Understanding the role of B cells in atherosclerosis: potential clinical implications

References

• Laslett Lj, Alagona P Jr, Clark Ba 3rd et al. The worldwide environment of cardiovascular disease: prevalence, diagnosis, therapy, and policy issues: a report from the American College of Cardiology. J. Am. Coll. Cardiol. 60(25 Suppl.), S1–S49 (2012).
   PubMed Web of Science ®Google Scholar
• Hansson GK, Hermansson A. The immune system in atherosclerosis. Nat. Immunol. 12(3), 204–212 (2011).
   PubMed Web of Science ®Google Scholar
• Tabas I, Williams KJ, Boren J. Subendothelial lipoprotein retention as the initiating process in atherosclerosis: update and therapeutic implications. Circulation 116(16), 1832–1844 (2007).
   PubMed Web of Science ®Google Scholar
• Wilson PW. Established risk factors and coronary artery disease: the Framingham Study. Am. J. Hypertens. 7(7 Pt 2), S7–S12 (1994).
   PubMed Web of Science ®Google Scholar
• Canto JG, Iskandrian AE. Major risk factors for cardiovascular disease: debunking the “only 50%” myth. JAMA 290(7), 947–949 (2003).
   PubMed Web of Science ®Google Scholar
• Petretta M, Cuocolo A. In search of a marker of vulnerable carotid plaque: is the key in the heart? Atherosclerosis 223(1), 95–97 (2012).
   PubMed Web of Science ®Google Scholar
• Kannel WB. Some lessons in cardiovascular epidemiology from Framingham. Am. J. Cardiol. 37(2), 269–282 (1976).
   PubMed Web of Science ®Google Scholar
• Ambrose JA, Winters SL, Arora RR et al. Angiographic evolution of coronary artery morphology in unstable angina. J. Am. Coll. Cardiol. 7(3), 472–478 (1986).
   PubMed Web of Science ®Google Scholar
• Ambrose JA, Tannenbaum MA, Alexopoulos D et al. Angiographic progression of coronary artery disease and the development of myocardial infarction. J. Am. Coll. Cardiol. 12(1), 56–62 (1988).
   PubMed Web of Science ®Google Scholar
• Little WC, Constantinescu M, Applegate RJ et al. Can coronary angiography predict the site of a subsequent myocardial infarction in patients with mild-to-moderate coronary artery disease? Circulation 78(5 Pt 1), 1157–1166 (1988).
   PubMed Web of Science ®Google Scholar
• Libby P, Lichtman AH, Hansson GK. Immune effector mechanisms implicated in atherosclerosis: from mice to humans. Immunity 38(6), 1092–1104 (2013).
   PubMed Web of Science ®Google Scholar
• Weber C, Zernecke A, Libby P. The multifaceted contributions of leukocyte subsets to atherosclerosis: lessons from mouse models. Nat. Rev. Immunol. 8(10), 802–815 (2008).
   PubMed Web of Science ®Google Scholar
• Lichtman AH, Binder CJ, Tsimikas S, Witztum JL. Adaptive immunity in atherogenesis: new insights and therapeutic approaches. J. Clin. Invest. 123(1), 27–36 (2013).
   PubMed Web of Science ®Google Scholar
• Swirski FK, Nahrendorf M. Leukocyte behavior in atherosclerosis, myocardial infarction, and heart failure. Science 339(6116), 161–166 (2013).
   PubMed Web of Science ®Google Scholar
• Perry HM, Bender TP, Mcnamara CA. B cell subsets in atherosclerosis. Front. Immunol. 3, 373 (2012).
   PubMed Web of Science ®Google Scholar
• Gerlis LM. The significance of adventitial infiltrations in coronary atherosclerosis. Br. Heart J. 18(2), 166–172 (1956).
   PubMedGoogle Scholar
• Houtkamp MA, De Boer OJ, Van Der Loos CM, Van Der Wal AC, Becker AE. Adventitial infiltrates associated with advanced atherosclerotic plaques: structural organization suggests generation of local humoral immune responses. J. Pathol. 193(2), 263–269 (2001).
