1932

Abstract

B cells are traditionally known for their ability to produce antibodies in the context of adaptive immune responses. However, over the last decade B cells have been increasingly recognized as modulators of both adaptive and innate immune responses, as well as players in an important role in the pathogenesis of a variety of human diseases. Here, after briefly summarizing our current understanding of B cell biology, we present a systematic review of the literature from both animal models and human studies that highlight the important role that B lymphocytes play in cardiac and vascular disease. While many aspects of B cell biology in the vasculature and, to an even greater extent, in the heart remain unclear, B cells are emerging as key regulators of cardiovascular adaptation to injury.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-immunol-042617-053104
2020-04-26
2024-04-18
Loading full text...

Full text loading...

/deliver/fulltext/immunol/38/1/annurev-immunol-042617-053104.html?itemId=/content/journals/10.1146/annurev-immunol-042617-053104&mimeType=html&fmt=ahah

Literature Cited

  1. 1. 
    LeBien TW, Tedder TF. 2008. B lymphocytes: how they develop and function. Blood 112:1570–80
    [Google Scholar]
  2. 2. 
    Parra D, Takizawa F, Sunyer JO 2013. Evolution of B cell immunity. Annu. Rev. Anim. Biosci. 1:65–97
    [Google Scholar]
  3. 3. 
    Naradikian MS, Scholz JL, Oropallo MA, Cancro MP 2014. Understanding B cell biology. Drugs Targeting B-Cells in Autoimmune Diseases X Bosch, M Ramos-Casals, MA Khamashta 11–35 Basel: Springer
    [Google Scholar]
  4. 4. 
    Kantor AB, Herzenberg LA. 1993. Origin of murine B cell lineages. Annu. Rev. Immunol. 11:501–38
    [Google Scholar]
  5. 5. 
    Holodick NE, Rodriguez-Zhurbenko N, Hernandez AM 2017. Defining natural antibodies. Front. Immunol. 8:872
    [Google Scholar]
  6. 6. 
    Rajewsky K. 1996. Clonal selection and learning in the antibody system. Nature 381:751–58
    [Google Scholar]
  7. 7. 
    Bos NA, Kimura H, Meeuwsen CG, De Visser H, Hazenberg MP et al. 1989. Serum immunoglobulin levels and naturally occurring antibodies against carbohydrate antigens in germ-free BALB/c mice fed chemically defined ultrafiltered diet. Eur. J. Immunol. 19:2335–39
    [Google Scholar]
  8. 8. 
    Palma J, Tokarz-Deptula B, Deptula J, Deptula W 2018. Natural antibodies—facts known and unknown. Cent. Eur. J. Immunol. 43:466–75
    [Google Scholar]
  9. 9. 
    Montecino-Rodriguez E, Dorshkind K. 2012. B-1 B cell development in the fetus and adult. Immunity 36:13–21
    [Google Scholar]
  10. 10. 
    Adamo L, Staloch LJ, Rocha-Resende C, Matkovich SJ, Jiang W et al. 2018. Modulation of subsets of cardiac B lymphocytes improves cardiac function after acute injury. JCI Insight 3:120137
    [Google Scholar]
  11. 11. 
    Cerutti A, Cols M, Puga I 2013. Marginal zone B cells: virtues of innate-like antibody-producing lymphocytes. Nat. Rev. Immunol. 13:118–32
    [Google Scholar]
  12. 12. 
    Kurosaki T, Kometani K, Ise W 2015. Memory B cells. Nat. Rev. Immunol. 15:149–59
    [Google Scholar]
  13. 13. 
    Goodnow CC, Crosbie J, Adelstein S, Lavoie TB, Smith-Gill SJ et al. 1988. Altered immunoglobulin expression and functional silencing of self-reactive B lymphocytes in transgenic mice. Nature 334:676–82
    [Google Scholar]
  14. 14. 
    Chung JB, Silverman M, Monroe JG 2003. Transitional B cells: step by step towards immune competence. Trends Immunol 24:343–49
    [Google Scholar]
  15. 15. 
    Adamo L, Garcia-Cardena G. 2012. The vascular origin of hematopoietic cells. Dev. Biol. 362:1–10
    [Google Scholar]
  16. 16. 
    Melchers F. 2015. Checkpoints that control B cell development. J. Clin. Investig. 125:2203–10
    [Google Scholar]
  17. 17. 
