Login Register Cart 0
Generic placeholder image

Current Pharmaceutical Design

Editor-in-Chief

ISSN (Print): 1381-6128
ISSN (Online): 1873-4286

Back
Journal Home About Journal Editorial Board Journal Insight Current Issue Volumes/Issues
Subscribe
Review Article

Vascular Inflammation in Cardiovascular Disease: Is Immune System Protective or Bystander?

Author(s): Khalid Muhammad, Mohammed A. Ayoub and Rabah Iratni*

Volume 27, Issue 18, 2021

Published on: 18 January, 2021

Page: [2141 - 2150] Pages: 10

DOI: 10.2174/1381612827666210118121952

Price: $65

Abstract

Cardiovascular disease (CVD) is one of the leading causes of death worldwide. Chronic atherosclerosis induced vascular inflammation and perturbation of lipid metabolism is believed to be a major cause of CVD. Interplay of innate and adaptive Immune system has been interwined with various risk factors associated with the initiation and progression of atherosclerosis in CVD. A large body of evidence indicates a correlation between immunity and atherosclerosis. Retention of plasma lipoproteins in arterial subendothelial wall triggers the T helper type 1 (Th1) cells and monocyte-derived macrophages to form atherosclerotic plaques. In the present review, we will discuss the pathogenesis of CVD in relation to atherosclerosis with a particular focus on pro-atherogenic role of immune cells. Recent findings have also suggested anti-atherogenic roles of different B cell subsets. Therapeutic approaches to target atherosclerosis risk factors have reduced the mortality, but a need exists for the novel therapies to treat arterial vascular inflammation. These insights into the immune pathogenesis of atherosclerosis can lead to new targeted therapeutics to abate cardiovascular mortality and morbidity.

Keywords: Cardiovascular disease, atherosclerosis, T cells, B cells, dendritic cells, lipoproteins.

