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Review Articles

Multiple potential roles for B cells in atherosclerosis

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Pages 297-303 | Received 07 Jan 2014, Accepted 27 Feb 2014, Published online: 09 May 2014

References

  • Mendis S, Pekka P, Norrving B. Global atlas on cardiovascular disease prevention and control. Geneva: World Health Organization; 2011.
  • Legein B, Temmerman L, Biessen EAL, Lutgens E. Inflammation and immune system interactions in atherosclerosis. Cell Mol Life Sci CMLS. 2013;70:3847–69.
  • Lichtman AH, Binder CJ, Tsimikas S, Witztum JL. Adaptive immunity in atherogenesis: new insights and therapeutic approaches. J Clin Invest. 2013;123:27–36.
  • Hansson GK, Hermansson A. The immune system in atherosclerosis. Nat Immunol. 2011;12:204–12.
  • Grundtman C, Wick G. The autoimmune concept of atherosclerosis. Curr Opin Lipidol. 2011;22:327–34.
  • Cancro MP. Peripheral B-cell maturation: the intersection of selection and homeostasis. Immunol Rev. 2004;197:89–101.
  • Hardy RR, Kincade PW, Dorshkind K. The protean nature of cells in the B lymphocyte lineage. Immunity. 2007;26:703–14.
  • Montecino-Rodriguez E, Dorshkind K. New perspectives in B-1 B cell development and function. Trends Immunol. 2006;27:428–33.
  • Kantor AB, Herzenberg LA. Origin of murine B cell lineages. Annu Rev Immunol. 1993;11:501–38.
  • Duan B, Morel L. Role of B-1a cells in autoimmunity. Autoimmun Rev. 2006;5:403–8.
  • Campbell KA, Lipinski MJ, Doran AC, Skaflen MD, Fuster V, McNamara CA. Lymphocytes and the adventitial immune response in atherosclerosis. Circ Res. 2012;110:889–900.
  • Scholz JL, Cancro MP. Resolve, revise, and relax: the 3 Rs of B cell repertoire adjustment. Immunol Lett. 2012;143:2–8.
  • Von Boehmer H, Melchers F. Checkpoints in lymphocyte development and autoimmune disease. Nat Immunol. 2010;11:14–20.
  • Liu Z, Davidson A. BAFF and selection of autoreactive B cells. Trends Immunol. 2011;32:388–94.
  • Schiemann B, Gommerman JL, Vora K, Cachero TG, Shulga-Morskaya S, Dobles M, et al. An essential role for BAFF in the normal development of B cells through a BCMA-independent pathway. Science. 2001;293:2111–14.
  • Gorelik L, Gilbride K, Dobles M, Kalled SL, Zandman D, Scott ML. Normal B cell homeostasis requires B cell activation factor production by radiation-resistant cells. J Exp Med. 2003;198:937–45.
  • Sasaki Y, Casola S, Kutok JL, Rajewsky K, Schmidt-Supprian M. TNF family member B cell-activating factor (BAFF) receptor-dependent and -independent roles for BAFF in B cell physiology. J Immunol. 2004;173:2245–52.
  • Yan M, Wang H, Chan B, Roose-Girma M, Erickson S, Baker T, et al. Activation and accumulation of B cells in TACI-deficient mice. Nat Immunol. 2001;2:638–43.
  • Tsuji S, Cortesão C, Bram RJ, Platt JL, Cascalho M. TACI deficiency impairs sustained Blimp-1 expression in B cells decreasing long-lived plasma cells in the bone marrow. Blood. 2011;118:5832–9.
  • Bossen C, Cachero TG, Tardivel A, Ingold K, Willen L, Dobles M, et al. TACI, unlike BAFF-R, is solely activated by oligomeric BAFF and APRIL to support survival of activated B cells and plasmablasts. Blood. 2008;111:1004–12.
  • O’Connor BP, Raman VS, Erickson LD, Cook WJ, Weaver LK, Ahonen C, et al. BCMA is essential for the survival of long-lived bone marrow plasma cells. J Exp Med. 2004;199:91–8.
