B1a B lymphocytes are atheroprotective by secreting natural IgM that increases IgM deposits and reduces necrotic cores in atherosclerotic lesions

Circulation Research

Volumn 109, Issue 8, 2011, Pages 830-840

  Kyaw, Tin ^a,b   Tay, Christopher ^a,b   Krishnamurthi, Surendran ^a,b,c   Kanellakis, Peter ^a   Agrotis, Alex ^a,d   Tipping, Peter ^b   Bobik, Alex ^a   Toh, Ban Hock ^b  

^a BAKER IDI HEART AND DIABETES INSTITUTE   (Australia)

^b MONASH UNIVERSITY   (Australia)

^c Quality Control Lonza Bioscience Singapore Pte Ltd   (Singapore)

^d MONASH UNIVERSITY   (Australia)

Author keywords

apoptosis; B lymphocytes; immunoglobulin M; inflammation; splenectomy

Indexed keywords

APOLIPOPROTEIN E; COLLAGEN; IMMUNOGLOBULIN M; LOW DENSITY LIPOPROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; ATHEROSCLEROSIS; B LYMPHOCYTE; BODY WEIGHT; CELL POPULATION; CONTROLLED STUDY; HEART PROTECTION; LIPID BLOOD LEVEL; LYMPHOCYTE; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; SPLENECTOMY;

ANIMALS; ATHEROSCLEROSIS; B-LYMPHOCYTE SUBSETS; IMMUNOGLOBULIN M; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NECROSIS; SPLENECTOMY; TUNICA INTIMA;

EID: 80053574700     PISSN: 00097330     EISSN: 15244571     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.111.248542     Document Type: Article

References (37)

