Toll-like Receptor 7-Dependent Loss of B Cell Tolerance in Pathogenic Autoantibody Knockin Mice

Immunity

Volumn 25, Issue 3, 2006, Pages 429-440

  Berland, Robert ^a   Fernandez, Luis ^a   Kari, Elina ^a   Han, Jin Hwan ^a   Lomakin, Ina ^b   Akira, Shizuo ^c   Wortis, Henry H ^a   Kearney, John F ^d   Ucci, Angelo A ^b   Imanishi Kari, Thereza ^a  

^a TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Tufts NEMCH ^*  (United States)

^c OSAKA UNIVERSITY   (Japan)

^d University of Alabama at Birmingham   (United States)

Author keywords

CELLIMMUNO; HUMDISEASE; MOLIMMUNO

Indexed keywords

ANTIGEN; AUTOANTIBODY; IMMUNOGLOBULIN; RNA; SINGLE STRANDED DNA; TOLL LIKE RECEPTOR 7;

ANIMAL CELL; ANIMAL MODEL; ANTIBODY PRODUCTION; ARTICLE; B LYMPHOCYTE; CLONAL ANERGY; CONTROLLED STUDY; GENE; GENE LOCUS; GENE TARGETING; HEAVY CHAIN; IMMUNOLOGICAL TOLERANCE; IMMUNOREGULATION; KIDNEY DISEASE; LIGHT CHAIN; MOLECULAR RECOGNITION; MOUSE; MOUSE STRAIN; NONHUMAN; NUCLEOSOME; PRIORITY JOURNAL; PROTEIN EXPRESSION; SYSTEMIC LUPUS ERYTHEMATOSUS;

ANIMALS; AUTOANTIBODIES; B-LYMPHOCYTES; CELL LINE, TUMOR; FEMALE; HUMANS; IMMUNE TOLERANCE; LUPUS ERYTHEMATOSUS, SYSTEMIC; MEMBRANE GLYCOPROTEINS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; TOLL-LIKE RECEPTOR 7;

EID: 33748470505     PISSN: 10747613     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.immuni.2006.07.014     Document Type: Article

References (49)

