Immunity and early atherosclerosis in the course of systemic lupus erythematosus, mixed connective tissue disease and antiphospholipid syndrome
Data nadesłania: 17-03-2016
Data ostatniej rewizji: 12-04-2016
Data akceptacji: 18-08-2016
Data publikacji online: 05-10-2016
Data publikacji: 31-08-2016
Reumatologia 2016;54(4):187-195
Atherosclerosis is a chronic inflammatory disease of the arteries associated with various risk factors that promote lipid abnormalities, development and progression of atherosclerotic lesions, plaque rupture, and vascular thrombosis. Atherosclerosis is accelerated in autoimmune diseases. Non-invasive investigations showed increased intima-media thickness (IMT), carotid plaque, and coronary artery calcifications in patients with antiphospholipid syndrome, systemic lupus erythematosus and mixed connective tissue disease compared to controls. The balance between the proinflammatory and anti-inflammatory cytokines allows the immune equilibrium to be maintained. In autoimmune diseases the prevalence of proinflammatory factors leads to premature atherosclerosis. This review presents complementary knowledge on innate and adaptive immunity, cytokines and the role of inflammasomes in progression of early atherosclerosis.
Shoenfeld Y, Gerli R, Doria A, et al. Accelerated atherosclerosis in autoimmune rheumatic diseases. Circulation 2005; 112: 3337-3347.
Soltész P, Kerekes G, Dér H, et al. Comparative assessment of vascular function in autoimmune rheumatic diseases: considerations of prevention and treatment. Autoimmun Rev 2011; 10: 416-425.
Ruiz-Irastorza G, Khamashta MA, Castellino G, et al. Systemic lupus erythematosus. Lancet 2001; 357: 1027-1032.
Wick G, Schett A, Amberger A, et al. Is atherosclerosis an immunological mediated disease? Immunol Today 1995; 16: 27-33.
López-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; 2010: 607084.
Szücs G, Tímár O, Szekanecz Z, et al. Endothelial dysfunction precedes atherosclerosis in systemic sclerosis-relevance for prevention of vascular complications. Rheumatology (Oxford) 2007; 46: 759-762.
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.
Yang K, Li D, Luo M, et al. Generation of HSP60-specific regulatory T cell and effect on atherosclerosis. Cell Immunol 2006; 243: 90-95.
Hu Z, Li D, Hu Y, et al. Changes of CD4+CD25+ regulatory T cells in patients with acute coronary syndrome and the effects of atorvastatin. J Huazhong Univ SciTechnol Med Sci 2007; 27: 524-527.
Tu H, Li Q, Jiang H, et al. Dual effects of statins therapy in systemic lupus erythematosus and SLE-related atherosclerosis: The potential role for regulatory T cells. Atherosclerosis 2012; 222: 29-33.
Stutz A, Golenbock DT, Latz E. Inflammasomes: too big to miss. J Clin Invest 2009; 119: 3502-3511.
Goldbach-Mansky R, Dailey NJ, Canna SW, et al. Neonatal-onset multisystem inflammatory disease responsive to interleukin-1B inhibition. N Engl J Med 2006; 355: 581-592.
Yang J, Chu Y, Yang X, et al. Th17 and natural Treg cell population dynamics in systemic lupus erythematosus, Arthritis Rheum 2009; 60: 1472-1483.
Madamanchi NR, Vendrov A, Runge MS. Oxidative stress and vascular disease. Arterioscler Thromb Vasc Biol 2005; 25: 29-38.
Stone NJ, Bilek S, Rosenbaum S. Recent National Cholesterol Education Program Adult Treatment Panel III Update: adjustments and options. Am J Cardiol 2005; 96: 53E-59E.
Chobanian AV, Bakris GL, Black HR, et al. The Seventh Report of the Joint National Committee on Prevention, Detection, Evaluation, and Treatment of High Blood Pressure: the JNC 7 report. JAMA 2003; 289: 2560-2572.
Costenbader KH, Karlson EW, Gall V, et al. Barriers to a trial of atherosclerosis prevention in systemic lupus erythematosus. Arthritis Rheum 2005; 53: 718-723.
Durán-Barragán S, McGwin G Jr, Vilá LM, et al. Angiotensin-converting enzyme inhibitors delay the occurrence of renal involvement and are associated with a decreased risk of disease activity in patients with systemic lupus erythematosus – results from LUMINA (LIX): a multiethnic US cohort. Rheumatology (Oxford) 2008; 47: 1093-1096.