1. 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;193:263-269. (Pubitemid 32118139)
2. 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. 1994;14:32-40.
3. Zhou X, Hansson GK. Detection of B cells and proinflammatory cytokines in atherosclerotic plaques of hypercholesterolaemic apolipoprotein E knockout mice. Scand J Immunol. 1999;50:25-30. (Pubitemid 29298023)
4. Galkina E, Ley K. Immune and inflammatory mechanisms of atherosclerosis (*). Annu Rev Immunol. 2009;27:165-197.
5. Caligiuri G, Nicoletti A, Poirier B, Hansson GK. Protective immunity against atherosclerosis carried by B cells of hypercholesterolemic mice. J Clin Invest. 2002;109:745-753. (Pubitemid 34263151)
6. Major AS, Fazio S, Linton MF. B-lymphocyte deficiency increases atherosclerosis in LDL receptor-null mice. Arterioscler Thromb Vasc Biol. 2002; 22:1892-1898. (Pubitemid 35315778)
7. Kyaw T, Tay C, Khan A, Dumouchel V, Cao A, To K, Kehry M, Dunn R, Agrotis A, Tipping P, Bobik A, Toh BH. Conventional B2 B cell depletion ameliorates whereas its adoptive transfer aggravates atherosclerosis. J Immunol. 2010;185:4410-4419.
8. Ait-Oufella H, Herbin O, Bouaziz JD, Binder CJ, Uyttenhove C, Laurans L, Taleb S, Van Vre E, Esposito B, Vilar J, Sirvent J, Van Snick J, Tedgui A, Tedder TF, Mallat Z. B cell depletion reduces the development of atherosclerosis in mice. J Exp Med. 2010;207:1579-1587.
9. Robinette CD, Fraumeni JF Jr. Splenectomy and subsequent mortality in veterans of the 1939-45 war. Lancet. 1977;2:127-129. (Pubitemid 8124956)
10. Asai K, Kuzuya M, Naito M, Funaki C, Kuzuya F. Effects of splenectomy on serum lipids and experimental atherosclerosis. Angiology. 1988;39:497-504.
11. Shapiro S. The influence of thyroidectomy, splenectomy, gonadectomy, and suprarenalectomy upon the development of experimental atherosclerosis in rabbits. J Exp Med. 1927;45:595-607.
12. Wardemann H, Boehm T, Dear N, Carsetti R. B-1a B cells that link the innate and adaptive immune responses are lacking in the absence of the spleen. J Exp Med. 2002;195:771-780. (Pubitemid 34259721)
13. Baumgarth N, Tung JW, Herzenberg LA. Inherent specificities in natural antibodies: a key to immune defense against pathogen invasion. Springer Semin Immunopathol. 2005;26:347-362. (Pubitemid 40468889)
14. Lewis MJ, Malik TH, Ehrenstein MR, Boyle JJ, Botto M, Haskard DO. Immunoglobulin M is required for protection against atherosclerosis in lowdensity lipoprotein receptor-deficient mice. Circulation. 2009;120:417-426.
15. Thorp E, Cui D, Schrijvers DM, Kuriakose G, Tabas I. Mertk receptor mutation reduces efferocytosis efficiency and promotes apoptotic cell accumulation and plaque necrosis in atherosclerotic lesions of apoe-/-mice. Arterioscler Thromb Vasc Biol. 2008;28:1421-1428.
16. 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;101:1717-1725. (Pubitemid 28198502)
17. Akan AA, Sengul N, Simsek S, Demirer S. The effects of splenectomy and splenic autotransplantation on plasma lipid levels. J Invest Surg. 2008;21: 369-372.
18. Sathish JG, Walters J, Luo JC, Johnson KG, Leroy FG, Brennan P, Kim KP, Gygi SP, Neel BG, Matthews RJ. CD22 is a functional ligand for SH2 domain-containing protein-tyrosine phosphatase-1 in primary T cells. J Biol Chem. 2004;279:47783-47791. (Pubitemid 39540927)
19. Shaw PX, Horkko S, Chang MK, Curtiss LK, Palinski W, Silverman GJ, Witztum JL. Natural antibodies with the T15 idiotype may act in atherosclerosis, apoptotic clearance, and protective immunity. J Clin Invest. 2000;105: 1731-1740. (Pubitemid 30421754)
20. Boes M, Esau C, Fischer MB, Schmidt T, Carroll M, Chen J. Enhanced B-1 cell development, but impaired IgG antibody responses in mice deficient in secreted IgM. J Immunol. 1998;160:4776-4787. (Pubitemid 28215311)
21. Ehrenstein MR, Notley CA. The importance of natural IgM: scavenger, protector and regulator. Nat Rev Immunol. 2010;10:778-786.
22. Chou MY, Fogelstrand L, Hartvigsen K, Hansen LF, Woelkers D, Shaw PX, Choi J, Perkmann T, Backhed F, Miller YI, Horkko S, Corr M, Witztum JL, Binder CJ. Oxidation-specific epitopes are dominant targets of innate natural antibodies in mice and humans. J Clin Invest. 2009;119:1335-1349.
23. Hayakawa K, Hardy RR, Herzenberg LA. Progenitors for Ly-1 B cells are distinct from progenitors for other B cells. J Exp Med. 1985;161:1554-1568. (Pubitemid 15046047)
24. Martin F, Kearney JF. B1 cells: similarities and differences with other B cell subsets. Curr Opin Immunol. 2001;13:195-201. (Pubitemid 32176039)
25. Choi YS, Baumgarth N. Dual role for B-1a cells in immunity to influenza virus infection. J Exp Med. 2008;205:3053-3064.
26. Martin F, Oliver AM, Kearney JF. Marginal zone and B1 B cells unite in the early response against T-independent blood-borne particulate antigens. Immunity. 2001;14:617-629. (Pubitemid 32520872)
27. Coutinho A, Kazatchkine MD, Avrameas S. Natural autoantibodies. Curr Opin Immunol. 1995;7:812-818. (Pubitemid 26038522)
28. Haury M, Sundblad A, Grandien A, Barreau C, Coutinho A, Nobrega A. The repertoire of serum IgM in normal mice is largely independent of external antigenic contact. Eur J Immunol. 1997;27:1557-1563. (Pubitemid 27254850)
29. Baumgarth N, Herman OC, Jager GC, Brown LE, Herzenberg LA, Chen J. B-1 and B-2 cell-derived immunoglobulin M antibodies are nonredundant components of the protective response to influenza virus infection. J Exp Med. 2000;192:271-280. (Pubitemid 30470309)
30. Binder CJ, Horkko S, Dewan A, Chang MK, Kieu EP, Goodyear CS, Shaw PX, Palinski W, Witztum JL, Silverman GJ. Pneumococcal vaccination decreases atherosclerotic lesion formation: molecular mimicry between Streptococcus pneumoniae and oxidized LDL. Nat Med. 2003;9:736-743. (Pubitemid 36749223)
31. Binder CJ, Shaw PX, Chang MK, Boullier A, Hartvigsen K, Horkko S, Miller YI, Woelkers DA, Corr M, Witztum JL. The role of natural antibodies in atherogenesis. J Lipid Res. 2005;46:1353-1363. (Pubitemid 43109798)
32. Hartvigsen K, Chou MY, Hansen LF, Shaw PX, Tsimikas S, Binder CJ, Witztum JL. The role of innate immunity in atherogenesis. J Lipid Res. 2009;50(suppl):S388-S393.
33. Horkko S, Bird DA, Miller E, Itabe H, Leitinger N, Subbanagounder G, Berliner JA, Friedman P, Dennis EA, Curtiss LK, Palinski W, Witztum JL. Monoclonal autoantibodies specific for oxidized phospholipids or oxidized phospholipid-protein adducts inhibit macrophage uptake of oxidized lowdensity lipoproteins. J Clin Invest. 1999;103:117-128. (Pubitemid 29031170)
34. Shaw PX, Horkko S, Tsimikas S, Chang MK, Palinski W, Silverman GJ, Chen PP, Witztum JL. 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;21:1333-1339. (Pubitemid 34219841)
35. Vieira P, Rajewsky K. The half-lives of serum immunoglobulins in adult mice. Eur J Immunol. 1988;18:313-316. (Pubitemid 18078861)
36. Townsend MJ, Monroe JG, Chan AC. B-cell targeted therapies in human autoimmune diseases: an updated perspective. Immunol Rev. 2010;237: 264-283.
37. Hansson GK, Nilsson J. Vaccination against atherosclerosis? Induction of atheroprotective immunity. Semin Immunopathol. 2009;31:95-101.