Cardiovascular disease in lupus: Insights and updates

Current Opinion in Rheumatology

Volumn 25, Issue 5, 2013, Pages 597-605

  Knight, Jason S ^a   Kaplan, Mariana J ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

atherosclerosis; cardiovascular disease; neutrophil extracellular traps; systemic lupus erythematosus; type I interferons

Indexed keywords

2,4 THIAZOLIDINEDIONE DERIVATIVE; ALPHA INTERFERON; APOLIPOPROTEIN A1; APOLIPOPROTEIN E; ATORVASTATIN; BETA INTERFERON; C REACTIVE PROTEIN; CHAPERONIN 60; CHLOROQUINE; CYCLOPHOSPHAMIDE; HIGH DENSITY LIPOPROTEIN; INTERLEUKIN 18; INTERLEUKIN 1BETA; MYCOPHENOLIC ACID 2 MORPHOLINOETHYL ESTER; PIOGLITAZONE; PREDNISONE; ROSIGLITAZONE; SIMVASTATIN; THROMBOPLASTIN; TOLL LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR ALPHA; VASCULOTROPIN;

ADJUVANT THERAPY; APOPTOSIS; ATHEROSCLEROSIS; CARDIOVASCULAR DISEASE; CARDIOVASCULAR MORTALITY; CARDIOVASCULAR RISK; CAUSE OF DEATH; COGNITIVE DEFECT; DEPRESSION; DISEASE ASSOCIATION; DISEASE COURSE; DISEASE MARKER; ENDOTHELIAL DYSFUNCTION; ENDOTHELIUM CELL; GENE EXPRESSION; HUMAN; INNATE IMMUNITY; LOWEST INCOME GROUP; NEUTROPHIL; NONHUMAN; PATHOGENESIS; PLASMACYTOID DENDRITIC CELL; PRIORITY JOURNAL; REVIEW; SYSTEMIC LUPUS ERYTHEMATOSUS; T LYMPHOCYTE ACTIVATION; THROMBOCYTE ACTIVATION; UPREGULATION;

ANIMALS; ANTIMALARIALS; BIOLOGICAL MARKERS; CARDIOVASCULAR DISEASES; DISEASE MODELS, ANIMAL; HUMANS; IMMUNITY, INNATE; IMMUNOSUPPRESSIVE AGENTS; LUPUS ERYTHEMATOSUS, SYSTEMIC; RISK FACTORS;

EID: 84881543805     PISSN: 10408711     EISSN: 15316963     Source Type: Journal    
DOI: 10.1097/BOR.0b013e328363eba3     Document Type: Review

References (129)

1. 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.
2. Hak AE, Karlson EW, Feskanich D, et al. Systemic lupus erythematosus and the risk of cardiovascular disease: results from the nurses' health study. Arthritis Rheum 2009; 61:1396-1402.
3. Rajagopalan S, Somers EC, Brook RD, et al. Endothelial cell apoptosis in systemic lupus erythematosus: a common pathway for abnormal vascular function and thrombosis propensity. Blood 2004; 103:3677-3683.
4. Roman MJ, Shanker BA, Davis A, et al. Prevalence and correlates of accelerated atherosclerosis in systemic lupus erythematosus. N Engl J Med 2003; 349:2399-2406.
5. Bruce IN, Burns RJ, Gladman DD, Urowitz MB. Single photon emission computed tomography dual isotope myocardial perfusion imaging in women with systemic lupus erythematosus. I. Prevalence and distribution of abnormalities. J Rheumatol 2000; 27:2372-2377.
6. 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.
7. Nossent J, Cikes N, Kiss E, et al. Current causes of death in systemic lupus erythematosus in Europe, 2000-2004: relation to disease activity and damage accrual. Lupus 2007; 16:309-317.
8. Kahlenberg JM, Kaplan MJ. Mechanisms of premature atherosclerosis in rheumatoid arthritis and lupus. Annu Rev Med 2013; 64:249-263.
9. Skaggs BJ, Hahn BH, McMahon M. Accelerated atherosclerosis in patients with SLE: mechanisms and management. Nat Rev Rheumatol 2012; 8:214-223.