    Nagasawa T. 2006. Microenvironmental niches in the bone marrow required for B-cell development. Nat. Rev. Immunol. 6:107–16
    [Google Scholar]
  18. 18. 
    Allman D, Lindsley RC, DeMuth W, Rudd K, Shinton SA, Hardy RR 2001. Resolution of three nonproliferative immature splenic B cell subsets reveals multiple selection points during peripheral B cell maturation. J. Immunol. 167:6834–40
    [Google Scholar]
  19. 19. 
    Marshall-Clarke S, Tasker L, Parkhouse RM 2000. Immature B lymphocytes from adult bone marrow exhibit a selective defect in induced hyperexpression of major histocompatibility complex class II and fail to show B7.2 induction. Immunology 100:141–51
    [Google Scholar]
  20. 20. 
    Savage HP, Baumgarth N. 2015. Characteristics of natural antibody-secreting cells. Ann. N. Y. Acad. Sci. 1362:132–42
    [Google Scholar]
  21. 21. 
    Nutt SL, Hodgkin PD, Tarlinton DM, Corcoran LM 2015. The generation of antibody-secreting plasma cells. Nat. Rev. Immunol. 15:160–71
    [Google Scholar]
  22. 22. 
    Yong-Rui Zou CG, Diamond B 2017. B cells. Kelley and Firestein's Textbook of Rheumatology E-Book RB Gary, S Firestein, SE Gabriel, IB McInnes, JR O'Dell Philadelphia, PA: Elsevier
    [Google Scholar]
  23. 23. 
    Jones GW, Hill DG, Jones SA 2016. Understanding immune cells in tertiary lymphoid organ development: It is all starting to come together. Front. Immunol. 7:401
    [Google Scholar]
  24. 24. 
    Bortnick A, Allman D. 2013. What is and what should always have been: long-lived plasma cells induced by T cell-independent antigens. J. Immunol. 190:5913–18
    [Google Scholar]
  25. 25. 
    Crotty S. 2019. T follicular helper cell biology: a decade of discovery and diseases. Immunity 50:1132–48
    [Google Scholar]
  26. 26. 
    Chen X, Jensen PE. 2008. The role of B lymphocytes as antigen-presenting cells. Arch. Immunol. Ther. Exp. 56:77–83
    [Google Scholar]
  27. 27. 
    Hong S, Zhang Z, Liu H, Tian M, Zhu X et al. 2018. B cells are the dominant antigen-presenting cells that activate naive CD4+ T cells upon immunization with a virus-derived nanoparticle antigen. Immunity 49:695–708.e4
    [Google Scholar]
  28. 28. 
    Shen P, Fillatreau S. 2015. Antibody-independent functions of B cells: a focus on cytokines. Nat. Rev. Immunol. 15:441–51
    [Google Scholar]
  29. 29. 
    Zouggari Y, Ait-Oufella H, Bonnin P, Simon T, Sage AP et al. 2013. B lymphocytes trigger monocyte mobilization and impair heart function after acute myocardial infarction. Nat. Med. 19:1273–80
    [Google Scholar]
  30. 30. 
    Chousterman BG, Swirski FK. 2015. Innate response activator B cells: origins and functions. Int. Immunol. 27:537–41
    [Google Scholar]
  31. 31. 
    Rosser EC, Mauri C. 2015. Regulatory B cells: origin, phenotype, and function. Immunity 42:607–12
    [Google Scholar]
  32. 32. 
    Chimen M, McGettrick HM, Apta B, Kuravi SJ, Yates CM et al. 2015. Homeostatic regulation of T cell trafficking by a B cell-derived peptide is impaired in autoimmune and chronic inflammatory disease. Nat. Med. 21:467–75
    [Google Scholar]
  33. 33. 
    Gowans JL, Knight EJ. 1964. The route of re-circulation of lymphocytes in the rat. Proc. R. Soc. Lond. B 159:257–82
    [Google Scholar]
  34. 34. 
    Kunkel EJ, Butcher EC. 2002. Chemokines and the tissue-specific migration of lymphocytes. Immunity 16:1–4
    [Google Scholar]
  35. 35. 