« Previous Next »
[1]
Hansson GK. Inflammation, atherosclerosis, and coronary artery disease. N Engl J Med 2005; 352(16): 1685-95.
[http://dx.doi.org/10.1056/NEJMra043430] [PMID: 15843671]
[2]
Tabas I, Lichtman AH. Monocyte-Macrophages and T Cells in Atherosclerosis. Immunity 2017; 47(4): 621-34.
[http://dx.doi.org/10.1016/j.immuni.2017.09.008] [PMID: 29045897]
[3]
Hansson GK, Hermansson A. The immune system in atherosclerosis. Nat Immunol 2011; 12(3): 204-12.
[http://dx.doi.org/10.1038/ni.2001] [PMID: 21321594]
[4]
Libby P. Mechanisms of acute coronary syndromes and their implications for therapy. N Engl J Med 2013; 368(21): 2004-13.
[http://dx.doi.org/10.1056/NEJMra1216063] [PMID: 23697515]
[5]
Tabas I, Williams KJ, Borén J. Subendothelial lipoprotein retention as the initiating process in atherosclerosis: update and therapeutic implications. Circulation 2007; 116(16): 1832-44.
[http://dx.doi.org/10.1161/CIRCULATIONAHA.106.676890] [PMID: 17938300]
[6]
Döring Y, Drechsler M, Soehnlein O, Weber C. Neutrophils in atherosclerosis: from mice to man. Arterioscler Thromb Vasc Biol 2015; 35(2): 288-95.
[http://dx.doi.org/10.1161/ATVBAHA.114.303564] [PMID: 25147339]
[7]
Albany CJ, Trevelin SC, Giganti G, Lombardi G, Scottà C. Getting to the Heart of the Matter: The Role of Regulatory T-Cells (Tregs) in Cardiovascular Disease (CVD) and Atherosclerosis. Front Immunol 2019; 10: 2795.
[http://dx.doi.org/10.3389/fimmu.2019.02795] [PMID: 31849973]
[8]
Munteanu AI, Raica M, Zota EG. Immunohistochemical study of the role of mast cells and macrophages in the process of angiogenesis in the atherosclerotic plaques in patients with metabolic syndrome. Arkh Patol 2016; 78(2): 19-28.
[http://dx.doi.org/10.17116/patol201678219-28] [PMID: 27070771]
[9]
Li B, Li W, Li X, Zhou H. Inflammation: A Novel Therapeutic Target/Direction in Atherosclerosis. Curr Pharm Des 2017; 23(8): 1216-27.
[http://dx.doi.org/10.2174/1381612822666161230142931] [PMID: 28034355]
[10]
Zernecke A, Shagdarsuren E, Weber C. Chemokines in atherosclerosis: an update. Arterioscler Thromb Vasc Biol 2008; 28(11): 1897-908.
[http://dx.doi.org/10.1161/ATVBAHA.107.161174] [PMID: 18566299]
[11]
Bochkov VN, Mechtcheriakova D, Lucerna M, et al. Oxidized phospholipids stimulate tissue factor expression in human endothelial cells via activation of ERK/EGR-1 and Ca(++)/NFAT. Blood 2002; 99(1): 199-206.
[http://dx.doi.org/10.1182/blood.V99.1.199] [PMID: 11756172]
[12]
Gargalovic PS, Gharavi NM, Clark MJ, et al. The unfolded protein response is an important regulator of inflammatory genes in endothelial cells. Arterioscler Thromb Vasc Biol 2006; 26(11): 2490-6.
[http://dx.doi.org/10.1161/01.ATV.0000242903.41158.a1] [PMID: 16931790]
[13]
Gharavi NM, Alva JA, Mouillesseaux KP, et al. Role of the Jak/STAT pathway in the regulation of interleukin-8 transcription by oxidized phospholipids in vitro and in atherosclerosis in vivo. J Biol Chem 2007; 282(43): 31460-8.
[http://dx.doi.org/10.1074/jbc.M704267200] [PMID: 17726017]
[14]
Libby P, Pasterkamp G. Requiem for the ‘vulnerable plaque’. Eur Heart J 2015; 36(43): 2984-7.
[PMID: 26206212]
[15]
Virmani R, Kolodgie FD, Burke AP, Farb A, Schwartz SM. Lessons from sudden coronary death: a comprehensive morphological classification scheme for atherosclerotic lesions. Arterioscler Thromb Vasc Biol 2000; 20(5): 1262-75.
[http://dx.doi.org/10.1161/01.ATV.20.5.1262] [PMID: 10807742]
[16]
Amento EP, Ehsani N, Palmer H, Libby P. Cytokines and growth factors positively and negatively regulate interstitial collagen gene expression in human vascular smooth muscle cells. Arterioscler Thromb 1991; 11(5): 1223-30.
[http://dx.doi.org/10.1161/01.ATV.11.5.1223] [PMID: 1911708]
[17]
Bäck M, Ketelhuth DF, Agewall S. Matrix metalloproteinases in atherothrombosis. Prog Cardiovasc Dis 2010; 52(5): 410-28.
[http://dx.doi.org/10.1016/j.pcad.2009.12.002] [PMID: 20226959]
[18]
Gisterå A, Hansson GK. The immunology of atherosclerosis. Nat Rev Nephrol 2017; 13(6): 368-80.
[http://dx.doi.org/10.1038/nrneph.2017.51] [PMID: 28392564]
[19]
Baigent C, Blackwell L, Emberson J, et al. Cholesterol Treatment Trialists’ (CTT) Collaboration. Efficacy and safety of more intensive lowering of LDL cholesterol: a meta-analysis of data from 170,000 participants in 26 randomised trials. Lancet 2010; 376(9753): 1670-81.
[http://dx.doi.org/10.1016/S0140-6736(10)61350-5] [PMID: 21067804]
[20]
Mihaylova B, Emberson J, Blackwell L, et al. Cholesterol Treatment Trialists’ (CTT) Collaborators. The effects of lowering LDL cholesterol with statin therapy in people at low risk of vascular disease: meta-analysis of individual data from 27 randomised trials. Lancet 2012; 380(9841): 581-90.