   PubMed Web of Science ®Google Scholar
• Ramshaw AL, Parums DV. Immunohistochemical characterization of inflammatory cells associated with advanced atherosclerosis. Histopathology 17(6), 543–552 (1990).
   PubMed Web of Science ®Google Scholar
• Zhou X, Hansson GK. Detection of B cells and proinflammatory cytokines in atherosclerotic plaques of hypercholesterolaemic apolipoprotein E knockout mice. Scand. J. Immunol. 50(1), 25–30 (1999).
   PubMed Web of Science ®Google Scholar
• Hamze M, Desmetz C, Berthe ML et al. Characterization of resident B cells of vascular walls in human atherosclerotic patients. J. Immunol. 191(6), 3006–3016 (2013).
   PubMed Web of Science ®Google Scholar
• Grabner R, Lotzer K, Dopping S et al. Lymphotoxin beta receptor signaling promotes tertiary lymphoid organogenesis in the aorta adventitia of aged ApoE-/- mice. J. Exp. Med. 206(1), 233–248 (2009).
   PubMed Web of Science ®Google Scholar
• Moos MP, John N, Grabner 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. 25(11), 2386–2391 (2005).
   PubMed Web of Science ®Google Scholar
• Caligiuri G, Nicoletti A, Poirier B, Hansson GK. Protective immunity against atherosclerosis carried by B cells of hypercholesterolemic mice. J. Clin. Invest. 109(6), 745–753 (2002).
   PubMed Web of Science ®Google Scholar
• Major AS, Fazio S, Linton MF. B-lymphocyte deficiency increases atherosclerosis in LDL receptor-null mice. Arterioscler. Thromb. Vasc. Biol. 22(11), 1892–1898 (2002).
   PubMed Web of Science ®Google Scholar
• Yla-Herttuala S, Palinski W, Butler SW, Picard S, Steinberg D, Witztum JL. Rabbit and human atherosclerotic lesions contain IgG that recognizes epitopes of oxidized LDL. Arterioscler. Thromb. 14(1), 32–40 (1994).
   PubMed Web of Science ®Google Scholar
• Palinski W, Miller E, Witztum JL. Immunization of low density lipoprotein (LDL) receptor-deficient rabbits with homologous malondialdehyde-modified LDL reduces atherogenesis. Proc. Natl Acad. Sci. USA 92(3), 821–825 (1995).
   Google Scholar
• Chang MK, Bergmark C, Laurila A et al. Monoclonal antibodies against oxidized low-density lipoprotein bind to apoptotic cells and inhibit their phagocytosis by elicited macrophages: evidence that oxidation-specific epitopes mediate macrophage recognition. Proc. Natl Acad. Sci. USA 96(11), 6353–6358 (1999).
   Google Scholar
• Lewis MJ, Malik TH, Ehrenstein MR, Boyle JJ, Botto M, Haskard DO. Immunoglobulin M is required for protection against atherosclerosis in low-density lipoprotein receptor-deficient mice. Circulation 120(5), 417–426 (2009).
   PubMed Web of Science ®Google Scholar
• Kyaw T, Tay C, Khan A et al. Conventional B2 B cell depletion ameliorates whereas its adoptive transfer aggravates atherosclerosis. J. Immunol. 185(7), 4410–4419 (2010).
   PubMed Web of Science ®Google Scholar
• Ait-Oufella H, Herbin O, Bouaziz JD et al. B cell depletion reduces the development of atherosclerosis in mice. J. Exp. Med. 207(8), 1579–1587 (2011).
   Web of Science ®Google Scholar
• Kyaw T, Tay C, Hosseini H et al. Depletion of B2 but not B1a B cells in BAFF receptor-deficient ApoE mice attenuates atherosclerosis by potently ameliorating arterial inflammation. PLoS ONE 7(1), e29371 (2012).