    Tanaka T, Ebisuno Y, Kanemitsu N, Umemoto E, Yang BG et al. 2004. Molecular determinants controlling homeostatic recirculation and tissue-specific trafficking of lymphocytes. Int. Arch. Allergy Immunol. 134:120–34
    [Google Scholar]
  36. 36. 
    Osborn L. 1990. Leukocyte adhesion to endothelium in inflammation. Cell 62:3–6
    [Google Scholar]
  37. 37. 
    Bonner F, Borg N, Burghoff S, Schrader J Resident cardiac immune cells and expression of the ectonucleotidase enzymes CD39 and CD73 after ischemic injury. PLOS ONE 7:e34730
    [Google Scholar]
  38. 38. 
    Ramos GC, van den Berg A, Nunes-Silva V, Weirather J, Peters L et al. 2017. Myocardial aging as a T-cell-mediated phenomenon. PNAS 114:E2420–29
    [Google Scholar]
  39. 39. 
    Horckmans M, Bianchini M, Santovito D, Megens RTA, Springael JY et al. 2017. Pericardial adipose tissue regulates granulopoiesis, fibrosis and cardiac function after myocardial infarction. Circulation 137:948–60
    [Google Scholar]
  40. 40. 
    Rauch PJ, Chudnovskiy A, Robbins CS, Weber GF, Etzrodt M et al. 2012. Innate response activator B cells protect against microbial sepsis. Science 335:597–601
    [Google Scholar]
  41. 41. 
    Yan X, Anzai A, Katsumata Y, Matsuhashi T, Ito K et al. 2013. Temporal dynamics of cardiac immune cell accumulation following acute myocardial infarction. J. Mol. Cell Cardiol. 62:24–35
    [Google Scholar]
  42. 42. 
    Wu L, Zhao F, Dai M, Li H, Chen C et al. 2017. P2y12 receptor promotes pressure overload-induced cardiac remodeling via platelet-driven inflammation in mice. Hypertension 70:759–69
    [Google Scholar]
  43. 43. 
    Goodchild TT, Robinson KA, Pang W, Tondato F, Cui J et al. 2009. Bone marrow-derived B cells preserve ventricular function after acute myocardial infarction. JACC Cardiovasc. Interv. 2:1005–16
    [Google Scholar]
  44. 44. 
    Sánchez-Trujillo L, Jerjes-Sanchez C, Rodriguez D, Panneflek J, Ortiz-Ledesma C et al. 2019. Phase II clinical trial testing the safety of a humanised monoclonal antibody anti-CD20 in patients with heart failure with reduced ejection fraction, ICFEr-RITU2: study protocol. BMJ Open 9:e022826
    [Google Scholar]
  45. 45. 
    Cordero-Reyes AM, Youker KA, Trevino AR, Celis R, Hamilton DJ et al. 2016. Full expression of cardiomyopathy is partly dependent on B-cells: a pathway that involves cytokine activation, immunoglobulin deposition, and activation of apoptosis. J. Am. Heart. Assoc. 5:e002484
    [Google Scholar]
  46. 46. 
    Kallikourdis M, Martini E, Carullo P, Sardi C, Roselli G et al. 2017. T cell costimulation blockade blunts pressure overload-induced heart failure. Nat. Commun. 8:14680
    [Google Scholar]
  47. 47. 
    Zhang M, Michael LH, Grosjean SA, Kelly RA, Carroll MC, Entman ML 2006. The role of natural IgM in myocardial ischemia-reperfusion injury. J. Mol. Cell Cardiol. 41:62–67
    [Google Scholar]
  48. 48. 
    Zhang M, Austen WG Jr., Chiu I, Alicot EM, Hung R et al. 2004. Identification of a specific self-reactive IgM antibody that initiates intestinal ischemia/reperfusion injury. PNAS 101:3886–91
    [Google Scholar]
  49. 49. 
    Matsui S, Fu ML, Katsuda S, Hayase M, Yamaguchi N et al. 1997. Peptides derived from cardiovascular G-protein-coupled receptors induce morphological cardiomyopathic changes in immunized rabbits. J. Mol. Cell Cardiol. 29:641–55
    [Google Scholar]
  50. 50. 
    Okazaki T, Tanaka Y, Nishio R, Mitsuiye T, Mizoguchi A et al. 2003. Autoantibodies against cardiac troponin I are responsible for dilated cardiomyopathy in PD-1-deficient mice. Nat. Med. 9:1477–83
    [Google Scholar]
  51. 51. 