10. Zoller B, Li X, Sundquist J, Sundquist K. Risk of subsequent coronary heart disease in patients hospitalized for immune-mediated diseases: a nationwide follow-up study from Sweden. PLoS One 2012; 7:e33442.
11. Souza DC, Santo AH, Sato EI. Mortality profile related to systemic lupus erythematosus: a multiple cause-of-death analysis. J Rheumatol 2012; 39:496-503.
12. Steiman AJ, Gladman DD, Ibanez D, Urowitz MB. Outcomes in patients with systemic lupus erythematosus with and without a prolonged serologically active clinically quiescent period. Arthritis Care Res (Hoboken) 2012; 64:511-518.
13. Murray SG, Yazdany J, Kaiser R, et al. Cardiovascular disease and cognitive dysfunction in systemic lupus erythematosus. Arthritis Care Res (Hoboken) 2012; 64:1328-1333.
14. Greco CM, Li T, Sattar A, et al. Association between depression and vascular disease in systemic lupus erythematosus. J Rheumatol 2012; 39:262-268.
15. Maynard JW, Fang H, Petri M. Low socioeconomic status is associated with cardiovascular risk factors and outcomes in systemic lupus erythematosus. J Rheumatol 2012; 39:777-783.
16. Magder LS, Petri M. Incidence of and risk factors for adverse cardiovascular events among patients with systemic lupus erythematosus. Am J Epidemiol 2012; 176:708-719.
17. Wang XY, Tang XQ, Huang YJ, et al. Frequency of established cardiovascular disease and its risk factors in Chinese patients with systemic lupus erythematosus. Clin Rheumatol 2012; 31:669-675.
18. Romero-Diaz J, Vargas-Vorackova F, Kimura-Hayama E, et al. Systemic lupus erythematosus risk factors for coronary artery calcifications. Rheumatology (Oxford) 2012; 51:110-119.
19. Karp I, Abrahamowicz M, Fortin PR, et al. Longitudinal evolution of risk of coronary heart disease in systemic lupus erythematosus. J Rheumatol 2012; 39:968-973.
20. Yang L, Tao J, Tang X, et al. Prevalence and correlation of conventional and lupus-specific risk factors for cardiovascular disease in Chinese systemic lupus erythematosus patients. J Eur Acad Dermatol Venereol 2012; 26:95-101.
21. Gustafsson JT, Simard JF, Gunnarsson I, et al. Risk factors for cardiovascular mortality in patients with systemic lupus erythematosus, a prospective cohort study. Arthritis Res Ther 2012; 14:R46.
22. Kaiser R, Li Y, Chang M, et al. Genetic risk factors for thrombosis in systemic lupus erythematosus. J Rheumatol 2012; 39:1603-1610.
23. Chang YH, Lin IL, Tsay GJ, et al. Elevated circulatory MMP-2 and MMP-9 levels and activities in patients with rheumatoid arthritis and systemic lupus erythematosus. Clin Biochem 2008; 41:955-959.
24. Galis ZS, Khatri JJ. Matrix metalloproteinases in vascular remodeling and atherogenesis: the good, the bad, and the ugly. Circ Res 2002; 90:251-262.
25. Bahrehmand F, Vaisi-Raygani A, Kiani A, et al. Matrix metalloproteinase-2 functional promoter polymorphism G1575A is associated with elevated circulatory MMP-2 levels and increased risk of cardiovascular disease in systemic lupus erythematosus patients. Lupus 2012; 21:616-624.
26. Narshi CB, Giles IP, Rahman A. The endothelium: an interface between autoimmunity and atherosclerosis in systemic lupus erythematosus? Lupus 2011; 20:5-13.
27. Baron MA, Khamashta MA, Hughes GR, D'Cruz DP. Prevalence of an abnormal ankle-brachial index in patients with primary antiphospholipid syndrome: preliminary data. Ann Rheum Dis 2005; 64:144-146.
28. Ames PR, Margarita A, Delgado Alves J, et al. Anticardiolipin antibody titre and plasma homocysteine level independently predict intima media thickness of carotid arteries in subjects with idiopathic antiphospholipid antibodies. Lupus 2002; 11:208-214.