[http://dx.doi.org/10.1016/S0140-6736(12)60367-5] [PMID: 22607822]
[21]
Mihos CG, Pineda AM, Santana O. Cardiovascular effects of statins, beyond lipid-lowering properties. Pharmacol Res 2014; 88: 12-9.
[http://dx.doi.org/10.1016/j.phrs.2014.02.009] [PMID: 24631782]
[22]
Moos MP, John N, Gräbner R, et al. The lamina adventitia is the major site of immune cell accumulation in standard chow-fed apolipoprotein E-deficient mice. Arterioscler Thromb Vasc Biol 2005; 25(11): 2386-91.
[http://dx.doi.org/10.1161/01.ATV.0000187470.31662.fe] [PMID: 16179593]
[23]
Gabriel SE. Cardiovascular morbidity and mortality in rheumatoid arthritis. Am J Med 2008; 121(10)(Suppl. 1): S9-S14.
[http://dx.doi.org/10.1016/j.amjmed.2008.06.011] [PMID: 18926169]
[24]
Dixon WG, Watson KD, Lunt M, Hyrich KL, Silman AJ, Symmons DP. British Society for Rheumatology Biologics Register Control Centre Consortium; British Society for Rheumatology Biologics Register. Reduction in the incidence of myocardial infarction in patients with rheumatoid arthritis who respond to anti-tumor necrosis factor alpha therapy: results from the British Society for Rheumatology Biologics Register. Arthritis Rheum 2007; 56(9): 2905-12.
[http://dx.doi.org/10.1002/art.22809] [PMID: 17763428]
[25]
Frostegård J. Immunity, atherosclerosis and cardiovascular disease. BMC Med 2013; 11: 117.
[http://dx.doi.org/10.1186/1741-7015-11-117] [PMID: 23635324]
[26]
Packard RR, Lichtman AH, Libby P. Innate and adaptive immunity in atherosclerosis. Semin Immunopathol 2009; 31(1): 5-22.
[http://dx.doi.org/10.1007/s00281-009-0153-8] [PMID: 19449008]
[27]
Bartlett B, Ludewick HP, Misra A, Lee S, Dwivedi G. Macrophages and T cells in atherosclerosis: a translational perspective. Am J Physiol Heart Circ Physiol 2019; 317(2): H375-86.
[http://dx.doi.org/10.1152/ajpheart.00206.2019] [PMID: 31199186]
[28]
Song L, Leung C, Schindler C. Lymphocytes are important in early atherosclerosis. J Clin Invest 2001; 108(2): 251-9.
[http://dx.doi.org/10.1172/JCI200111380] [PMID: 11457878]
[29]
Smith JD, Trogan E, Ginsberg M, Grigaux C, Tian J, Miyata M. Decreased atherosclerosis in mice deficient in both macrophage colony-stimulating factor (op) and apolipoprotein E. Proc Natl Acad Sci USA 1995; 92(18): 8264-8.
[http://dx.doi.org/10.1073/pnas.92.18.8264] [PMID: 7667279]
[30]
Tacke F, Alvarez D, Kaplan TJ, et al. Monocyte subsets differentially employ CCR2, CCR5, and CX3CR1 to accumulate within atherosclerotic plaques. J Clin Invest 2007; 117(1): 185-94.
[http://dx.doi.org/10.1172/JCI28549] [PMID: 17200718]
[31]
Swirski FK, Libby P, Aikawa E, et al. Ly-6Chi monocytes dominate hypercholesterolemia-associated monocytosis and give rise to macrophages in atheromata. J Clin Invest 2007; 117(1): 195-205.
[http://dx.doi.org/10.1172/JCI29950] [PMID: 17200719]
[32]
Schaftenaar F, Frodermann V, Kuiper J, Lutgens E. Atherosclerosis: the interplay between lipids and immune cells. Curr Opin Lipidol 2016; 27(3): 209-15.
[http://dx.doi.org/10.1097/MOL.0000000000000302] [PMID: 27031276]
[33]
Murphy AJ, Tall AR. Disordered haematopoiesis and athero-thrombosis. Eur Heart J 2016; 37(14): 1113-21.
[http://dx.doi.org/10.1093/eurheartj/ehv718] [PMID: 26869607]
[34]
Robbins CS, Chudnovskiy A, Rauch PJ, et al. Extramedullary hematopoiesis generates Ly-6C(high) monocytes that infiltrate atherosclerotic lesions. Circulation 2012; 125(2): 364-74.
[http://dx.doi.org/10.1161/CIRCULATIONAHA.111.061986] [PMID: 22144566]
[35]
Dutta P, Courties G, Wei Y, et al. Myocardial infarction accelerates atherosclerosis. Nature 2012; 487(7407): 325-9.
[http://dx.doi.org/10.1038/nature11260] [PMID: 22763456]
[36]
Yvan-Charvet L, Pagler T, Gautier EL, et al. ATP-binding cassette transporters and HDL suppress hematopoietic stem cell proliferation. Science 2010; 328(5986): 1689-93.
[http://dx.doi.org/10.1126/science.1189731] [PMID: 20488992]
[37]
de Gaetano M, Crean D, Barry M, Belton O. M1- and M2-Type Macrophage Responses Are Predictive of Adverse Outcomes in Human Atherosclerosis. Front Immunol 2016; 7: 275.
[http://dx.doi.org/10.3389/fimmu.2016.00275] [PMID: 27486460]
[38]
Lee SG, Oh J, Bong SK, et al. Macrophage polarization and acceleration of atherosclerotic plaques in a swine model. PLoS One 2018; 13(3): e0193005.
[http://dx.doi.org/10.1371/journal.pone.0193005] [PMID: 29561847]
[39]
Khallou-Laschet J, Varthaman A, Fornasa G, et al. Macrophage plasticity in experimental atherosclerosis. PLoS One 2010; 5(1): e8852.
[http://dx.doi.org/10.1371/journal.pone.0008852] [PMID: 20111605]
[40]