   PubMed Web of Science ®Google Scholar
• Sage AP, Tsiantoulas D, Baker L et al. BAFF receptor deficiency reduces the development of atherosclerosis in mice--brief report. Arterioscler. Thromb. Vasc. Biol. 32(7), 1573–1576 (2012).
   PubMed Web of Science ®Google Scholar
• Kyaw T, Tay C, Krishnamurthi S et al. B1a B lymphocytes are atheroprotective by secreting natural IgM that increases IgM deposits and reduces necrotic cores in atherosclerotic lesions. Circ. Res. 109(8), 830–840 (2011).
   PubMed Web of Science ®Google Scholar
• Doran AC, Lipinski MJ, Oldham SN et al. B-cell aortic homing and atheroprotection depend on Id3. Circ. Res. 110(1), e1–e12 (2012).
   Web of Science ®Google Scholar
• Lipinski MJ, Perry HM, Doran AC, Oldham SN, Mcnamara CA. Comment on “Conventional B2 B cell depletion ameliorates whereas its adoptive transfer aggravates atherosclerosis”. J. Immunol. 186(1), 4, author reply 6 (2011).
   PubMed Web of Science ®Google Scholar
• Yoshimoto M, Montecino-Rodriguez E, Ferkowicz MJ et al. Embryonic day 9 yolk sac and intra-embryonic hemogenic endothelium independently generate a B-1 and marginal zone progenitor lacking B-2 potential. Proc. Natl Acad. Sci. USA 108(4), 1468–1473 (2011).
   Google Scholar
• Barber CL, Montecino-Rodriguez E, Dorshkind K. Developmental relationships between B-1 and B-2 progenitors. Cell Cycle 10(22), 3810–3811 (2011).
   PubMed Web of Science ®Google Scholar
• Pennell CA, Mercolino TJ, Grdina TA, Arnold LW, Haughton G, Clarke SH. Biased immunoglobulin variable region gene expression by Ly-1 B cells due to clonal selection. Eur. J. Immunol. 19(7), 1289–1295 (1989).
   PubMed Web of Science ®Google Scholar
• Mercolino TJ, Locke AL, Afshari A et al. Restricted immunoglobulin variable region gene usage by normal Ly-1 (CD5+) B cells that recognize phosphatidyl choline. J. Exp. Med. 169(6), 1869–1877 (1989).
   PubMed Web of Science ®Google Scholar
• Binder CJ. Natural IgM antibodies against oxidation-specific epitopes. J. Clin. Immunol. 30(Suppl. 1), S56–S60 (2010).
   Google Scholar
• Chou MY, Fogelstrand L, Hartvigsen K et al. Oxidation-specific epitopes are dominant targets of innate natural antibodies in mice and humans. J. Clin. Invest. 119(5), 1335–1349 (2009).
   PubMed Web of Science ®Google Scholar
• Binder CJ, Horkko S, Dewan A et al. Pneumococcal vaccination decreases atherosclerotic lesion formation: molecular mimicry between Streptococcus pneumoniae and oxidized LDL. Nat. Med. 9(6), 736–743 (2003).
   PubMed Web of Science ®Google Scholar
• 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. 114(3), 427–437 (2004).
   PubMed Web of Science ®Google Scholar
• Rauch PJ, Chudnovskiy A, Robbins CS et al. Innate response activator B cells protect against microbial sepsis. Science 335(6068), 597–601 (2012).
   PubMed Web of Science ®Google Scholar
• Di Gregoli K, Johnson JL. Role of colony-stimulating factors in atherosclerosis. Curr. Opin. Lipidol. 23(5), 412–421 (2012).
   PubMed Web of Science ®Google Scholar
• Mauri C, Bosma A. Immune regulatory function of B cells. Annu. Rev. Immunol. 30, 221–241 (2012).
   PubMed Web of Science ®Google Scholar
• Dilillo DJ, Matsushita T, Tedder TF. B10 cells and regulatory B cells balance immune responses during inflammation, autoimmunity, and cancer. Ann. NY Acad. Sci. 1183, 38–57 (2010).
