Apolipoprotein E4 impairs macrophage efferocytosis and potentiates apoptosis by accelerating endoplasmic reticulum stress

Journal of Biological Chemistry

Volumn 287, Issue 33, 2012, Pages 27876-27884

  Cash, James G ^a   Kuhel, David G ^a   Basford, Joshua E ^a   Jaeschke, Anja ^a   Chatterjee, Tapan K ^a   Weintraub, Neal L ^a   Hui, David Y ^a  

^a UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADIPOSE TISSUE; ALZHEIMER DISEASE; APOLIPOPROTEINS; BODY WEIGHT; CELL LYSATES; CELL STRESS; ENDOPLASMIC RETICULUM STRESS; ER STRESS; FUNCTIONAL PROPERTIES; GENE REPLACEMENT; GENETIC RISKS; METABOLIC DISEASE; METABOLIC DISORDERS; PERITONEAL MACROPHAGE; WESTERN-BLOT ANALYSIS; WIDE SPECTRUM;

ACTIVATION ANALYSIS; CELL DEATH; CELL MEMBRANES; GENES; MAMMALS; METABOLISM; NUTRITION; PATHOLOGY; PHOSPHORYLATION; TISSUE;

MACROPHAGES;

APOLIPOPROTEIN E3; APOLIPOPROTEIN E4; LIPOPOLYSACCHARIDE; MESSENGER RNA; OXIDIZED LIPOPOLYSACCHARIDE; STRESS ACTIVATED PROTEIN KINASE; TAURODEOXYCHOLIC ACID; UNCLASSIFIED DRUG;

ADIPOSE TISSUE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL DEATH; CELL LYSATE; CELL STIMULATION; CELL STRESS; CONTROLLED STUDY; DIETARY INTAKE; EFFEROCYTOSIS; ENDOPLASMIC RETICULUM STRESS; ENZYME PHOSPHORYLATION; GENETIC MANIPULATION; HUMAN; HUMAN CELL; HYPERINSULINEMIA; INFLAMMATION; INTRACELLULAR SIGNALING; MACROPHAGE FUNCTION; METABOLIC DISORDER; MOUSE; NONHUMAN; PERITONEUM MACROPHAGE; PHAGOCYTOSIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN POLYMORPHISM; WEIGHT GAIN; WESTERN BLOTTING;

ADIPOSE TISSUE; ALZHEIMER DISEASE; ANIMALS; APOLIPOPROTEIN E3; APOLIPOPROTEIN E4; APOPTOSIS; CELLS, CULTURED; CHOLAGOGUES AND CHOLERETICS; ENDOPLASMIC RETICULUM STRESS; GENE EXPRESSION REGULATION; HYPERINSULINISM; INFLAMMATION; LIPOPOLYSACCHARIDES; LIPOPROTEINS, LDL; MACROPHAGES, PERITONEAL; MAP KINASE KINASE 4; METABOLIC DISEASES; MICE; MICE, TRANSGENIC; PHOSPHORYLATION; POLYMORPHISM, GENETIC; SIGNAL TRANSDUCTION; TAUROCHENODEOXYCHOLIC ACID;

EID: 84865011518     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.377549     Document Type: Article

References (58)