1. Akira S., and Hemmi H. Recognition of pathogen-associated molecular patterns by TLR family. Immunol. Lett. 85 (2003) 85-95
2. Barton G.M., Kagan J.C., and Medzhitov R. Intracellular localization of Toll-like receptor 9 prevents recognition of self DNA but facilitates access to viral DNA. Nat. Immunol. 7 (2006) 49-56
3. Bolland S., Yim Y.S., Tus K., Wakeland E.K., and Ravetch J.V. Genetic modifiers of systemic lupus erythematosus in FcgammaRIIB(-/-) mice. J. Exp. Med. 195 (2002) 1167-1174
4. Boule M.W., Broughton C., Mackay F., Akira S., Marshak-Rothstein A., and Rifkin I.R. Toll-like receptor 9-dependent and -independent dendritic cell activation by chromatin-immunoglobulin G complexes. J. Exp. Med. 199 (2004) 1631-1640
5. Bygrave A.E., Rose K.L., Cortes-Hernandez J., Warren J., Rigby R.J., Cook H.T., Walport M.J., Vyse T.J., and Botto M. Spontaneous autoimmunity in 129 and C57BL/6 mice-implications for autoimmunity described in gene-targeted mice. PLoS Biol. 2 (2004) E243 10.1371/journal.pbio.0020243
6. Casellas R., Shih T.A., Kleinewietfeld M., Rakonjac J., Nemazee D., Rajewsky K., and Nussenzweig M.C. Contribution of receptor editing to the antibody repertoire. Science 291 (2001) 1541-1544
7. Chen C., Prak E.L., and Weigert M. Editing disease-associated autoantibodies. Immunity 6 (1997) 97-105
8. Christensen S.R., Kashgarian M., Alexopoulou L., Flavell R.A., Akira S., and Shlomchik M.J. Toll-like receptor 9 controls anti-DNA autoantibody production in murine lupus. J. Exp. Med. 202 (2005) 321-331
9. Cyster J.G., Hartley S.B., and Goodnow C.C. Competition for follicular niches excludes self-reactive cells from the recirculating B-cell repertoire. Nature 371 (1994) 389-395
10. Diebold S.S., Kaisho T., Hemmi H., Akira S., and Reis e Sousa C. Innate antiviral responses by means of TLR7-mediated recognition of single-stranded RNA. Science 303 (2004) 1529-1531
11. Ehlers M., Fukuyama H., McGaha T.L., Aderem A., and Ravetch J.V. TLR9/MyD88 signaling is required for class switching to pathogenic IgG2a and 2b autoantibodies in SLE. J. Exp. Med. 203 (2006) 553-561
12. Fernandez, L.P.J. (2001). B cell tolerance to nucleosomes in normal mice and its breakdown in autoimmune-prone mice. PhD thesis, Tufts University, Somerville, Massachusetts.
13. Fields M.L., and Erikson J. The regulation of lupus-associated autoantibodies: immunoglobulin transgenic models. Curr. Opin. Immunol. 15 (2003) 709-717
14. Fukuyama H., Nimmerjahn F., and Ravetch J.V. The inhibitory Fcgamma receptor modulates autoimmunity by limiting the accumulation of immunoglobulin G+ anti-DNA plasma cells. Nat. Immunol. 6 (2005) 99-106
15. Gauld S.B., Benschop R.J., Merrell K.T., and Cambier J.C. Maintenance of B cell anergy requires constant antigen receptor occupancy and signaling. Nat. Immunol. 6 (2005) 1160-1167
16. Gavalchin J., and Datta S.K. The NZB X SWR model of lupus nephritis. II. Autoantibodies deposited in renal lesions show a distinctive and restricted idiotypic diversity. J. Immunol. 138 (1987) 138-148
17. Gavalchin J., Seder R.A., and Datta S.K. The NZB X SWR model of lupus nephritis. I. Cross-reactive idiotypes of monoclonal anti-DNA antibodies in relation to antigenic specificity, charge, and allotype. Identification of interconnected idiotype families inherited from the normal SWR and the autoimmune NZB parents. J. Immunol. 138 (1987) 128-137
18. Gerth A.J., Lin L., and Peng S.L. T-bet regulates T-independent IgG2a class switching. Int. Immunol. 15 (2003) 937-944
19. Goodnow C.C., Sprent J., Fazekas de St Groth B., and Vinuesa C.G. Cellular and genetic mechanisms of self tolerance and autoimmunity. Nature 435 (2005) 590-597
20. Healy J.I., Dolmetsch R.E., Timmerman L.A., Cyster J.G., Thomas M.L., Crabtree G.R., Lewis R.S., and Goodnow C.C. Different nuclear signals are activated by the B cell receptor during positive versus negative signaling. Immunity 6 (1997) 419-428
21. Heil F., Ahmad-Nejad P., Hemmi H., Hochrein H., Ampenberger F., Gellert T., Dietrich H., Lipford G., Takeda K., Akira S., et al. The Toll-like receptor 7 (TLR7)-specific stimulus loxoribine uncovers a strong relationship within the TLR7, 8 and 9 subfamily. Eur. J. Immunol. 33 (2003) 2987-2997
22. Heil F., Hemmi H., Hochrein H., Ampenberger F., Kirschning C., Akira S., Lipford G., Wagner H., and Bauer S. Species-specific recognition of single-stranded RNA via toll-like receptor 7 and 8. Science 303 (2004) 1526-1529
23. Hemmi H., Takeuchi O., Kawai T., Kaisho T., Sato S., Sanjo H., Matsumoto M., Hoshino K., Wagner H., Takeda K., and Akira S. A Toll-like receptor recognizes bacterial DNA. Nature 408 (2000) 740-745
24. Hemmi H., Kaisho T., Takeuchi O., Sato S., Sanjo H., Hoshino K., Horiuchi T., Tomizawa H., Takeda K., and Akira S. Small anti-viral compounds activate immune cells via the TLR7 MyD88-dependent signaling pathway. Nat. Immunol. 3 (2002) 196-200
