Foam cells in atherosclerosis

Clinica Chimica Acta

Volumn 424, Issue , 2013, Pages 245-252

  Yu, Xiao Hua ^a   Fu, Yu Chang ^b   Zhang, Da Wei ^c   Yin, Kai ^a   Tang, Chao Ke ^a  

^a UNIVERSITY OF SOUTH CHINA   (China)

^b UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^c UNIVERSITY OF ALBERTA   (Canada)

Author keywords

ABCA1; ABCG1; ACAT1; Atherosclerosis; CD36; Foam cells

Indexed keywords

ABC TRANSPORTER A1; ABC TRANSPORTER G1; ALPHA INTERFERON; ATORVASTATIN; CANDESARTAN; CD36 ANTIBODY; CD36 ANTIGEN; CHOLESTEROL ACYLTRANSFERASE; CHOLESTEROL ACYLTRANSFERASE 1; CHOLESTEROL ESTERASE; CORIOLIC ACID; CURCUMIN; HIGH DENSITY LIPOPROTEIN CHOLESTEROL; HYDROGEN SULFIDE; KAEMPFEROL; LIPOPROTEIN; LOW DENSITY LIPOPROTEIN RECEPTOR; MULBERRY EXTRACT; OMEGA 3 FATTY ACID; PROTEIN ANTIBODY; PROTOCATECHUIC ACID; RESVERATROL; SCAVENGER RECEPTOR A; SCAVENGER RECEPTOR BI; TANSHINONE IIA; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ABCA1 GENE; ACUTE CORONARY SYNDROME; AORTA ATHEROSCLEROSIS; ATHEROGENESIS; ATHEROSCLEROSIS; ATHEROSCLEROTIC PLAQUE; CARDIOVASCULAR RISK; CHOLESTEROL ESTERIFICATION; CHOLESTEROL TRANSPORT; DIET SUPPLEMENTATION; FOAM CELL; GENE; GENE EXPRESSION REGULATION; GENE SILENCING; HUMAN; HYPERLIPIDEMIA; LIPID COMPOSITION; LIPID STORAGE; NCEH GENE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; RISK REDUCTION; SR A GENE; SR BI GENE;

ABCA1; ABCG1; ACAT1; ACYL COENZYME A:CHOLESTEROL ACYLTRANSFERASE-1; ADVANCED GLYCATION END PRODUCTS; AGE; APOA-I; APOE; APOLIPOPROTEIN A-I; APOLIPOPROTEIN E; ATHEROSCLEROSIS; ATP-BINDING CASSETTE TRANSPORTER A1; ATP-BINDING CASSETTE TRANSPORTER G1; CD36; CE; CHOLESTEROL ESTER; ERK1/2; EXTRACELLULAR SIGNAL-REGULATED KINASES 1 AND 2; FC; FOAM CELLS; FREE CHOLESTEROL; HDL; HIGH-DENSITY LIPOPROTEIN; LDLR; LIVER X RECEPTOR; LOW-DENSITY LIPOPROTEIN RECEPTOR; LXR; MAPK; MITOGEN-ACTIVATED PROTEIN KINASE; NCEH; NEUTRAL CHOLESTERYL ESTER HYDROLASE; OX-LDL; OXIDIZED LOW-DENSITY LIPOPROTEIN; PEROXISOME PROLIFERATOR-ACTIVATED RECEPTOR-Γ; PHOSPHATIDYLINOSITOL 3-KINASE; PI3K; PKB; PKC; PPAR RESPONSE ELEMENTS; PPAR-Γ; PPRES; PROTEIN KINASE B; PROTEIN KINASE C; RCT; RETINOID X RECEPTOR; REVERSE CHOLESTEROL TRANSPORT; RXR; SCAVENGER RECEPTOR BI; SCAVENGER RECEPTOR CLASS A; SR-A; SR-BI; TGF-Β; TRANSFORMING GROWTH FACTOR-Β;

ACETYL-COA C-ACETYLTRANSFERASE; ANTIGENS, CD36; ATHEROSCLEROSIS; ATP BINDING CASSETTE TRANSPORTER 1; ATP-BINDING CASSETTE TRANSPORTERS; BIOLOGICAL TRANSPORT; CARBOXYLIC ESTER HYDROLASES; CHOLESTEROL; FOAM CELLS; GENE EXPRESSION REGULATION; HUMANS; LIPOPROTEINS, LDL; SCAVENGER RECEPTORS, CLASS A; SCAVENGER RECEPTORS, CLASS B; SIGNAL TRANSDUCTION;