29. Gresele P, Migliacci R, Vedovati MC, et al. Patients with primary antiphospholipid antibody syndrome and without associated vascular risk factors present a normal endothelial function. Thromb Res 2009; 123:444-451.
30. Ames PR, Margarita A, Sokoll KB, et al. Premature atherosclerosis in primary antiphospholipid syndrome: preliminary data. Ann Rheum Dis 2005; 64:315-317.
31. Petri M. Update on antiphospholipid antibodies in SLE: the Hopkins' Lupus Cohort. Lupus 2010; 19:419-423.
32. Ames PR, Margarita A, Alves JD. Antiphospholipid antibodies and atherosclerosis: insights from systemic lupus erythematosus and primary antiphospholipid syndrome. Clin Rev Allergy Immunol 2009; 37:29-35.
33. Dinu AR, Merrill JT, Shen C, et al. Frequency of antibodies to the cholesterol transport protein apolipoprotein A1 in patients with SLE. Lupus 1998; 7:355-360.
34. O'Neill SG, Giles I, Lambrianides A, et al. Antibodies to apolipoprotein A-I, high-density lipoprotein, and C-reactive protein are associated with disease activity in patients with systemic lupus erythematosus. Arthritis Rheum 2010; 62:845-854.
35. Mandal K, Foteinos G, Jahangiri M, Xu Q. Role of antiheat shock protein 60 autoantibodies in atherosclerosis. Lupus 2005; 14:742-746.
36. Motoki Y, Nojima J, Yanagihara M, et al. Antiphospholipid antibodies contribute to arteriosclerosis in patients with systemic lupus erythematosus through induction of tissue factor expression and cytokine production from peripheral blood mononuclear cells. Thromb Res 2012; 130:667-673.
37. Loeffen R, Spronk HM, ten Cate H. The impact of blood coagulability on atherosclerosis and cardiovascular disease. J Thromb Haemost 2012; 10:1207-1216.
38. Boles J, Mackman N. Role of tissue factor in thrombosis in antiphospholipid antibody syndrome. Lupus 2010; 19:370-378.
39. Kinev AV, Roubey RA. Tissue factor in the antiphospholipid syndrome. Lupus 2008; 17:952-958.
40. 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.
41. McMahon M, Grossman J, Skaggs B, et al. Dysfunctional proinflammatory high-density lipoproteins confer increased risk of atherosclerosis in women with systemic lupus erythematosus. Arthritis Rheum 2009; 60:2428-2437.
42. 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.
43. Thacker SG, Zhao W, Smith CK, et al. Type I interferons modulate vascular function, repair, thrombosis, and plaque progression in murine models of lupus and atherosclerosis. Arthritis Rheum 2012; 64:2975-2985.
44. 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.
45. Dhaun N, Kluth DC. Oxidative stress promotes hypertension and albuminuria during the autoimmune disease systemic lupus erythematosus. Hypertension 2012; 59:e47; author reply e48.
46. Hanasand M, Omdal R, Norheim KB, et al. Improved detection of advanced oxidation protein products in plasma. Clin Chim Acta 2012; 413:901-906.
47. Li KJ, Wu CH, Hsieh SC, et al. Deranged bioenergetics and defective redox capacity in T lymphocytes and neutrophils are related to cellular dysfunction and increased oxidative stress in patients with active systemic lupus erythematosus. Clin Dev Immunol 2012; 2012:548516.
48. Nikpour M, Harvey PJ, Ibanez D, et al. High-sensitivity C-reactive protein as a marker of cardiovascular risk in systemic lupus erythematosus. Arthritis Rheum 2012; 64:3052-3053.
49. Lehrer RI, Ganz T. Defensins of vertebrate animals. Curr Opin Immunol 2002; 14:96-102.
50. Lehrer RI, Lichtenstein AK, Ganz T. Defensins: antimicrobial and cytotoxic peptides of mammalian cells. Annu Rev Immunol 1993; 11:105-128.
