes, which is partially attenuated by the Mer receptor. J. Biol. Chem. 281, 6707-6717.
27. Accad, M., Smith, S. J., Newland, D. L., Sanan, D. A., King, L. E., Jr., Linton, M. F., Fazio, S., Farese, R. V., Jr. (2000) Massive xanthomatosis and altered composition of atherosclerotic lesions in hyperlipidemic mice lacking acyl CoA:cholesterol acyltransferase 1. J. Clin. Invest. 105, 711-719.
28. Tabas, I., Boykow, G. C., Tall, A. R. (1987) Foam cell-forming J774 macrophages have markedly elevated acyl coenzyme A:cholesterol acyl transferase activity compared with mouse peritoneal macrophages in the presence of low density lipoproteins (LDL) despite similar LDL receptor activity. J. Clin. Invest. 79, 418-426.
29. Lowry, O. H., Rosenbrough, N. J., Farr, A. L., Randall, R. J. (1951) Protein measurement with the folin phenol reagent. J. Biol. Chem. 193, 265-275.
30. Shiratori, Y., Okwu, A. K., Tabas, I. (1994) Free cholesterol loading of macrophages stimulates phosphatidylcholine biosynthesis and up-regulation of CTP:phosphocholine cytidylyltransferase. J. Biol. Chem. 269, 11337-11348.
31. Katz, S. S., Shipley, G. G., Small, D. M. (1976) Physical chemistry of the lipids of human atherosclerotic lesions. Demonstration of a lesion intermediate between fatty streaks and advanced plaques. J. Clin. Invest. 58, 200-211.
32. Rapp, J. H., Connor, W. E., Lin, D. S., Inahara, T., Porter, J. M. (1983) Lipids of human atherosclerotic plaques and xanthomas: clues to the mechanism of plaque progression. J. Lipid Res. 24, 1329-1335.
33. Shio, H., Haley, N. J., Fowler, S. (1979) Characterization of lipid-laden aortic cells from cholesterol-fed rabbits. III. Intracellular localization of cholesterol and cholesteryl ester. Lab. Invest. 41, 160-167.
34. Kruth, H. S., Fry, D. L. (1984) Histochemical detection and differentiation of free and esterified cholesterol in swine atherosclerosis using filipin. Exp. Mol. Pathol. 40, 288-294.
35. Kellner-Weibel, G., Jerome, W. G., Small, D. M., Warner, G. J., Stoltenborg, J. K., Kearney, M. A., Corjay, M. H., Phillips, M. C., Rothblat, G. H. (1998) Effects of intracellular free cholesterol accumulation on macrophage viability: a model for foam cell death. Arterioscler. Thromb. Vasc. Biol. 18, 423-431.
36. Feng, B., Zhang, D., Kuriakose, G., Devlin, C. M., Kockx, M., Tabas, I. (2003) Niemann-Pick C heterozygosity confers resistance to lesional necrosis and macrophage apoptosis in murine atherosclerosis. Proc. Natl. Acad. Sci. USA 100, 10423-10428.
37. DeVries-Seimon, T., Li, Y., Yao, P. M., Stone, E., Wang, Y., Davis, R. J., Flavell, R., Tabas, I. (2005) Cholesterol-induced macrophage apoptosis requires ER stress pathways and engagement of the type A scavenger receptor. J. Cell Biol. 171, 61-73.
38. Seimon, T. A., Obstfeld, A., Moore, K. J., Golenbock, D. T., Tabas, I. (2006) Combinatorial pattern recognition receptor signaling alters the balance of life and death in macrophages. Proc. Natl. Acad. Sci. USA 103, 19794-19799.
39. Zhou, J., Lhotak, S., Hilditch, B. A., Austin, R. C. (2005) Activation of the unfolded protein response occurs at all stages of atherosclerotic lesion development in apolipoprotein E-deficient mice. Circulation 111, 1814-1821.
40. Maxfield, F. R., Tabas, I. (2005) Role of cholesterol and lipid organization in disease. Nature 438, 612-621.
41. Cuchel, M., Rader, D. J. (2006) Macrophage reverse cholesterol transport: key to the regression of atherosclerosis? Circulation 113, 2548-2555.
