Contribution of IRF5 in B cells to the development of murine SLE-like disease through its transcriptional control of the IgG2a locus

Proceedings of the National Academy of Sciences of the United States of America

Volumn 107, Issue 22, 2010, Pages 10154-10159

  Savitsky, David A ^a,b   Yanai, Hideyuki ^a,b   Tamura, Tomohiko ^a,c   Taniguchi, Tadatsugu ^a,b   Honda, Kenya ^a,b  

^a UNIVERSITY OF TOKYO   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^c YOKOHAMA CITY UNIVERSITY   (Japan)

Author keywords

Autoimmunity; B lymphocytes; TLR signaling

Indexed keywords

ANTINUCLEAR ANTIBODY; COLLAGEN; IMMUNOGLOBULIN G2A; IMMUNOGLOBULIN G2B; INTERFERON REGULATORY FACTOR 5; PRISTANE; TOLL LIKE RECEPTOR 9;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY PRODUCTION; ANTIBODY RESPONSE; ARTHRITIS; ARTICLE; AUTOIMMUNITY; B LYMPHOCYTE; CELL ACTIVATION; DISEASE COURSE; FEMALE; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; SYSTEMIC LUPUS ERYTHEMATOSUS;

ANIMALS; ARTHRITIS, EXPERIMENTAL; AUTOANTIBODIES; B-LYMPHOCYTES; DISEASE MODELS, ANIMAL; FEMALE; HUMANS; IMMUNITY, INNATE; IMMUNOGLOBULIN G; INTERFERON REGULATORY FACTORS; LUPUS ERYTHEMATOSUS, SYSTEMIC; LYMPHOCYTE ACTIVATION; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; TOLL-LIKE RECEPTOR 9; TRANSCRIPTION, GENETIC;

MURINAE; MUS;

EID: 77953368347     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1005599107     Document Type: Article

References (52)