51. Tamiya H, Tani K, Miyata J, et al. Defensins- and cathepsin G-ANCA in systemic lupus erythematosus. Rheumatol Int 2006; 27:147-152.
52. Sthoeger ZM, Bezalel S, Chapnik N, et al. High alpha-defensin levels in patients with systemic lupus erythematosus. Immunology 2009; 127:116-122.
53. Vordenbaumen S, Fischer-Betz R, Timm D, et al. Elevated levels of human beta-defensin 2 and human neutrophil peptides in systemic lupus erythematosus. Lupus 2010; 19:1648-1653.
54. Vordenbaumen S, Sander O, Bleck E, et al. Cardiovascular disease and serum defensin levels in systemic lupus erythematosus. Clin Exp Rheumatol 2012; 30:364-370.
55. Knight JS, Carmona-Rivera C, Kaplan MJ. Proteins derived from neutrophil extracellular traps may serve as self-antigens and mediate organ damage in autoimmune diseases. Front Immunol 2012; 3:380.
56. Westerweel PE, Luijten RK, Hoefer IE, et al. Haematopoietic and endothelial progenitor cells are deficient in quiescent systemic lupus erythematosus. Ann Rheum Dis 2007; 66:865-870.
57. Denny MF, Thacker S, Mehta H, et al. Interferon-alpha promotes abnormal vasculogenesis in lupus: a potential pathway for premature atherosclerosis. Blood 2007; 110:2907-2915.
58. Thacker SG, Berthier CC, Mattinzoli D, et al. The detrimental effects of IFN-alpha on vasculogenesis in lupus are mediated by repression of IL-1 pathways: potential role in atherogenesis and renal vascular rarefaction. J Immunol 2010; 185:4457-4469.
59. Schmidt-Lucke C, Rossig L, Fichtlscherer S, et al. Reduced number of circulating endothelial progenitor cells predicts future cardiovascular events: proof of concept for the clinical importance of endogenous vascular repair. Circulation 2005; 111:2981-2987.
60. Lee PY, Li Y, Richards HB, et al. Type I interferon as a novel risk factor for endothelial progenitor cell depletion and endothelial dysfunction in systemic lupus erythematosus. Arthritis Rheum 2007; 56:3759-3769.
61. Somers EC, Zhao W, Lewis EE, et al. Type I interferons are associated with subclinical markers of cardiovascular disease in a cohort of systemic lupus erythematosus patients. PLoS One 2012; 7:e37000.
62. Kahlenberg JM, Thacker SG, Berthier CC, et al. Inflammasome activation of IL-18 results in endothelial progenitor cell dysfunction in systemic lupus erythematosus. J Immunol 2011; 187:6143-6156.
63. Goossens P, Gijbels MJ, Zernecke A, et al. Myeloid type I interferon signaling promotes atherosclerosis by stimulating macrophage recruitment to lesions. Cell Metab 2010; 12:142-153.
64. Macritchie N, Grassia G, Sabir SR, et al. Plasmacytoid dendritic cells play a key role in promoting atherosclerosis in apolipoprotein E-deficient mice. Arterioscler Thromb Vasc Biol 2012; 32:2569-2579.
65. Niessner A, Shin MS, Pryshchep O, et al. Synergistic proinflammatory effects of the antiviral cytokine interferon-alpha and toll-like receptor 4 ligands in the atherosclerotic plaque. Circulation 2007; 116:2043-2052.
66. Li J, Fu Q, Cui H, et al. Interferon-alpha priming promotes lipid uptake and macrophage-derived foam cell formation: a novel link between interferonalpha and atherosclerosis in lupus. Arthritis Rheum 2011; 63:492-502.
67. Niessner A, Sato K, Chaikof EL, et al. Pathogen-sensing plasmacytoid dendritic cells stimulate cytotoxic T-cell function in the atherosclerotic plaque through interferon-alpha. Circulation 2006; 114:2482-2489.
68. Trinchieri G. Type I interferon: friend or foe? J Exp Med 2010; 207:2053-2063.
69. Agrawal H, Jacob N, Carreras E, et al. Deficiency of type I IFN receptor in lupus-prone New Zealand mixed 2328 mice decreases dendritic cell numbers and activation and protects from disease. J Immunol 2009; 183:6021-6029.