   PubMed Web of Science ®Google Scholar
• Vitale G, Mion F, Pucillo C. Regulatory B cells: evidence, developmental origin and population diversity. Mol. Immunol. 48(1–3), 1–8 (2010).
   PubMed Web of Science ®Google Scholar
• Ait-Oufella H, Taleb S, Mallat Z, Tedgui A. Recent advances on the role of cytokines in atherosclerosis. Arterioscler. Thromb. Vasc. Biol. 31(5), 969–979 (2011).
   PubMed Web of Science ®Google Scholar
• Blair PA, Norena LY, Flores-Borja F et al. CD19(+)CD24(hi)CD38(hi) B cells exhibit regulatory capacity in healthy individuals but are functionally impaired in systemic Lupus Erythematosus patients. Immunity 32(1), 129–140 (2010).
   PubMed Web of Science ®Google Scholar
• Correale J, Farez M, Razzitte G. Helminth infections associated with multiple sclerosis induce regulatory B cells. Ann. Neurol. 64(2), 187–199 (2008).
   PubMed Web of Science ®Google Scholar
• Huan T, Zhang B, Wang Z et al. A systems biology framework identifies molecular underpinnings of coronary heart disease. Arterioscler. Thromb. Vasc. Biol. 33(6), 1427–1434 (2013).
   PubMed Web of Science ®Google Scholar
• Tanigawa T, Kitamura A, Yamagishi K et al. Relationships of differential leukocyte and lymphocyte subpopulations with carotid atherosclerosis in elderly men. J. Clin. Immunol. 23(6), 469–476 (2003).
   PubMed Web of Science ®Google Scholar
• Lee J, Kuchen S, Fischer R, Chang S, Lipsky PE. Identification and characterization of a human CD5+ pre-naive B cell population. J. Immunol. 182(7), 4116–4126 (2009).
   PubMed Web of Science ®Google Scholar
• Griffin DO, Holodick NE, Rothstein TL. Human B1 cells in umbilical cord and adult peripheral blood express the novel phenotype CD20+ CD27+ CD43+ CD70. J. Exp. Med. 208(1), 67–80 (2011).
   PubMed Web of Science ®Google Scholar
• Griffin DO, Rothstein TL. Human “orchestrator” CD11b(+) B1 cells spontaneously secrete interleukin-10 and regulate T-cell activity. Mol. Med. 18, 1003–1008 (2012).
   PubMed Web of Science ®Google Scholar
• Descatoire M, Weill JC, Reynaud CA, Weller S. A human equivalent of mouse B-1 cells? J. Exp. Med. 208(13), 2563–2564, author reply 2566–2569 (2011).
   PubMed Web of Science ®Google Scholar
• Reynaud CA, Weill JC. Gene profiling of CD11b(+) and CD11b(-) B1 cell subsets reveals potential cell sorting artifacts. J. Exp. Med. 209(3), 433–434, author reply 434–436 (2012).
   PubMed Web of Science ®Google Scholar
• Perez-Andres M, Grosserichter-Wagener C, Teodosio C, Van Dongen JJ, Orfao A, Van Zelm MC. The nature of circulating CD27+CD43+ B cells. J. Exp. Med. 208(13), 2565–2566, author reply 2566–2569 (2011).
   PubMed Web of Science ®Google Scholar
• Griffin DO, Rothstein TL. Human b1 cell frequency: isolation and analysis of human b1 cells. Front. Immunol. 3, 122 (2012).
   PubMed Web of Science ®Google Scholar
• Baumgarth N. The double life of a B-1 cell: self-reactivity selects for protective effector functions. Nat. Rev. Immunol. 11(1), 34–46 (2011).
   PubMed Web of Science ®Google Scholar
• Covens K, Verbinnen B, Geukens N et al. Characterization of proposed human B-1 cells reveals pre-plasmablast phenotype. Blood 121(26), 5176–5183 (2013).
   PubMed Web of Science ®Google Scholar
• Coller BS. Leukocytosis and ischemic vascular disease morbidity and mortality: is it time to intervene? Arterioscler. Thromb. Vasc. Biol. 25(4), 658–670 (2005).