1. Mahley, R. W. (1988) Apolipoprotein E. Cholesterol transport protein with expanding role in cell biology. Science 240, 622-630
2. Getz, G. S., and Reardon, C. A. (2009) Apoprotein E as a lipid transport and signaling protein in the blood, liver, and artery wall. J. Lipid Res. 50, S156-S161
3. Mahley, R. W., Weisgraber, K. H., and Huang, Y. (2009) Apolipoprotein E. Structure determines function, from atherosclerosis to Alzheimer disease to AIDS. J. Lipid Res. 50, S183-S188
4. Song, Y., Stampfer, M. J., and Liu, S. (2004) Meta-analysis. Apolipoprotein E genotypes and risk for coronary heart disease. Ann. Intern. Med. 141, 137-147
5. Bu, G. (2009) Apolipoprotein E and its receptors in Alzheimer disease. Pathways, pathogenesis, and therapy. Nat. Rev. Neurosci. 10, 333-344
6. Jofre-Monseny, L., Minihane, A. M., and Rimbach, G. (2008) Impact of apoE genotype on oxidative stress, inflammation, and disease risk. Mol. Nutr. Food Res. 52, 131-145
7. Zhu, Y., Kodvawala, A., and Hui, D. Y. (2010) Apolipoprotein E inhibits Toll-like receptor (TLR)-3- and TLR-4-mediated macrophage activation through distinct mechanisms. Biochem. J. 428, 47-54
8. Baitsch, D., Bock, H. H., Engel, T., Telgmann, R., Müller-Tidow, C., Varga, G., Bot, M., Herz, J., Robenek, H., von Eckardstein, A., and Nofer, J. R. (2011) Apolipoprotein E induces anti-inflammatory phenotype in macrophages. Arterioscler. Thromb. Vasc. Biol. 31, 1160-1168
9. Sacre, S. M., Stannard, A. K., and Owen, J. S. (2003) Apolipoprotein E (apoE) isoforms differentially induce nitric oxide production in endothelial cells. FEBS Lett. 540, 181-187
10. Ishigami, M., Swertfeger, D. K., Granholm, N. A., and Hui, D. Y. (1998) Apolipoprotein E inhibits platelet-derived growth factor-induced vascular smooth muscle cell migration and proliferation by suppressing signal transduction and preventing cell entry to G1 phase. J. Biol. Chem. 273, 20156-20161
11. Ishigami, M., Swertfeger, D. K., Hui, M. S., Granholm, N. A., and Hui, D. Y. (2000) Apolipoprotein E inhibition of vascular smooth muscle cell proliferation but not the inhibition of migration is mediated through activation of inducible nitric-oxide synthase. Arterioscler. Thromb. Vasc. Biol. 20, 1020-1026
12. Moore, Z. W., and Hui, D. Y. (2005) Apolipoprotein E inhibition of vascular hyperplasia and neointima formation requires inducible nitric-oxide synthase. J. Lipid Res. 46, 2083-2090
13. Moore, Z. W., Zhu, B., Kuhel, D. G., and Hui, D. Y. (2004) Vascular apolipoprotein E expression and recruitment from circulation to modulate smooth muscle cell response to endothelial denudation. Am. J. Pathol. 164, 2109-2116
14. Marques, M. A., and Crutcher, K. A. (2003) Apolipoprotein E-related neurotoxicity as a therapeutic target for Alzheimer disease. J. Mol. Neurosci. 20, 327-337
15. Ji, Z. S., Miranda, R. D., Newhouse, Y. M., Weisgraber, K. H., Huang, Y., and Mahley, R. W. (2002) Apolipoprotein E4 potentiates amyloid β peptide- induced lysosomal leakage and apoptosis in neuronal cells. J. Biol. Chem. 277, 21821-21828
16. Ji, Z. S., Müllendorff, K., Cheng, I. H., Miranda, R. D., Huang, Y., and Mahley, R. W. (2006) Reactivity of apolipoprotein E4 and amyloid β peptide. Lysosomal stability and neurodegeneration. J. Biol. Chem. 281, 2683-2692
17. Volcik, K. A., Barkley, R. A., Hutchinson, R. G., Mosley, T. H., Heiss, G., Sharrett, A. R., Ballantyne, C. M., and Boerwinkle, E. (2006) Apolipoprotein E polymorphisms predict low density lipoprotein cholesterol levels and carotid artery wall thickness but not incident coronary heart disease in 12,491 ARIC study participants. Am. J. Epidemiol. 164, 342-348
18. Sima, A., Iordan, A., and Stancu, C. (2007) Apolipoprotein E polymorphism. A risk factor for metabolic syndrome. Clin. Chem. Lab. Med. 45, 1149-1153
19. Anthopoulos, P. G., Hamodrakas, S. J., and Bagos, P. G. (2010) Apolipoprotein E polymorphisms and type 2 diabetes. A meta-analysis of 30 studies, including 5423 cases and 8192 controls. Mol. Genet. Metab. 100, 283-291
20. Vaisi-Raygani, A., Rahimi, Z., Nomani, H., Tavilani, H., and Pourmotabbed, T. (2007) The presence of apolipoprotein ε4 and ε2 alleles augments the risk of coronary artery disease in type 2 diabetic patients. Clin. Biochem. 40, 1150-1156