Forrester JS, Libby P. The inflammation hypothesis and its potential relevance to statin therapy. Am J Cardiol 2007; 99: 732-738.
Kajiwara T, Yasuda T, Matsuura E. Intracellular trafficking of beta2-glycoprotein I complexes with lipid vesicles in macrophages: implications on the development of antiphospholipid syndrome. J Autoimmun 2007; 29: 164-173.
Kuwana M, Matsuura E, Kobayashi K, et al. Binding of beta2-glycoprotein I to anionic phospholipids facilitates processing and presentation of a cryptic epitope that activates pathogenic autoreactive T cells. Blood 2005; 105: 1552-1557.
Toms TE, Panoulas VF, Kitas GD. Dyslipidaemia in rheumatological autoimmune diseases. Open Cardiovasc Med J 2011; 5: 64-75.
Medina-Gomez G, Gray S, Vidal-Puig A. Adipogenesis and lipotoxicity: role of peroxisome proliferator-activated receptor gamma (PPARgamma) and PPARgammacoactivator-1 (PGC1). Public Health Nutr 2007; 10: 1132-1137.
van Es T, van Puijvelde GHM, Ramos OH, et al. Attenuated atherosclerosis upon IL-17R signaling disruption in LDLr deficient mice. Biochem Biophys Res Commun 2009; 388: 261-265.
Chen S, Crother TR, Ardit M. Emerging role of IL-17 in atherosclerosis. J Innate Immun 2010; 2: 325-333.
Wade NS, Major AS. The problem of accelerated atherosclerosis in systemic lupus erythematosus: Insights into a complex co-morbidity. Thromb Haemost 2011; 106: 849-857.
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.
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 (Greenwich) 2011; 13: 492-496.
Gojova A, Brun V, Esposito B, et al. Specific abrogation of transforming growth factor-beta signalling in T cells alters atherosclerotic lesion size and composition in mice. Blood 2003; 102: 4052-4058.
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.
Niessner A, Sato K, Chaikof EL, et al. Pathogen-sensing plasmacytoid dendritic cells stimulate cytotoxic T-cell function in the atherosclerotic plaquethrough interferon-alpha. Circulation 2006; 114: 2482-2489.
Levy Z, Rachmani R, Trestman S, et al. Low-dose interferon-gamma accelerates atherosclerosis in an LDL receptor-deficient mouse model. Eur J Intern Med 2003; 14: 479-483.
Secchiero P, Rimondi E, di Iasio MG, et al. C-Reactive protein downregulates TRAIL expression in human peripheral monocytes via an Egr-1-dependent pathway. Clin Cancer Res 2013; 19: 1949-1959.
Di Bartolo BA, Cartland SP, Harith HH, et al. TRAIL-deficiency accelerates vascular calcification in atherosclerosis via modulation of RANKL. PLoS ONE 2013; 8: e74211.
Higashiyama M, Hokari R, Kurihara C, et al. Interferon-alpha increases monocyte migration via platelet-monocyte interaction inmurine intestinal microvessels. Clin Exp Immunol 2010; 162: 156-162.
Hansson GK. Immune mechanisms in atherosclerosis. Arterioscler Thromb Vasc Biol 2001; 21: 1876-1890.
Fernandes JL, Mamoni RL, Orford JL, et al. Increased Th1 activity in patients with coronary artery disease. Cytokine 2004; 26: 131-137.
Rho YH, Chung CP, Oeser A, et al. Novel cardiovascular risk factors in premature coronary atherosclerosis associated with systemic lupus erythematosus. J Rheum 2008; 35: 1789-1794.
Blanco-Colio LM, Martín-Ventura JL, Munoz-Garcia B, et al. TWEAK and Fn14: new players in the pathogenesis of atherosclerosis. Front Biosci 2007; 12: 3648-3655.
Schwartz N, Su L, Burkly LC, et al. Urinary TWEAK and the activity of lupus nephritis. J Autoimmun 2006; 27: 242-250.
Chung C, Long A, Solus J, et al. Adipocytokines in systemic lupus erythematosus: relationship to inflammation, insulin resistance and coronary atherosclerosis. Lupus 2009; 18: 799-806.