  • Huard B, McKee T, Bosshard C, Durual S, Matthes T, Myit S, et al. APRIL secreted by neutrophils binds to heparan sulfate proteoglycans to create plasma cell niches in human mucosa. J Clin Invest. 2008; 118:2887–95.
  • Miller YI, Choi S-H, Wiesner P, Fang L, Harkewicz R, Hartvigsen K, et al. Oxidation-specific epitopes are danger-associated molecular patterns recognized by pattern recognition receptors of innate immunity. Circ Res. 2011;108:235–48.
  • Tarlinton D, Good-Jacobson K. Diversity among memory B cells: origin, consequences, and utility. Science. 2013;341:1205–11.
  • Good-Jacobson KL, Shlomchik MJ. Plasticity and heterogeneity in the generation of memory B cells and long-lived plasma cells: the influence of germinal center interactions and dynamics. J Immunol. 2010;185:3117–25.
  • Nimmerjahn F, Ravetch JV. Fcgamma receptors: old friends and new family members. Immunity. 2006;24:19–28.
  • Haskard DO, Boyle JJ, Mason JC. The role of complement in atherosclerosis. Curr Opin Lipidol. 2008;19:478–82.
  • Carroll MC, Isenman DE. Regulation of humoral immunity by complement. Immunity. 2012;37:199–207.
  • Barr TA, Shen P, Brown S, Lampropoulou V, Roch T, Lawrie S, et al. B cell depletion therapy ameliorates autoimmune disease through ablation of IL-6-producing B cells. J Exp Med. 2012;209:1001–10.
  • Rauch PJ, Chudnovskiy A, Robbins CS, Weber GF, Etzrodt M, Hilgendorf I, et al. Innate response activator B cells protect against microbial sepsis. Science. 2012;335:597–601.
  • Zouggari Y, Ait-Oufella H, Bonnin P, Simon T, Sage AP, Guérin C, et al. B lymphocytes trigger monocyte mobilization and impair heart function after acute myocardial infarction. Nat Med. 2013;19: 1273–80.
  • DiLillo DJ, Horikawa M, Tedder TF. B-lymphocyte effector functions in health and disease. Immunol Res. 2011;49:281–92.
  • Bouaziz J-D, Yanaba K, Venturi GM, Wang Y, Tisch RM, Poe JC, et al. Therapeutic B cell depletion impairs adaptive and autoreactive CD4 + T cell activation in mice. Proc Natl Acad Sci U S A. 2007; 104:20878–83.
  • Jordö ED, Wermeling F, Chen Y, Karlsson MCI. Scavenger receptors as regulators of natural antibody responses and B cell activation in autoimmunity. Mol Immunol. 2011;48:1307–18.
  • Gray D, Gray M, Barr T. Innate responses of B cells. Eur J Immunol. 2007;37:3304–10.
  • Mackay F, Schneider P. Cracking the BAFF code. Nat Rev Immunol. 2009;9:491–502.
  • Waltner-Romen M, Falkensammer G, Rabl W, Wick G. A previously unrecognized site of local accumulation of mononuclear cells. The vascular-associated lymphoid tissue. J Histochem Cytochem. 1998;46: 1347–50.
  • 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. 2001;193:263–9.
  • 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; 101:1717–25.
  • Hamze M, Desmetz C, Berthe ML, Roger P, Boulle N, Brancherau P, et al. Characterization of resident B cells of vascular walls in human atherosclerotic patients. J Immunol. 2013;191:3006–16.
  • Moos MPW, John N, Gräbner R, Nossmann S, Günther B, Vollandt 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;25:2386–91.
  • Gräbner R, Lötzer K, Döpping S, Hildner M, Radke D, Beer M, et al. Lymphotoxin beta receptor signaling promotes tertiary lymphoid organogenesis in the aorta adventitia of aged ApoE-/- mice. J Exp Med. 2009;206:233–48.
