The problem of accelerated atherosclerosis in systemic lupus erythematosus: Insights into a complex co-morbidity

Thrombosis and Haemostasis

Volumn 106, Issue 5, 2011, Pages 849-857

  Wade, Nekeithia S ^a   Major, Amy S ^a  

^a VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Atherosclerosis; Autoimmunity; Cardiovascular disease; Systemic lupus erythematosus

Indexed keywords

ATORVASTATIN; BELIMUMAB; BETA2 GLYCOPROTEIN 1 ANTIBODY; CARDIOLIPIN ANTIBODY; CD20 ANTIGEN; GAMMA INTERFERON; HIGH DENSITY LIPOPROTEIN; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE INHIBITOR; INTERLEUKIN 10; INTERLEUKIN 17; INTERLEUKIN 6; LOW DENSITY LIPOPROTEIN; MALONALDEHYDE; MYCOPHENOLIC ACID 2 MORPHOLINOETHYL ESTER; NEUTRALIZING ANTIBODY; OXIDIZED LOW DENSITY LIPOPROTEIN; PHOSPHOLIPID ANTIBODY; PLACEBO; RITUXIMAB; TRANSCRIPTION FACTOR FOXP3; TRANSFORMING GROWTH FACTOR BETA;

ANTIBODY PRODUCTION; ANTIPHOSPHOLIPID SYNDROME; ARTERIAL WALL THICKNESS; ARTICLE; ATHEROGENESIS; ATHEROSCLEROSIS; ATHEROSCLEROTIC PLAQUE; AUTOIMMUNITY; B LYMPHOCYTE; CARDIOVASCULAR DISEASE; CD4+ T LYMPHOCYTE; CHRONIC INFLAMMATION; COMORBIDITY; CYTOKINE RELEASE; DISEASE ASSOCIATION; DISEASE PREDISPOSITION; DRUG MEGADOSE; DYSLIPIDEMIA; HUMAN; IMMUNOMODULATION; NONHUMAN; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; RHEUMATOID ARTHRITIS; RISK FACTOR; SPLENOMEGALY; SYSTEMIC LUPUS ERYTHEMATOSUS; TH17 CELL;

ANIMALS; ARTERIES; ATHEROSCLEROSIS; AUTOIMMUNITY; COMORBIDITY; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; HUMANS; INFLAMMATION; LUPUS ERYTHEMATOSUS, SYSTEMIC; RISK ASSESSMENT; RISK FACTORS; TIME FACTORS;

EID: 80155214027     PISSN: 03406245     EISSN: None     Source Type: Journal    
DOI: 10.1160/TH11-05-0330     Document Type: Article

References (97)