EID: 84880356469     PISSN: 00098981     EISSN: 18733492     Source Type: Journal    
DOI: 10.1016/j.cca.2013.06.006     Document Type: Review

References (85)

1. Collot-Teixeira S., Martin J., McDermott-Roe C., Poston R., McGregor J.L. CD36 and macrophages in atherosclerosis. Cardiovasc Res 2007, 75:468-477.
2. Ghosh S., Zhao B., Bie J., Song J. Macrophage cholesteryl ester mobilization and atherosclerosis. Vascul Pharmacol 2010, 52:1-10.
3. Jessup W., Gelissen I.C., Gaus K., Kritharides L. Roles of ATP binding cassette transporters A1 and G1, scavenger receptor BI and membrane lipid domains in cholesterol export from macrophages. Curr Opin Lipidol 2006, 17:247-257.
4. Kunjathoor V.V., Febbraio M., Podrez E.A., et al. Scavenger receptors class A-I/II and CD36 are the principal receptors responsible for the uptake of modified low density lipoprotein leading to lipid loading in macrophages. J Biol Chem 2002, 277:49982-49988.
5. Handberg A., Hojlund K., Gastaldelli A., et al. Plasma sCD36 is associated with markers of atherosclerosis, insulin resistance and fatty liver in a nondiabetic healthy population. J Intern Med 2012, 271:294-304.
6. Piechota M., Banaszewska A., Dudziak J., Slomczynski M., Plewa R. Highly upregulated expression of CD36 and MSR1 in circulating monocytes of patients with acute coronary syndromes. Protein J 2012, 31:511-518.
7. Geloen A., Helin L., Geeraert B., Malaud E., Holvoet P., Marguerie G. CD36 inhibitors reduce postprandial hypertriglyceridemia and protect against diabetic dyslipidemia and atherosclerosis. PLoS One 2012, 7:e37633.
8. Rac M.E., Safranow K., Rac M., et al. CD36 gene is associated with thickness of atheromatous plaque and ankle-brachial index in patients with early coronary artery disease. Kardiol Pol 2012, 70:918-923.
9. Moore K.J., Kunjathoor V.V., Koehn S.L., et al. Loss of receptor-mediated lipid uptake via scavenger receptor A or CD36 pathways does not ameliorate atherosclerosis in hyperlipidemic mice. J Clin Invest 2005, 115:2192-2201.
10. Yuasa-Kawase M., Masuda D., Yamashita T., et al. Patients with CD36 deficiency are associated with enhanced atherosclerotic cardiovascular diseases. J Atheroscler Thromb 2012, 19:263-275.
11. Inoue M., Tanabe H., Matsumoto A., et al. Astaxanthin functions differently as a selective peroxisome proliferator-activated receptor gamma modulator in adipocytes and macrophages. Biochem Pharmacol 2012, 84:692-700.
12. Mimche P.N., Thompson E., Taramelli D., Vivas L. Curcumin enhances non-opsonic phagocytosis of Plasmodium falciparum through up-regulation of CD36 surface expression on monocytes/macrophages. J Antimicrob Chemother 2012, 67:1895-1904.
13. Gao D., Pararasa C., Dunston C.R., Bailey C.J., Griffiths H.R. Palmitate promotes monocyte atherogenicity via de novo ceramide synthesis. Free Radic Biol Med 2012, 53:796-806.
14. Goncalves J.L., Roma E.H., Gomes-Santos A.C., et al. Pro-inflammatory effects of the mushroom Agaricus blazei and its consequences on atherosclerosis development. Eur J Nutr 2012, 51:927-937.
15. Choi J.S., Bae J.Y., Kim D.S., et al. Dietary compound quercitrin dampens VEGF induction and PPARgamma activation in oxidized LDL-exposed murine macrophages: association with scavenger receptor CD36. J Agric Food Chem 2010, 58:1333-1341.
16. -/-) mice through down-regulation of scavenger receptor expression. Eur J Pharmacol 2011, 650:275-284.
17. Chiurchiu V., Izzi V., D'Aquilio F., et al. Endomorphin-1 prevents lipid accumulation via CD36 down-regulation and modulates cytokines release from human lipid-laden macrophages. Peptides 2011, 32:80-85.