Cochain C, Vafadarnejad E, Arampatzi P, et al. Single-Cell RNA-Seq Reveals the Transcriptional Landscape and Heterogeneity of Aortic Macrophages in Murine Atherosclerosis. Circ Res 2018; 122(12): 1661-74.
[http://dx.doi.org/10.1161/CIRCRESAHA.117.312509] [PMID: 29545365]
[41]
Stöger JL, Gijbels MJ, van der Velden S, et al. Distribution of macrophage polarization markers in human atherosclerosis. Atherosclerosis 2012; 225(2): 461-8.
[http://dx.doi.org/10.1016/j.atherosclerosis.2012.09.013] [PMID: 23078881]
[42]
Greaves DR, Gordon S. The macrophage scavenger receptor at 30 years of age: current knowledge and future challenges. J Lipid Res 2009; 50(Suppl.): S282-6.
[http://dx.doi.org/10.1194/jlr.R800066-JLR200] [PMID: 19074372]
[43]
Tall AR, Yvan-Charvet L. Cholesterol, inflammation and innate immunity. Nat Rev Immunol 2015; 15(2): 104-16.
[http://dx.doi.org/10.1038/nri3793] [PMID: 25614320]
[44]
Robbins CS, Hilgendorf I, Weber GF, et al. Local proliferation dominates lesional macrophage accumulation in atherosclerosis. Nat Med 2013; 19(9): 1166-72.
[http://dx.doi.org/10.1038/nm.3258] [PMID: 23933982]
[45]
Moore KJ, Tabas I. Macrophages in the pathogenesis of atherosclerosis. Cell 2011; 145(3): 341-55.
[http://dx.doi.org/10.1016/j.cell.2011.04.005] [PMID: 21529710]
[46]
Subramanian M, Tabas I. Dendritic cells in atherosclerosis. Semin Immunopathol 2014; 36(1): 93-102.
[http://dx.doi.org/10.1007/s00281-013-0400-x] [PMID: 24196454]
[47]
Gil-Pulido J, Zernecke A. Antigen-presenting dendritic cells in atherosclerosis. Eur J Pharmacol 2017; 816: 25-31.
[http://dx.doi.org/10.1016/j.ejphar.2017.08.016] [PMID: 28822856]
[48]
Musilli C, Paccosi S, Pala L, et al. Characterization of circulating and monocyte-derived dendritic cells in obese and diabetic patients. Mol Immunol 2011; 49(1-2): 234-8.
[http://dx.doi.org/10.1016/j.molimm.2011.08.019] [PMID: 21940050]
[49]
Paccosi S, Musilli C, Caporale R, et al. Stimulatory interactions between human coronary smooth muscle cells and dendritic cells. PLoS One 2014; 9(6): e99652.
[http://dx.doi.org/10.1371/journal.pone.0099652] [PMID: 24932497]
[50]
Alderman CJ, Bunyard PR, Chain BM, Foreman JC, Leake DS, Katz DR. Effects of oxidised low density lipoprotein on dendritic cells: a possible immunoregulatory component of the atherogenic micro-environment? Cardiovasc Res 2002; 55(4): 806-19.
[http://dx.doi.org/10.1016/S0008-6363(02)00447-9] [PMID: 12176130]
[51]
Perrin-Cocon L, Coutant F, Agaugué S, Deforges S, André P, Lotteau V. Oxidized low-density lipoprotein promotes mature dendritic cell transition from differentiating monocyte. J Immunol 2001; 167(7): 3785-91.
[http://dx.doi.org/10.4049/jimmunol.167.7.3785] [PMID: 11564795]
[52]
Gautier EL, Huby T, Saint-Charles F, et al. Conventional dendritic cells at the crossroads between immunity and cholesterol homeostasis in atherosclerosis. Circulation 2009; 119(17): 2367-75.
[http://dx.doi.org/10.1161/CIRCULATIONAHA.108.807537] [PMID: 19380622]
[53]
Hjerpe C, Johansson D, Hermansson A, Hansson GK, Zhou X. Dendritic cells pulsed with malondialdehyde modified low density lipoprotein aggravate atherosclerosis in Apoe(-/-) mice. Atherosclerosis 2010; 209(2): 436-41.
[http://dx.doi.org/10.1016/j.atherosclerosis.2009.10.003] [PMID: 19897195]
[54]
Hermansson A, Johansson DK, Ketelhuth DF, Andersson J, Zhou X, Hansson GK. Immunotherapy with tolerogenic apolipoprotein B-100-loaded dendritic cells attenuates atherosclerosis in hypercholesterolemic mice. Circulation 2011; 123(10): 1083-91.
[http://dx.doi.org/10.1161/CIRCULATIONAHA.110.973222] [PMID: 21357823]
[55]
Andersson J, Libby P, Hansson GK. Adaptive immunity and atherosclerosis. Clin Immunol 2010; 134(1): 33-46.
[http://dx.doi.org/10.1016/j.clim.2009.07.002] [PMID: 19635683]
[56]
Reardon CA, Blachowicz L, White T, et al. Effect of immune deficiency on lipoproteins and atherosclerosis in male apolipoprotein E-deficient mice. Arterioscler Thromb Vasc Biol 2001; 21(6): 1011-6.
[http://dx.doi.org/10.1161/01.ATV.21.6.1011] [PMID: 11397712]
[57]
Zhou X, Nicoletti A, Elhage R, Hansson GK. Transfer of CD4(+) T cells aggravates atherosclerosis in immunodeficient apolipoprotein E knockout mice. Circulation 2000; 102(24): 2919-22.
[http://dx.doi.org/10.1161/01.CIR.102.24.2919] [PMID: 11113040]
[58]
Caligiuri G, Nicoletti A, Poirier B, Hansson GK. Protective immunity against atherosclerosis carried by B cells of hypercholesterolemic mice. J Clin Invest 2002; 109(6): 745-53.
[http://dx.doi.org/10.1172/JCI7272] [PMID: 11901183]
[59]
Tse K, Tse H, Sidney J, Sette A, Ley K. T cells in atherosclerosis. Int Immunol 2013; 25(11): 615-22.
[http://dx.doi.org/10.1093/intimm/dxt043] [PMID: 24154816]
[60]
Corthay A. How do regulatory T cells work? Scand J Immunol 2009; 70(4): 326-36.