1. Mok CC, Lau CS. Pathogenesis of systemic lupus erythematosus. J Clin Pathol 2003; 56: 481-490.
2. Vanholder R, De Keyser F, Kips J, et al. The pathophysiology of lupus erythematosus. Eur J Dermatol 1998; 8: 4-7.
3. Munoz LE, van Bavel C, Franz S, et al. Apoptosis in the pathogenesis of systemic lupus erythematosus. Lupus 2008; 17: 371-375.
4. Liu Z, Bethunaickan R, Huang W, et al. Interferon-alpha accelerates murine systemic lupus erythematosus in a T cell-dependent manner. Arthritis Rheum 2011; 63: 219-229.
5. Mathian A, Weinberg A, Gallegos M, et al. IFN-alpha induces early lethal lupus in preautoimmune (New Zealand Black x New Zealand White) F1 but not in BALB/c mice. J Immunol 2005; 174: 2499-2506.
6. Bengtsson AA, Sturfelt G, Truedsson L, et al. Activation of type I interferon system in systemic lupus erythematosus correlates with disease activity but not with antiretroviral antibodies. Lupus 2000; 9: 664-671.
7. Ronnblom L, Alm GV, Eloranta ML. The type I interferon system in the development of lupus. Semin Immunol 2011; 23: 113-121.
8. Urowitz MB, Bookman AA, Koehler BE, et al. The bimodal mortality pattern of systemic lupus erythematosus. Am J Med 1976; 60: 221-225.
9. Trager J, Ward MM. Mortality and causes of death in systemic lupus erythematosus. Curr Opin Rheumatol 2001; 13: 345-351.
10. Esdaile JM, Abrahamowicz M, Grodzicky T, et al. Traditional Framingham risk factors fail to fully account for accelerated atherosclerosis in systemic lupus erythematosus. Arthritis Rheum 2001; 44: 2331-2337.
11. Manzi S, Selzer F, Sutton-Tyrrell K, et al. Prevalence and risk factors of carotid plaque in women with systemic lupus erythematosus. Arthritis Rheum 1999; 42: 51-60.
12. Manzi S, Meilahn EN, Rairie JE, et al. Age-specific incidence rates of myocardial infarction and angina in women with systemic lupus erythematosus: comparison with the Framingham Study. Am J Epidemiol 1997; 145: 408-415.
13. Tyrrell PN, Beyene J, Feldman BM, et al. Rheumatic disease and carotid intimamedia thickness: a systematic review and meta-analysis. Arterioscl Thromb Vasc Biol 2010; 30: 1014-1026.
14. Sherer Y, Shoenfeld Y. Mechanisms of disease: atherosclerosis in autoimmune diseases. Nat Clin Pract Rheumatol 2006; 2: 99-106.
15. Kaplan MJ. Cardiovascular disease in rheumatoid arthritis. Curr Opin Rheumatol 2006; 18: 289-297.
16. Gerli R, Schillaci G, Giordano A, et al. CD4+CD28- T lymphocytes contribute to early atherosclerotic damage in rheumatoid arthritis patients. Circulation 2004; 109: 2744-2748.
17. Pasceri V, Yeh ET. A tale of two diseases: atherosclerosis and rheumatoid arthritis. Circulation 1999; 100: 2124-2126.
18. 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: 2227-2230.
19. Lopes-Virella MF, Binzafar N, Rackley S, et al. The uptake of LDL-IC by human macrophages: predominant involvement of the Fc gamma RI receptor. Atherosclerosis 1997; 135: 161-170.
20. Hasunuma Y, Matsuura E, Makita Z, et al. Involvement of beta 2-glycoprotein I and anticardiolipin antibodies in oxidatively modified low-density lipoprotein uptake by macrophages. Clin Exp Immunol 1997; 107: 569-573.
21. Haque S, Gordon C, Isenberg D, et al. Risk factors for clinical coronary heart disease in systemic lupus erythematosus: the lupus and atherosclerosis evaluation of risk (LASER) study. J Rheumatol 2010; 37: 322-329.
22. McMahon M, Grossman J, FitzGerald J, et al. Proinflammatory high-density lipoprotein as a biomarker for atherosclerosis in patients with systemic lupus erythematosus and rheumatoid arthritis. Arthritis Rheum 2006; 54: 2541-2549.
23. Srivastava R, Yu S, Parks BW, et al. Autoimmune-mediated reduction of high-density lipoprotein-cholesterol and paraoxonase 1 activity in systemic lupus erythematosus-prone gld mice. Arthritis Rheum 2011; 63: 201-211.
24. McMahon M, Grossman J, Skaggs B, et al. Dysfunctional Pro-Inflammatory High Density Lipoproteins Confer Increased Risk for Atherosclerosis in Women with Systemic Lupus Erythematosus. Arthritis Rheum 2009; 60: 2428-2437.
25. Lahita RG, Rivkin E, Cavanagh I, et al. Low levels of total cholesterol, high-density lipoprotein, and apolipoprotein A1 in association with anticardiolipin antibodies in patients with systemic lupus erythematosus. Arthritis Rheum 1993; 36: 1566-1574.
