The role of immune complexes in atherogenesis

Angiology

Volumn 61, Issue 7, 2010, Pages 679-689

  Burut, Dayangku Fatiha Pengiran ^a   Karim, Yousuf ^b   Ferns, Gordon A A ^c  

^a UNIVERSITY OF SURREY   (United Kingdom)

^b ROYAL SURREY COUNTY HOSPITAL   (United Kingdom)

^c KEELE UNIVERSITY   (United Kingdom)

Author keywords

antigen antibody complex; complement; Fc receptors; inflammation

Indexed keywords

FC RECEPTOR; HEAT SHOCK PROTEIN; IMMUNOGLOBULIN G; IMMUNOGLOBULIN M; OXIDIZED LOW DENSITY LIPOPROTEIN; ANTIGEN ANTIBODY COMPLEX;

ANTIGEN ANTIBODY COMPLEX; ARTICLE; ATHEROGENESIS; AUTOIMMUNITY; COMPLEMENT ACTIVATION; CROSS LINKING; HUMAN; INFLAMMATION; NONHUMAN; SIGNAL TRANSDUCTION; ANIMAL; ANIMAL MODEL; ATHEROSCLEROSIS; CARDIOVASCULAR DISEASE; DISEASE COURSE; IMMUNOLOGY; MACROPHAGE; PHYSIOLOGY;

ANIMALS; ANTIGEN-ANTIBODY COMPLEX; ATHEROSCLEROSIS; CARDIOVASCULAR DISEASES; COMPLEMENT ACTIVATION; DISEASE PROGRESSION; HEAT-SHOCK PROTEINS; HUMANS; MACROPHAGES; MODELS, ANIMAL; RECEPTORS, FC;

EID: 77956485170     PISSN: 00033197     EISSN: None     Source Type: Journal    
DOI: 10.1177/0003319710366124     Document Type: Article

References (107)