18. Granados-Principal S., Quiles J.L., Ramirez-Tortosa C.L., et al. Squalene ameliorates atherosclerotic lesions through the reduction of CD36 scavenger receptor expression in macrophages. Mol Nutr Food Res 2012, 56:733-740.
19. Li X.Y., Kong L.X., Li J., He H.X., Zhou Y.D. Kaempferol suppresses lipid accumulation in macrophages through the downregulation of cluster of differentiation 36 and the upregulation of scavenger receptor class B type I and ATP-binding cassette transporters A1 and G1. Int J Mol Med 2013, 31:331-338.
20. Nergiz-Unal R., Kuijpers M.J., de Witt S.M., et al. Atheroprotective effect of dietary walnut intake in ApoE-deficient mice: involvement of lipids and coagulation factors. Thromb Res 2013, 131:411-417.
21. Chu E.M., Tai D.C., Beer J.L., Hill J.S. Macrophage heterogeneity and cholesterol homeostasis: classically-activated macrophages are associated with reduced cholesterol accumulation following treatment with oxidized LDL. Biochim Biophys Acta 1831, 2013:378-386.
22. Dai X.Y., Cai Y., Mao D.D., et al. Increased stability of phosphatase and tensin homolog by intermedin leading to scavenger receptor A inhibition of macrophages reduces atherosclerosis in apolipoprotein E-deficient mice. J Mol Cell Cardiol 2012, 53:509-520.
23. Makinen P.I., Lappalainen J.P., Heinonen S.E., et al. Silencing of either SR-A or CD36 reduces atherosclerosis in hyperlipidaemic mice and reveals reciprocal upregulation of these receptors. Cardiovasc Res 2010, 88:530-538.
24. Manning-Tobin J.J., Moore K.J., Seimon T.A., et al. Loss of SR-A and CD36 activity reduces atherosclerotic lesion complexity without abrogating foam cell formation in hyperlipidemic mice. Arterioscler Thromb Vasc Biol 2009, 29:19-26.
25. Li K., Yao W., Zheng X., Liao K. Berberine promotes the development of atherosclerosis and foam cell formation by inducing scavenger receptor A expression in macrophage. Cell Res 2009, 19:1006-1017.
26. Hashizume M., Mihara M. Atherogenic effects of TNF-alpha and IL-6 via up-regulation of scavenger receptors. Cytokine 2012, 58:424-430.
27. Yang Y., Wang Y.F., Yang X.F., et al. Specific Kv1.3 blockade modulates key cholesterol-metabolism-associated molecules in human macrophages exposed to ox-LDL. J Lipid Res 2013, 54:34-43.
28. Zhao Z.Z., Wang Z., Li G.H., et al. Hydrogen sulfide inhibits macrophage-derived foam cell formation. Exp Biol Med (Maywood) 2011, 236:169-176.
29. Zhao J.F., Ching L.C., Huang Y.C., et al. Molecular mechanism of curcumin on the suppression of cholesterol accumulation in macrophage foam cells and atherosclerosis. Mol Nutr Food Res 2012, 56:691-701.
30. Yang M.Y., Huang C.N., Chan K.C., Yang Y.S., Peng C.H., Wang C.J. Mulberry leaf polyphenols possess antiatherogenesis effect via inhibiting LDL oxidation and foam cell formation. J Agric Food Chem 2011, 59:1985-1995.
31. Okazaki H., Igarashi M., Nishi M., et al. Identification of neutral cholesterol ester hydrolase, a key enzyme removing cholesterol from macrophages. J Biol Chem 2008, 283:33357-33364.
32. Dove D.E., Su Y.R., Swift L.L., Linton M.F., Fazio S. ACAT1 deficiency increases cholesterol synthesis in mouse peritoneal macrophages. Atherosclerosis 2006, 186:267-274.
33. Yang L., Yang J.B., Chen J., et al. Enhancement of human ACAT1 gene expression to promote the macrophage-derived foam cell formation by dexamethasone. Cell Res 2004, 14:315-323.