[http://dx.doi.org/10.1111/j.1365-3083.2009.02308.x] [PMID: 19751267]
[61]
Josefowicz SZ, Lu LF, Rudensky AY. Regulatory T cells: mechanisms of differentiation and function. Annu Rev Immunol 2012; 30: 531-64.
[http://dx.doi.org/10.1146/annurev.immunol.25.022106.141623] [PMID: 22224781]
[62]
Zhou X, Paulsson G, Stemme S, Hansson GK. Hypercholesterolemia is associated with a T helper (Th) 1/Th2 switch of the autoimmune response in atherosclerotic apo E-knockout mice. J Clin Invest 1998; 101(8): 1717-25.
[http://dx.doi.org/10.1172/JCI1216] [PMID: 9541503]
[63]
Formanowicz D, Gutowska K, Formanowicz P. Theoretical Studies on the Engagement of Interleukin 18 in the Immuno-Inflammatory Processes Underlying Atherosclerosis. Int J Mol Sci 2018; 19(11): E3476.
[http://dx.doi.org/10.3390/ijms19113476] [PMID: 30400655]
[64]
Frostegård J, Ulfgren AK, Nyberg P, et al. Cytokine expression in advanced human atherosclerotic plaques: dominance of pro-inflammatory (Th1) and macrophage-stimulating cytokines. Atherosclerosis 1999; 145(1): 33-43.
[http://dx.doi.org/10.1016/S0021-9150(99)00011-8] [PMID: 10428293]
[65]
van Duijn J, Kritikou E, Benne N, et al. CD8+ T-cells contribute to lesion stabilization in advanced atherosclerosis by limiting macrophage content and CD4+ T-cell responses. Cardiovasc Res 2019; 115(4): 729-38.
[http://dx.doi.org/10.1093/cvr/cvy261] [PMID: 30335148]
[66]
Stemme S, Faber B, Holm J, Wiklund O, Witztum JL, Hansson GK. T lymphocytes from human atherosclerotic plaques recognize oxidized low density lipoprotein. Proc Natl Acad Sci USA 1995; 92(9): 3893-7.
[http://dx.doi.org/10.1073/pnas.92.9.3893] [PMID: 7732003]
[67]
Xu Q, Kleindienst R, Waitz W, Dietrich H, Wick G. Increased expression of heat shock protein 65 coincides with a population of infiltrating T lymphocytes in atherosclerotic lesions of rabbits specifically responding to heat shock protein 65. J Clin Invest 1993; 91(6): 2693-702.
[http://dx.doi.org/10.1172/JCI116508] [PMID: 8514876]
[68]
Tedgui A, Mallat Z. Cytokines in atherosclerosis: pathogenic and regulatory pathways. Physiol Rev 2006; 86(2): 515-81.
[http://dx.doi.org/10.1152/physrev.00024.2005] [PMID: 16601268]
[69]
Ponnuswamy P, Van Vré EA, Mallat Z, Tedgui A. Humoral and cellular immune responses in atherosclerosis: spotlight on B- and T-cells. Vascul Pharmacol 2012; 56(5-6): 193-203.
[http://dx.doi.org/10.1016/j.vph.2012.01.009] [PMID: 22329947]
[70]
Engelbertsen D, Rattik S, Knutsson A, Björkbacka H, Bengtsson E, Nilsson J. Induction of T helper 2 responses against human apolipoprotein B100 does not affect atherosclerosis in ApoE-/- mice. Cardiovasc Res 2014; 103(2): 304-12.
[http://dx.doi.org/10.1093/cvr/cvu131] [PMID: 24866382]
[71]
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(3): 427-37.
[http://dx.doi.org/10.1172/JCI200420479] [PMID: 15286809]
[72]
Ketelhuth DF, Hansson GK. Adaptive Response of T and B Cells in Atherosclerosis. Circ Res 2016; 118(4): 668-78.
[http://dx.doi.org/10.1161/CIRCRESAHA.115.306427] [PMID: 26892965]
[73]
Wang J, Cheng X, Xiang MX, et al. IgE stimulates human and mouse arterial cell apoptosis and cytokine expression and promotes atherogenesis in Apoe-/- mice. J Clin Invest 2011; 121(9): 3564-77.
[http://dx.doi.org/10.1172/JCI46028] [PMID: 21821913]
[74]
Tsiantoulas D, Sage AP, Mallat Z, Binder CJ. Targeting B cells in atherosclerosis: closing the gap from bench to bedside. Arterioscler Thromb Vasc Biol 2015; 35(2): 296-302.
[http://dx.doi.org/10.1161/ATVBAHA.114.303569] [PMID: 25359862]
[75]
Cardilo-Reis L, Gruber S, Schreier SM, et al. Interleukin-13 protects from atherosclerosis and modulates plaque composition by skewing the macrophage phenotype. EMBO Mol Med 2012; 4(10): 1072-86.
[http://dx.doi.org/10.1002/emmm.201201374] [PMID: 23027612]
[76]
Taleb S, Tedgui A, Mallat Z. Interleukin-17: friend or foe in atherosclerosis? Curr Opin Lipidol 2010; 21(5): 404-8.
[http://dx.doi.org/10.1097/MOL.0b013e32833dc7f9] [PMID: 20683328]
[77]
Arican O, Aral M, Sasmaz S, Ciragil P. Serum levels of TNF-alpha, IFN-gamma, IL-6, IL-8, IL-12, IL-17, and IL-18 in patients with active psoriasis and correlation with disease severity. Mediators Inflamm 2005; 2005(5): 273-9.
[http://dx.doi.org/10.1155/MI.2005.273] [PMID: 16258194]
[78]
Cătană CS, Berindan Neagoe I, Cozma V, Magdaş C, Tăbăran F, Dumitraşcu DL. Contribution of the IL-17/IL-23 axis to the pathogenesis of inflammatory bowel disease. World J Gastroenterol 2015; 21(19): 5823-30.
[http://dx.doi.org/10.3748/wjg.v21.i19.5823] [PMID: 26019446]
[79]
Kirkham BW, Kavanaugh A, Reich K. Interleukin-17A: a unique pathway in immune-mediated diseases: psoriasis, psoriatic arthritis and rheumatoid arthritis. Immunology 2014; 141(2): 133-42.