   PubMed Web of Science ®Google Scholar
• Lipinski MJ, Martin RE, Cowley MJ et al. Effect of statins and white blood cell count on mortality in patients with ischemic left ventricular dysfunction undergoing percutaneous coronary intervention. Clin. Cardiol. 29(1), 36–41 (2006).
   PubMed Web of Science ®Google Scholar
• Asadollahi K, Beeching NJ, Gill GV. Leukocytosis as a predictor for non-infective mortality and morbidity. QJM 103(5), 285–292 (2010).
   PubMed Web of Science ®Google Scholar
• Barron HV, Cannon CP, Murphy SA, Braunwald E, Gibson CM. Association between white blood cell count, epicardial blood flow, myocardial perfusion, and clinical outcomes in the setting of acute myocardial infarction: a thrombolysis in myocardial infarction 10 substudy. Circulation 102(19), 2329–2334 (2000).
   PubMed Web of Science ®Google Scholar
• Arbel Y, Finkelstein A, Halkin A et al. Neutrophil/lymphocyte ratio is related to the severity of coronary artery disease and clinical outcome in patients undergoing angiography. Atherosclerosis 225(2), 456–460 (2012).
   PubMed Web of Science ®Google Scholar
• Sbrana F, Cocci F, Papa A et al. Routine laboratory tests to risk-stratify patients with chronic coronary artery disease. J. Cardiol. 61(2), 132–137 (2013).
   PubMed Web of Science ®Google Scholar
• Tsimikas S, Brilakis ES, Lennon RJ et al. Relationship of IgG and IgM autoantibodies to oxidized low density lipoprotein with coronary artery disease and cardiovascular events. J. Lipid Res. 48(2), 425–433 (2007).
   PubMed Web of Science ®Google Scholar
• Muscari A, Bozzoli C, Gerratana C et al. Association of serum IgA and C4 with severe atherosclerosis. Atherosclerosis 74(1–2), 179–186 (1988).
   PubMed Web of Science ®Google Scholar
• Choi SH, Chae A, Miller E et al. Relationship between biomarkers of oxidized low-density lipoprotein, statin therapy, quantitative coronary angiography, and atheroma: volume observations from the REVERSAL (Reversal of Atherosclerosis with Aggressive Lipid Lowering) study. J. Am. Coll. Cardiol. 52(1), 24–32 (2008).
   PubMed Web of Science ®Google Scholar
• Fraley AE, Schwartz GG, Olsson AG et al. Relationship of oxidized phospholipids and biomarkers of oxidized low-density lipoprotein with cardiovascular risk factors, inflammatory biomarkers, and effect of statin therapy in patients with acute coronary syndromes: results from the MIRACL (Myocardial Ischemia Reduction With Aggressive Cholesterol Lowering) trial. J. Am. Coll. Cardiol. 53(23), 2186–2196 (2009).
   PubMed Web of Science ®Google Scholar
• Bjorkbacka H, Fredrikson GN, Nilsson J. Emerging biomarkers and intervention targets for immune-modulation of atherosclerosis – a review of the experimental evidence. Atherosclerosis 227(1), 9–17 (2013).
   PubMed Web of Science ®Google Scholar
• Galkina E, Kadl A, Sanders J, Varughese D, Sarembock IJ, Ley K. Lymphocyte recruitment into the aortic wall before and during development of atherosclerosis is partially L-selectin dependent. J. Exp. Med. 203(5), 1273–1282 (2006).
   PubMed Web of Science ®Google Scholar
• Campbell KA, Lipinski MJ, Doran AC, Skaflen MD, Fuster V, Mcnamara CA. Lymphocytes and the adventitial immune response in atherosclerosis. Circ. Res. 110(6), 889–900 (2012).
   PubMed Web of Science ®Google Scholar
• Sampi M, Ukkola O, Paivansalo M, Kesaniemi YA, Binder CJ, Horkko S. Plasma interleukin-5 levels are related to antibodies binding to oxidized low-density lipoprotein and to decreased subclinical atherosclerosis. J. Am. Coll. Cardiol. 52(17), 1370–1378 (2008).
