TLR9 in peritoneal B-1b cells is essential for production of protective self-reactive IgM to control Th17 cells and severe autoimmunity

Journal of Immunology

Volumn 187, Issue 6, 2011, Pages 2953-2965

  Stoehr, Alexander D ^a   Schoen, Carolin T ^a   Mertes, Maria M M ^a   Eiglmeier, Susanne ^a   Holecska, Vivien ^a   Lorenz, Alexandra K ^a   Schommartz, Tim ^b   Schoen, Anna Lena ^b   Hess, Constanze ^a   Winkler, Andrë ^a   Wardemann, Hedda ^c   Ehlers, Marc ^a,b  

^a Leibniz Association   (Germany)

^b UNIVERSITY OF LÜBECK   (Germany)

^c MAX PLANCK INSTITUTE FOR INFECTION BIOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN M; TOLL LIKE RECEPTOR 7; TOLL LIKE RECEPTOR 9;

ANIMAL CELL; ARTICLE; AUTOIMMUNITY; B 1B CELL; B LYMPHOCYTE; CD4 LYMPHOCYTE COUNT; CELL MATURATION; CELL PROTECTION; CONTROLLED STUDY; FEMALE; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PERITONEUM CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; SYSTEMIC LUPUS ERYTHEMATOSUS; TH17 CELL;

ANIMALS; ASCITIC FLUID; AUTOANTIBODIES; AUTOIMMUNITY; B-LYMPHOCYTES; CELL SEPARATION; DISEASE MODELS, ANIMAL; ENZYME-LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE; IMMUNOGLOBULIN M; LUPUS ERYTHEMATOSUS, SYSTEMIC; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TH1 CELLS; TH17 CELLS; TOLL-LIKE RECEPTOR 9;

EID: 80053071417     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1003340     Document Type: Article

References (54)