[http://dx.doi.org/10.1111/imm.12142] [PMID: 23819583]
[80]
Grän F, Kerstan A, Serfling E, Goebeler M, Muhammad K. Current Developments in the Immunology of Psoriasis. Yale J Biol Med 2020; 93(1): 97-110.
[PMID: 32226340]
[81]
Liuzzo G, Trotta F, Pedicino D. Interleukin-17 in atherosclerosis and cardiovascular disease: the good, the bad, and the unknown. Eur Heart J 2013; 34(8): 556-9.
[http://dx.doi.org/10.1093/eurheartj/ehs399] [PMID: 23178645]
[82]
Lim H, Kim YU, Sun H, et al. Proatherogenic conditions promote autoimmune T helper 17 cell responses in vivo. Immunity 2014; 40(1): 153-65.
[http://dx.doi.org/10.1016/j.immuni.2013.11.021] [PMID: 24412615]
[83]
Smith E, Prasad KM, Butcher M, et al. Blockade of interleukin-17A results in reduced atherosclerosis in apolipoprotein E-deficient mice. Circulation 2010; 121(15): 1746-55.
[http://dx.doi.org/10.1161/CIRCULATIONAHA.109.924886] [PMID: 20368519]
[84]
Erbel C, Chen L, Bea F, et al. Inhibition of IL-17A attenuates atherosclerotic lesion development in apoE-deficient mice. J Immunol 2009; 183(12): 8167-75.
[http://dx.doi.org/10.4049/jimmunol.0901126] [PMID: 20007582]
[85]
Butcher MJ, Gjurich BN, Phillips T, Galkina EV. The IL-17A/IL-17RA axis plays a proatherogenic role via the regulation of aortic myeloid cell recruitment. Circ Res 2012; 110(5): 675-87.
[http://dx.doi.org/10.1161/CIRCRESAHA.111.261784] [PMID: 22302786]
[86]
Madhur MS, Funt SA, Li L, et al. Role of interleukin 17 in inflammation, atherosclerosis, and vascular function in apolipoprotein e-deficient mice. Arterioscler Thromb Vasc Biol 2011; 31(7): 1565-72.
[http://dx.doi.org/10.1161/ATVBAHA.111.227629] [PMID: 21474820]
[87]
Gisterå A, Robertson AK, Andersson J, et al. Transforming growth factor-β signaling in T cells promotes stabilization of atherosclerotic plaques through an interleukin-17-dependent pathway. Sci Transl Med 2013; 5(196): 196ra100.
[http://dx.doi.org/10.1126/scitranslmed.3006133] [PMID: 23903754]
[88]
Cheng X, Yu X, Ding YJ, et al. The Th17/Treg imbalance in patients with acute coronary syndrome. Clin Immunol 2008; 127(1): 89-97.
[http://dx.doi.org/10.1016/j.clim.2008.01.009] [PMID: 18294918]
[89]
Simon T, Taleb S, Danchin N, et al. Circulating levels of interleukin-17 and cardiovascular outcomes in patients with acute myocardial infarction. Eur Heart J 2013; 34(8): 570-7.
[http://dx.doi.org/10.1093/eurheartj/ehs263] [PMID: 22956509]
[90]
de Boer OJ, van der Meer JJ, Teeling P, van der Loos CM, van der Wal AC. Low numbers of FOXP3 positive regulatory T cells are present in all developmental stages of human atherosclerotic lesions. PLoS One 2007; 2(8): e779.
[http://dx.doi.org/10.1371/journal.pone.0000779] [PMID: 17712427]
[91]
Mor A, Luboshits G, Planer D, Keren G, George J. Altered status of CD4(+)CD25(+) regulatory T cells in patients with acute coronary syndromes. Eur Heart J 2006; 27(21): 2530-7.
[http://dx.doi.org/10.1093/eurheartj/ehl222] [PMID: 16954132]
[92]
Wigren M, Björkbacka H, Andersson L, et al. Low levels of circulating CD4+FoxP3+ T cells are associated with an increased risk for development of myocardial infarction but not for stroke. Arterioscler Thromb Vasc Biol 2012; 32(8): 2000-4.
[http://dx.doi.org/10.1161/ATVBAHA.112.251579] [PMID: 22628434]
[93]
Mor A, Planer D, Luboshits G, et al. Role of naturally occurring CD4+ CD25+ regulatory T cells in experimental atherosclerosis. Arterioscler Thromb Vasc Biol 2007; 27(4): 893-900.
[http://dx.doi.org/10.1161/01.ATV.0000259365.31469.89] [PMID: 17272749]
[94]
Kita T, Yamashita T, Sasaki N, et al. Regression of atherosclerosis with anti-CD3 antibody via augmenting a regulatory T-cell response in mice. Cardiovasc Res 2014; 102(1): 107-17.
[http://dx.doi.org/10.1093/cvr/cvu002] [PMID: 24403315]
[95]
Mallat Z, Besnard S, Duriez M, et al. Protective role of interleukin-10 in atherosclerosis. Circ Res 1999; 85(8): e17-24.
[http://dx.doi.org/10.1161/01.RES.85.8.e17] [PMID: 10521249]
[96]
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(1-2): 10-7.
[http://dx.doi.org/10.1007/BF03402102] [PMID: 12765335]
[97]
Pinderski Oslund LJ, Hedrick CC, Olvera T, et al. Interleukin-10 blocks atherosclerotic events in vitro and in vivo. Arterioscler Thromb Vasc Biol 1999; 19(12): 2847-53.
[http://dx.doi.org/10.1161/01.ATV.19.12.2847] [PMID: 10591660]
[98]
Foks AC, Frodermann V, ter Borg M, et al. Differential effects of regulatory T cells on the initiation and regression of atherosclerosis. Atherosclerosis 2011; 218(1): 53-60.
[http://dx.doi.org/10.1016/j.atherosclerosis.2011.04.029] [PMID: 21621777]
[99]