34. Kusunoki J., Hansoty D.K., Aragane K., Fallon J.T., Badimon J.J., Fisher E.A. Acyl-CoA:cholesterol acyltransferase inhibition reduces atherosclerosis in apolipoprotein E-deficient mice. Circulation 2001, 103:2604-2609.
35. Fazio S., Major A.S., Swift L.L., et al. Increased atherosclerosis in LDL receptor-null mice lacking ACAT1 in macrophages. J Clin Invest 2001, 107:163-171.
36. Su Y.R., Dove D.E., Major A.S., et al. Reduced ABCA1-mediated cholesterol efflux and accelerated atherosclerosis in apolipoprotein E-deficient mice lacking macrophage-derived ACAT1. Circulation 2005, 111:2373-2381.
37. Duewell P., Kono H., Rayner K.J., et al. NLRP3 inflammasomes are required for atherogenesis and activated by cholesterol crystals. Nature 2010, 464:1357-1361.
38. Ge J., Zhai W., Cheng B., et al. Insulin induces human acyl-coenzyme A: cholesterol acyltransferase1 gene expression via MAP kinases and CCAAT/enhancer-binding protein alpha. J Cell Biochem 2013, [Epub ahead of print] [in press].
39. Liu W., He P., Cheng B., Mei C.L., Wang Y.F., Wan J.J. Chlamydia pneumoniae disturbs cholesterol homeostasis in human THP-1 macrophages via JNK-PPARgamma dependent signal transduction pathways. Microbes Infect 2010, 12:1226-1235.
40. Hongo S., Watanabe T., Arita S., et al. Leptin modulates ACAT1 expression and cholesterol efflux from human macrophages. Am J Physiol Endocrinol Metab 2009, 297:E474-E482.
41. Hayashi K., Sasamura H., Azegami T., Itoh H. Regression of atherosclerosis in apolipoprotein E-deficient mice is feasible using high-dose angiotensin receptor blocker, candesartan. J Atheroscler Thromb 2012, 19:736-746.
42. Nagashima M., Watanabe T., Terasaki M., et al. Native incretins prevent the development of atherosclerotic lesions in apolipoprotein E knockout mice. Diabetologia 2011, 54:2649-2659.
43. Cheng B., Wan J., Wang Y., et al. Ghrelin inhibits foam cell formation via simultaneously down-regulating the expression of acyl-coenzyme A:cholesterol acyltransferase 1 and up-regulating adenosine triphosphate-binding cassette transporter A1. Cardiovasc Pathol 2010, 19:e159-e166.
44. Igarashi M., Osuga J., Isshiki M., et al. Targeting of neutral cholesterol ester hydrolase to the endoplasmic reticulum via its N-terminal sequence. J Lipid Res 2010, 51:274-285.
45. Igarashi M., Osuga J., Uozaki H., et al. The critical role of neutral cholesterol ester hydrolase 1 in cholesterol removal from human macrophages. Circ Res 2010, 107:1387-1395.
46. Sekiya M., Osuga J., Nagashima S., et al. Ablation of neutral cholesterol ester hydrolase 1 accelerates atherosclerosis. Cell Metab 2009, 10:219-228.
47. Zhao B., Song J., Chow W.N., St Clair R.W., Rudel L.L., Ghosh S. Macrophage-specific transgenic expression of cholesteryl ester hydrolase significantly reduces atherosclerosis and lesion necrosis in Ldlr mice. J Clin Invest 2007, 117:2983-2992.
48. Napolitano M., Avella M., Botham K.M., Bravo E. Chylomicron remnant induction of lipid accumulation in J774 macrophages is associated with up-regulation of triacylglycerol synthesis which is not dependent on oxidation of the particles. Biochim Biophys Acta 2003, 1631:255-264.
49. Yamashita M., Tamasawa N., Matsuki K., et al. Insulin suppresses HDL-mediated cholesterol efflux from macrophages through inhibition of neutral cholesteryl ester hydrolase and ATP-binding cassette transporter G1 expressions. J Atheroscler Thromb 2010, 17:1183-1189.
50. McLaren J.E., Michael D.R., Salter R.C., et al. IL-33 reduces macrophage foam cell formation. J Immunol 2010, 185:1222-1229.