1. Arbuckle, M. R., M. T. McClain, M. V. Rubertone, R. H. Scofield, G. J. Dennis, J. A. James, and J. B. Harley. 2003. Development of autoantibodies before the clinical onset of systemic lupus erythematosus. N. Engl. J. Med. 349: 1526-1533. (Pubitemid 37255038)
2. Witte, T., K. Hartung, C. Sachse, T. Matthias, M. Fricke, H. Deicher, J. R. Kalden, H. J. Lakomek, H. H. Peter, and R. E. Schmidt. 1998. IgM anti-dsDNA antibodies in systemic lupus erythematosus: negative association with nephritis. SLE Study Group. Rheumatol. Int. 18: 85-91. (Pubitemid 28505328)
3. Forger, F., T. Matthias, M. Oppermann, H. Becker, and K. Helmke. 2004. Clinical significance of anti-dsDNA antibody isotypes: IgG/IgM ratio of anti-dsDNA antibodies as a prognostic marker for lupus nephritis. Lupus 13: 36-44. (Pubitemid 38129349)
4. Witte, T. 2008. IgM antibodies against dsDNA in SLE. Clin. Rev. Allergy Immunol. 34: 345-347.
5. Werwitzke, S., D. Trick, K. Kamino, T. Matthias, K. Kniesch, B. Schlegelberger, R. E. Schmidt, and T. Witte. 2005. Inhibition of lupus disease by anti-double-stranded DNA antibodies of the IgM isotype in the (NZB x NZW)F1 mouse. Arthritis Rheum. 52: 3629-3638. (Pubitemid 41612234)
6. Guiducci, C., M. Gong, Z. Xu, M. Gill, D. Chaussabel, T. Meeker, J. H. Chan, T. Wright, M. Punaro, S. Bolland, et al. 2010. TLR recognition of self nucleic acids hampers glucocorticoid activity in lupus. Nature 465: 937-941.
7. Leadbetter, E. A., I. R. Rifkin, A. M. Hohlbaum, B. C. Beaudette, M. J. Shlomchik, and A. Marshak-Rothstein. 2002. Chromatin-IgG complexes activate B cells by dual engagement of IgM and Toll-like receptors. Nature 416: 603-607. (Pubitemid 34406754)
8. Viglianti, G. A., C. M. Lau, T. M. Hanley, B. A. Miko, M. J. Shlomchik, and A. Marshak-Rothstein. 2003. Activation of autoreactive B cells by CpG dsDNA. Immunity 19: 837-847. (Pubitemid 37542304)
9. Lau, C. M., C. Broughton, A. S. Tabor, S. Akira, R. A. Flavell, M. J. Mamula, S. R. Christensen, M. J. Shlomchik, G. A. Viglianti, I. R. Rifkin, and A. Marshak-Rothstein. 2005. RNA-associated autoantigens activate B cells by combined B cell antigen receptor/Toll-like receptor 7 engagement. J. Exp. Med. 202: 1171-1177. (Pubitemid 41586947)
10. Liu, N., N. Ohnishi, L. Ni, S. Akira, and K. B. Bacon. 2003. CpG directly induces T-bet expression and inhibits IgG1 and IgE switching in B cells. Nat. Immunol. 4: 687-693. (Pubitemid 36874446)
11. Christensen, S. R., J. Shupe, K. Nickerson, M. Kashgarian, R. A. Flavell, and M. J. Shlomchik. 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. (Pubitemid 44354217)
12. Ehlers, M., H. Fukuyama, T. L. McGaha, A. Aderem, and J. V. Ravetch. 2006. TLR9/MyD88 signaling is required for class switching to pathogenic IgG2a and 2b autoantibodies in SLE. J. Exp. Med. 203: 553-561.
13. Pisitkun, P., J. A. Deane, M. J. Difilippantonio, T. Tarasenko, A. B. Satterthwaite, and S. Bolland. 2006. Autoreactive B cell responses to RNA-related antigens due to TLR7 gene duplication. Science 312: 1669-1672. (Pubitemid 43902669)
14. Lanzavecchia, A., and F. Sallusto. 2007. Toll-like receptors and innate immunity in B-cell activation and antibody responses. Curr. Opin. Immunol. 19: 268-274. (Pubitemid 46687008)
15. Ehlers, M., and J. V. Ravetch. 2007. Opposing effects of Toll-like receptor stimulation induce autoimmunity or tolerance. Trends Immunol. 28: 74-79. (Pubitemid 46176735)
16. Christensen, S. R., and M. J. Shlomchik. 2007. Regulation of lupus-related autoantibody production and clinical disease by Toll-like receptors. Semin. Immunol. 19: 11-23. (Pubitemid 46498753)
17. Nickerson, K. M., S. R. Christensen, J. Shupe, M. Kashgarian, D. Kim, K. Elkon, and M. J. Shlomchik. 2010. TLR9 regulates TLR7- and MyD88-dependent autoantibody production and disease in a murine model of lupus. J. Immunol. 184: 1840-1848.
18. Christensen, S. R., M. Kashgarian, L. Alexopoulou, R. A. Flavell, S. Akira, and M. J. Shlomchik. 2005. Toll-like receptor 9 controls anti-DNA autoantibody production in murine lupus. J. Exp. Med. 202: 321-331. (Pubitemid 41043827)