Klingenberg R, Gerdes N, Badeau RM, et al. Depletion of FOXP3+ regulatory T cells promotes hypercholesterolemia and atherosclerosis. J Clin Invest 2013; 123(3): 1323-34.
[http://dx.doi.org/10.1172/JCI63891] [PMID: 23426179]
[100]
Von Der Thüsen JH, Kuiper J, Fekkes ML, De Vos P, Van Berkel TJ, Biessen EA. Attenuation of atherogenesis by systemic and local adenovirus-mediated gene transfer of interleukin-10 in LDLr-/- mice. FASEB J 2001; 15(14): 2730-2.
[PMID: 11687507]
[101]
Reifenberg K, Cheng F, Orning C, et al. Overexpression of TGF-ß1 in macrophages reduces and stabilizes atherosclerotic plaques in ApoE-deficient mice. PLoS One 2012; 7(7): e40990.
[http://dx.doi.org/10.1371/journal.pone.0040990] [PMID: 22829904]
[102]
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(10): 930-4.
[http://dx.doi.org/10.1161/hh2201.099415] [PMID: 11701621]
[103]
Robertson AK, Rudling M, Zhou X, Gorelik L, Flavell RA, Hansson GK. Disruption of TGF-beta signaling in T cells accelerates atherosclerosis. J Clin Invest 2003; 112(9): 1342-50.
[http://dx.doi.org/10.1172/JCI18607] [PMID: 14568988]
[104]
Klein-Hessling S, Muhammad K, Klein M, et al. NFATc1 controls the cytotoxicity of CD8+ T cells. Nat Commun 2017; 8(1): 511.
[http://dx.doi.org/10.1038/s41467-017-00612-6] [PMID: 28894104]
[105]
van Duijn J, Kuiper J, Slütter B. The many faces of CD8+ T cells in atherosclerosis. Curr Opin Lipidol 2018; 29(5): 411-6.
[http://dx.doi.org/10.1097/MOL.0000000000000541] [PMID: 30020198]
[106]
Ammirati E, Moroni F, Magnoni M, Camici PG. The role of T and B cells in human atherosclerosis and atherothrombosis. Clin Exp Immunol 2015; 179(2): 173-87.
[http://dx.doi.org/10.1111/cei.12477] [PMID: 25352024]
[107]
Lichtman AH, Binder CJ, Tsimikas S, Witztum JL. Adaptive immunity in atherogenesis: new insights and therapeutic approaches. J Clin Invest 2013; 123(1): 27-36.
[http://dx.doi.org/10.1172/JCI63108] [PMID: 23281407]
[108]
Kolbus D, Ramos OH, Berg KE, et al. CD8+ T cell activation predominate early immune responses to hypercholesterolemia in Apoe-(/)- mice. BMC Immunol 2010; 11: 58.
[http://dx.doi.org/10.1186/1471-2172-11-58] [PMID: 21126329]
[109]
Cochain C, Koch M, Chaudhari SM, et al. CD8+ T Cells Regulate Monopoiesis and Circulating Ly6C-high Monocyte Levels in Atherosclerosis in Mice. Circ Res 2015; 117(3): 244-53.
[http://dx.doi.org/10.1161/CIRCRESAHA.117.304611] [PMID: 25991812]
[110]
Chyu KY, Zhao X, Dimayuga PC, et al. CD8+ T cells mediate the athero-protective effect of immunization with an ApoB-100 peptide. PLoS One 2012; 7(2): e30780.
[http://dx.doi.org/10.1371/journal.pone.0030780] [PMID: 22347402]
[111]
Dimayuga PC, Zhao X, Yano J, et al. Identification of apoB-100 Peptide-Specific CD8+ T Cells in Atherosclerosis. J Am Heart Assoc 2017; 6(7): e005318.
[http://dx.doi.org/10.1161/JAHA.116.005318] [PMID: 28711866]
[112]
Dimayuga PC, Chyu KY, Kirzner J, et al. Enhanced neointima formation following arterial injury in immune deficient Rag-1-/- mice is attenuated by adoptive transfer of CD8 T cells. PLoS One 2011; 6(5): e20214.
[http://dx.doi.org/10.1371/journal.pone.0020214] [PMID: 21629656]
[113]
Sage AP, Tsiantoulas D, Binder CJ, Mallat Z. The role of B cells in atherosclerosis. Nat Rev Cardiol 2019; 16(3): 180-96.
[http://dx.doi.org/10.1038/s41569-018-0106-9] [PMID: 30410107]
[114]
Edwards JC, Leandro MJ, Cambridge G. B-lymphocyte depletion therapy in rheumatoid arthritis and other autoimmune disorders. Biochem Soc Trans 2002; 30(4): 824-8.
[http://dx.doi.org/10.1042/bst0300824] [PMID: 12196207]
[115]
Leandro MJ, Edwards JC, Cambridge G, Ehrenstein MR, Isenberg DA. An open study of B lymphocyte depletion in systemic lupus erythematosus. Arthritis Rheum 2002; 46(10): 2673-7.
[http://dx.doi.org/10.1002/art.10541] [PMID: 12384926]
[116]
Muhammad K, Roll P, Einsele H, Dörner T, Tony HP. Delayed acquisition of somatic hypermutations in repopulated IGD+CD27+ memory B cell receptors after rituximab treatment. Arthritis Rheum 2009; 60(8): 2284-93.
[http://dx.doi.org/10.1002/art.24722] [PMID: 19644860]
[117]
Ylä-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.
[http://dx.doi.org/10.1161/01.ATV.14.1.32] [PMID: 7506053]
[118]
Aubry MC, Riehle DL, Edwards WD, et al. B-Lymphocytes in plaque and adventitia of coronary arteries in two patients with rheumatoid arthritis and coronary atherosclerosis: preliminary observations. Cardiovasc Pathol 2004; 13(4): 233-6.
[http://dx.doi.org/10.1016/j.carpath.2004.02.005] [PMID: 15210141]
[119]
Munro JM, van der Walt JD, Munro CS, Chalmers JA, Cox EL. An immunohistochemical analysis of human aortic fatty streaks. Hum Pathol 1987; 18(4): 375-80.
[http://dx.doi.org/10.1016/S0046-8177(87)80168-5] [PMID: 3549534]