   PubMed Web of Science ®Google Scholar
• Hollan I, Meroni PL, Ahearn JM et al. Cardiovascular disease in autoimmune rheumatic diseases. Autoimmun. Rev. 12(10), 1004–1015 (2013).
   PubMed Web of Science ®Google Scholar
• Zinger H, Sherer Y, Shoenfeld Y. Atherosclerosis in autoimmune rheumatic diseases-mechanisms and clinical findings. Clin. Rev. Allergy Immunol. 37(1), 20–28 (2009).
   PubMed Web of Science ®Google Scholar
• Aubry MC, Maradit-Kremers H, Reinalda MS, Crowson CS, Edwards WD, Gabriel SE. Differences in atherosclerotic coronary heart disease between subjects with and without rheumatoid arthritis. J. Rheumatol. 34(5), 937–942 (2007).
   PubMed Web of Science ®Google Scholar
• Moura RA, Graca L, Fonseca JE. To B or not to B the conductor of rheumatoid arthritis orchestra. Clin. Rev. Allergy Immunol. 43(3), 281–291 (2012).
   PubMed Web of Science ®Google Scholar
• O'neill SK, Shlomchik MJ, Glant TT, Cao Y, Doodes PD, Finnegan A. Antigen-specific B cells are required as APCs and autoantibody-producing cells for induction of severe autoimmune arthritis. J. Immunol. 174(6), 3781–3788 (2005).
   PubMed Web of Science ®Google Scholar
• Furst DE, Breedveld FC, Kalden JR et al. Updated consensus statement on biological agents for the treatment of rheumatic diseases, 2007. Ann. Rheum. Dis. 66(Suppl. 3), iii2–iii22 (2007).
   PubMed Web of Science ®Google Scholar
• Teng YK, Wheater G, Hogan VE et al. Induction of long-term B-cell depletion in refractory rheumatoid arthritis patients preferentially affects autoreactive more than protective humoral immunity. Arthritis Res. Ther. 14(2), R57 (2012).
   Web of Science ®Google Scholar
• Benucci M, Saviola G, Manfredi M, Sarzi-Puttini P, Atzeni F. Factors correlated with improvement of endothelial dysfunction during rituximab therapy in patients with rheumatoid arthritis. Biologics 7, 69–75 (2013).
   PubMedGoogle Scholar
• Kerekes G, Soltesz P, Der H et al. Effects of rituximab treatment on endothelial dysfunction, carotid atherosclerosis, and lipid profile in rheumatoid arthritis. Clin. Rheumatol. 28(6), 705–710 (2009).
   PubMed Web of Science ®Google Scholar
• Raterman HG, Levels H, Voskuyl AE, Lems WF, Dijkmans BA, Nurmohamed MT. HDL protein composition alters from proatherogenic into less atherogenic and proinflammatory in rheumatoid arthritis patients responding to rituximab. Ann. Rheum. Dis. 72(4), 560–565 (2013).
   PubMed Web of Science ®Google Scholar
• Mathieu S, Pereira B, Dubost JJ, Lusson JR, Soubrier M. No significant change in arterial stiffness in RA after 6 months and 1 year of rituximab treatment. Rheumatology (Oxford) 51(6), 1107–1111 (2012).
   PubMed Web of Science ®Google Scholar
• Cohen SB, Emery P, Greenwald MW et al. Rituximab for rheumatoid arthritis refractory to anti-tumor necrosis factor therapy: Results of a multicenter, randomized, double-blind, placebo-controlled, phase III trial evaluating primary efficacy and safety at twenty-four weeks. Arthritis Rheum. 54(9), 2793–2806 (2006).
   PubMed Web of Science ®Google Scholar
• Edwards JC, Szczepanski L, Szechinski J et al. Efficacy of B-cell-targeted therapy with rituximab in patients with rheumatoid arthritis. N. Engl. J. Med. 350(25), 2572–2581 (2004).