1. Martin F, Chan AC (2004) Pathogenic roles of B cells in human autoimmunity; insights from the clinic. Immunity 20:517-527. (Pubitemid 38638122)
2. Anolik JH (2007) B cell biology and dysfunction in SLE. Bull NYU Hosp Jt Dis 65:182-186.
3. Bhat P, Radhakrishnan J (2008) B lymphocytes and lupus nephritis: New insights into pathogenesis and targeted therapies. Kidney Int 73:261-268.
4. Blanco F, et al. (1992) IgG subclasses in systemic lupus erythematosus and other autoimmune rheumatic diseases. Lupus 1:391-399.
5. Manolova I, Dancheva M, Halacheva K (2002) Predominance of IgG1 and IgG3 subclasses of autoantibodies to neutrophil cytoplasmic antigens in patients with systemic lupus erythematosus. Rheumatol Int 21:227-233. (Pubitemid 34328057)
6. Tiikkainen U, Wangel A, Appleton SL, Arthur D (1991) Subclasses of IgG anticardiolipin antibodies in patients with systemic lupus erythematosus. Scand J Immunol 34:265-271.
7. Yung S, Chan TM (2008) Anti-DNA antibodies in the pathogenesis of lupus nephritis - The emerging mechanisms. Autoimmun Rev 7:317-321.
8. Coutelier JP, van der Logt JT, Heessen FW, Warnier G, Van Snick J (1987) IgG2a restriction of murine antibodies elicited by viral infections. J Exp Med 165:64-69.
9. Kipps TJ, Parham P, Punt J, Herzenberg LA (1985) Importance of immunoglobulin isotype in human antibody-dependent, cell-mediated cytotoxicity directed by murine monoclonal antibodies. J Exp Med 161:1-17. (Pubitemid 15169717)
10. Nimmerjahn F, Ravetch JV (2005) Divergent immunoglobulin G subclass activity through selective Fc receptor binding. Science 310:1510-1512. (Pubitemid 41746349)
11. Fossati-Jimack L, et al. (2000) Markedly different pathogenicity of four immunoglobulin G isotype-switch variants of an antierythrocyte autoantibody is based on their capacity to interact in vivo with the low-affinity Fcγ receptor III. J Exp Med 191:1293-1302. (Pubitemid 30227118)
12. Nimmerjahn F, Ravetch JV (2006) Fcγ receptors: Old friends and new family members. Immunity 24:19-28. (Pubitemid 43077197)
13. Liu N, Ohnishi N, Ni L, Akira S, Bacon KB (2003) CpG directly induces T-bet expression and inhibits IgG1 and IgE switching in B cells. Nat Immunol 4:687-693. (Pubitemid 36874446)
14. Peng SL, Szabo SJ, Glimcher LH (2002) T-bet regulates IgG class switching and pathogenic autoantibody production. Proc Natl Acad Sci USA 99:5545-5550.
15. Xu W, Zhang JJ (2005) Stat1-dependent synergistic activation of T-bet for IgG2a production during early stage of B cell activation. J Immunol 175:7419-7424. (Pubitemid 41713439)
16. Thibault DL, et al. (2008) IRF9 and STAT1 are required for IgG autoantibody production and B cell expression of TLR7 in mice. J Clin Invest 118:1417-1426.
17. Barnes BJ, Moore PA, Pitha PM (2001) Virus-specific activation of a novel interferon regulatory factor, IRF-5, results in the induction of distinct interferon α genes. J Biol Chem 276:23382-23390. (Pubitemid 37410722)
18. Takaoka A, et al. (2005) Integral role of IRF-5 in the gene induction programme activated by Toll-like receptors. Nature 434:243-249. (Pubitemid 40388058)
19. Sigurdsson S, et al. (2005) Polymorphisms in the tyrosine kinase 2 and interferon regulatory factor 5 genes are associated with systemic lupus erythematosus. Am J Hum Genet 76:528-537. (Pubitemid 40250533)
20. Graham RR, et al.; Argentine and Spanish Collaborative Groups (2006) A common haplotype of interferon regulatory factor 5 (IRF5) regulates splicing and expression and is associated with increased risk of systemic lupus erythematosus. Nat Genet 38:550-555.
21. Kyogoku C, Tsuchiya N (2007) A compass that points to lupus: Genetic studies on type I interferon pathway. Genes Immun 8:445-455. (Pubitemid 47365611)
22. Kozyrev SV, Alarcon-Riquelme ME (2007) The genetics and biology of Irf5-mediated signaling in lupus. Autoimmunity 40:591-601. (Pubitemid 350302184)
23. Marshak-Rothstein A (2006) Toll-like receptors in systemic autoimmune disease. Nat Rev Immunol 6:823-835. (Pubitemid 44631651)
24. Christensen SR, et al. (2006) Toll-like receptor 7 and TLR9 dictate autoantibody specificity and have opposing inflammatory and regulatory roles in a murine model of lupus. Immunity 25:417-428.
25. Ehlers M, Ravetch JV (2007) Opposing effects of Toll-like receptor stimulation induce autoimmunity or tolerance. Trends Immunol 28:74-79. (Pubitemid 46176735)
26. -/- mouse models of systemic lupus erythematosus. J Immunol 184:796-806.