42. Beg, A. A., Baltimore, D. (1996) An essential role for NF-κB in preventing TNF-alpha-induced cell death. Science 274, 782-784.
43. Karin, M. (1998) The NF-κ B activation pathway: its regulation and role in inflammation and cell survival. Cancer J. Sci. Am. 4, Suppl 1, S92-S99.
44. Amaravadi, R., Thompson, C. B. (2005) The survival kinases Akt and Pim as potential pharmacological targets. J. Clin. Invest. 115, 2618-2624.
45. Dudek, H., Datta, S. R., Franke, T. F., Birnbaum, M. J., Yao, R., Cooper, G. M., Segal, R. A., Kaplan, D. R., Greenberg, M. E. (1997) Regulation of neuronal survival by the serine-threonine protein kinase Akt. Science 275, 661-665.
46. Gerbod-Giannone, M. C., Li, Y., Holleboom, A., Han, S., Hsu, L. C., Tabas, I., Tall, A. R. (2006) TNFα induces ABCA1 through NF-κB in macrophages and in phagocytes ingesting apoptotic cells. Proc. Natl. Acad. Sci. USA 103, 3112-3117.
47. Kiss, R. S., Elliott, M. R., Ma, Z., Marcel, Y. L., Ravichandran, K. S. (2006) Apoptotic cells induce a phosphatidylserine-dependent homeostatic response from phagocytes. Curr. Biol. 16, 2252-2258.
48. Feng, B., Tabas, I. (2002) ABCA1-mediated cholesterol efflux is defective in free cholesterol-loaded macrophages. Mechanism involves enhanced ABCA1 degradation in a process requiring full NPC1 activity. J. Biol. Chem. 277, 43271-43280.
49. Li, Y., Schwabe, R. F., DeVries-Seimon, T., Yao, P. M., Gerbod-Giannone, M. C., Tall, A. R., Davis, R. J., Flavell, R., Brenner, D. A., Tabas, I. (2005) Free cholesterol-loaded macrophages are an abundant source of tumor necrosis factor-alpha and interleukin-6: model of NF-κB- and MAP kinase-dependent inflammation in advanced atherosclerosis. J. Biol. Chem. 280, 21763-21772.
50. Marshall, J. G., Booth, J. W., Stambolic, V., Mak, T., Balla, T., Schreiber, A. D., Meyer, T., Grinstein, S. (2001) Restricted accumulation of phosphatidylinositol 3-kinase products in a plasmalemmal subdomain during Fc gamma receptor-mediated phagocytosis. J. Cell Biol. 153, 1369-1380.
51. Chawla, A., Boisvert, W. A., Lee, C. H., Laffitte, B. A., Barak, Y., Joseph, S. B., Liao, D., Nagy, L., Edwards, P. A., Curtiss, L. K., et al. (2001) A PPAR gamma-LXR-ABCA1 pathway in macrophages is involved in cholesterol efflux and atherogenesis. Mol. Cell 7, 161-171.
52. Joseph, S. B., Bradley, M. N., Castrillo, A., Bruhn, K. W., Mak, P. A., Pei, L., Hogenesch, J., O'Connell, R. M., Cheng, G., Saez, E. et al. (2004) LXR-dependent gene expression is important for macrophage survival and the innate immune response. Cell 119, 299-309.
53. Reddy, S. M., Hsiao, K. H., Abernethy, V. E., Fan, H., Longacre, A., Lieberthal, W., Rauch, J., Koh, J. S., Levine, J. S. (2002) Phagocytosis of apoptotic cells by macrophages induces novel signaling events leading to cytokine-independent survival and inhibition of proliferation: activation of Akt and inhibition of extracellular signal-regulated kinases 1 and 2. J. Immunol. 169, 702-713.
54. Weigert, A., Johann, A. M., von Knethen, A., Schmidt, H., Geisslinger, G., Brune, B. (2006) Apoptotic cells promote macrophage survival by releasing the anti-apoptotic mediator sphingosine-1-phosphate. Blood 108, 1635-1642.