    Alvarez FL, Neu N, Rose NR, Craig SW, Beisel KW 1987. Heart-specific autoantibodies induced by Coxsackievirus B3: identification of heart autoantigens. Clin. Immunol. Immunopathol. 43:129–39
    [Google Scholar]
  52. 52. 
    Karahan GE, Claas FH, Heidt S 2017. B cell immunity in solid organ transplantation. Front. Immunol. 7:686
    [Google Scholar]
  53. 53. 
    Zeng Q, Ng YH, Singh T, Jiang K, Sheriff KA et al. 2014. B cells mediate chronic allograft rejection independently of antibody production. J. Clin. Investig. 124:1052–56
    [Google Scholar]
  54. 54. 
    Noorchashm H, Reed AJ, Rostami SY, Mozaffari R, Zekavat G et al. 2006. B cell-mediated antigen presentation is required for the pathogenesis of acute cardiac allograft rejection. J. Immunol. 177:7715–22
    [Google Scholar]
  55. 55. 
    Noutsias M, Pauschinger M, Schultheiss H, Kühl U 2002. Phenotypic characterization of infiltrates in dilated cardiomyopathy—diagnostic significance of T-lymphocytes and macrophages in inflammatory cardiomyopathy. Med. Sci. Monit. 8:CR478–87
    [Google Scholar]
  56. 56. 
    Li Y, Zhou Z, Xin F, Zhang C, Zhang R et al. 2019. Primary cardiac lymphoma in both atria: a case report. J. Clin. Ultrasound 47:561–63
    [Google Scholar]
  57. 57. 
    Grantomo J, Pratita J, Rachmat J, Saraswati M 2018. A rare case of primary cardiac lymphoma and the role of early surgical debulking: a case report. Eur. Heart J. Case Rep. 2:yty116
    [Google Scholar]
  58. 58. 
    Thiagaraj A, Kalamkar P, Rahman R, Farah V, Poornima I 2018. An unprecedented case report of primary cardiac lymphoma exclusive to left ventricle: a diagnostic and therapeutic challenge. Eur. Heart J. Case Rep. 2:yty029
    [Google Scholar]
  59. 59. 
    Tada H, Asazuma K, Ohya E, Hayashi T, Nakai T et al. 1998. Images in cardiovascular medicine: primary cardiac B-cell lymphoma. Circulation 97:220–21
    [Google Scholar]
  60. 60. 
    Boag SE, Das R, Shmeleva EV, Bagnall A, Egred M et al. 2015. T lymphocytes and fractalkine contribute to myocardial ischemia/reperfusion injury in patients. J. Clin. Investig. 125:3063–76
    [Google Scholar]
  61. 61. 
    Yu M, Wen S, Wang M, Liang W, Li HH et al. 2013. TNF-α-secreting B cells contribute to myocardial fibrosis in dilated cardiomyopathy. J. Clin. Immunol. 33:1002–8
    [Google Scholar]
  62. 62. 
    Guo Y, Cen Z, Wei B, Wu W, Zhou Q 2015. Increased circulating interleukin 10-secreting B cells in patients with dilated cardiomyopathy. Int. J. Clin. Exp. Pathol. 8:8107–14
    [Google Scholar]
  63. 63. 
    Jiao J, Lu YZ, Xia N, Wang YQ, Tang TT et al. 2018. Defective circulating regulatory B cells in patients with dilated cardiomyopathy. Cell Physiol. Biochem. 46:23–35
    [Google Scholar]
  64. 64. 
    Tschope C, Van Linthout S, Spillmann F, Posch MG, Reinke P et al. 2019. Targeting CD20+ B-lymphocytes in inflammatory dilated cardiomyopathy with rituximab improves clinical course: a case series. Eur. Heart J. Case Rep. 3:ytz131
    [Google Scholar]
  65. 65. 
    Nussinovitch U, Shoenfeld Y. 2013. The clinical significance of anti-beta-1 adrenergic receptor autoantibodies in cardiac disease. Clin. Rev. Allergy Immunol. 44:75–83
    [Google Scholar]
  66. 66. 
    Pankuweit S, Portig I, Lottspeich F, Maisch B 1997. Autoantibodies in sera of patients with myocarditis: characterization of the corresponding proteins by isoelectric focusing and N-terminal sequence analysis. J. Mol. Cell Cardiol. 29:77–84
    [Google Scholar]
  67. 67. 