21. Arbones-Mainar, J. M., Johnson, L. A., Altenburg, M. K., and Maeda, N. (2008) Differential modulation of diet-induced obesity and adipocyte functionality by human apolipoprotein E3 and E4 in mice. Int. J. Obes. 32, 1595-1605
22. Arbones-Mainar, J. M., Johnson, L. A., Altenburg, M. K., Kim, H. S., and Maeda, N. (2010) Impaired adipogenic response to thiazolidinediones in mice expressing human apolipoprotein E4. FASEB J. 24, 3809-3818
23. Johnson, L. A., Arbones-Mainar, J. M., Fox, R. G., Pendse, A. A., Altenburg, M. K., Kim, H. S., and Maeda, N. (2011) Apolipoprotein E4 exaggerates diabetic dyslipidemia and atherosclerosis in mice lacking the LDL receptor. Diabetes 60, 2285-2294
24. Altenburg, M., Johnson, L., Wilder, J., and Maeda, N. (2007) Apolipoprotein E4 in macrophages enhances atherogenesis in a low density lipoprotein receptor-dependent manner. J. Biol. Chem. 282, 7817-7824
25. Ley, K., Miller, Y. I., and Hedrick, C. C. (2011) Monocyte and macrophage dynamics during atherogenesis. Arterioscler. Thromb. Vasc. Biol. 31, 1506-1516
26. Olefsky, J. M., and Glass, C. K. (2010) Macrophages, inflammation, and insulin resistance. Annu. Rev. Physiol. 72, 219-246
27. Chinetti-Gbaguidi, G., and Staels, B. (2011) Macrophage polarization in metabolic disorders. Functions and regulation. Curr. Opin. Lipidol. 22, 365-372
28. Sullivan, P. M., Mezdour, H., Aratani, Y., Knouff, C., Najib, J., Reddick, R. L., Quarfordt, S. H., and Maeda, N. (1997) Targeted replacement of the mouse apolipoprotein E gene with the common human apoE3 allele enhances diet-induced hypercholesterolemia and atherosclerosis. J. Biol. Chem. 272, 17972-17980
29. Knouff, C., Hinsdale, M. E., Mezdour, H., Altenburg, M. K., Watanabe, M., Quarfordt, S. H., Sullivan, P. M., and Maeda, N. (1999) ApoE structure determines VLDL clearance and atherosclerosis risk in mice. J. Clin. Invest. 103, 1579-1586
30. Hofmann, S. M., Zhou, L., Perez-Tilve, D., Greer, T., Grant, E., Wancata, L., Thomas, A., Pfluger, P. T., Basford, J. E., Gilham, D., Herz, J., Tschöp, M. H., and Hui, D. Y. (2007) Adipocyte LDL receptor-related protein-1 expression modulates postprandial lipid transport and glucose homeostasis in mice. J. Clin. Invest. 117, 3271-3282
31. Cash, J. G., Kuhel, D. G., Goodin, C., and Hui, D. Y. (2011) Pancreatic acinar cell-specific overexpression of group 1B phospholipase A2 exacerbates diet-induced obesity and insulin resistance in mice. Int. J. Obes. 35, 877-881
32. Kodvawala, A., Ghering, A. B., Davidson, W. S., and Hui, D. Y. (2005) Carboxyl ester lipase expression in macrophages increases cholesteryl ester accumulation and promotes atherosclerosis. J. Biol. Chem. 280, 38592-38598
33. Mahley, R. W., and Rall, S. C. (1989) in The Metabolic Basis of Inherited Disease (Scriver, C. R., Beaudet, A. L., Sly, W. S., and Valle, D., eds) pp. 1195-1213, McGraw-Hill, Inc., New York
34. Weisberg, S. P., McCann, D., Desai, M., Rosenbaum, M., Leibel, R. L., and Ferrante, A. W., Jr. (2003) Obesity is associated with macrophage accumulation in adipose tissue. J. Clin. Invest. 112, 1796-1808
35. Savill, J., Dransfield, I., Gregory, C., and Haslett, C. (2002) A blast from the past. Clearance of apoptotic cells regulates immune responses. Nat. Rev. Immunol. 2, 965-975
36. Elliott, M. R., and Ravichandran, K. S. (2010) Clearance of apoptotic cells. Implications in health and disease. J. Cell Biol. 189, 1059-1070
37. Xaus, J., Comalada, M., Valledor, A. F., Lloberas, J., López-Soriano, F., Argilés, J. M., Bogdan, C., and Celada, A. (2000) LPS induces apoptosis in macrophages mostly through the autocrine production of TNF-α. Blood 95, 3823-3831
38. Terasaka, N., Wang, N., Yvan-Charvet, L., and Tall, A. R. (2007) High density lipoprotein protects macrophages from oxidized low density lipo-protein- induced apoptosis by promoting efflux of 7-ketocholesterol via ABCG1. Proc. Natl. Acad. Sci. U.S.A. 104, 15093-15098
39. Martinon, F., Chen, X., Lee, A. H., and Glimcher, L. H. (2010) TLR activation of the transcription factor XBP1 regulates innate immune responses in macrophages. Nat. Immunol. 11, 411-418
40. Uemura, A., Oku, M., Mori, K., and Yoshida, H. (2009) Unconventional splicing of XBP1 mRNA occurs in the cytoplasm during the mammalian unfolded protein response. J. Cell Sci. 122, 2877-2886