51. Miller A.M., Liew F.Y. The IL-33/ST2 pathway - a new therapeutic target in cardiovascular disease. Pharmacol Ther 2011, 131:179-186.
52. Bochem A.E., van Wijk D.F., Holleboom A.G., et al. ABCA1 mutation carriers with low high-density lipoprotein cholesterol are characterized by a larger atherosclerotic burden. Eur Heart J 2013, 34:286-291.
53. Zhao Y., Pennings M., Vrins C.L., et al. Hypocholesterolemia, foam cell accumulation, but no atherosclerosis in mice lacking ABC-transporter A1 and scavenger receptor BI. Atherosclerosis 2011, 218:314-322.
54. Joyce C.W., Wagner E.M., Basso F., et al. ABCA1 overexpression in the liver of LDLr-KO mice leads to accumulation of pro-atherogenic lipoproteins and enhanced atherosclerosis. J Biol Chem 2006, 281:33053-33065.
55. Lee S.M., Moon J., Cho Y., Chung J.H., Shin M.J. Quercetin up-regulates expressions of peroxisome proliferator-activated receptor gamma, liver X receptor alpha, and ATP binding cassette transporter A1 genes and increases cholesterol efflux in human macrophage cell line. Nutr Res 2013, 33:136-143.
56. Liu X.Y., Lu Q., Ouyang X.P., et al. Apelin-13 increases expression of ATP-binding cassette transporter A1 via activating protein kinase C alpha signaling in THP-1 macrophage-derived foam cells. Atherosclerosis 2013, 226:398-407.
57. Park D.W., Lee H.K., Lyu J.H., et al. TLR2 stimulates ABCA1 expression via PKC-eta and PLD2 pathway. Biochem Biophys Res Commun 2013, 430:933-937.
58. Malekpour-Dehkordi Z., Javadi E., Doosti M., et al. S-allylcysteine, a garlic compound, increases ABCA1 expression in human THP-1 macrophages. Phytother Res 2013, 27:357-361.
59. Ku C.S., Park Y., Coleman S.L., Lee J. Unsaturated fatty acids repress expression of ATP binding cassette transporter A1 and G1 in RAW 264.7 macrophages. J Nutr Biochem 2012, 23:1271-1276.
60. Yu X.H., Jiang H.L., Chen W.J., et al. Interleukin-18 and interleukin-12 together downregulate ATP-binding cassette transporter A1 expression through the interleukin-18R/nuclear factor-kappaB signaling pathway in THP-1 macrophage-derived foam cells. Circ J 2012, 76:1780-1791.
61. Sun D., Zhang J., Xie J., Wei W., Chen M., Zhao X. MiR-26 controls LXR-dependent cholesterol efflux by targeting ABCA1 and ARL7. FEBS Lett 2012, 586:1472-1479.
62. Schou J., Frikke-Schmidt R., Kardassis D., et al. Genetic variation in ABCG1 and risk of myocardial infarction and ischemic heart disease. Arterioscler Thromb Vasc Biol 2012, 32:506-515.
63. Out R., Hoekstra M., Hildebrand R.B., et al. Macrophage ABCG1 deletion disrupts lipid homeostasis in alveolar macrophages and moderately influences atherosclerotic lesion development in LDL receptor-deficient mice. Arterioscler Thromb Vasc Biol 2006, 26:2295-2300.
64. -/- bone marrow. Arterioscler Thromb Vasc Biol 2006, 26:2308-2315.
65. -/- bone marrow. Arterioscler Thromb Vasc Biol 2006, 26:2301-2307.
66. Meurs I., Lammers B., Zhao Y., et al. The effect of ABCG1 deficiency on atherosclerotic lesion development in LDL receptor knockout mice depends on the stage of atherogenesis. Atherosclerosis 2012, 221:41-47.
67. Jun H.J., Hoang M.H., Yeo S.K., Jia Y., Lee S.J. Induction of ABCA1 and ABCG1 expression by the liver X receptor modulator cineole in macrophages. Bioorg Med Chem Lett 2013, 23:579-583.
68. Hoang M.H., Jia Y., Jun H.J., Lee J.H., Lee B.Y., Lee S.J. Fucosterol is a selective liver X receptor modulator that regulates the expression of key genes in cholesterol homeostasis in macrophages, hepatocytes, and intestinal cells. J Agric Food Chem 2012, 60:11567-11575.