  • Huan T, Zhang B, Wang Z, Joehanes R, Zhu J, Johnson AD, et al. A systems biology framework identifies molecular underpinnings of coronary heart disease. Arterioscler Thromb Vasc Biol. 2013;33:1427–34.
  • Mantani PT, Ljungcrantz I, Andersson L, Alm R, Hedblad B, Björkbacka H, et al. Circulating CD40 + and CD86 + B cell subsets demonstrate opposing associations with risk of stroke. Arterioscler Thromb Vasc Biol. 2014;34:211–18.
  • Hansson GK, Bondjers G, Bylock A, Hjalmarsson L. Ultrastructural studies on the localization of IgG in the aortic endothelium and subendothelial intima of atherosclerotic and nonatherosclerotic rabbits. Exp Mol Pathol. 1980;33:302–15.
  • 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. 2009;120:417–26.
  • Virella G, Virella I, Leman RB, Pryor MB, Lopes-Virella MF. Anti-oxidized low-density lipoprotein antibodies in patients with coronary heart disease and normal healthy volunteers. Int J Clin Lab Res. 1993;23:95–101.
  • Shaw PX, Hörkkö S, Tsimikas S, Chang MK, Palinski W, Silverman GJ, et al. Human-derived anti-oxidized LDL autoantibody blocks uptake of oxidized LDL by macrophages and localizes to atherosclerotic lesions in vivo. Arterioscler Thromb Vasc Biol. 2001;21:1333–9.
  • Xu Q, Luef G, Weimann S, Gupta RS, Wolf H, Wick G. Staining of endothelial cells and macrophages in atherosclerotic lesions with human heat-shock protein-reactive antisera. Arterioscler Thromb J Vasc Biol Am Heart Assoc. 1993;13:1763–9.
  • Hulthe J. Antibodies to oxidized LDL in atherosclerosis development— clinical and animal studies. Clin Chim Acta Int J Clin Chem. 2004;348:1–8.
  • Tsimikas S, Brilakis ES, Lennon RJ, Miller ER, Witztum JL, McConnell JP, et al. Relationship of IgG and IgM autoantibodies to oxidized low density lipoprotein with coronary artery disease and cardiovascular events. J Lipid Res. 2007;48:425–33.
  • Carbone F, Nencioni A, Mach F, Vuilleumier N, Montecucco F. Evidence on the pathogenic role of auto-antibodies in acute cardiovascular diseases. Thromb Haemost. 2013;109:854–68.
  • Tinahones FJ, Gómez-Zumaquero JM, Garrido-Sánchez L, García-Fuentes E, Rojo-Martínez G, Esteva I, et al. Influence of age and sex on levels of anti-oxidized LDL antibodies and anti-LDL immune complexes in the general population. J Lipid Res. 2005; 46:452–7.
  • Kyaw T, Tay C, Krishnamurthi S, Kanellakis P, Agrotis A, Tipping P, et al. B1a B lymphocytes are atheroprotective by secreting natural IgM that increases IgM deposits and reduces necrotic cores in atherosclerotic lesions. Circ Res. 2011;109:830–40.
  • Lopes-Virella MF, Hunt KJ, Baker NL, Virella G, Moritz T; VADT Investigators. The levels of MDA-LDL in circulating immune complexes predict myocardial infarction in the VADT study. Atherosclerosis. 2012;224:526–31.
  • Ravandi A, Boekholdt SM, Mallat Z, Talmud PJ, Kastelein JJP, Wareham NJ, et al. Relationship of IgG and IgM autoantibodies and immune complexes to oxidized LDL with markers of oxidation and inflammation and cardiovascular events: results from the EPIC-Norfolk Study. J Lipid Res. 2011;52:1829–36.
  • Peters MJL, van Halm VP, Voskuyl AE, Smulders YM, Boers M, Lems WF, et al. Does rheumatoid arthritis equal diabetes mellitus as an independent risk factor for cardiovascular disease?A prospective study. Arthritis Rheum. 2009;61:1571–9.