[120]
Zhou X, Hansson GK. Detection of B cells and proinflammatory cytokines in atherosclerotic plaques of hypercholesterolaemic apolipoprotein E knockout mice. Scand J Immunol 1999; 50(1): 25-30.
[http://dx.doi.org/10.1046/j.1365-3083.1999.00559.x] [PMID: 10404048]
[121]
Doran AC, Lipinski MJ, Oldham SN, et al. B-cell aortic homing and atheroprotection depend on Id3. Circ Res 2012; 110(1): e1-e12.
[http://dx.doi.org/10.1161/CIRCRESAHA.111.256438] [PMID: 22034493]
[122]
Robinette CD, Fraumeni JF Jr. Splenectomy and subsequent mortality in veterans of the 1939-45 war. Lancet 1977; 2(8029): 127-9.
[http://dx.doi.org/10.1016/S0140-6736(77)90132-5] [PMID: 69206]
[123]
Huan T, Zhang B, Wang Z, et al. Coronary ARteryDIsease Genome wide Replication and Meta-analysis (CARDIoGRAM) Consortium, International Consortium for Blood Pressure GWAS (ICBP). A systems biology framework identifies molecular underpinnings of coronary heart disease. Arterioscler Thromb Vasc Biol 2013; 33(6): 1427-34.
[http://dx.doi.org/10.1161/ATVBAHA.112.300112] [PMID: 23539213]
[124]
Meeuwsen JAL, van Duijvenvoorde A, Gohar A, et al. High Levels of (Un)Switched Memory B Cells Are Associated With Better Outcome in Patients With Advanced Atherosclerotic Disease. J Am Heart Assoc 2017; 6(9): e005747.
[http://dx.doi.org/10.1161/JAHA.117.005747] [PMID: 28882820]
[125]
Mantani PT, Ljungcrantz I, Andersson L, et al. Circulating CD40+ and CD86+ B cell subsets demonstrate opposing associations with risk of stroke. Arterioscler Thromb Vasc Biol 2014; 34(1): 211-8.
[http://dx.doi.org/10.1161/ATVBAHA.113.302667] [PMID: 24202305]
[126]
Wolf D, Ley K. Immunity and Inflammation in Atherosclerosis. Circ Res 2019; 124(2): 315-27.
[http://dx.doi.org/10.1161/CIRCRESAHA.118.313591] [PMID: 30653442]
[127]
Gillotte-Taylor K, Boullier A, Witztum JL, Steinberg D, Quehenberger O. Scavenger receptor class B type I as a receptor for oxidized low density lipoprotein. J Lipid Res 2001; 42(9): 1474-82.
[PMID: 11518768]
[128]
Hörkkö 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(1): 117-28.
[http://dx.doi.org/10.1172/JCI4533] [PMID: 9884341]
[129]
Foks AC, van Puijvelde GH, Bot I, et al. Interruption of the OX40-OX40 ligand pathway in LDL receptor-deficient mice causes regression of atherosclerosis. J Immunol 2013; 191(9): 4573-80.
[http://dx.doi.org/10.4049/jimmunol.1200708] [PMID: 24068673]
[130]
Ait-Oufella H, Herbin O, Bouaziz JD, et al. B cell depletion reduces the development of atherosclerosis in mice. J Exp Med 2010; 207(8): 1579-87.
[http://dx.doi.org/10.1084/jem.20100155] [PMID: 20603314]
[131]
Fillatreau S, Sweenie CH, McGeachy MJ, Gray D, Anderton SM. B cells regulate autoimmunity by provision of IL-10. Nat Immunol 2002; 3(10): 944-50.
[http://dx.doi.org/10.1038/ni833] [PMID: 12244307]
[132]
Wolf SD, Dittel BN, Hardardottir F, Janeway CA Jr. Experimental autoimmune encephalomyelitis induction in genetically B cell-deficient mice. J Exp Med 1996; 184(6): 2271-8.
[http://dx.doi.org/10.1084/jem.184.6.2271] [PMID: 8976182]
[133]
Yanaba K, Bouaziz JD, Haas KM, Poe JC, Fujimoto M, Tedder TF. A regulatory B cell subset with a unique CD1dhiCD5+ phenotype controls T cell-dependent inflammatory responses. Immunity 2008; 28(5): 639-50.
[http://dx.doi.org/10.1016/j.immuni.2008.03.017] [PMID: 18482568]
[134]
Yanaba K, Yoshizaki A, Asano Y, Kadono T, Tedder TF, Sato S. IL-10-producing regulatory B10 cells inhibit intestinal injury in a mouse model. Am J Pathol 2011; 178(2): 735-43.
[http://dx.doi.org/10.1016/j.ajpath.2010.10.022] [PMID: 21281806]
[135]
Matsushita T, Yanaba K, Bouaziz JD, Fujimoto M, Tedder TF. Regulatory B cells inhibit EAE initiation in mice while other B cells promote disease progression. J Clin Invest 2008; 118(10): 3420-30.
[http://dx.doi.org/10.1172/JCI36030] [PMID: 18802481]
[136]
Alrefai H, Muhammad K, Rudolf R, et al. NFATc1 supports imiquimod-induced skin inflammation by suppressing IL-10 synthesis in B cells. Nat Commun 2016; 7: 11724.
[http://dx.doi.org/10.1038/ncomms11724] [PMID: 27222343]
[137]
Rincón-Arévalo H, Villa-Pulgarín J, Tabares J, et al. Interleukin-10 production and T cell-suppressive capacity in B cell subsets from atherosclerotic apoE -/- mice. Immunol Res 2017; 65(5): 995-1008.
[http://dx.doi.org/10.1007/s12026-017-8939-6] [PMID: 28744806]
[138]
Rincón-Arévalo H, Quintero JC, Fortich F, et al. Low frequency of IL-10+ B cells in patients with atherosclerosis is related with inflammatory condition. Heliyon 2020; 6(3): e03441.
[http://dx.doi.org/10.1016/j.heliyon.2020.e03441] [PMID: 32154409]

Rights & Permissions Print Cite
Article Metrics
25
1
© 2024 Bentham Science Publishers | Privacy Policy