A novel subpopulation of B-1 cells is enriched with autoreactivity in normal and lupus-prone mice

Arthritis and Rheumatism

Volumn 60, Issue 12, 2009, Pages 3734-3743

  Zhong, Xuemei ^a   Lau, Stanley ^a   Bai, Chunyan ^a   Degauque, Nicolas ^b   Holodick, Nichol E ^d   Steven, Scott J ^e   Tumang, Joseph ^c,d   Gao, Wenda ^b   Rothstein, Thomas L ^d  

^a BOSTON UNIVERSITY MEDICAL CENTER   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c EMD Serono Research Center   (United States)

^d FEINSTEIN INSTITUTE FOR MEDICAL RESEARCH   (United States)

^e BOSTON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

6 CARBOXYFLUORESCEIN; ANTINUCLEAR ANTIBODY; AUTOANTIGEN; CD5 ANTIGEN; DOUBLE STRANDED DNA ANTIBODY; IMMUNOGLOBULIN CLASS; IMMUNOGLOBULIN G1; IMMUNOGLOBULIN G2B; INTERLEUKIN 21; THYMIDINE;

ANIMAL CELL; ANTIBODY PRODUCTION; ANTIBODY TITER; ANTIGEN PRESENTATION; ANTIGEN PRESENTING CELL; ARTICLE; AUTOIMMUNITY; B LYMPHOCYTE; CELL PROLIFERATION; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; LUPUS ERYTHEMATOSUS; LYMPHOCYTE DIFFERENTIATION; LYMPHOCYTE SUBPOPULATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; TH17 CELL;

ANIMALS; ANTIBODIES, ANTINUCLEAR; ANTIGENS, CD5; AUTOIMMUNITY; B-LYMPHOCYTES; CELL PROLIFERATION; DISEASE MODELS, ANIMAL; DNA; HYBRIDOMAS; IMMUNOGLOBULIN CLASS SWITCHING; IMMUNOGLOBULIN G; INTERLEUKINS; LUPUS ERYTHEMATOSUS, SYSTEMIC; MICE; MICE, INBRED BALB C; PEPTIDES;

EID: 73249130668     PISSN: 00043591     EISSN: 15290131     Source Type: Journal    
DOI: 10.1002/art.25015     Document Type: Article

References (38)