70. Thacker SG, Duquaine D, Park J, Kaplan MJ. Lupus-prone New Zealand black/New Zealand white F1 mice display endothelial dysfunction and abnormal phenotype and function of endothelial progenitor cells. Lupus 2010; 19:288-299.
71. 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.
72. Baechler EC, Batliwalla FM, Karypis G, et al. Interferon-inducible gene expression signature in peripheral blood cells of patients with severe lupus. Proc Natl Acad Sci U S A 2003; 100:2610-2615.
73. Kim T, Kanayama Y, Negoro N, et al. Serum levels of interferons in patients with systemic lupus erythematosus. Clin Exp Immunol 1987; 70:562-569.
74. McBride JM, Jiang J, Abbas AR, et al. Safety and pharmacodynamics of rontalizumab in patients with systemic lupus erythematosus: results of a phase I, placebo-controlled, double-blind, dose-escalation study. Arthritis Rheum 2012; 64:3666-3676.
75. Merrill JT, Wallace DJ, Petri M, et al. Safety profile and clinical activity of sifalimumab, a fully human antiinterferon alpha monoclonal antibody, in systemic lupus erythematosus: a phase I, multicentre, double-blind randomised study. Ann Rheum Dis 2011; 70:1905-1913.
76. Elkon KB, Wiedeman A. Type I IFN system in the development and manifestations of SLE. Curr Opin Rheumatol 2012; 24:499-505.
77. Denny MF, Yalavarthi S, Zhao W, et al. A distinct subset of proinflammatory neutrophils isolated from patients with systemic lupus erythematosus induces vascular damage and synthesizes type I IFNs. J Immunol 2010; 184:3284-3297.
78. Folkman J, Ingber D. Inhibition of angiogenesis. Semin Cancer Biol 1992; 3:89-96.
79. Hansson GK, Hermansson A. The immune system in atherosclerosis. Nat Immunol 2011; 12:204-212.
80. 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.
81. Braun N, Wade NS, Wakeland EK, Major AS. Accelerated atherosclerosis is independent of feeding high fat diet in systemic lupus erythematosussusceptible LDLr(-/-) mice. Lupus 2008; 17:1070-1078.
82. 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.
83. Ma Z, Choudhury A, Kang SA, et al. Accelerated atherosclerosis in ApoE deficient lupus mouse models. Clin Immunol 2008; 127:168-175.
84. Stanic AK, Stein CM, Morgan AC, et al. Immune dysregulation accelerates atherosclerosis and modulates plaque composition in systemic lupus erythematosus. Proc Natl Acad Sci U S A 2006; 103:7018-7023.
85. Lewis MJ, Malik TH, Fossati-Jimack L, et al. Distinct roles for complement in glomerulonephritis and atherosclerosis revealed in mice with a combination of lupus and hyperlipidemia. Arthritis Rheum 2012; 64:2707-2718.
86. Doring Y, Manthey HD, Drechsler M, et al. Auto-antigenic protein-DNA complexes stimulate plasmacytoid dendritic cells to promote atherosclerosis. Circulation 2012; 125:1673-1683.
87. Lande R, Ganguly D, Facchinetti V, et al. Neutrophils activate plasmacytoid dendritic cells by releasing self-DNA-peptide complexes in systemic lupus erythematosus. Sci Transl Med 2011; 3:73ra19.
88. Garcia-Romo GS, Caielli S, Vega B, et al. Netting neutrophils are major inducers of type I IFN production in pediatric systemic lupus erythematosus. Sci Transl Med 2011; 3:73ra20.
89. Villanueva E, Yalavarthi S, Berthier CC, et al. Netting neutrophils induce endothelial damage, infiltrate tissues, and expose immunostimulatory molecules in systemic lupus erythematosus. J Immunol 2011; 187:538-552.
90. Doring Y, Drechsler M, Wantha S, et al. Lack of neutrophil-derived CRAMP reduces atherosclerosis in mice. Circ Res 2012; 110:1052-1056.