    Neumann DA, Burek CL, Baughman KL, Rose NR, Herskowitz A 1990. Circulating heart-reactive antibodies in patients with myocarditis or cardiomyopathy. J. Am. Coll. Cardiol. 16:839–46
    [Google Scholar]
  68. 68. 
    Youker KA, Assad-Kottner C, Cordero-Reyes AM, Trevino AR, Flores-Arredondo JH et al. 2014. High proportion of patients with end-stage heart failure regardless of aetiology demonstrates anti-cardiac antibody deposition in failing myocardium: humoral activation, a potential contributor of disease progression. Eur. Heart J. 35:1061–68
    [Google Scholar]
  69. 69. 
    Felix SB, Staudt A, Landsberger M, Grosse Y, Stangl V et al. 2002. Removal of cardiodepressant antibodies in dilated cardiomyopathy by immunoadsorption. J. Am. Coll. Cardiol. 39:646–52
    [Google Scholar]
  70. 70. 
    Doing A, Griffin D, Jacobson JA, Amber IJ, Gilbert E 2001. B-cell function in chronic heart failure: antibody response to pneumococcal vaccine. J. Card. Fail. 7:318–21
    [Google Scholar]
  71. 71. 
    APEX AMI Investig. Armstrong PW, Granger CB, Adams PX, Hamm C et al. 2007. Pexelizumab for acute ST-elevation myocardial infarction in patients undergoing primary percutaneous coronary intervention: a randomized controlled trial. JAMA 297:43–51
    [Google Scholar]
  72. 72. 
    Martel C, Granger CB, Ghitescu M, Stebbins A, Fortier A et al. 2012. Pexelizumab fails to inhibit assembly of the terminal complement complex in patients with ST-elevation myocardial infarction undergoing primary percutaneous coronary intervention: insight from a substudy of the Assessment of Pexelizumab in Acute Myocardial Infarction (APEX-AMI) trial. Am. Heart J. 164:43–51
    [Google Scholar]
  73. 73. 
    Baldwin WM 3rd, Halushka MK, Valujskikh A, Fairchild RL 2012. B cells in cardiac transplants: from clinical questions to experimental models. Semin. Immunol. 24:122–30
    [Google Scholar]
  74. 74. 
    Colvin MM, Cook JL, Chang P, Francis G, Hsu DT et al. 2015. Antibody-mediated rejection in cardiac transplantation: emerging knowledge in diagnosis and management: a scientific statement from the American Heart Association. Circulation 131:1608–39
    [Google Scholar]
  75. 75. 
    Starling RC, Armstrong B, Bridges ND, Eisen H, Givertz MM et al. 2019. Accelerated allograft vasculopathy with rituximab after cardiac transplantation. J. Am. Coll. Cardiol. 74:36–51
    [Google Scholar]
  76. 76. 
    Galkina E, Kadl A, Sanders J, Varughese D, Sarembock IJ, Ley K 2006. Lymphocyte recruitment into the aortic wall before and during development of atherosclerosis is partially L-selectin dependent. J. Exp. Med. 203:1273–82
    [Google Scholar]
  77. 77. 
    McClure M, Gopaluni S, Jayne D, Jones R 2018. B cell therapy in ANCA-associated vasculitis: current and emerging treatment options. Nat. Rev. Rheumatol. 14:580–91
    [Google Scholar]
  78. 78. 
    Zhang L, Wang Y. 2015. B lymphocytes in abdominal aortic aneurysms. Atherosclerosis 242:311–17
    [Google Scholar]
  79. 79. 
    Dimayuga P, Cercek B, Oguchi S, Fredrikson GN, Yano J et al. 2002. Inhibitory effect on arterial injury-induced neointimal formation by adoptive B-cell transfer in Rag-1 knockout mice. Arterioscler. Thromb. Vasc. Biol. 22:644–49
    [Google Scholar]
  80. 80. 
    Chan CT, Sobey CG, Lieu M, Ferens D, Kett MM et al. 2015. Obligatory role for B cells in the development of angiotensin II-dependent hypertension. Hypertension 66:1023–33
    [Google Scholar]
  81. 81. 