26. O'Neill SG, Giles I, Lambrianides A, et al. Antibodies to apolipoprotein A-I, highdensity lipoprotein, and C-reactive protein are associated with disease activity in paients with systemic lupus erythematosus. Arthritis Rheum 2010; 62: 845-854.
27. Bolland S, Ravetch JV. Spontaneous autoimmune disease in Fc(gamma)RIIBdeficient mice results from strain-specific epistasis. Immunity 2000; 13: 277-285.
28. Furukawa F, Tanaka H, Sekita K, et al. Dermatopathological studies on skin lesions of MRL mice. Arch Dermatol Res 1984; 276: 186-194.
29. Furukawa F, Yoshimasu T. Animal models of spontaneous and drug-induced cutaneous lupus erythematosus. Autoimmun Rev 2005; 4: 345-350.
30. Morel L. Mouse models of human autoimmune diseases: essential tools that require the proper controls. PLoS Biol 2004; 2: E241.
31. Aprahamian T, Rifkin I, Bonegio R, et al. Impaired clearance of apoptotic cells promotes synergy between atherogenesis and autoimmune disease. J Exp Med 2004; 199: 1121-1131.
32. Feng X, Li H, Rumbin AA, et al. ApoE-/-Fas-/-C57BL/6 mice: a novel murine model simultaneously exhibits lupus nephritis, atherosclerosis and osteopenia. J Lipid Res 2007; 48: 794-805.
33. Ma Z, Choudhury A, Kang SA, et al. Accelerated Atherosclerosis in ApoE-Deficient Lupus Mouse Models1. Clin Immunol 2008; 127: 168-175.
34. Morel L, Rudofsky UH, Longmate JA, et al. Polygenic control of susceptibility to murine systemic lupus erythematosus. Immunity 1994; 1: 219-229.
35. Morel L, Yu Y, Blenman KR, et al. Production of congenic mouse strains carrying genomic intervals containing SLE-susceptibility genes derived from the SLEprone NZM2410 strain. Mamm Genome 1996; 7: 335-339.
36. Morel L, Mohan C, Yu Y, et al. Functional dissection of systemic lupus erythematosus using congenic mouse strains. J Immunol 1997; 158: 6019-6028.
37. Stanic AK, Stein CM, Morgan AC, et al. Immune dysregulation accelerates atherosclerosis and modulates plaque composition in systemic lupus erythematosus. Proc Natl Acad Sci USA 2006; 103: 7018-7023.
38. Braun N, Wade N, Wakeland E, et al. Accelerated atherosclerosis is independent of feeding high fat diet in systemic lupus erythematosus-susceptible LDLr-/- mice. Lupus 2008; 17: 1070-1078.
39. Wade NS, Stevenson BG, Dunlap DS, et al. The lupus susceptibility locus Sle3 is not sufficient to accelerate atherosclerosis in lupus-susceptible low density lipoprotein receptor-deficient mice. Lupus 2010; 19: 34-42.
40. Ait-Oufella H, Herbin O, Bouaziz JD, et al. B cell depletion reduces the development of atherosclerosis in mice. J Exp Med 2010; 207: 1579-1587.
41. Kyaw T, Tay C, Khan A, et al. Conventional B2 B cell depletion ameliorates whereas its adoptive transfer aggravates atherosclerosis. J Immunol 2010; 185: 4410-4419.
42. Asanuma Y, Chung CP, Oeser A, et al. Increased concentration of proatherogenic inflammatory cytokines in systemic lupus erythematosus: relationship to cardiovascular risk factors. J Rheumatol 2006; 33: 539-545.
43. Svenungsson E, Fei GZ, Jensen-Urstad K, et al. TNF-alpha: a link between hypertriglyceridaemia and inflammation in SLE patients with cardiovascular disease. Lupus 2003; 12: 454-461.
44. Lopez-Pedrera C, Aguirre MA, Barbarroja N, et al. Accelerated atherosclerosis in systemic lupus erythematosus: role of proinflammatory cytokines and therapeutic approaches. J Biomed Biotechnol 2010; epub ahead of print.
45. Huber SA, Sakkinen P, Conze D, et al. Interleukin-6 exacerbates early atherosclerosis in mice. Arterioscler Thromb Vasc Biol 1999; 19: 2364-2367.
46. Schieffer B, Selle T, Hilfiker A, et al. Impact of interleukin-6 on plaque development and morphology in experimental atherosclerosis. Circulation. United States, 2004, pp. 3493-3500.
47. Mallat Z, Gojova A, Marchiol-Fournigault C, et al. Inhibition of transforming growth factor-beta signaling accelerates atherosclerosis and induces an unstable plaque phenotype in mice. Circ Res 2001; 89: 930-934.
48. Caligiuri G, Rudling M, Ollivier V, et al. Interleukin-10 deficiency increases atherosclerosis, thrombosis, and low-density lipoproteins in apolipoprotein E knockout mice. Mol Med 2003; 9: 10-17.