  • Skaggs BJ, Hahn BH, McMahon M. Accelerated atherosclerosis in patients with SLE—mechanisms and management. Nat Rev Rheumatol. 2012;8:214–23.
  • Wada Y, Kuroda T, Murasawa A, Tanabe N, Nakano M, Gejyo F. Autoantibodies against oxidized low-density lipoprotein (LDL) and carotid atherosclerosis in patients with rheumatoid arthritis. Clin Exp Rheumatol. 2005;23:482–6.
  • Peters MJL, van Halm VP, Nurmohamed MT, Damoiseaux J, Tervaert JWC, Twisk JWR, et al. Relations between autoantibodies against oxidized low-density lipoprotein, inflammation, subclinical atherosclerosis, and cardiovascular disease in rheumatoid arthritis. J Rheumatol. 2008;35:1495–9.
  • Ahmed HMMS, Youssef M, Mosaad YM. Antibodies against oxidized low-density lipoprotein are associated with subclinical atherosclerosis in recent-onset rheumatoid arthritis. Clin Rheumatol. 2010;29: 1237–43.
  • Kiani AN, Vogel-Claussen J, Arbab-Zadeh A, Magder LS, Lima J, Petri M. Semiquantified noncalcified coronary plaque in systemic lupus erythematosus. J Rheumatol. 2012;39:2286–93.
  • Wang J, Cheng X, Xiang M-X, Alanne-Kinnunen M, Wang J-A, Chen H, et al. IgE stimulates human and mouse arterial cell apoptosis and cytokine expression and promotes atherogenesis in Apoe-/- mice. J Clin Invest. 2011;121:3564–77.
  • Major AS, Fazio S, Linton MF. B-lymphocyte deficiency increases atherosclerosis in LDL receptor-null mice. Arterioscler Thromb Vasc Biol. 2002;22:1892–8.
  • Caligiuri G, Nicoletti A, Poirier B, Hansson GK. Protective immunity against atherosclerosis carried by B cells of hypercholesterolemic mice. J Clin Invest. 2002;109:745–53.
  • Ait-Oufella H, Herbin O, Bouaziz J-D, Binder CJ, Uyttenhove C, Laurans L, et al. B cell depletion reduces the development of atherosclerosis in mice. J Exp Med. 2010;207:1579–87.
  • Kyaw T, Tay C, Khan A, Dumouchel V, Cao A, To K, et al. Conventional B2 B cell depletion ameliorates whereas its adoptive transfer aggravates atherosclerosis. J Immunol. 2010;185:4410–19.
  • Sage AP, Tsiantoulas D, Baker L, Harrison J, Masters L, Murphy D, et al. BAFF receptor deficiency reduces the development of atherosclerosis in mice—brief report. Arterioscler Thromb Vasc Biol. 2012;32:1573–6.
  • Kyaw T, Tay C, Hosseini H, Kanellakis P, Gadowski T, MacKay F, 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. 2012;7:e29371.
  • Doran AC, Lipinski MJ, Oldham SN, Garmey JC, Campbell KA, Skaflen MD, et al. B-cell aortic homing and atheroprotection depend on Id3. Circ Res. 2012;110:e1–12.
  • Wigren M, Kolbus D, Dunér P, Ljungcrantz I, Söderberg I, Björkbacka H, et al. Evidence for a role of regulatory T cells in mediating the atheroprotective effect of apolipoprotein B peptide vaccine. J Intern Med. 2011;269:546–56.
  • Schiopu A, Frendéus B, Jansson B, Söderberg I, Ljungcrantz I, Araya Z, et al. Recombinant antibodies to an oxidized low-density lipoprotein epitope induce rapid regression of atherosclerosis in apobec-1(-/-)/ low-density lipoprotein receptor(-/-) mice. J Am Coll Cardiol. 2007; 50:2313–18.
  • Burut DFP, Karim Y, Ferns GAA. The role of immune complexes in atherogenesis. Angiology. 2010;61:679–89.