    Srikakulapu P, McNamara CA. 2017. B cells and atherosclerosis. Am. J. Physiol. Heart Circ. Physiol. 312:H1060–67
    [Google Scholar]
  82. 82. 
    Martinez HG, Quinones MP, Jimenez F, Estrada C, Clark KM et al. 2012. Important role of CCR2 in a murine model of coronary vasculitis. BMC Immunol 13:56
    [Google Scholar]
  83. 83. 
    Schaheen B, Downs EA, Serbulea V, Almenara CC, Spinosa M et al. 2016. B-cell depletion promotes aortic infiltration of immunosuppressive cells and is protective of experimental aortic aneurysm. Arterioscler. Thromb. Vasc. Biol. 36:2191–202
    [Google Scholar]
  84. 84. 
    Furusho A, Aoki H, Ohno-Urabe S, Nishihara M, Hirakata S et al. 2018. Involvement of B cells, immunoglobulins, and Syk in the pathogenesis of abdominal aortic aneurysm. J. Am. Heart Assoc. 7:e007750
    [Google Scholar]
  85. 85. 
    Ketelhuth DF, Hansson GK. 2016. Adaptive response of T and B cells in atherosclerosis. Circ. Res. 118:668–78
    [Google Scholar]
  86. 86. 
    Sage AP, Tsiantoulas D, Binder CJ, Mallat Z 2019. The role of B cells in atherosclerosis. Nat. Rev. Cardiol. 16:180–96
    [Google Scholar]
  87. 87. 
    Hansson GK, Libby P. 2006. The immune response in atherosclerosis: a double-edged sword. Nat. Rev. Immunol. 6:508–19
    [Google Scholar]
  88. 88. 
    Binder CJ, Papac-Milicevic N, Witztum JL 2016. Innate sensing of oxidation-specific epitopes in health and disease. Nat. Rev. Immunol. 16:485–97
    [Google Scholar]
  89. 89. 
    Tsiantoulas D, Diehl CJ, Witztum JL, Binder CJ 2014. B cells and humoral immunity in atherosclerosis. Circ. Res. 114:1743–56
    [Google Scholar]
  90. 90. 
    Miller YI, Choi SH, Wiesner P, Fang L, Harkewicz R et al. 2011. Oxidation-specific epitopes are danger-associated molecular patterns recognized by pattern recognition receptors of innate immunity. Circ. Res. 108:235–48
    [Google Scholar]
  91. 91. 
    Yla-Herttuala S, Palinski W, Butler SW, Picard S, Steinberg D, Witztum JL 1994. Rabbit and human atherosclerotic lesions contain IgG that recognizes epitopes of oxidized LDL. Arterioscler. Thromb. 14:32–40
    [Google Scholar]
  92. 92. 
    Nus M, Tsiantoulas D, Mallat Z 2017. Plan B (-cell) in atherosclerosis. Eur. J. Pharmacol. 816:76–81
    [Google Scholar]
  93. 93. 
    Houtkamp MA, de Boer OJ, van der Loos CM, van der Wal AC, Becker AE 2001. Adventitial infiltrates associated with advanced atherosclerotic plaques: structural organization suggests generation of local humoral immune responses. J. Pathol. 193:263–69
    [Google Scholar]
  94. 94. 
    Caligiuri G, Nicoletti A, Poirier B, Hansson GK 2002. Protective immunity against atherosclerosis carried by B cells of hypercholesterolemic mice. J. Clin. Investig. 109:745–53
    [Google Scholar]
  95. 95. 
    Major AS, Fazio S, Linton MF 2002. B-lymphocyte deficiency increases atherosclerosis in LDL receptor-null mice. Arterioscler. Thromb. Vasc. Biol. 22:1892–98
    [Google Scholar]
  96. 96. 
    Doran AC, Lipinski MJ, Oldham SN, Garmey JC, Campbell KA et al. 2012. B-cell aortic homing and atheroprotection depend on Id3. Circ. Res. 110:e1–12
    [Google Scholar]
  97. 97. 
    Ait-Oufella H, Herbin O, Bouaziz JD, Binder CJ, Uyttenhove C et al. 2010. B cell depletion reduces the development of atherosclerosis in mice. J. Exp. Med. 207:1579–87
    [Google Scholar]
  98. 98. 
