WASp-deficient B cells play a critical, cell-intrinsic role in triggering autoimmunity

Journal of Experimental Medicine

Volumn 208, Issue 10, 2011, Pages 2033-2042

  Becker Herman, Shirly ^a,d   Meyer Bahlburg, Almut ^a,d,e   Schwartz, Marc A ^a   Jackson, Shaun W ^a,d   Hudkins, Kelly L ^a   Liu, Chaohong ^b   Sather, Blythe D ^a,d   Khim, Socheath ^a,d   Liggitt, Denny ^a   Song, Wenxia ^b   Silverman, Gregg J ^c   Alpers, Charles E ^a   Rawlings, David J ^a,d  

^a UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^b Bldg 142   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d SEATTLE CHILDREN S RESEARCH INSTITUTE   (United States)

^e HANNOVER MEDICAL SCHOOL   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

AUTOANTIBODY; B LYMPHOCYTE RECEPTOR; CD4 ANTIGEN; MYELOID DIFFERENTIATION FACTOR 88; TOLL LIKE RECEPTOR; WISKOTT ALDRICH SYNDROME PROTEIN;

ANIMAL CELL; ANIMAL TISSUE; ANTIBODY PRODUCTION; ARTICLE; AUTOIMMUNE DISEASE; AUTOIMMUNITY; B LYMPHOCYTE; CELL LINEAGE; CHIMERA; CONTROLLED STUDY; DISEASE SEVERITY; GENE; GENE MUTATION; GERMINAL CENTER; HISTOPATHOLOGY; HUMORAL IMMUNITY; IMMUNOLOGICAL TOLERANCE; IN VITRO STUDY; MORTALITY; MOUSE; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; STEM CELL TRANSPLANTATION; T LYMPHOCYTE; WAS GENE; WISKOTT ALDRICH SYNDROME;

ANIMALS; ANTIBODIES, ANTINUCLEAR; AUTOANTIBODIES; AUTOIMMUNITY; B-LYMPHOCYTES; CD4-POSITIVE T-LYMPHOCYTES; CHIMERA; FEMALE; HUMANS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MYELOID DIFFERENTIATION FACTOR 88; RECEPTORS, ANTIGEN, B-CELL; TOLL-LIKE RECEPTORS; WISKOTT-ALDRICH SYNDROME PROTEIN;

EID: 80053132181     PISSN: 00221007     EISSN: 15409538     Source Type: Journal    
DOI: 10.1084/jem.20110200     Document Type: Article

References (35)