1. Hansson GK, Libby P., Schonbeck U., Yan ZQ Innate and adaptive immunity in the pathogenesis of atherosclerosis. Circ Res. 2002 ; 91 (4). 281-291.
2. Tsimikas S., Brilakis ES, Lennon RJ, et al. Relationship of IgG and IgM autoantibodies to oxidized low density lipoprotein with coronary artery disease and cardiovascular events. J Lipid Res. 2007 ; 48 (2). 425-433.
3. Zhang X., He M., Cheng L., et al. Elevated heat shock protein 60 levels are associated with higher risk of coronary heart disease in Chinese. Circulation. 2008 ; 118 (25). 2687-2693.
4. Turesson C., Jacobsson LT, Matteson EL Cardiovascular co-morbidity in rheumatic diseases. Vasc Health Risk Manag. 2008 ; 4 (3). 605-614.
5. Soltesz P., Szekanecz Z., Kiss E., Shoenfeld Y. Cardiac manifestations in antiphospholipid syndrome. Autoimmun Rev. 2007 ; 6 (6). 379-386.
6. McMahon M., Hahn BH Atherosclerosis and systemic lupus erythematosus: mechanistic basis of the association. Curr Opin Immunol. 2007 ; 19 (6). 633-639.
7. Ravetch JV, Kinet JP Fc receptors. Annu Rev Immunol. 1991 ; 9: 457-492.
8. Kubagawa H., Oka S., Kubagawa Y., et al. Identity of the elusive IgM Fc receptor (Fc{micro}R) in humans. J Exp Med. 2009 ; 206 (12). 2779-2793.
9. Monteiro RC Role of IgA and IgA Fc Receptors in Inflammation. J Clin Immunol. 2010 ; 30 (1). 1-9.
10. Ratcliffe NR, Kennedy SM, Morganelli PM Immunocytochemical detection of Fcgamma receptors in human atherosclerotic lesions. Immunol Lett. 2001 ; 77 (3). 169-174.
11. Oksjoki R., Kovanen PT, Lindstedt KA, Jansson B., Pentikainen MO OxLDL-IgG immune complexes induce survival of human monocytes. Arterioscler Thromb Vasc Biol. 2006 ; 26 (3). 576-583.
12. Hammad SM, Taha TA, Nareika A., Johnson KR, Lopes-Virella MF, Obeid LM. Oxidized LDL immune complexes induce release of sphingosine kinase in human U937 monocytic cells. Prostaglandins Other Lipid Mediat. 2006 ; 79 (1-2). 126-140.
13. Hammad SM, Twal WO, Barth JL, et al. Oxidized LDL immune complexes and oxidized LDL differentially affect the expression of genes involved with inflammation and survival in human U937 monocytic cells. Atherosclerosis. 2009 ; 202 (2). 394-404.
14. Kiener PA, Rankin BM, Davis PM, Yocum SA, Warr GA, Grove RI Immune complexes of LDL induce atherogenic responses in human monocytic cells. Arterioscler Thromb Vasc Biol. 1995 ; 15 (7). 990-999.
15. Virella G., Atchley D., Koskinen S., Zheng D., Lopes-Virella MF Proatherogenic and proinflammatory properties of immune complexes prepared with purified human oxLDL antibodies and human oxLDL. Clin Immunol. 2002 ; 105 (1). 81-92.
16. Saad AF, Virella G., Chassereau C., Boackle RJ, Lopes-Virella MF OxLDL immune complexes activate complement and induce cytokine production by MonoMac 6 cells and human macrophages. J Lipid Res. 2006 ; 47 (9). 1975-1983.
17. Huang Y., Fleming AJ, Wu S., Virella G., Lopes-Virella MF Fcgamma receptor cross-linking by immune complexes induces matrix metalloproteinase-1 in U937 cells via mitogen-activated protein kinase. Arterioscler Thromb Vasc Biol. 2000 ; 20 (12). 2533-2538.
18. Lopes-Virella MF, Binzafar N., Rackley S., Takei A., La VM, Virella G. The uptake of LDL-IC by human macrophages: predominant involvement of the Fc gamma RI receptor. Atherosclerosis. 1997 ; 135 (2). 161-170.
19. Hernandez-Vargas P., Ortiz-Munoz G., Lopez-Franco O., et al. Fcgamma receptor deficiency confers protection against atherosclerosis in apolipoprotein E knockout mice. Circ Res. 2006 ; 99 (11). 1188-1196.
20. Laufer J., Boichis H., Farzam N., Passwell JH IgA and IgG immune complexes increase human macrophage C3 biosynthesis. Immunology. 1995 ; 84 (2). 207-212.