    Kyaw T, Tay C, Khan A, Dumouchel V, Cao A et al. 2010. Conventional B2 B cell depletion ameliorates whereas its adoptive transfer aggravates atherosclerosis. J. Immunol. 185:4410–19
    [Google Scholar]
  99. 99. 
    Kyaw T, Tay C, Krishnamurthi S, Kanellakis P, Agrotis A et al. 2011. B1a B lymphocytes are atheroprotective by secreting natural IgM that increases IgM deposits and reduces necrotic cores in atherosclerotic lesions. Circ. Res. 109:830–40
    [Google Scholar]
  100. 100. 
    Rosenfeld SM, Perry HM, Gonen A, Prohaska TA, Srikakulapu P et al. 2015. B-1b cells secrete atheroprotective IgM and attenuate atherosclerosis. Circ. Res. 117:e28–39
    [Google Scholar]
  101. 101. 
    Gruber S, Hendrikx T, Tsiantoulas D, Ozsvar-Kozma M, Goderle L et al. 2016. Sialic acid-binding immunoglobulin-like lectin G promotes atherosclerosis and liver inflammation by suppressing the protective functions of B-1 cells. Cell Rep 14:2348–61
    [Google Scholar]
  102. 102. 
    Hosseini H, Yi L, Kanellakis P, Cao A, Tay C et al. 2018. Anti-TIM-1 monoclonal antibody (RMT1–10) attenuates atherosclerosis by expanding IgM-producing B1a cells. J. Am. Heart Assoc. 7:e008447
    [Google Scholar]
  103. 103. 
    Hosseini H, Li Y, Kanellakis P, Tay C, Cao A et al. 2016. Toll-like receptor (TLR)4 and MyD88 are essential for atheroprotection by peritoneal B1a B cells. J. Am. Heart Assoc. 5:e002947
    [Google Scholar]
  104. 104. 
    Sage AP, Tsiantoulas D, Baker L, Harrison J, Masters L et al. 2012. BAFF receptor deficiency reduces the development of atherosclerosis in mice—brief report. Arterioscler. Thromb. Vasc. Biol. 32:1573–76
    [Google Scholar]
  105. 105. 
    Kyaw T, Cui P, Tay C, Kanellakis P, Hosseini H et al. 2013. BAFF receptor mAb treatment ameliorates development and progression of atherosclerosis in hyperlipidemic ApoE−/− mice. PLOS ONE 8:e60430
    [Google Scholar]
  106. 106. 
    Nus M, Sage AP, Lu Y, Masters L, Lam BYH et al. 2017. Marginal zone B cells control the response of follicular helper T cells to a high-cholesterol diet. Nat. Med. 23:601–10
    [Google Scholar]
  107. 107. 
    Strom AC, Cross AJ, Cole JE, Blair PA, Leib C et al. 2015. B regulatory cells are increased in hyper-cholesterolaemic mice and protect from lesion development via IL-10. Thromb. Haemost. 114:835–47
    [Google Scholar]
  108. 108. 
    Sage AP, Nus M, Baker LL, Finigan AJ, Masters LM, Mallat Z 2015. Regulatory B cell-specific interleukin-10 is dispensable for atherosclerosis development in mice. Arterioscler. Thromb. Vasc. Biol. 35:1770–73
    [Google Scholar]
  109. 109. 
    Hilgendorf I, Theurl I, Gerhardt LM, Robbins CS, Weber GF et al. 2014. Innate response activator B cells aggravate atherosclerosis by stimulating T helper-1 adaptive immunity. Circulation 129:1677–87
    [Google Scholar]
  110. 110. 
    Tsiantoulas D, Sage AP, Mallat Z, Binder CJ 2015. Targeting B cells in atherosclerosis: closing the gap from bench to bedside. Arterioscler. Thromb. Vasc. Biol. 35:296–302
    [Google Scholar]
  111. 111. 
    Palinski W, Ord VA, Plump AS, Breslow JL, Steinberg D, Witztum JL 1994. ApoE-deficient mice are a model of lipoprotein oxidation in atherogenesis: demonstration of oxidation-specific epitopes in lesions and high titers of autoantibodies to malondialdehyde-lysine in serum. Arterioscler. Thromb. 14:605–16
    [Google Scholar]
  112. 112. 
    Chou MY, Fogelstrand L, Hartvigsen K, Hansen LF, Woelkers D et al. 2009. Oxidation-specific epitopes are dominant targets of innate natural antibodies in mice and humans. J. Clin. Investig. 119:1335–49
    [Google Scholar]
  113. 113. 