19. Wu, X., and S. L. Peng. 2006. Toll-like receptor 9 signaling protects against murine lupus. Arthritis Rheum. 54: 336-342. (Pubitemid 43122217)
20. Lartigue, A., P. Courville, I. Auquit, A. François, C. Arnoult, F. Tron, D. Gilbert, and P. Musette. 2006. Role of TLR9 in anti-nucleosome and anti-DNA antibody production in lpr mutation-induced murine lupus. J. Immunol. 177: 1349-1354. (Pubitemid 44036642)
21. Yu, P., U. Wellmann, S. Kunder, L. Quintanilla-Martinez, L. Jennen, N. Dear, K. Amann, S. Bauer, T. H. Winkler, and H. Wagner. 2006. Toll-like receptor 9-independent aggravation of glomerulonephritis in a novel model of SLE. Int. Immunol. 18: 1211-1219. (Pubitemid 44349296)
22. Bolland, S., and J. V. Ravetch. 2000. Spontaneous autoimmune disease in Fc (gamma)RIIB-deficient mice results from strain-specific epistasis. Immunity 13: 277-285.
23. Hemmi, H., O. Takeuchi, T. Kawai, T. Kaisho, S. Sato, H. Sanjo, M. Matsumoto, K. Hoshino, H. Wagner, K. Takeda, and S. Akira. 2000. A Toll-like receptor recognizes bacterial DNA. Nature 408: 740-745. (Pubitemid 32015992)
24. Gu, H., Y. R. Zou, and K. Rajewsky. 1993. Independent control of immunoglobulin switch recombination at individual switch regions evidenced through Cre-loxP-mediated gene targeting. Cell 73: 1155-1164. (Pubitemid 23180489)
25. Ehrenstein, M. R., T. L. O'Keefe, S. L. Davies, and M. S. Neuberger. 1998. Targeted gene disruption reveals a role for natural secretory IgM in the maturation of the primary immune response. Proc. Natl. Acad. Sci. USA 95: 10089-10093. (Pubitemid 28415299)
26. Ye, P., F. H. Rodriguez, S. Kanaly, K. L. Stocking, J. Schurr, P. Schwarzenberger, P. Oliver, W. Huang, P. Zhang, J. Zhang, et al. 2001. Requirement of interleukin 17 receptor signaling for lung CXC chemokine and granulocyte colony-stimulating factor expression, neutrophil recruitment, and host defense. J. Exp. Med. 194: 519-527. (Pubitemid 32835046)
27. Fillatreau, S., and D. Gray. 2003. T cell accumulation in B cell follicles is regulated by dendritic cells and is independent of B cell activation. J. Exp. Med. 197: 195-206. (Pubitemid 36152314)
28. Whipple, E. C., R. S. Shanahan, A. H. Ditto, R. P. Taylor, and M. A. Lindorfer. 2004. Analyses of the in vivo trafficking of stoichiometric doses of an anticomplement receptor 1/2 monoclonal antibody infused intravenously in mice. J. Immunol. 173: 2297-2306. (Pubitemid 39063085)
29. Wardemann, H., S. Yurasov, A. Schaefer, J. W. Young, E. Meffre, and M. C. Nussenzweig. 2003. Predominant autoantibody production by early human B cell precursors. Science 301: 1374-1377. (Pubitemid 37075812)
30. Tiller, T., J. Kofer, C. Kreschel, C. E. Busse, S. Riebel, S. Wickert, F. Oden, M. M. Mertes, M. Ehlers, and H. Wardemann. 2010. Development of self-reactive germinal center B cells and plasma cells in autoimmune Fc gammaRIIB-deficient mice. J. Exp. Med. 207: 2767-2778.
31. Lampropoulou, V., K. Hoehlig, T. Roch, P. Neves, E. Calderön Gömez, C. H. Sweenie, Y. Hao, A. A. Freitas, U. Steinhoff, S. M. Anderton, and S. Fillatreau. 2008. TLR-activated B cells suppress T cell-mediated autoimmunity. J. Immunol. 180: 4763-4773.
32. Boes, M., T. Schmidt, K. Linkemann, B. C. Beaudette, A. Marshak-Rothstein, and J. Chen. 2000. Accelerated development of IgG autoantibodies and autoimmune disease in the absence of secreted IgM. Proc. Natl. Acad. Sci. USA 97: 1184-1189. (Pubitemid 30080833)
33. Martin, F., A. M. Oliver, and J. F. Kearney. 2001. Marginal zone and B1 B cells unite in the early response against T-independent blood-borne particulate antigens. Immunity 14: 617-629. (Pubitemid 32520872)
34. Viau, M., and M. Zouali. 2005. B-lymphocytes, innate immunity, and autoimmunity. Clin. Immunol. 114: 17-26. (Pubitemid 39642786)
35. Ferry, H., P. K. Potter, T. L. Crockford, A. Nijnik, M. R. Ehrenstein, M. J. Walport, M. Botto, and R. J. Cornall. 2007. Increased positive selection of B1 cells and reduced B cell tolerance to intracellular antigens in c1q-deficient mice. J. Immunol. 178: 2916-2922. (Pubitemid 46333170)