  • Chyu K-Y, Nilsson J, Shah PK. Immune mechanisms in atherosclerosis and potential for an atherosclerosis vaccine. Discov Med. 2011;11: 403–12.
  • Schwab I, Nimmerjahn F. Intravenous immunoglobulin therapy: how does IgG modulate the immune system?Nat Rev Immunol. 2013;13:176–89.
  • Ephrem A, Chamat S, Miquel C, Fisson S, Mouthon L, Caligiuri G, et al. Expansion of CD4 + CD25+ regulatory T cells by intravenous immunoglobulin: a critical factor in controlling experimental autoimmune encephalomyelitis. Blood. 2008;111:715–22.
  • Fredrikson GN, Söderberg I, Lindholm M, Dimayuga P, Chyu K-Y, Shah PK, et al. Inhibition of atherosclerosis in apoE-null mice by immunization with apoB-100 peptide sequences. Arterioscler Thromb Vasc Biol. 2003;23:879–84.
  • Chyu K-Y, Zhao X, Reyes OS, Babbidge SM, Dimayuga PC, Yano J, et al. Immunization using an Apo B-100 related epitope reduces atherosclerosis and plaque inflammation in hypercholesterolemic apo E (-/-) mice. Biochem Biophys Res Commun. 2005;338:1982–9.
  • Klingenberg R, Lebens M, Hermansson A, Fredrikson GN, Strodthoff D, Rudling M, et al. Intranasal immunization with an apolipoprotein B-100 fusion protein induces antigen-specific regulatory T cells and reduces atherosclerosis. Arterioscler Thromb Vasc Biol. 2010;30:946–52.
  • Herbin O, Ait-Oufella H, Yu W, Fredrikson GN, Aubier B, Perez N, et al. Regulatory T-cell response to apolipoprotein B100-derived peptides reduces the development and progression of atherosclerosis in mice. Arterioscler Thromb Vasc Biol. 2012;32:605–12.
  • Xu Q, Dietrich H, Steiner HJ, Gown AM, Schoel B, Mikuz G, et al. Induction of arteriosclerosis in normocholesterolemic rabbits by immunization with heat shock protein 65. Arterioscler Thromb J Vasc Biol Am Heart Assoc. 1992;12:789–99.
  • George J, Shoenfeld Y, Afek A, Gilburd B, Keren P, Shaish A, et al. Enhanced fatty streak formation in C57BL/6J mice by immunization with heat shock protein-65. Arterioscler Thromb Vasc Biol. 1999; 19:505–10.
  • Afek A, George J, Gilburd B, Rauova L, Goldberg I, Kopolovic J, et al. Immunization of low-density lipoprotein receptor deficient (LDL-RD) mice with heat shock protein 65 (HSP-65) promotes early atherosclerosis. J Autoimmun. 2000;14:115–21.
  • Harats D, Yacov N, Gilburd B, Shoenfeld Y, George J. Oral tolerance with heat shock protein 65 attenuates Mycobacterium tuberculosis-induced and high-fat-diet-driven atherosclerotic lesions. J Am Coll Cardiol. 2002;40:1333–8.
  • Maron R, Sukhova G, Faria A-M, Hoffmann E, Mach F, Libby P, et al. Mucosal administration of heat shock protein-65 decreases atherosclerosis and inflammation in aortic arch of low-density lipoprotein receptor-deficient mice. Circulation. 2002;106:1708–15.
  • Klingenberg R, Ketelhuth DFJ, Strodthoff D, Gregori S, Hansson GK. Subcutaneous immunization with heat shock protein-65 reduces atherosclerosis in Apoe− mice. Immunobiology. 2012; 217:540–7.
  • George J, Afek A, Gilburd B, Blank M, Levy Y, Aron-Maor A, et al. Induction of early atherosclerosis in LDL-receptor-deficient mice immunized with beta2-glycoprotein I. Circulation. 1998;98:1108–15.