21. Iakoubova OA, Tong CH, Chokkalingam AP, et al. Asp92Asn polymorphism in the myeloid IgA Fc receptor is associated with myocardial infarction in two disparate populations: CARE and WOSCOPS. Arterioscler Thromb Vasc Biol. 2006 ; 26 (12). 2763-2768.
22. Ohno T., Kubagawa H., Sanders SK, Cooper MD Biochemical nature of an Fc mu receptor on human B-lineage cells. J Exp Med. 1990 ; 172 (4). 1165-1175.
23. Pricop L., Rabinowich H., Morel PA, Sulica A., Whiteside TL, Herberman RB Characterization of the Fc mu receptor on human natural killer cells. Interaction with its physiologic ligand, human normal IgM, specificity of binding, and functional effects. J Immunol. 1993 ; 151 (6). 3018-3029.
24. Vanderlaan PA, Reardon CA Thematic review series: the immune system and atherogenesis. The unusual suspects:an overview of the minor leukocyte populations in atherosclerosis. J Lipid Res. 2005 ; 46 (5). 829-838.
25. Whitman SC, Rateri DL, Szilvassy SJ, Yokoyama W., Daugherty A. Depletion of natural killer cell function decreases atherosclerosis in low-density lipoprotein receptor null mice. Arterioscler Thromb Vasc Biol. 2004 ; 24 (6). 1049-1054.
26. Vlaicu R., Rus HG, Niculescu F., Cristea A. Immunoglobulins and complement components in human aortic atherosclerotic intima. Atherosclerosis. 1985 ; 55 (1). 35-50. (Pubitemid 15064937)
27. Lozada C., Levin RI, Huie M., et al. Identification of C1q as the heat-labile serum cofactor required for immune complexes to stimulate endothelial expression of the adhesion molecules E-selectin and intercellular and vascular cell adhesion molecules 1. Proc Natl Acad Sci U S A. 1995 ; 92 (18). 8378-8382.
28. Reiss AB, Awadallah NW, Malhotra S., et al. Immune complexes and IFN-gamma decrease cholesterol 27-hydroxylase in human arterial endothelium and macrophages. J Lipid Res. 2001 ; 42 (11). 1913-1922.
29. Galkina E., Ley K. Vascular adhesion molecules in atherosclerosis. Arterioscler Thromb Vasc Biol. 2007 ; 27 (11). 2292-2301.
30. Babiker A., Andersson O., Lund E., et al. Elimination of cholesterol in macrophages and endothelial cells by the sterol 27-hydroxylase mechanism. Comparison with high density lipoprotein-mediated reverse cholesterol transport. J Biol Chem. 1997 ; 272 (42). 26253-26261.
31. Bjorkhem I., Andersson O., Diczfalusy U., et al. Atherosclerosis and sterol 27-hydroxylase: evidence for a role of this enzyme in elimination of cholesterol from human macrophages. Proc Natl Acad Sci U S A. 1994 ; 91 (18). 8592-8596.
32. Oksjoki R., Kovanen PT, Meri S., Pentikainen MO Function and regulation of the complement system in cardiovascular diseases. Front Biosci. 2007 ; 12: 4696-4708.
33. Sylvestre D., Clynes R., Ma M., Warren H., Carroll MC, Ravetch JV. Immunoglobulin G-mediated inflammatory responses develop normally in complement-deficient mice. J Exp Med. 1996 ; 184 (6). 2385-2392.
34. Ravetch JV, Bolland S. IgG Fc receptors. Annu Rev Immunol. 2001 ; 19 (): 275-290.
35. Pfeiffer JR, Howes PS, Waters MA, et al. Levels of expression of Fcgamma receptor IIA (CD32) are decreased on peripheral blood monocytes in patients with severe atherosclerosis. Atherosclerosis. 2001 ; 155 (1). 211-218.
36. Lewis MJ, Malik TH, Ehrenstein MR, Boyle JJ, Botto M., Haskard DO. Immunoglobulin M is required for protection against atherosclerosis in low-density lipoprotein receptor-deficient mice. Circulation. 2009 ; 120 (5). 417-426.
37. Aderem AA, Wright SD, Silverstein SC, Cohn ZA Ligated complement receptors do not activate the arachidonic acid cascade in resident peritoneal macrophages. J Exp Med. 1985 ; 161 (3). 617-622.