91. Knight JS, Kaplan MJ. Lupus neutrophils: 'NET' gain in understanding lupus pathogenesis. Curr Opin Rheumatol 2012; 24:441-450.
92. Brinkmann V, Reichard U, Goosmann C, et al. Neutrophil extracellular traps kill bacteria. Science 2004; 303:1532-1535.
93. Brinkmann V, Zychlinsky A. Neutrophil extracellular traps: is immunity the second function of chromatin? J Cell Biol 2012; 198:773-783.
94. Hakkim A, Furnrohr BG, Amann K, et al. Impairment of neutrophil extracellular trap degradation is associated with lupus nephritis. Proc Natl Acad Sci U S A 2010; 107:9813-9818.
95. Leffler J, Martin M, Gullstrand B, et al. Neutrophil extracellular traps that are not degraded in systemic lupus erythematosus activate complement exacerbating the disease. J Immunol 2012; 188:3522-3531.
96. Kahlenberg JM, Carmona-Rivera C, Smith CK, Kaplan MJ. Neutrophil extracellular trap-associated protein activation of the NLRP3 inflammasome is enhanced in lupus macrophages. J Immunol 2013; 190:1217-1226.
97. Caudrillier A, Kessenbrock K, Gilliss BM, et al. Platelets induce neutrophil extracellular traps in transfusion-related acute lung injury. J Clin Invest 2012; 122:2661-2671.
98. Gupta AK, Joshi MB, Philippova M, et al. Activated endothelial cells induce neutrophil extracellular traps and are susceptible to NETosis-mediated cell death. FEBS Lett 2010; 584:3193-3197.
99. Megens RT, Vijayan S, Lievens D, et al. Presence of luminal neutrophil extracellular traps in atherosclerosis. Thromb Haemost 2012; 107:597-598.
100. Fuchs TA, Brill A, Wagner DD. Neutrophil extracellular trap (NET) impact on deep vein thrombosis. Arterioscler Thromb Vasc Biol 2012; 32:1777-1783.
101. Knight JS, Zhao W, Luo W, et al. Peptidylarginine deiminase inhibition is immunomodulatory and vasculoprotective in murine lupus. J Clin Invest 2013; doi:pii: 67390. 10.1172/JCI67390. [Epub ahead of print]
102. Davi G, Patrono C. Platelet activation and atherothrombosis. N Engl J Med 2007; 357:2482-2494.
103. Vieira-de-Abreu A, Campbell RA, Weyrich AS, Zimmerman GA. Platelets: versatile effector cells in hemostasis, inflammation, and the immune continuum. Semin Immunopathol 2012; 34:5-30.
104. Nagahama M, Nomura S, Ozaki Y, et al. Platelet activation markers and soluble adhesion molecules in patients with systemic lupus erythematosus. Autoimmunity 2001; 33:85-94.
105. Tam LS, Fan B, Li EK, et al. Patients with systemic lupus erythematosus show increased platelet activation and endothelial dysfunction induced by acute hyperhomocysteinemia. J Rheumatol 2003; 30:1479-1484.
106. Lood C, Amisten S, Gullstrand B, et al. Platelet transcriptional profile and protein expression in patients with systemic lupus erythematosus: up-regulation of the type I interferon system is strongly associated with vascular disease. Blood 2010; 116:1951-1957.
107. Duffau P, Seneschal J, Nicco C, et al. Platelet CD154 potentiates interferonalpha secretion by plasmacytoid dendritic cells in systemic lupus erythematosus. Sci Transl Med 2010; 2:47ra63.
108. Clark SR, Ma AC, Tavener SA, et al. Platelet TLR4 activates neutrophil extracellular traps to ensnare bacteria in septic blood. Nat Med 2007; 13:463-469.
109. Petri M, Perez-Gutthann S, Spence D, Hochberg MC. Risk factors for coronary artery disease in patients with systemic lupus erythematosus. Am J Med 1992; 93:513-519.
110. Selzer F, Sutton-Tyrrell K, Fitzgerald S, et al. Vascular stiffness in women with systemic lupus erythematosus. Hypertension 2001; 37:1075-1082.