49. Von Der Thusen JH, Kuiper J, Fekkes ML, et al. Attenuation of atherogenesis by systemic and local adenovirus-mediated gene transfer of interleukin-10 in LDLr-/- mice. Faseb J 2001; 15: 2730-2732.
50. Houssiau FA, Lefebvre C, Vanden Berghe M, et al. Serum interleukin 10 titers in systemic lupus erythematosus reflect disease activity. Lupus 1995; 4: 393-395.
51. Mageed RA, Prud'homme GJ. Immunopathology and the gene therapy of lupus. Gene Ther 2003; 10: 861-874.
52. Robertson AK, Rudling M, Zhou X, et al. Disruption of TGF-beta signaling in T cells accelerates atherosclerosis. J Clin Invest 2003; 112: 1342-1350.
53. Gojova A, Brun V, Esposito B, et al. Specific abrogation of transforming growth factor-beta signaling in T cells alters atherosclerotic lesion size and composition in mice. Blood 2003; 102: 4052-4058.
54. Kohut E, Hajdu M, Gergely P, et al. Expression of TGFbeta1 and its signaling components by peripheral lymphocytes in systemic lupus erythematosus. Pathol Oncol Res 2009; 15: 251-256.
55. Elbeldi-Ferchiou A, Ben Ahmed M, Smiti-Khanfir M, et al. Resistance to Exogenous TGF-beta Effects in Patients with Systemic Lupus Erythematosus. J Clin Immunol 2011; 31: 574-583.
56. Jackson M, Ahmad Y, Bruce IN, et al. Activation of transforming growth factorbeta1 and early atherosclerosis in systemic lupus erythematosus. Arthritis Res Ther 2006; 8: R81.
57. Wofsy D, Seaman WE. Reversal of advanced murine lupus in NZB/NZW F1 mice by treatment with monoclonal antibody to L3T4. J Immunol 1987; 138: 3247-3253.
58. Jevnikar AM, Grusby MJ, Glimcher LH. Prevention of nephritis in major histocompatibility complex class II-deficient MRL-lpr mice. J Exp Med 1994; 179: 1137-1143.
59. Koh DR, Ho A, Rahemtulla A, et al. Murine lupus in MRL/lpr mice lacking CD4 or CD8 T cells. Eur J Immunol 1995; 25: 2558-2562.
60. La Cava A. Lupus and T cells. Lupus 2009; 18: 196-201.
61. Crispin JC, Kyttaris VC, Terhorst C, et al. T cells as therapeutic targets in SLE. Nature Rev Rheumatol 2010; 6: 317-325.
62. Liossis SN, Ding XZ, Dennis GJ, et al. Altered pattern of TCR/CD3-mediated protein- tyrosyl phosphorylation in T cells from patients with systemic lupus erythematosus. Deficient expression of the T cell receptor zeta chain. J Clin Invest 1998; 101: 1448-1457.
63. Valencia X, Yarboro C, Illei G, et al. Deficient CD4+CD25high T regulatory cell function in patients with active systemic lupus erythematosus. J Immunol 2007; 178: 2579-2588.
64. Hsu WT, Suen JL, Chiang BL. The role of CD4CD25 T cells in autoantibody production in murine lupus. Clin Exp Immunol 2006; 145: 513-519.
65. Liu MF, Wang CR, Fung LL, et al. Decreased CD4+CD25+ T cells in peripheral blood of patients with systemic lupus erythematosus. Scand J Immunol 2004; 59: 198-202.
66. Wan S, Xia C, Morel L. IL-6 produced by dendritic cells from lupus-prone mice inhibits CD4+CD25+ T cell regulatory functions. J Immunol 2007; 178: 271-279.
67. de Boer OJ, van der Meer JJ, Teeling P, et al. Low Numbers of FOXP3 Positive Regulatory T Cells Are Present in all Developmental Stages of Human Atherosclerotic Lesions. PLoS One 2007; 2: e779.
68. Ait-Oufella H, Salomon BL, Potteaux S, et al. Natural regulatory T cells control the development of atherosclerosis in mice. Nat Med 2006; 12: 178-180.
69. Mor A, Planer D, Luboshits G, et al. Role of naturally occurring CD4+ CD25+ regulatory T cells in experimental atherosclerosis. Arterioscl Thromb Vasc Biol 2007; 27: 893-900.
70. Wong CK, Lit LC, Tam LS, et al. Hyperproduction of IL-23 and IL-17 in patients with systemic lupus erythematosus: implications for Th17-mediated inflammation in auto-immunity. Clin Immunol 2008; 127: 385-393.
71. Crispin JC, Oukka M, Bayliss G, et al. Expanded double negative T cells in patients with systemic lupus erythematosus produce IL-17 and infiltrate the kidneys. J Immunol 2008; 181: 8761-8766.
72. Hsu HC, Yang P, Wang J, et al. Interleukin 17-producing T helper cells and interleukin 17 orchestrate autoreactive germinal center development in autoimmune BXD2 mice. Nat Immunol 2008; 9: 166-175.
73. Kang HK, Liu M, Datta SK. Low-dose peptide tolerance therapy of lupus generates plasmacytoid dendritic cells that cause expansion of autoantigen-specific regulatory T cells and contraction of inflammatory Th17 cells. J Immunol 2007; 178: 7849-7858.