25. Hippen K.L., Tze L.E., and Behrens T.W. CD5 maintains tolerance in anergic B cells. J. Exp. Med. 191 (2000) 883-890
26. Lau C.M., Broughton C., Tabor A.S., Akira S., Flavell R.A., Mamula M.J., Christensen S.R., Shlomchik M.J., Viglianti G.A., Rifkin I.R., and Marshak-Rothstein A. RNA-associated autoantigens activate B cells by combined B cell antigen receptor/Toll-like receptor 7 engagement. J. Exp. Med. 202 (2005) 1171-1177
27. Leadbetter E.A., Rifkin I.R., Hohlbaum A.M., Beaudette B.C., Shlomchik M.J., and Marshak-Rothstein A. Chromatin-IgG complexes activate B cells by dual engagement of IgM and Toll-like receptors. Nature 416 (2002) 603-607
28. Li Y., Li H., Ni D., and Weigert M. Anti-DNA B cells in MRL/lpr mice show altered differentiation and editing pattern. J. Exp. Med. 196 (2002) 1543-1552
29. Lin L., Gerth A.J., and Peng S.L. CpG DNA redirects class-switching towards "Th1-like" Ig isotype production via TLR9 and MyD88. Eur. J. Immunol. 34 (2004) 1483-1487
30. Liu N., Ohnishi N., Ni L., Akira S., and Bacon K.B. CpG directly induces T-bet expression and inhibits IgG1 and IgE switching in B cells. Nat. Immunol. 4 (2003) 687-693
31. Liu S., Velez M.G., Humann J., Rowland S., Conrad F.J., Halverson R., Torres R.M., and Pelanda R. Receptor editing can lead to allelic inclusion and development of B cells that retain antibodies reacting with high avidity autoantigens. J. Immunol. 175 (2005) 5067-5076
32. Mohan C., Adams S., Stanik V., and Datta S.K. Nucleosome: a major immunogen for pathogenic autoantibody-inducing T cells of lupus. J. Exp. Med. 177 (1993) 1367-1381
33. Murakami M., Tsubata T., Okamoto M., Shimizu A., Kumagai S., Imura H., and Honjo T. Antigen-induced apoptotic death of Ly-1 B cells responsible for autoimmune disease in transgenic mice. Nature 357 (1992) 77-80
34. Oliver A.M., Martin F., and Kearney J.F. IgMhighCD21high lymphocytes enriched in the splenic marginal zone generate effector cells more rapidly than the bulk of follicular B cells. J. Immunol. 162 (1999) 7198-7207
35. Peng S.L., Szabo S.J., and Glimcher L.H. T-bet regulates IgG class switching and pathogenic autoantibody production. Proc. Natl. Acad. Sci. USA 99 (2002) 5545-5550
36. Phan T.G., Amesbury M., Gardam S., Crosbie J., Hasbold J., Hodgkin P.D., Basten A., and Brink R. B cell receptor-independent stimuli trigger immunoglobulin (Ig) class switch recombination and production of IgG autoantibodies by anergic self-reactive B cells. J. Exp. Med. 197 (2003) 845-860
37. Qian Y., Santiago C., Borrero M., Tedder T.F., and Clarke S.H. Lupus-specific antiribonucleoprotein B cell tolerance in nonautoimmune mice is maintained by differentiation to B-1 and governed by B cell receptor signaling thresholds. J. Immunol. 166 (2001) 2412-2419
38. Radic M.Z., Mackle J., Erikson J., Mol C., Anderson W.F., and Weigert M. Residues that mediate DNA binding of autoimmune antibodies. J. Immunol. 150 (1993) 4966-4977
39. Rui L., Vinuesa C.G., Blasioli J., and Goodnow C.C. Resistance to CpG DNA-induced autoimmunity through tolerogenic B cell antigen receptor ERK signaling. Nat. Immunol. 4 (2003) 594-600
40. Szabo S.J., Kim S.T., Costa G.L., Zhang X., Fathman C.G., and Glimcher L.H. A novel transcription factor, T-bet, directs Th1 lineage commitment. Cell 100 (2000) 655-669
41. Takeda K., Kaisho T., and Akira S. Toll-like receptors. Annu. Rev. Immunol. 21 (2003) 335-376
42. Viglianti G.A., Lau C.M., Hanley T.M., Miko B.A., Shlomchik M.J., and Marshak-Rothstein A. Activation of autoreactive B cells by CpG dsDNA. Immunity 19 (2003) 837-847
43. Vlahakos D.V., Foster M.H., Adams S., Katz M., Ucci A.A., Barrett K.J., Datta S.K., and Madaio M.P. Anti-DNA antibodies form immune deposits at distinct glomerular and vascular sites. Kidney Int. 41 (1992) 1690-1700
44. Vollmer J., Tluk S., Schmitz C., Hamm S., Jurk M., Forsbach A., Akira S., Kelly K.M., Reeves W.H., Bauer S., and Krieg A.M. Immune stimulation mediated by autoantigen binding sites within small nuclear RNAs involves Toll-like receptors 7 and 8. J. Exp. Med. 202 (2005) 1575-1585
45. Wakeland E., Morel L., Achey K., Yui M., and Longmate J. Speed congenics: a classic technique in the fast lane (relatively speaking). Immunol. Today 18 (1997) 472-477
46. Wardemann H., Yurasov S., Schaefer A., Young J.W., Meffre E., and Nussenzweig M.C. Predominant autoantibody production by early human B cell precursors. Science 301 (2003) 1374-1377
47. Wu X., and Peng S.L. Toll-like receptor 9 signaling protects against murine lupus. Arthritis Rheum. 54 (2006) 336-342
48. Xu H., Li H., Suri-Payer E., Hardy R.R., and Weigert M. Regulation of anti-DNA B cells in recombination-activating gene-deficient mice. J. Exp. Med. 188 (1998) 1247-1254
49. Yachimovich N., Mostoslavsky G., Yarkoni Y., Verbovetski I., and Eilat D. The efficiency of B cell receptor (BCR) editing is dependent on BCR light chain rearrangement status. Eur. J. Immunol. 32 (2002) 1164-1174