27. Yasuda K, et al. (2007) Murine dendritic cell type I IFN production induced by human IgG-RNA immune complexes is IFN regulatory factor (IRF)5 and IRF7 dependent and is required for IL-6 production. J Immunol 178:6876-6885. (Pubitemid 46847413)
28. Lien C, et al. (2010) Critical role of IRF-5 in regulation of B-cell differentiation. Proc Natl Acad Sci USA 107:4664-4668.
29. Satoh M, Reeves WH (1994) Induction of lupus-associated autoantibodies in BALB/c mice by intraperitoneal injection of pristane. J Exp Med 180:2341-2346. (Pubitemid 24351616)
30. Christensen SR, et al. (2005) Toll-like receptor 9 controls anti-DNA autoantibody production in murine lupus. J Exp Med 202:321-331.
31. Pisitkun P, et al. (2006) Autoreactive B cell responses to RNA-related antigens due to TLR7 gene duplication. Science 312:1669-1672. (Pubitemid 43902669)
32. Ehlers M, Fukuyama H, McGaha TL, Aderem A, Ravetch JV (2006) TLR9/MyD88 signaling is required for class switching to pathogenic IgG2a and 2b autoantibodies in SLE. J Exp Med 203:553-561.
33. De Gregorio E, D'Oro U, Wack A (2009) Immunology of TLR-independent vaccine adjuvants. Curr Opin Immunol 21:339-345.
34. Sciammas R, et al. (2006) Graded expression of interferon regulatory factor-4 coordinates isotype switching with plasma cell differentiation. Immunity 25:225-236. (Pubitemid 44224149)
35. Oganesyan G, et al. (2008) IRF3-dependent type I interferon response in B cells regulates CpG-mediated antibody production. J Biol Chem 283:802-808.
36. Chan OT, Hannum LG, Haberman AM, Madaio MP, Shlomchik MJ (1999) A novel mouse with B cells but lacking serum antibody reveals an antibody-independent role for B cells in murine lupus. J Exp Med 189:1639-1648.
37. Richards HB, et al. (1998) Interleukin 6 dependence of anti-DNA antibody production: Evidence for two pathways of autoantibody formation in pristane-induced lupus. J Exp Med 188:985-990.
38. Fujii Y, et al. (1999) Crystal structure of an IRF-DNA complex reveals novel DNA recognition and cooperative binding to a tandem repeat of core sequences. EMBO J 18:5028-5041. (Pubitemid 29443805)
39. Peng SL, Li J, Lin L, Gerth A (2003) The role of T-bet in B cells. Nat Immunol 4:1041, author reply 1041.
40. Inglis JJ, et al. (2007) Collagen-induced arthritis in C57BL/6 mice is associated with a robust and sustained T-cell response to type II collagen. Arthritis Res Ther 9:R113.
41. Ma Y, et al. (2004) Fas ligation on macrophages enhances IL-1R1-Toll-like receptor 4 signaling and promotes chronic inflammation. Nat Immunol 5:380-387. (Pubitemid 38500086)
42. Lau CM, et al. (2005) RNA-associated autoantigens activate B cells by combined B cell antigen receptor/Toll-like receptor 7 engagement. J Exp Med 202:1171-1177.
43. Gavin AL, et al. (2006) Adjuvant-enhanced antibody responses in the absence of Toll-like receptor signaling. Science 314:1936-1938.
44. Palm NW, Medzhitov R (2009) Pattern recognition receptors and control of adaptive immunity. Immunol Rev 227:221-233.
45. Pullen SS, Dang TT, Crute JJ, Kehry MR (1999) CD40 signaling through tumor necrosis factor receptor-associated factors (TRAFs). Binding site specificity and activation of downstream pathways by distinct TRAFs. J Biol Chem 274:14246-14254. (Pubitemid 129518736)
46. Christensen SR, Shlomchik MJ (2007) Regulation of lupus-related autoantibody production and clinical disease by Toll-like receptors. Semin Immunol 19:11-23. (Pubitemid 46498753)
47. Banchereau J, Pascual V, Palucka AK (2004) Autoimmunity through cytokine-induced dendritic cell activation. Immunity 20:539-550. (Pubitemid 38638124)
48. Amoura Z, et al. (2000) Presence of antinucleosome autoantibodies in a restricted set of connective tissue diseases: Antinucleosome antibodies of the IgG3 subclass are markers of renal pathogenicity in systemic lupus erythematosus. Arthritis Rheum 43:76-84. (Pubitemid 30368215)
49. Lin GG, Li JM (2009) IgG subclass serum levels in systemic lupus erythematosus patients. Clin Rheumatol 28:1315-1318.
50. Hartmann G, Krieg AM (2000) Mechanism and function of a newly identified CpG DNA motif in human primary B cells. J Immunol 164:944-953. (Pubitemid 30043721)
51. Khachigian LM (2006) Collagen antibody-induced arthritis. Nat Protoc 1:2512-2516.
52. Collins JT, Dunnick WA (1993) Germline transcripts of the murine immunoglobulin γ 2a gene: Structure and induction by IFN-γ. Int Immunol 5:885-891.