38. Oksjoki R., Kovanen PT, Mayranpaa MI, et al. Complement regulation in human atherosclerotic coronary lesions. Immunohistochemical evidence that C4b-binding protein negatively regulates the classical complement pathway, and that C5b-9 is formed via the alternative complement pathway. Atherosclerosis. 2007 ; 192 (1). 40-48.
39. Hollander W., Colombo MA, Kirkpatrick B., Paddock J. Soluble proteins in the human atherosclerotic plaque. With spectral reference to immunoglobulins, C3-complement component, alpha 1-antitrypsin and alpha 2-macroglobulin. Atherosclerosis. 1979 ; 34 (4). 391-405.
40. Mironova M., Virella G., Lopes-Virella MF Isolation and characterization of human antioxidized LDL autoantibodies. Arterioscler Thromb Vasc Biol. 1996 ; 16 (2). 222-229.
41. Karvonen J., Paivansalo M., Kesaniemi YA, Horkko S. Immunoglobulin M type of autoantibodies to oxidized low-density lipoprotein has an inverse relation to carotid artery atherosclerosis. Circulation. 2003 ; 108 (17). 2107-2112.
42. Su J., Georgiades A., Wu R., Thulin T., de FU, Frostegard J. Antibodies of IgM subclass to phosphorylcholine and oxidized LDL are protective factors for atherosclerosis in patients with hypertension. Atherosclerosis. 2006 ; 188 (1). 160-166.
43. Binder CJ, Shaw PX, Chang MK, et al. The role of natural antibodies in atherogenesis. J Lipid Res. 2005 ; 46 (7). 1353-1363.
44. Pengiran Burut DF, Shams S., Ferns G. Changes in serum heat shock protein 27 antigen and IgM concentrations in patients with acute coronary syndrome. Ann Clin Biochem. 2009 ; 46 (suppl 1). 105 [Abstract].
45. Mironova M., Virella G., Virella-Lowell I., Lopes-Virella MF Anti-modified LDL antibodies and LDL-containing immune complexes in IDDM patients and healthy controls. Clin Immunol Immunopathol. 1997 ; 85 (1). 73-82.
46. Lopes-Virella MF, Virella G., Orchard TJ, et al. Antibodies to oxidized LDL and LDL-containing immune complexes as risk factors for coronary artery disease in diabetes mellitus. Clin Immunol. 1999 ; 90 (2). 165-172.
47. Russell MW, Mansa B. Complement-fixing properties of human IgA antibodies. Alternative pathway complement activation by plastic-bound, but not specific antigen-bound, IgA. Scand J Immunol. 1989 ; 30 (2). 175-183.
48. Saito E., Fujioka T., Kanno H., et al. Complement receptors in atherosclerotic lesions. Artery. 1992 ; 19 (1). 47-62.
49. Seifert PS, Hansson GK Complement receptors and regulatory proteins in human atherosclerotic lesions. Arteriosclerosis. 1989 ; 9 (6). 802-811.
50. Lucisano Valim YM, Lachmann PJ The effect of antibody isotype and antigenic epitope density on the complement-fixing activity of immune complexes: a systematic study using chimaeric anti-NIP antibodies with human Fc regions. Clin Exp Immunol. 1991 ; 84 (1). 1-8.
51. Ravetch JV, Clynes RA Divergent roles for Fc receptors and complement in vivo. Annu Rev Immunol. 1998 ; 16: 421-432.
52. Yla-Herttuala S., Palinski W., Rosenfeld ME, et al. Evidence for the presence of oxidatively modified low density lipoprotein in atherosclerotic lesions of rabbit and man. J Clin Invest. 1989 ; 84 (4). 1086-1095.
53. Yla-Herttuala S., Palinski W., Butler SW, Picard S., Steinberg D., Witztum JL Rabbit and human atherosclerotic lesions contain IgG that recognizes epitopes of oxidized LDL. Arterioscler Thromb. 1994 ; 14 (1). 32-40.
54. Kanwar RK, Kanwar JR, Wang D., Ormrod DJ, Krissansen GW Temporal expression of heat shock proteins 60 and 70 at lesion-prone sites during atherogenesis in ApoE-deficient mice. Arterioscler Thromb Vasc Biol. 2001 ; 21 (12). 1991-1997.
55. Berberian PA, Myers W., Tytell M., Challa V., Bond MG Immunohistochemical localization of heat shock protein-70 in normal-appearing and atherosclerotic specimens of human arteries. Am J Pathol. 1990 ; 136 (1). 71-80.