    Lewis MJ, Malik TH, Ehrenstein MR, Boyle JJ, Botto M, Haskard DO 2009. Immunoglobulin M is required for protection against atherosclerosis in low-density lipoprotein receptor-deficient mice. Circulation 120:417–26
    [Google Scholar]
  114. 114. 
    Nicoletti A, Kaveri S, Caligiuri G, Bariety J, Hansson GK 1998. Immunoglobulin treatment reduces atherosclerosis in apo E knockout mice. J. Clin. Investig. 102:910–18
    [Google Scholar]
  115. 115. 
    Palinski W, Miller E, Witztum JL 1995. Immunization of low density lipoprotein (LDL) receptor-deficient rabbits with homologous malondialdehyde-modified LDL reduces atherogenesis. PNAS 92:821–25
    [Google Scholar]
  116. 116. 
    Nilsson J, Calara F, Regnstrom J, Hultgardh-Nilsson A, Ameli S et al. 1997. Immunization with homologous oxidized low density lipoprotein reduces neointimal formation after balloon injury in hypercholesterolemic rabbits. J. Am. Coll. Cardiol. 30:1886–91
    [Google Scholar]
  117. 117. 
    Tsiantoulas D, Bot I, Ozsvar-Kozma M, Goderle L, Perkmann T et al. 2017. Increased plasma IgE accelerate atherosclerosis in secreted IgM deficiency. Circ. Res. 120:78–84
    [Google Scholar]
  118. 118. 
    Tay C, Liu YH, Hosseini H, Kanellakis P, Cao A et al. 2016. B-cell-specific depletion of tumour necrosis factor alpha inhibits atherosclerosis development and plaque vulnerability to rupture by reducing cell death and inflammation. Cardiovasc. Res. 111:385–97
    [Google Scholar]
  119. 119. 
    Meiler S, Smeets E, Winkels H, Shami A, Pascutti MF et al. 2016. Constitutive GITR activation reduces atherosclerosis by promoting regulatory CD4+ T-cell responses—brief report. Arterioscler. Thromb. Vasc. Biol. 36:1748–52
    [Google Scholar]
  120. 120. 
    Skaggs BJ, Hahn BH, McMahon M 2012. Accelerated atherosclerosis in patients with SLE—mechanisms and management. Nat. Rev. Rheumatol. 8:214–23
    [Google Scholar]
  121. 121. 
    Ketelhuth DF, Tonini GC, Carvalho MD, Ramos RF, Boschcov P, Gidlund M 2008. Autoantibody response to chromatographic fractions from oxidized LDL in unstable angina patients and healthy controls. Scand. J. Immunol. 68:456–62
    [Google Scholar]
  122. 122. 
    Hamze M, Desmetz C, Berthe ML, Roger P, Boulle N et al. 2013. Characterization of resident B cells of vascular walls in human atherosclerotic patients. J. Immunol. 191:3006–16
    [Google Scholar]
  123. 123. 
    Popa ER, Stegeman CA, Bos NA, Kallenberg CG, Tervaert JW 1999. Differential B- and T-cell activation in Wegener's granulomatosis. J. Allergy Clin. Immunol. 103:885–94
    [Google Scholar]
  124. 124. 
    Meeuwsen JAL, van Duijvenvoorde A, Gohar A, Kozma MO, van de Weg SM et al. 2017. High levels of (un)switched memory B cells are associated with better outcome in patients with advanced atherosclerotic disease. J. Am. Heart Assoc. 6:e005747
    [Google Scholar]
  125. 125. 
    Mantani PT, Ljungcrantz I, Andersson L, Alm R, Hedblad B et al. 2014. Circulating CD40+ and CD86+ B cell subsets demonstrate opposing associations with risk of stroke. Arterioscler. Thromb. Vasc. Biol. 34:211–18
    [Google Scholar]
  126. 126. 
    Kyaw T, Tipping P, Bobik A, Toh BH 2017. Opposing roles of B lymphocyte subsets in atherosclerosis. Autoimmunity 50:52–56
    [Google Scholar]
/content/journals/10.1146/annurev-immunol-042617-053104
Loading
/content/journals/10.1146/annurev-immunol-042617-053104
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error