69. Helal O., Berrougui H., Loued S., Khalil A. Extra-virgin olive oil consumption improves the capacity of HDL to mediate cholesterol efflux and increases ABCA1 and ABCG1 expression in human macrophages. Br J Nutr 2012, 1-12.
70. Wang D., Xia M., Yan X., et al. Gut microbiota metabolism of anthocyanin promotes reverse cholesterol transport in mice via repressing miRNA-10b. Circ Res 2012, 111:967-981.
71. Maitra U., Li L. Molecular mechanisms responsible for the reduced expression of cholesterol transporters from macrophages by low-dose endotoxin. Arterioscler Thromb Vasc Biol 2013, 33:24-33.
72. Vergeer M., Korporaal S.J., Franssen R., et al. Genetic variant of the scavenger receptor BI in humans. N Engl J Med 2011, 364:136-145.
73. Zhang W., Yancey P.G., Su Y.R., et al. Inactivation of macrophage scavenger receptor class B type I promotes atherosclerotic lesion development in apolipoprotein E-deficient mice. Circulation 2003, 108:2258-2263.
74. Van Eck M., Bos I.S., Hildebrand R.B., Van Rij B.T., Van Berkel T.J. Dual role for scavenger receptor class B, type I on bone marrow-derived cells in atherosclerotic lesion development. Am J Pathol 2004, 165:785-794.
75. Demetz E., Tancevski I., Duwensee K., et al. Inhibition of hepatic scavenger receptor-class B type I by RNA interference decreases atherosclerosis in rabbits. Atherosclerosis 2012, 222:360-366.
76. Voloshyna I., Hai O., Littlefield M.J., Carsons S., Reiss A.B. Resveratrol mediates anti-atherogenic effects on cholesterol flux in human macrophages and endothelium via PPARgamma and adenosine. Eur J Pharmacol 2013, 698:299-309.
77. Kammerer I., Ringseis R., Biemann R., Wen G., Eder K. 13-hydroxy linoleic acid increases expression of the cholesterol transporters ABCA1, ABCG1 and SR-BI and stimulates apoA-I-dependent cholesterol efflux in RAW264.7 macrophages. Lipids Health Dis 2011, 10:222-229.
78. Uto-Kondo H., Ayaori M., Ogura M., et al. Coffee consumption enhances high-density lipoprotein-mediated cholesterol efflux in macrophages. Circ Res 2010, 106:779-787.
79. Song G., Tian H., Qin S., et al. Hydrogen decreases athero-susceptibility in apolipoprotein B-containing lipoproteins and aorta of apolipoprotein E knockout mice. Atherosclerosis 2012, 221:55-65.
80. Tang S.L., Chen W.J., Yin K., et al. PAPP-A negatively regulates ABCA1, ABCG1 and SR-B1 expression by inhibiting LXRalpha through the IGF-I-mediated signaling pathway. Atherosclerosis 2012, 222:344-354.
81. Yoshinaka Y., Shibata H., Kobayashi H., et al. A selective ACAT-1 inhibitor, K-604, stimulates collagen production in cultured smooth muscle cells and alters plaque phenotype in apolipoprotein E-knockout mice. Atherosclerosis 2010, 213:85-91.
82. Netherland C., Thewke D.P. Rimonabant is a dual inhibitor of acyl CoA:cholesterol acyltransferases 1 and 2. Biochem Biophys Res Commun 2010, 398:671-676.
83. Xie C., Kang J., Chen J.R., Nagarajan S., Badger T.M., Wu X. Phenolic acids are in vivo atheroprotective compounds appearing in the serum of rats after blueberry consumption. J Agric Food Chem 2011, 59:10381-10387.
84. Boden W.E., Probstfield J.L., Anderson T., et al. Niacin in patients with low HDL cholesterol levels receiving intensive statin therapy. N Engl J Med 2011, 365:2255-2267.
85. Voight B.F., Peloso G.M., Orho-Melander M., et al. Plasma HDL cholesterol and risk of myocardial infarction: a mendelian randomisation study. Lancet 2012, 380:572-580.