56. Bobryshev YV, Lord RS Expression of heat shock protein-70 by dendritic cells in the arterial intima and its potential significance in atherogenesis. J Vasc Surg. 2002 ; 35 (2). 368-375.
57. Kleindienst R., Xu Q., Willeit J., Waldenberger FR, Weimann S., Wick G. Immunology of atherosclerosis. Demonstration of heat shock protein 60 expression and T lymphocytes bearing alpha/ beta or gamma/delta receptor in human atherosclerotic lesions. Am J Pathol. 1993 ; 142 (6). 1927-1937.
58. Xu Q., Luef G., Weimann S., Gupta RS, Wolf H., Wick G. Staining of endothelial cells and macrophages in atherosclerotic lesions with human heat-shock protein-reactive antisera. Arterioscler Thromb. 1993 ; 13 (12). 1763-1769.
59. Mayr M., Metzler B., Kiechl S., et al. Endothelial cytotoxicity mediated by serum antibodies to heat shock proteins of Escherichia coli and Chlamydia pneumoniae: immune reactions to heat shock proteins as a possible link between infection and atherosclerosis. Circulation. 1999 ; 99 (12). 1560-1566.
60. Park HK, Park EC, Bae SW, et al. Expression of heat shock protein 27 in human atherosclerotic plaques and increased plasma level of heat shock protein 27 in patients with acute coronary syndrome. Circulation. 2006 ; 114 (9). 886-893.
61. Shams S., Shafi S., Bodman-Smith K., Williams P., Mehta S., Ferns GA Anti-heat shock protein-27 (Hsp-27) antibody levels in patients with chest pain: association with established cardiovascular risk factors. Clin Chim Acta. 2008 ; 395 (1-2). 42-46.
62. Pengiran Burut DF, Borai A., Livingstone C., Ferns G. Serum heat shock protein 27 antigen and antibody levels appear to be related to the macrovascular complications associated with insulin resistance: a pilot study. Cell Stress Chaperones. 2009.
63. Businaro R., Profumo E., Tagliani A., et al. Heat-shock protein 90: a novel autoantigen in human carotid atherosclerosis. Atherosclerosis. 2009 ; 207 (1). 74-83.
64. George J., Harats D., Gilburd B., et al. Immunolocalization of beta2-glycoprotein I (apolipoprotein H) to human atherosclerotic plaques: potential implications for lesion progression. Circulation. 1999 ; 99 (17). 2227-2230.
65. Del PN, Guidali L., Spatola L., et al. Relationship between antiphospholipid and anti-endothelial cell antibodies III: beta 2 glycoprotein I mediates the antibody binding to endothelial membranes and induces the expression of adhesion molecules. Clin Exp Rheumatol. 1995 ; 13 (2). 179-185.
66. Kobayashi K., Kishi M., Atsumi T., et al. Circulating oxidized LDL forms complexes with beta2-glycoprotein I: implication as an atherogenic autoantigen. J Lipid Res. 2003 ; 44 (4). 716-726.
67. Ritzmann SE, Daniels JC Immune complexes: characteristics, clinical correlations, and interpretive approaches in the clinical laboratory. Clin Chem. 1982 ; 28 (6). 1259-1271.
68. Theofilopoulos AN, Dixon FJ Immune complexes in human diseases: a review. Am J Pathol. 1980 ; 100 (2). 529-594.
69. Levinson SS, Goldman JO. Evaluation of anti-C1q capture assay for detecting circulating immune complexes and comparison with polyethylene glycol-immunoglobulin G, C1q-binding, and Raji cell methods. J Clin Microbiol. 1987 ; 25 (8). 1567-1569.
70. Creighton WD, Lambert PH, Miescher PA Detection of antibodies and soluble antigen-antibody complexes by precipitation with polyethylene glycol. J Immunol. 1973 ; 111 (4). 1219-1227.
71. Wang J., Qiang H., Zhang C., Liu X., Chen D., Wang S. Detection of IgG-bound lipoprotein(a) immune complexes in patients with coronary heart disease. Clin Chim Acta. 2003 ; 327 (1-2). 115-122.