36. Ohdan, H., K. G. Swenson, H. S. Kruger Gray, Y. G. Yang, Y. Xu, A. D. Thall, and M. Sykes. 2000. Mac-1-negative B-1b phenotype of natural antibody-producing cells, including those responding to Gal alpha 1,3Gal epitopes in alpha 1,3-galactosyltransferase-deficient mice. J. Immunol. 165: 5518-5529.
37. Genestier, L., M. Taillardet, P. Mondiere, H. Gheit, C. Bella, and T. Defrance. 2007. TLR agonists selectively promote terminal plasma cell differentiation of B cell subsets specialized in thymus-independent responses. J. Immunol. 178: 7779-7786. (Pubitemid 46898049)
38. Kubo, T., Y. Uchida, Y. Watanabe, M. Abe, A. Nakamura, M. Ono, S. Akira, and T. Takai. 2009. Augmented TLR9-induced Btk activation in PIR-B-deficient B-1 cells provokes excessive autoantibody production and autoimmunity. J. Exp. Med. 206: 1971-1982.
39. Booth, J. S., J. J. Buza, A. Potter, L. A. Babiuk, and G. K. Mutwiri. 2010. Costimulation with TLR7/8 and TLR9 agonists induce down-regulation of innate immune responses in sheep blood mononuclear and B cells. Dev. Comp. Immunol. 34: 572-578.
40. Pasare, C., and R. Medzhitov. 2005. Control of B-cell responses by Toll-like receptors. Nature 438: 364-368. (Pubitemid 41643953)
41. Rahman, A. H., and R. A. Eisenberg. 2006. The role of toll-like receptors in systemic lupus erythematosus. Springer Semin. Immunopathol. 28: 131-143. (Pubitemid 46628482)
42. Chen, Y., S. Khanna, C. S. Goodyear, Y. B. Park, E. Raz, S. Thiel, C. Grönwall, J. Vas, D. L. Boyle, M. Corr, et al. 2009. Regulation of dendritic cells and macrophages by an anti-apoptotic cell natural antibody that suppresses TLR responses and inhibits inflammatory arthritis. J. Immunol. 183: 1346-1359.
43. Notley, C. A., M. A. Brown, G. P. Wright, and M. R. Ehrenstein. 2011. Natural IgM is required for suppression of inflammatory arthritis by apoptotic cells. J. Immunol. 186: 4967-4972.
44. De Lorenzo, B. H., R. R. Brito, L. C. Godoy, J. D. Lopes, and M. Mariano. 2007. Tolerogenic property of B-1b cells in a model of allergic reaction. Immunol. Lett. 114: 110-118. (Pubitemid 350180099)
45. Shimizu, I., T. Kawahara, F. Haspot, P. D. Bardwell, M. C. Carroll, and M. Sykes. 2007. B-cell extrinsic CR1/CR2 promotes natural antibody production and tolerance induction of anti-alphaGAL-producing B-1 cells. Blood 109: 1773-1781. (Pubitemid 46239614)
46. Bos, N. A., C. G. Meeuwsen, B. S. Wostmann, J. R. Pleasants, and R. Benner. 1988. The influence of exogenous antigenic stimulation on the specificity repertoire of background immunoglobulin-secreting cells of different isotypes. Cell. Immunol. 112: 371-380.
47. Haury, M., A. Sundblad, A. Grandien, C. Barreau, A. Coutinho, and A. Nobrega. 1997. The repertoire of serum IgM in normal mice is largely independent of external antigenic contact. Eur. J. Immunol. 27: 1557-1563. (Pubitemid 27254850)
48. Ono, M., S. Bolland, P. Tempst, and J. V. Ravetch. 1996. Role of the inositol phosphatase SHIP in negative regulation of the immune system by the receptor Fc(gamma)RIIB. Nature 383: 263-266. (Pubitemid 26317676)
49. Alugupalli, K. R., and R. M. Gerstein. 2005. Divide and conquer: division of labor by B-1 B cells. Immunity 23: 1-2. (Pubitemid 41019650)
50. Alugupalli, K. R., J. M. Leong, R. T. Woodland, M. Muramatsu, T. Honjo, and R. M. Gerstein. 2004. B1b lymphocytes confer T cell-independent long-lasting immunity. Immunity 21: 379-390. (Pubitemid 39208339)
51. Haas, K. M., J. C. Poe, D. A. Steeber, and T. F. Tedder. 2005. B-1a and B-1b cells exhibit distinct developmental requirements and have unique functional roles in innate and adaptive immunity to S. pneumoniae. Immunity 23: 7-18. (Pubitemid 41019653)
52. Montecino-Rodriguez, E., and K. Dorshkind. 2006. New perspectives in B-1 B cell development and function. Trends Immunol. 27: 428-433. (Pubitemid 44216193)
53. Avalos, A. M., L. Busconi, and A. Marshak-Rothstein. 2010. Regulation of autoreactive B cell responses to endogenous TLR ligands. Autoimmunity 43: 76-83.
54. Kawahara, T., H. Ohdan, G. Zhao, Y. G. Yang, and M. Sykes. 2003. Peritoneal cavity B cells are precursors of splenic IgM natural antibody-producing cells. J. Immunol. 171: 5406-5414. (Pubitemid 37432827)