74. Eid RE, Rao DA, Zhou J, et al. Interleukin-17 and interferon-gamma are produced concomitantly by human coronary artery-infiltrating T cells and act synergistically on vascular smooth muscle cells. Circulation 2009; 119: 1424-1432.
75. Pejnovic N, Vratimos A, Lee SH, et al. Increased atherosclerotic lesions and Th17 in interleukin-18 deficient apolipoprotein E-knockout mice fed high-fat diet. Mol Immunol 2009; 47: 37-45.
76. Erbel C, Chen L, Bea F, et al. Inhibition of IL-17A attenuates atherosclerotic lesion development in apoE-deficient mice. J Immunol 2009; 183: 8167-8175.
77. Smith E, Prasad KM, Butcher M, et al. Blockade of interleukin-17A results in reduced atherosclerosis in apolipoprotein E-deficient mice. Circulation 2010; 121: 1746-1755.
78. van Es T, van Puijvelde GH, Ramos OH, et al. Attenuated atherosclerosis upon IL-17R signaling disruption in LDLr deficient mice. Biochem Biophys Res Commun 2009; 388: 261-265.
79. Taleb S, Romain M, Ramkhelawon B, et al. Loss of SOCS3 expression in T cells reveals a regulatory role for interleukin-17 in atherosclerosis. J Exp Med 2009; 206: 2067-2077.
80. Cheng X, Taleb S, Wang J, et al. Inhibition of IL-17A in atherosclerosis. Atherosclerosis 2011; 215: 471-474.
81. Taleb S, Tedgui A, Mallat Z. Interleukin-17: friend or foe in atherosclerosis? Curr Opin Lipidol 2010; 21: 404-408.
82. Jacob N, Stohl W. Autoantibody-dependent and autoantibody-independent roles for B cells in systemic lupus erythematosus: past, present, and future. Autoimmunity 2010; 43: 84-97.
83. Chan OT, Madaio MP, Shlomchik MJ. The central and multiple roles of B cells in lupus pathogenesis. Immunol Rev 1999; 169: 107-121.
84. Sanz I, Lee FE. B cells as therapeutic targets in SLE. Nature reviews Rheumatology 2010; 6: 326-337.
85. Stohl W, Scholz JL, Cancro MP. Targeting BLyS in rheumatic disease: the sometimes- bumpy road from bench to bedside. Curr Opin Rheumatol 2011; 23: 305-310.
86. Wiglesworth AK, Ennis KM, Kockler DR. Belimumab: a BLyS-specific inhibitor for systemic lupus erythematosus. Ann Pharmacother 2010; 44: 1955-1961.
87. Major AS, Fazio S, Linton MF. B-lymphocyte deficiency increases atherosclerosis in LDL receptor-null mice. Arterioscler Thromb Vasc Biol 2002; 22: 1892-1898.
88. Caligiuri G, Nicoletti A, Poirier B, et al. Protective immunity against atherosclerosis carried by B cells of hypercholesterolemic mice. J Clin Invest 2002; 109: 745-753.
89. Binder CJ, Hartvigsen K, Chang MK, et al. IL-5 links adaptive and natural immunity specific for epitopes of oxidized LDL and protects from atherosclerosis. J Clin Invest 2004; 114: 427-437.
90. Horkko S, Bird DA, Miller E, et al. Monoclonal autoantibodies specific for oxidized phospholipids or oxidized phospholipid-protein adducts inhibit macrophage uptake of oxidized low-density lipoproteins. J Clin Invest 1999; 103: 117-128.
91. Bedi U, Singh M, Singh P, et al. Effects of statins on progression of coronary artery disease as measured by intravascular ultrasound. J Clin Hypertens 2011; 13: 492-496.
92. van Leuven SI, Mendez-Fernandez YV, Stroes ES, et al. Statin therapy in lupusmediated atherogenesis: two birds with one stone? Ann Rheum Dis 2011; 70: 245-248.
93. Petri MA, Kiani AN, Post W, et al. Lupus Atherosclerosis Prevention Study (LAPS). Ann Rheum Dis 2011; 70: 760-765.
94. Aprahamian T, Bonegio R, Rizzo J, et al. Simvastatin treatment ameliorates autoimmune disease associated with accelerated atherosclerosis in a murine lupus model. J Immunol 2006; 177: 3028-3034.
95. Woo JM, Lin Z, Navab M, et al. Treatment with apolipoprotein A-1 mimetic peptide reduces lupus-like manifestations in a murine lupus model of accelerated atherosclerosis. Arthritis Res Ther 2010; 12: R93.
96. Zhou X, Paulsson G, Stemme S, et al. Hypercholesterolemia is associated with a T helper (Th) 1/Th2 switch of the autoimmune response in atherosclerotic apoEknockout mice. J Clin Invest 1998; 101: 1717-1725.
97. Robertson AK, Zhou X, Strandvik B, et al. Severe hypercholesterolaemia leads to strong Th2 responses to an exogenous antigen. Scand J Immunol 2004; 59: 285-293.