72. Orchard TJ, Virella G., Forrest KY, Evans RW, Becker DJ, Lopes-Virella MF Antibodies to oxidized LDL predict coronary artery disease in type 1 diabetes: a nested case-control study from the Pittsburgh Epidemiology of Diabetes Complications Study. Diabetes. 1999 ; 48 (7). 1454-1458.
73. Ahmed E., Nityanand S., Mustafa A., Brismar K., Lefvert AK Anticardiolipin antibodies and circulating immune complexes in type 1 diabetes mellitus: increased prevalence and relation to vascular complications. Clin Exp Immunol. 1999 ; 115 (2). 255-259.
74. Mustafa A., Nityanand S., Berglund L., Lithell H., Lefvert AK Circulating immune complexes in 50-year-old men as a strong and independent risk factor for myocardial infarction. Circulation. 2000 ; 102 (21). 2576-2581.
75. Szondy E., Mezey Z., Fust G., Szekely J., Gero S. Serial measurement of circulating immune complexes in myocardial infarction. Br Heart J. 1981 ; 46 (1). 93-98.
76. Tung KS, Woodroffe AJ, Ahlin TD, Williams RC Jr, Wilson CB Application of the solid phase C1q and Raji cell radioimmune assays for the detection of circulating immune complexes in glomerulonephritis. J Clin Invest. 1978 ; 62 (1). 61-72.
77. Farrell C., Bloth B., Nielsen H., Daugharty H., Lundman T., Svehag SE A survey for circulating immune complexes in patients with acute myocardial infarction. Use of a C1q-binding assay with soluble protein A as indicator. Scand J Immunol. 1977 ; 6 (12). 1233-1240.
78. Fust G., Szondy E., Szekely J., Nanai I., Gero S. Studies on the occurrence of circulating immune complexes in vascular diseases. Atherosclerosis. 1978 ; 29 (2). 181-190.
79. Smith GW, McArthur CJ, Simpson IJ Circulating immune complexes in myocardial infarction. J Clin Lab Immunol. 1983 ; 12 (4). 197-199.
80. Gallagher PJ, Jones DB, Casey CR, Sharratt GP Circulating immune complexes in cardiac disease. Atherosclerosis. 1982 ; 44 (2). 241-244.
81. Orekhov AN, Kalenich OS, Tertov VV, Novikov ID Lipoprotein immune complexes as markers of atherosclerosis. Int J Tissue React. 1991 ; 13 (5). 233-236.
82. Turk Z., Sesto M., Skodlar J., Ferencak G., Turk N., Stavljenic-Rukavina A. Soluble LDL-immune complexes in type 2 diabetes and vascular disease. Horm Metab Res. 2002 ; 34 (4). 196-201.
83. Turk Z., Ljubic S., Turk N., Benko B. Detection of autoantibodies against advanced glycation endproducts and AGE-immune complexes in serum of patients with diabetes mellitus. Clin Chim Acta. 2001 ; 303 (1-2). 105-115.
84. Lopes-Virella MF, McHenry MB, Lipsitz S., et al. Immune complexes containing modified lipoproteins are related to the progression of internal carotid intima-media thickness in patients with type 1 diabetes. Atherosclerosis. 2007 ; 190 (2). 359-369.
85. Zinger H., Sherer Y., Shoenfeld Y. Atherosclerosis in autoimmune rheumatic diseases-mechanisms and clinical findings. Clin Rev Allergy Immunol. 2009 ; 37 (1). 20-28.
86. Wang J., Hu B., Meng Y., Zhang C., Li K., Hui C. The level of malondialdehyde-modified LDL and LDL immune complexes in patients with rheumatoid arthritis. Clin Biochem. 2009 ; 42 (13-14). 1352-1357.
87. Jonasson L., Holm J., Skalli O., Bondjers G., Hansson GK Regional accumulations of T cells, macrophages, and smooth muscle cells in the human atherosclerotic plaque. Arteriosclerosis. 1986 ; 6 (2). 131-138.
88. Kniker WT, Cochrane CG The localization of circulating immune complexes in experimental serum sickness. The role of vasoactive amines and hydrodynamic forces. J Exp Med. 1968 ; 127 (1). 119-136.
89. Lachmann PJ, Smith RA. Taking complement to the clinic-has the time finally come? Scand J Immunol. 2009 ; 69 (6). 471-478.