Dong F, Zhang X, Ren J. Leptin regulates cardiomyocyte contractile function through endothelin-1 receptor-NADPH oxidase pathway. Hypertension 2006; 47: 222-229.
McMahon M, Skaggs BJ, Sahakian L, et al. Plasma leptin levels are associated with carotid artery plaque and intima-media thickness (IMT) in women with SLE and a matched population of healthy women. Arthritis Rheum 2007; 56 Suppl: S796.
McMahon M, Skaggs BJ, Sahakian L, et al. High plasma leptin levels confer increased risk of atherosclerosis in women with systemic lupus erythematosus, and are associated with inflammatory oxidised lipids. Ann Rheum Dis 2011; 70: 1619-1624.
Hahn BH, Lourencco EV, McMahon M, et al. Pro-inflammatory high-density lipoproteins and atherosclerosis are induced in lupus-prone mice by a high-fat diet and leptin. Lupus 2010; 19: 913-917.
Michaelson J, Wisniacki N, Burkly L, Putterman C. Role of TWEAK in Lupus Nephritis: A bench-to-bedside review. J Autoimmun 2012; 39: 130-142.
Tiemessen MM, Jagger AL, Evans HG, et al. CD4+CD25+Foxp3+ regulatory T cells induce alternative activation of human monocytes/macrophages. Proc Natl Acad Sci USA 2007; 104: 19446-19451.
Reynolds HR, Buyon J, Kim M, et al. Association of plasma soluble E-selectin and adiponectin with carotid plaque in patients with systemic lupus erythematosus. Atherosclerosis 2010; 210: 569-574.
Blanco-Colio LM, Martín-Ventura JL, Munoz-Garcia B, et al. Identification of soluble tumor necrosis factor-like weak inducer of apoptosis (sTWEAK) as a possible biomarker of subclinical atherosclerosis. Arterioscler Thromb Vasc Biol 2007; 27: 916-922.
Ouchi N, Kihara S, Arita Y, et al. Adiponectin, an adipocyte-derived plasma protein, inhibits endothelial NF-kappaB signaling through a cAMP-dependent pathway. Circulation 2000; 102: 1296-1301.
Aprahamian TR, Bonegio RG, Weitzner Z, et al. Peroxisome proliferator-activated receptor gamma agonists in the prevention and treatment of murine systemic lupus erythematosus. Immunology 2014; 142: 3633-3673.
Reilly MP, Lehrke M, Wolfe ML, et al. Resistin is an inflammatory marker of atherosclerosis in humans. Circulation 2005; 111: 932-939.
Baker JF, Morales M, Qatanani M, et al. Resistin levels in lupus and associations with disease-specific measures, insulin resistance, and coronary calcification. J Rheumatol 2011; 38: 2369-2375.
Ingelsson E, Larson MG, Fox CS, et al. Clinical correlates of circulating visfatin levels in a community-based sample. Diabetes Care 2007; 30: 1278-1280.
Brandt KJ, Kruithof EK, de Moerloose P. Receptors involved in cell activation by antiphospholipid antibodies. Thromb Res 2013; 132: 408-413.
Kiechl S, Lorenz E, Reindl M, et al. Toll-like receptor 4 polymorphisms and atherogenesis. N Engl J Med 347: 185-192.
Ameziane N, Beillat T, Verpillat P, et al. Association of the Toll-like receptor 4 gene Asp299Gly polymorphism with acute coronary events. Arterioscler Thromb Vasc Biol 2003; 23, e61-e64.
Wu XX, Guller S, Rand JH. Hydroxychloroquine reduces binding of antiphospholipid antibodies to syncytiotrophoblasts and restores annexin A5 expression. Am J Obstet Gynecol 2011; 205: 576.e7-576.e14.
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.
Duffau P, Seneschal J, Nicco C, et al. Platelet CD154 potentiates interferon-alpha secretion by plasmacytoid dendritic cells in systemic lupus erythematosus. Sci Transl Med 2010; 2: 47ra63.
Copyright: © Narodowy Instytut Geriatrii, Reumatologii i Rehabilitacji w Warszawie. This is an Open Access journal, all articles are distributed under the terms of the Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International (CC BY-NC-SA 4.0) License (https://creativecommons.org/licenses/by-nc-sa/4.0/), allowing third parties to copy and redistribute the material in any medium or format and to remix, transform, and build upon the material, provided the original work is properly cited and states its license.
Journals System - logo
Scroll to top