111. Rahman P, Gladman DD, Urowitz MB, et al. The cholesterol lowering effect of antimalarial drugs is enhanced in patients with lupus taking corticosteroid drugs. J Rheumatol 1999; 26:325-330.
112. Jung H, Bobba R, Su J, et al. The protective effect of antimalarial drugs on thrombovascular events in systemic lupus erythematosus. Arthritis Rheum 2010; 62:863-868.
113. Edwards MH, Pierangeli S, Liu X, et al. Hydroxychloroquine reverses thrombogenic properties of antiphospholipid antibodies in mice. Circulation 1997; 96:4380-4384.
114. Ouimet M, Franklin V, Mak E, et al. Autophagy regulates cholesterol efflux from macrophage foam cells via lysosomal acid lipase. Cell Metab 2011; 13:655-667.
115. van Leuven SI, van Wijk DF, Volger OL, et al. Mycophenolate mofetil attenuates plaque inflammation in patients with symptomatic carotid artery stenosis. Atherosclerosis 2010; 211:231-236.
116. David KM, Morris JA, Steffen BJ, et al. Mycophenolate mofetil vs. azathioprine is associated with decreased acute rejection, late acute rejection, and risk for cardiovascular death in renal transplant recipients with pretransplant diabetes. Clin Transplant 2005; 19:279-285.
117. van Leuven SI, Mendez-Fernandez YV, Wilhelm AJ, et al. Mycophenolate mofetil but not atorvastatin attenuates atherosclerosis in lupus-prone LDLr(-/-) mice. Ann Rheum Dis 2012; 71:408-414.
118. Kiani AN, Magder LS, Petri M. Mycophenolate mofetil (MMF) does not slow the progression of subclinical atherosclerosis in SLE over 2 years. Rheumatol Int 2012; 32:2701-2705.
119. Lawman S, Mauri C, Jury EC, et al. Atorvastatin inhibits autoreactive B cell activation and delays lupus development in New Zealand black/white F1 mice. J Immunol 2004; 173:7641-7646.
120. 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.
121. Abud-Mendoza C, de la Fuente H, Cuevas-Orta E, et al. Therapy with statins in patients with refractory rheumatic diseases: a preliminary study. Lupus 2003; 12:607-611.
122. Ferreira GA, Navarro TP, Telles RW, et al. Atorvastatin therapy improves endothelial-dependent vasodilation in patients with systemic lupus erythematosus: an 8 weeks controlled trial. Rheumatology (Oxford) 2007; 46:1560-1565.
123. Petri MA, Kiani AN, Post W, et al. Lupus Atherosclerosis Prevention Study (LAPS). Ann Rheum Dis 2011; 70:760-765.
124. Schanberg LE, Sandborg C, Barnhart HX, et al. Use of atorvastatin in systemic lupus erythematosus in children and adolescents. Arthritis Rheum 2012; 64:285-296.
125. Steichen O. A clinically relevant benefit of statins in young patients with systemic lupus erythematosus cannot be excluded: comment on the article by Schanberg et al. Arthritis Rheum 2012; 64:2805; author reply 2805-2806.
126. Aprahamian T, Bonegio RG, Richez C, et al. The peroxisome proliferatoractivated receptor gamma agonist rosiglitazone ameliorates murine lupus by induction of adiponectin. J Immunol 2009; 182:340-346.
127. Venegas-Pont M, Sartori-Valinotti JC, Maric C, et al. Rosiglitazone decreases blood pressure and renal injury in a female mouse model of systemic lupus erythematosus. Am J Physiol Regul Integr Comp Physiol 2009; 296:R1282-R1289.
128. Zhao W, Thacker SG, Hodgin JB, et al. The peroxisome proliferator- activated receptor gamma agonist pioglitazone improves cardiometabolic risk and renal inflammation in murine lupus. J Immunol 2009; 183:2729-2740.
129. Juarez-Rojas JG, Medina-Urrutia AX, Jorge-Galarza E, et al. Pioglitazone improves the cardiovascular profile in patients with uncomplicated systemic lupus erythematosus: a double-blind randomized clinical trial. Lupus 2012; 21:27-35.