90. Thorbjornsdottir P., Kolka R., Gunnarsson E., et al. Vaccinia virus complement control protein diminishes formation of atherosclerotic lesions: complement is centrally involved in atherosclerotic disease. Ann N Y Acad Sci. 2005 ; 1056: 1-15.
91. Shagdarsuren E., Bidzhekov K., Djalali-Talab Y., et al. C1-esterase inhibitor protects against neointima formation after arterial injury in atherosclerosis-prone mice. Circulation. 2008 ; 117 (1). 70-78.
92. Wu G., Hu W., Shahsafaei A., et al. Complement regulator CD59 protects against atherosclerosis by restricting the formation of complement membrane attack complex. Circ Res. 2009 ; 104 (4). 550-558.
93. Fattouch K., Bianco G., Speziale G., et al. Beneficial effects of C1 esterase inhibitor in ST-elevation myocardial infarction in patients who underwent surgical reperfusion: a randomised double-blind study. Eur J Cardiothorac Surg. 2007 ; 32 (2). 326-332.
94. Patel JA, Ghatak SB Pexelizumab and its role in the treatment of myocardial infarction and in coronary artery bypass graft surgery: a review. Recent Pat Cardiovasc Drug Discov. 2008 ; 3 (2). 145-152.
95. Hillyard DZ, Jardine AG, McDonald KJ, Cameron AJ Fluvastatin inhibits raft dependent Fcgamma receptor signalling in human monocytes. Atherosclerosis. 2004 ; 172 (2). 219-228.
96. Loike JD, Shabtai DY, Neuhut R., et al. Statin inhibition of Fc receptor-mediated phagocytosis by macrophages is modulated by cell activation and cholesterol. Arterioscler Thromb Vasc Biol. 2004 ; 24 (11). 2051-2056.
97. Aderem A., Underhill DM Mechanisms of phagocytosis in macrophages. Annu Rev Immunol. 1999 ; 17: 593-623.
98. Liao JK, Laufs U. Pleiotropic effects of statins. Annu Rev Pharmacol Toxicol. 2005 ; 45: 89-118.
99. Choi SH, Chae A., Miller E., et al. Relationship between biomarkers of oxidized low-density lipoprotein, statin therapy, quantitative coronary angiography, and atheroma: volume observations from the REVERSAL (Reversal of Atherosclerosis with Aggressive Lipid Lowering) study. J Am Coll Cardiol. 2008 ; 52 (1). 24-32.
100. Ky B., Burke A., Tsimikas S., et al. The influence of pravastatin and atorvastatin on markers of oxidative stress in hypercholesterolemic humans. J Am Coll Cardiol. 2008 ; 51 (17). 1653-1662.
101. Lopes-Virella MF, Mironova M., Stephan E., Durazo-Arvizu R., Virella G. Role of simvastatin as an immunomodulator in type 2 diabetes. Diabetes Care. 2004 ; 27 (4). 908-913.
102. Tsimikas S., Witztum JL, Miller ER, et al. High-dose atorvastatin reduces total plasma levels of oxidized phospholipids and immune complexes present on apolipoprotein B-100 in patients with acute coronary syndromes in the MIRACL trial. Circulation. 2004 ; 110 (11). 1406-1412.
103. Nicoletti A., Kaveri S., Caligiuri G., Bariety J., Hansson GK Immunoglobulin treatment reduces atherosclerosis in apo E knockout mice. J Clin Invest. 1998 ; 102 (5). 910-918.
104. Yuan Z., Kishimoto C., Sano H., Shioji K., Xu Y., Yokode M. Immunoglobulin treatment suppresses atherosclerosis in apolipoprotein E-deficient mice via the Fc portion. Am J Physiol Heart Circ Physiol. 2003 ; 285 (2). H899 - H906.
105. Persson L., Boren J., Nicoletti A., Hansson GK, Pekna M. Immunoglobulin treatment reduces atherosclerosis in apolipoprotein E-/-low-density lipoprotein receptor-/- mice via the complement system. Clin Exp Immunol. 2005 ; 142 (3). 441-445.
106. Braselmann S., Taylor V., Zhao H., et al. R406, an orally available spleen tyrosine kinase inhibitor blocks fc receptor signaling and reduces immune complex-mediated inflammation. J Pharmacol Exp Ther. 2006 ; 319 (3). 998-1008.
107. Werwitzke S., Trick D., Sondermann P., et al. Treatment of lupus-prone NZB/NZW F1 mice with recombinant soluble Fc gamma receptor II (CD32). Ann Rheum Dis. 2008 ; 67 (2). 154-161.