  • Hörkkö S, Bird DA, Miller E, Itabe H, Leitinger N, Subbanagounder G, et al. Monoclonal autoantibodies specific for oxidized phospholipids or oxidized phospholipid-protein adducts inhibit macrophage uptake of oxidized low-density lipoproteins. J Clin Invest. 1999;103:117–28.
  • Binder CJ, Hartvigsen K, Chang M-K, Miller M, Broide D, Palinski W, et al. IL-5 links adaptive and natural immunity specific for epitopes of oxidized LDL and protects from atherosclerosis. J Clin Invest. 2004;114:427–37.
  • Boyle JJ, Christou I, Iqbal MB, Nguyen AT, Leung VWY, Evans PC, et al. Solid-phase immunoglobulins IgG and IgM activate macrophages with solid-phase IgM acting via a novel scavenger receptor a pathway. Am J Pathol. 2012;181:347–61.
  • Smith KGC, Clatworthy MR. FcgammaRIIB in autoimmunity and infection: evolutionary and therapeutic implications. Nat Rev Immunol. 2010;10:328–43.
  • Kelly JA, Griffin ME, Fava RA, Wood SG, Bessette KA, Miller ER, et al. Inhibition of arterial lesion progression in CD16-deficient mice: evidence for altered immunity and the role of IL-10. Cardiovasc Res. 2010;85:224–31.
  • Ng HP, Burris RL, Nagarajan S. Attenuated atherosclerotic lesions in apoE-Fcγ-chain-deficient hyperlipidemic mouse model is associated with inhibition of Th17 cells and promotion of regulatory T cells. J Immunol. 2011;187:6082–93.
  • Mendez-Fernandez YV, Stevenson BG, Diehl CJ, Braun NA, Wade NS, Covarrubias R, et al. The inhibitory FcγRIIb modulates the inflammatory response and influences atherosclerosis in male apoE(-/-) mice. Atherosclerosis. 2011;214:73–80.
  • Virella G, Lopes-Virella MF. Atherogenesis and the humoral immune response to modified lipoproteins. Atherosclerosis. 2008; 200:239–46.
  • Moulin V, Andris F, Thielemans K, Maliszewski C, Urbain J, Moser M. B lymphocytes regulate dendritic cell (DC) function in vivo: increased interleukin 12 production by DCs from B cell-deficient mice results in T helper cell type 1 deviation. J Exp Med. 2000;192:475–82.
  • Zietara N, Łyszkiewicz M, Puchałka J, Pei G, Gutierrez MG, Lienenklaus S, et al. Immunoglobulins drive terminal maturation of splenic dendritic cells. Proc Natl Acad Sci U S A. 2013;110:2282–7.
  • Lund FE, Randall TD. Effector and regulatory B cells: modulators of CD4 + T cell immunity. Nat Rev Immunol. 2010;10:236–47.
  • Karper JC, de Jager SCA, Ewing MM, de Vries MR, Bot I, van Santbrink PJ, et al. An unexpected intriguing effect of toll-like receptor regulator RP105 (CD180) on atherosclerosis formation with alterations on B-cell activation. Arterioscler Thromb Vasc Biol. 2013;33:2810–17.
  • Hilgendorf I, Theurl I, Gerhardt LMS, Robbins CS, Weber GF, Gonen A, et al. Innate response activator B cells aggravate atherosclerosis by stimulating TH1 adaptive immunity. Circulation. 2014; doi:10.1161/CIRCULATIONAHA.113.006381.
  • Opata MM, Ye Z, Hollifield M, Garvy BA. B cell production of tumor necrosis factor in response to Pneumocystis murina infection in mice. Infect Immun. 2013;81:4252–60.
  • Turpeinen H, Raitoharju E, Oksanen A, Oksala N, Levula M, Lyytikäinen L-P, et al. Proprotein convertases in human atherosclerotic plaques: the overexpression of FURIN and its substrate cytokines BAFF and APRIL. Atherosclerosis. 2011;219:799–806.

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