41. Park, S. W., Zhou, Y., Lee, J., Lu, A., Sun, C., Chung, J., Ueki, K., and Ozcan, U. (2010) The regulatory subunits of PI3K, p85α and p85β, interact with XBP-1 and increase its nuclear translocation. Nat. Med. 16, 429-437
42. Vitek, M. P., Brown, C. M., and Colton, C. A. (2009) APOE genotypespecific differences in the innate immune response. Neurobiol. Aging 30, 1350-1360
43. Thorp, E., Li, G., Seimon, T. A., Kuriakose, G., Ron, D., and Tabas, I. (2009) Reduced apoptosis and plaque necrosis in advanced atherosclerotic lesions of apoE-/- and Ldlr-/- mice lacking CHOP. Cell Metab. 9, 474-481
44. Thorp, E., and Tabas, I. (2009) Mechanisms and consequences of efferocytosis in advanced atherosclerosis. J. Leukocyte Biol. 86, 1089-1095
45. Zhong, N., Ramaswamy, G., and Weisgraber, K. H. (2009) Apolipoprotein E4 domain interaction induces endoplasmic reticulum stress and impairs astrocyte function. J. Biol. Chem. 284, 27273-27280
46. Chen, H. K., Ji, Z. S., Dodson, S. E., Miranda, R. D., Rosenblum, C. I., Reynolds, I. J., Freedman, S. B., Weisgraber, K. H., Huang, Y., and Mahley, R. W. (2011) Apolipoprotein E4 domain interaction mediates detrimental effects on mitochondria and is a potential therapeutic target for Alzheimer disease. J. Biol. Chem. 286, 5215-5221
47. Vats, D., Mukundan, L., Odegaard, J. I., Zhang, L., Smith, K. L., Morel, C. R., Wagner, R. A., Greaves, D. R., Murray, P. J., and Chawla, A. (2006) Oxidative metabolism and PGC-1beta attenuate macrophage-mediated inflammation. Cell Metab. 4, 13-24
48. Madamanchi, N. R., and Runge, M. S. (2007) Mitochondrial dysfunction in atherosclerosis. Circ. Res. 100, 460-473
49. Lowell, B. B., and Shulman, G. I. (2005) Mitochondrial dysfunction and type 2 diabetes. Science 307, 384-387
50. Dong, L. M., and Weisgraber, K. H. (1996) Human apolipoprotein E4 domain interaction. Arginine 61 and glutamic acid 255 interact to direct the preference for very low density lipoproteins. J. Biol. Chem. 271, 19053-19057
51. Dong, L. M., Wilson, C., Wardell, M. R., Simmons, T., Mahley, R. W., Weisgraber, K. H., and Agard, D. A. (1994) Human apolipoprotein E. Role of arginine 61 in mediating the lipoprotein preferences of the E3 and E4 isoforms. J. Biol. Chem. 269, 22358-22365
52. Wilson, C., Wardell, M. R., Weisgraber, K. H., Mahley, R. W., and Agard, D. A. (1991) Three-dimensional structure of the LDL receptor binding domain of human apolipoprotein E. Science 252, 1817-1822
53. Morrow, J. A., Hatters, D. M., Lu, B., Hochtl, P., Oberg, K. A., Rupp, B., and Weisgraber, K. H. (2002) Apolipoprotein E4 forms a molten globule. A potential basis for its association with disease. J. Biol. Chem. 277, 50380-50385
54. Weisgraber, K. H. (1994) Apolipoprotein E. Structure-function relationships. Adv. Protein Chem. 45, 249-302
55. Hatters, D. M., Budamagunta, M. S., Voss, J. C., and Weisgraber, K. H. (2005) Modulation of apolipoprotein E structure by domain interaction. J. Biol. Chem. 280, 34288-34295
56. Eberlé, D., Kim, R. Y., Luk, F. S., de Mochel, N. S., Gaudreault, N., Olivas, V. R., Kumar, N., Posada, J. M., Birkeland, A. C., Rapp, J. H., and Raffai, R. L. (2012) Apolipoprotein E4 domain interaction accelerates diet-induced atherosclerosis in hypomorphic Arg-61 ApoE mice. Arterioscler. Thromb. Vasc. Biol. 32, 1116-1123
57. Brodbeck, J., McGuire, J., Liu, Z., Meyer-Franke, A., Balestra, M. E., Jeong, D. E., Pleiss, M., McComas, C., Hess, F., Witter, D., Peterson, S., Childers, M., Goulet, M., Liverton, N., Hargreaves, R., Freedman, S., Weisgraber, K. H., Mahley, R. W., and Huang, Y. (2011) Structure-dependent impairment of intracellular apolipoprotein E4 trafficking is rescued by small molecule structure correctors. J. Biol. Chem. 286, 17217-17226
58. Chen, H. K., Liu, Z., Meyer-Franke, A., Brodbeck, J., Miranda, R. D., McGuire, J. G., Pleiss, M. A., Ji, Z. S., Balestra, M. E., Walker, D. W., Xu, Q., Jeong, D. E., Budamagunta, M. S., Voss, J. C., Freedman, S. B., Weisgraber, K. H., Huang, Y., and Mahley, R. W. (2012) Small molecule structure correctors abolish detrimental effects of apolipoprotein E4 in cultured neurons. J. Biol. Chem. 287, 5253-5266