   PubMed Web of Science ®Google Scholar
• Emery P, Fleischmann R, Filipowicz-Sosnowska A et al. The efficacy and safety of rituximab in patients with active rheumatoid arthritis despite methotrexate treatment: results of a phase IIB randomized, double-blind, placebo-controlled, dose-ranging trial. Arthritis Rheum. 54(5), 1390–1400 (2006).
   PubMed Web of Science ®Google Scholar
• Emery P, Deodhar A, Rigby WF et al. Efficacy and safety of different doses and retreatment of rituximab: a randomised, placebo-controlled trial in patients who are biological naive with active rheumatoid arthritis and an inadequate response to methotrexate (Study Evaluating Rituximab's Efficacy in MTX iNadequate rEsponders (SERENE)). Ann. Rheum. Dis. 69(9), 1629–1635 (2010).
   PubMed Web of Science ®Google Scholar
• Greenwald MW, Shergy WJ, Kaine JL, Sweetser MT, Gilder K, Linnik MD. Evaluation of the safety of rituximab in combination with a tumor necrosis factor inhibitor and methotrexate in patients with active rheumatoid arthritis: results from a randomized controlled trial. Arthritis Rheum. 63(3), 622–632 (2011).
   PubMed Web of Science ®Google Scholar
• Tak PP, Rigby WF, Rubbert-Roth A et al. Inhibition of joint damage and improved clinical outcomes with rituximab plus methotrexate in early active rheumatoid arthritis: the IMAGE trial. Ann. Rheum. Dis. 70(1), 39–46 (2011).
   PubMed Web of Science ®Google Scholar
• Davatchi F, Shams H, Rezaipoor M et al. Rituximab in intractable ocular lesions of Behcet's disease; randomized single-blind control study (pilot study). Int. J. Rheum. Dis. 13(3), 246–252 (2010).
   PubMed Web of Science ®Google Scholar
• De Vita S, Quartuccio L, Isola M et al. A randomized controlled trial of rituximab for the treatment of severe cryoglobulinemic vasculitis. Arthritis Rheum. 64(3), 843–853 (2012).
   PubMed Web of Science ®Google Scholar
• Jones RB, Tervaert JW, Hauser T et al. Rituximab versus cyclophosphamide in ANCA-associated renal vasculitis. N. Engl. J. Med. 363(3), 211–220 (2010).
   PubMed Web of Science ®Google Scholar
• Sneller MC, Hu Z, Langford CA. A randomized controlled trial of rituximab following failure of antiviral therapy for hepatitis C virus-associated cryoglobulinemic vasculitis. Arthritis Rheum. 64(3), 835–842 (2012).
   PubMed Web of Science ®Google Scholar
• Stone JH, Merkel PA, Spiera R et al. Rituximab versus cyclophosphamide for ANCA-associated vasculitis. N. Engl. J. Med. 363(3), 221–232 (2010).
   PubMed Web of Science ®Google Scholar
• Merrill JT, Neuwelt CM, Wallace DJ et al. Efficacy and safety of rituximab in moderately-to-severely active systemic lupus erythematosus: the randomized, double-blind, phase II/III systemic lupus erythematosus evaluation of rituximab trial. Arthritis Rheum. 62(1), 222–233 (2010).
   PubMed Web of Science ®Google Scholar
• Rovin BH, Furie R, Latinis K et al. Efficacy and safety of rituximab in patients with active proliferative lupus nephritis: the Lupus Nephritis Assessment with Rituximab study. Arthritis Rheum. 64(4), 1215–1226 (2012).
   PubMed Web of Science ®Google Scholar
• Dass S, Bowman SJ, Vital EM et al. Reduction of fatigue in Sjogren syndrome with rituximab: results of a randomised, double-blind, placebo-controlled pilot study. Ann. Rheum. Dis. 67(11), 1541–1544 (2008).
   PubMed Web of Science ®Google Scholar
• Meijer JM, Meiners PM, Vissink A et al. Effectiveness of rituximab treatment in primary Sjogren's syndrome: a randomized, double-blind, placebo-controlled trial. Arthritis Rheum. 62(4), 960–968 (2010).