1. Boes M, Prodeus AP, Schmidt T, Carroll MC, Chen J. A critical role of natural immunoglobulin M in immediate defense against systemic bacterial infection. J Exp Med 1998;188:2381-6.
2. 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;14:617-29.
3. Forster I, Gu H, Muller W, Schmitt M, Tarlinton D, Rajewsky K. CD5 B cells in the mouse. Curr Top Microbiol Immunol 1991;173: 247-51.
4. Fagarasan S, Honjo T. T-independent immune response: new aspects of B cell biology. Science 2000;290:89-92.
5. Casali P, Burastero SE, Nakamura M, Inghirami G, Notkins AL. Human lymphocytes making rheumatoid factor and antibody to ssDNA belong to Leu-1+ B-cell subset. Science 1987;236:77-81.
6. Hardy RR, Hayakawa K, Shimizu M, Yamasaki K, Kishimoto T. Rheumatoid factor secretion from human Leu-1+ B cells. Science 1987;236:81-3.
7. Becker H, Weber C, Storch S, Federlin K. Relationship between CD5+ B lymphocytes and the activity of systemic autoimmunity. Clin Immunol Immunopathol 1990;56:219-25.
8. Kanno K, Okada T, Abe M, Hirose S, Shirai T. CD5+ B cells as precursors of CD5- IgG anti-DNA antibody-producing B cells in autoimmune-prone NZB/W F1 mice. Ann N Y Acad Sci 1992;651: 576-8.
9. Reap EA, Sobel ES, Cohen PL, Eisenberg RA. The role of CD5+ B cells in the production of autoantibodies in murine systemic lupus erythematosus. Ann N Y Acad Sci 1992;651:588-90.
10. Ishikawa S, Matsushima K. Aberrant B1 cell trafficking in a murine model for lupus. Front Biosci 2007;12:1790-803.
11. Youinou P, Renaudineau Y. The paradox of CD5-expressing B cells in systemic lupus erythematosus. Autoimmun Rev 2007;7: 149-54.
12. Keir ME, Butte MJ, Freeman GJ, Sharpe AH. PD-1 and its ligands in tolerance and immunity. Annu Rev Immunol 2008;26:677-704.
13. Zhong X, Tumang JR, Gao W, Bai C, Rothstein TL. PD-L2 expression extends beyond dendritic cells/macrophages to B1 cells enriched for V(H)11/V(H)12 and phosphatidylcholine binding. Eur J Immunol 2007;37:2405-10.
14. Loke P, Allison JP. PD-L1 and PD-L2 are differentially regulated by Th1 and Th2 cells. Proc Natl Acad Sci U S A 2003;100:5336-41.
15. Gu T, Zhu YB, Chen C, Li M, Chen YJ, Yu GH, et al. Fine-tuned expression of programmed death 1 ligands in mature dendritic cells stimulated by CD40 ligand is critical for the induction of an efficient tumor specific immune response. Cell Mol Immunol 2008;5:33-9.
16. Francis DA, Karras JG, Ke XY, Sen R, Rothstein TL. Induction of the transcription factors NF-κ B, AP-1 and NF-AT during B cell stimulation through the CD40 receptor. Int Immunol 1995;7: 151-61.
17. Mercolino TJ, Arnold LW, Hawkins LA, Haughton G. Normal mouse peritoneum contains a large population of Ly-1+ (CD5) B cells that recognize phosphatidyl choline: relationship to cells that secrete hemolytic antibody specific for autologous erythrocytes. J Exp Med 1988;168:687-98.
18. Mercolino TJ, Locke AL, Afshari A, Sasser D, Travis WW, Arnold LW, et al. Restricted immunoglobulin variable region gene usage by normal Ly-1 (CD5+) B cells that recognize phosphatidyl choline. J Exp Med 1989;169:1869-77.
19. 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 1989;19:1289-95.
20. Mercolino TJ, Arnold LW, Haughton G. Phosphatidyl choline is recognized by a series of Ly-1+ murine B cell lymphomas specific for erythrocyte membranes. J Exp Med 1986;163:155-65.
21. Reininger L, Kaushik A, Izui S, Jaton JC. A member of a new VH gene family encodes antibromelinized mouse red blood cell autoantibodies. Eur J Immunol 1988;18:1521-6.
22. Cabral AR, Cabiedes J, Alarcon-Segovia D. Hemolytic anemia related to an IgM autoantibody to phosphatidylcholine that binds in vitro to stored and to bromelain-treated human erythrocytes. J Autoimmun 1990;3:773-87.
23. Zhou ZH, Zhang Y, Hu YF, Wahl LM, Cisar JO, Notkins AL. The broad antibacterial activity of the natural antibody repertoire is due to polyreactive antibodies. Cell Host Microbe 2007;1:51-61.
24. Zhong X, Gao W, Degauque N, Bai C, Lu Y, Kenny J, et al. Reciprocal generation of Th1/Th17 and T(reg) cells by B1 and B2 B cells. Eur J Immunol 2007;37:2400-4.
25. Laurence A, Tato CM, Davidson TS, Kanno Y, Chen Z, Yao Z, et al. Interleukin-2 signaling via STAT5 constrains T helper 17 cell generation. Immunity 2007;26:371-81.
26. Ito T, Ishikawa S, Sato T, Akadegawa K, Yurino H, Kitabatake M, et al. Defective B1 cell homing to the peritoneal cavity and preferential recruitment of B1 cells in the target organs in a murine model for systemic lupus erythematosus. J Immunol 2004;172:3628-34.
27. Thurnheer MC, Zuercher AW, Cebra JJ, Bos NA. B1 cells contribute to serum IgM, but not to intestinal IgA, production in gnotobiotic Ig allotype chimeric mice. J Immunol 2003;170:4564-71.
28. Tarlinton DM, McLean M, Nossal GJ. B1 and B2 cells differ in their potential to switch immunoglobulin isotype. Eur J Immunol 1995;25:3388-93.
29. Wofsy D, Chiang NY. Proliferation of Ly-1 B cells in autoimmune NZB and (NZB x NZW)F1 mice. Eur J Immunol 1987;17:809-14.
30. Xu Z, Duan B, Croker BP, Wakeland EK, Morel L. Genetic dissection of the murine lupus susceptibility locus Sle2: contributions to increased peritoneal B-1a cells and lupus nephritis map to different loci. J Immunol 2005;175:936-43.
31. Morbach H, Singh SK, Faber C, Lipsky PE, Girschick HJ. Analysis of RAG expression by peripheral blood CD5+ and CD5- B cells of patients with childhood systemic lupus erythematosus. Ann Rheum Dis 2006;65:482-7.
32. Bernstein KA, Valerio RD, Lefkowith JB. Glomerular binding activity in MRL lpr serum consists of antibodies that bind to a DNA/histone/type IV collagen complex. J Immunol 1995;154: 2424-33.
33. Faaber P, Rijke TP, van de Putte LB, Capel PJ, Berden JH. Cross-reactivity of human and murine anti-DNA antibodies with heparan sulfate: the major glycosaminoglycan in glomerular basement membranes. J Clin Invest 1986;77:1824-30.
34. Mostoslavsky G, Fischel R, Yachimovich N, Yarkoni Y, Rosenmann E, Monestier M, et al. Lupus anti-DNA autoantibodies cross-react with a glomerular structural protein: a case for tissue injury by molecular mimicry. Eur J Immunol 2001;31:1221-7.
35. Baudino L, Azeredo da Silveira S, Nakata M, Izui S. Molecular and cellular basis for pathogenicity of autoantibodies: lessons from murine monoclonal autoantibodies. Springer Semin Immunopathol 2006;28:175-84.
36. Bubier JA, Sproule TJ, Foreman O, Spolski R, Shaffer DJ, Morse HC 3rd, et al. A critical role for IL-21 receptor signaling in the pathogenesis of systemic lupus erythematosus in BXSB-Yaa mice. Proc Natl Acad Sci U S A 2009;106:1518-23.
37. Li QZ, Xie C, Wu T, Mackay M, Aranow C, Putterman C, et al. Identification of autoantibody clusters that best predict lupus disease activity using glomerular proteome arrays. J Clin Invest 2005;115:3428-39.
38. Markeljevic J, Batinic D, Uzarevic B, Bozikov J, Cikes N, Babic-Naglic D, et al. Peripheral blood CD5+ B cell subset in the remission phase of systemic connective tissue diseases. J Rheumatol 1994;21:2225-30.