1. Andrews, S.F., and D.J. Rawlings. 2009. Transitional B cells exhibit a B cell receptor-specific nuclear defect in gene transcription. J. Immunol. 182: 2868-2878.
2. Antón, I.M., M.A. de la Fuente, T.N. Sims, S. Freeman, N. Ramesh, J.H. Hartwig, M.L. Dustin, and R.S. Geha. 2002. WIP deficiency reveals a differential role for WIP and the actin cytoskeleton in T and B cell activation. Immunity. 16:193-204.
3. Barr, T.A., S. Brown, P. Mastroeni, and D. Gray. 2009. B cell intrinsic MyD88 signals drive IFN-gamma production from T cells and control switching to IgG2c. J. Immunol. 183:1005-1012.
4. 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.
5. Bouma, G., S. Burns, and A.J. Thrasher. 2007. Impaired T-cell priming in vivo resulting from dysfunction of WASp-deficient dendritic cells. Blood. 110:4278-4284.
6. Bouma, G., S.O. Burns, and A.J. Thrasher. 2009. Wiskott-Aldrich Syndrome: Immunodeficiency resulting from defective cell migration and impaired immunostimulatory activation. Immunobiology. 214:778-790.
7. Cornall, R.J., J.G. Cyster, M.L. Hibbs, A.R. Dunn, K.L. Otipoby, E.A. Clark, and C.C. Goodnow. 1998. Polygenic autoimmune traits: Lyn, CD22, and SHP-1 are limiting elements of a biochemical pathway regulating BCR signaling and selection. Immunity. 8:497-508.
8. Curcio, C., T. Pannellini, S. Lanzardo, G. Forni, P. Musiani, and I.M. Antón. 2007. WIP null mice display a progressive immunological disorder that resembles Wiskott-Aldrich syndrome. J. Pathol. 211:67-75.
9. Dupuis-Girod, S., J. Medioni, E. Haddad, P. Quartier, M. Cavazzana-Calvo, F. Le Deist, G. de Saint Basile, J. Delaunay, K. Schwarz, J.L. Casanova, et al. 2003. Autoimmunity in Wiskott-Aldrich syndrome: risk factors, clinical features, and outcome in a single-center cohort of 55 patients. Pediatrics. 111:e622-e627.
10. 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.
11. Fields, M.L., H.H. Metzgar, B.D. Hondowicz, S.A. Kang, S.T. Alexander, K.D. Hazard, A.C. Hsu, Y.Z. Du, E.L. Prak, M. Monestier, and J. Erikson. 2006. Exogenous and endogenous TLR ligands activate anti-chromatin and polyreactive B cells. J. Immunol. 176:6491-6502.
12. Grimaldi, C.M., R. Hicks, and B. Diamond. 2005. B cell selection and susceptibility to autoimmunity. J. Immunol. 174:1775-1781.
13. Groom, J.R., C.A. Fletcher, S.N. Walters, S.T. Grey, S.V. Watt, M.J. Sweet, M.J. Smyth, C.R. Mackay, and F. Mackay. 2007. BAFF and MyD88 signals promote a lupuslike disease independent of T cells. J. Exp. Med. 204:1959-1971.
14. He, B., R. Santamaria, W. Xu, M. Cols, K. Chen, I. Puga, M. Shan, H. Xiong, J.B. Bussel, A. Chiu, et al. 2010. The transmembrane activator TACI triggers immunoglobulin class switching by activating B cells through the adaptor MyD88. Nat. Immunol. 11:836-845.
15. Herlands, R.A., S.R. Christensen, R.A. Sweet, U. Hershberg, and M.J. Shlomchik. 2008. T cell-independent and toll-like receptor-dependent antigen-driven activation of autoreactive B cells. Immunity. 29:249-260.
16. Humblet-Baron, S., B. Sather, S. Anover, S. Becker-Herman, D.J. Kasprowicz, S. Khim, T. Nguyen, K. Hudkins-Loya, C.E. Alpers, S.F. Ziegler, et al. 2007. Wiskott-Aldrich syndrome protein is required for regulatory T cell homeostasis. J. Clin. Invest. 117:407-418.
17. Imai, K., T. Morio, Y. Zhu, Y. Jin, S. Itoh, M. Kajiwara, J. Yata, S. Mizutani, H.D. Ochs, and S. Nonoyama. 2004. Clinical course of patients with WASP gene mutations. Blood. 103:456-464.
18. Luzina, I.G., S.P. Atamas, C.E. Storrer, L.C. daSilva, G. Kelsoe, J.C. Papadimitriou, and B.S. Handwerger. 2001. Spontaneous formation of germinal centers in autoimmune mice. J. Leukoc. Biol. 70:578-584.
19. + regulatory T cells. J. Exp. Med. 204:381-391.
20. + natural regulatory T cells. J. Exp. Med. 204:369-380.
21. Marshak-Rothstein, A., and I.R. Rifkin. 2007. Immunologically active autoantigens: the role of toll-like receptors in the development of chronic inflammatory disease. Annu. Rev. Immunol. 25:419-441.
22. Meyer-Bahlburg, A., S.F. Andrews, K.O. Yu, S.A. Porcelli, and D.J. Rawlings. 2008a. Characterization of a late transitional B cell population highly sensitive to BAFF-mediated homeostatic proliferation. J. Exp. Med. 205:155-168.
23. Meyer-Bahlburg, A., S. Becker-Herman, S. Humblet-Baron, S. Khim, M. Weber, G. Bouma, A.J. Thrasher, F.D. Batista, and D.J. Rawlings. 2008b. Wiskott-Aldrich syndrome protein deficiency in B cells results in impaired peripheral homeostasis. Blood. 112:4158-4169.
24. Nikolov, N.P., M. Shimizu, S. Cleland, D. Bailey, J. Aoki, T. Strom, P.L. Schwartzberg, F. Candotti, and R.M. Siegel. 2010. Systemic autoimmunity and defective Fas ligand secretion in the absence of the Wiskott-Aldrich syndrome protein. Blood. 116:740-747.
25. Nimmerjahn, F., and J.V. Ravetch. 2005. Divergent immunoglobulin g subclass activity through selective Fc receptor binding. Science. 310:1510- 1512.
26. Ozsahin, H., M. Cavazzana-Calvo, L.D. Notarangelo, A. Schulz, A.J. Thrasher, E. Mazzolari, M.A. Slatter, F. Le Deist, S. Blanche, P. Veys, et al. 2008. Long-term outcome following hematopoietic stem-cell transplantation in Wiskott-Aldrich syndrome: collaborative study of the European Society for Immunodeficiencies and European Group for Blood and Marrow Transplantation. Blood. 111:439-445.
27. Ramesh, N., and R. Geha. 2009. Recent advances in the biology of WASP and WIP. Immunol. Res. 44:99-111.
28. Sharma, S., G. Orlowski, and W. Song. 2009. Btk regulates B cell receptormediated antigen processing and presentation by controlling actin cytoskeleton dynamics in B cells. J. Immunol. 182:329-339.
29. Shlomchik, M.J. 2009. Activating systemic autoimmunity: B's, T's, and tolls. Curr. Opin. Immunol. 21:626-633.
30. Silverman, G.J., R. Srikrishnan, K. Germar, C.S. Goodyear, K.A. Andrews, E.M. Ginzler, and B.P. Tsao. 2008. Genetic imprinting of autoantibody repertoires in systemic lupus erythematosus patients. Clin. Exp. Immunol. 153:102-116.
31. Sullivan, K.E., C.A. Mullen, R.M. Blaese, and J.A. Winkelstein. 1994. A multiinstitutional survey of the Wiskott-Aldrich syndrome. J. Pediatr. 125:876-885.
32. Taneda, S., S. Segerer, K.L. Hudkins, Y. Cui, M. Wen, M. Segerer, M.H. Wener, C.G. Khairallah, A.G. Farr, and C.E. Alpers. 2001. Cryoglobulinemic glomerulonephritis in thymic stromal lymphopoietin transgenic mice. Am. J. Pathol. 159:2355-2369.
33. Thrasher, A.J. 2002. WASp in immune-system organization and function. Nat. Rev. Immunol. 2:635-646.
34. 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 selfreactive germinal center B cells and plasma cells in autoimmune FcγRIIBdeficient mice. J. Exp. Med. 207:2767-2778.
35. 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.