   PubMed Web of Science ®Google Scholar
• Pescovitz MD, Greenbaum CJ, Krause-Steinrauf H et al. Rituximab, B-lymphocyte depletion, and preservation of beta-cell function. N. Engl. J. Med. 361(22), 2143–2152 (2009).
   PubMed Web of Science ®Google Scholar
• Daoussis D, Liossis SN, Tsamandas AC et al. Experience with rituximab in scleroderma: results from a 1-year, proof-of-principle study. Rheumatology (Oxford) 49(2), 271–280 (2010).
   PubMed Web of Science ®Google Scholar
• Lahoute C, Herbin O, Mallat Z, Tedgui A. Adaptive immunity in atherosclerosis: mechanisms and future therapeutic targets. Nat. Rev. Cardiol. 8(6), 348–358 (2011).
   PubMed Web of Science ®Google Scholar
• Mackay F, Schneider P. Cracking the BAFF code. Nat. Rev. Immunol. 9(7), 491–502 (2009).
   PubMed Web of Science ®Google Scholar
• Carbonatto M, Yu P, Bertolino M et al. Nonclinical safety, pharmacokinetics, and pharmacodynamics of atacicept. Toxicol. Sci. 105(1), 200–210 (2008).
   PubMed Web of Science ®Google Scholar
• Yang M, Sun L, Wang S et al. Novel function of B cell-activating factor in the induction of IL-10-producing regulatory B cells. J. Immunol. 184(7), 3321–3325 (2010).
   PubMed Web of Science ®Google Scholar
• Leibundgut G, Witztum JL, Tsimikas S. Oxidation-specific epitopes and immunological responses: Translational biotheranostic implications for atherosclerosis. Curr. Opin. Pharmacol. 13(2), 168–179 (2013).
   PubMed Web of Science ®Google Scholar
• Herbin O, Ait-Oufella H, Yu W et al. Regulatory T-cell response to apolipoprotein B100-derived peptides reduces the development and progression of atherosclerosis in mice. Arterioscler. Thromb. Vasc. Biol. 32(3), 605–612 (2012).
   PubMed Web of Science ®Google Scholar
• Carter NA, Rosser EC, Mauri C. Interleukin-10 produced by B cells is crucial for the suppression of Th17/Th1 responses, induction of T regulatory type 1 cells and reduction of collagen-induced arthritis. Arthritis Res. Ther. 14(1), R32 (2012).
   PubMed Web of Science ®Google Scholar
• Bentzon JF, Falk E. Atherosclerotic lesions in mouse and man: is it the same disease? Curr. Opin. Lipidol. 21(5), 434–440 (2010).
   PubMed Web of Science ®Google Scholar
• Mestas J, Hughes CC. Of mice and not men: differences between mouse and human immunology. J. Immunol. 172(5), 2731–2738 (2004).
   PubMed Web of Science ®Google Scholar
• Bruhns P. Properties of mouse and human IgG receptors and their contribution to disease models. Blood 119(24), 5640–5649 (2012).
   PubMed Web of Science ®Google Scholar
• Doran AC, Lehtinen AB, Meller N et al. Id3 is a novel atheroprotective factor containing a functionally significant single-nucleotide polymorphism associated with intima-media thickness in humans. Circ. Res. 106(7), 1303–1311 (2010).
   PubMed Web of Science ®Google Scholar
• Hardy RR. B-1 B cell development. J. Immunol. 177(5), 2749–2754 (2006).
   PubMed Web of Science ®Google Scholar
• Allman D, Pillai S. Peripheral B cell subsets. Curr. Opin. Immunol. 20(2), 149–157 (2008).
   PubMed Web of Science ®Google Scholar
• Pillai S, Cariappa A. The follicular versus marginal zone B lymphocyte cell fate decision. Nat. Rev. Immunol. 9(11), 767–777 (2009).
   PubMed Web of Science ®Google Scholar