FAS Inactivation Releases Unconventional Germinal Center B Cells that Escape Antigen Control and Drive IgE and Autoantibody Production

Immunity

Volumn 42, Issue 5, 2015, Pages 890-902

  Butt, Danyal ^a,b   Chan, Tyani D ^a,b   Bourne, Katherine ^a   Hermes, Jana R ^a   Nguyen, Akira ^a   Statham, Aaron ^a   O'Reilly, Lorraine A ^c,d   Strasser, Andreas ^c,d   Price, Susan ^e   Schofield, Peter ^a   Christ, Daniel ^a,b   Basten, Antony ^a,b   Ma, Cindy S ^a,b   Tangye, Stuart G ^a,b   Phan, Tri Giang ^a,b   Rao, V Koneti ^e   Brink, Robert ^a,b  

^a GARVAN INSTITUTE OF MEDICAL RESEARCH   (Australia)

^b UNIVERSITY OF NEW SOUTH WALES   (Australia)

^c WALTER AND ELIZA HALL INSTITUTE OF MEDICAL RESEARCH   (Australia)

^d UNIVERSITY OF MELBOURNE   (Australia)

^e NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FAS ANTIGEN; IMMUNOGLOBULIN E ANTIBODY; AUTOANTIBODY; IMMUNOGLOBULIN E;

ANIMAL CELL; ANTIBODY PRODUCTION; ANTIGEN ANTIBODY REACTION; ARTICLE; B LYMPHOCYTE; CELL COUNT; CONTROLLED STUDY; GERMINAL CENTER; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PLASMA CELL; PRE B LYMPHOCYTE; PRIORITY JOURNAL; SOMATIC HYPERMUTATION; ANIMAL; BIOSYNTHESIS; CYTOLOGY; DEFICIENCY; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE; IMMUNOLOGY; METABOLISM; POLYMERASE CHAIN REACTION;

ANIMALS; ANTIGENS, CD95; AUTOANTIBODIES; B-LYMPHOCYTES; ENZYME-LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE; GERMINAL CENTER; HUMANS; IMMUNOGLOBULIN E; MICE; POLYMERASE CHAIN REACTION;

EID: 84929691400     PISSN: 10747613     EISSN: 10974180     Source Type: Journal    
DOI: 10.1016/j.immuni.2015.04.010     Document Type: Article

References (45)

1. Afshar-Sterle S., Zotos D., Bernard N.J., Scherger A.K., Rödling L., Alsop A.E., Walker J., Masson F., Belz G.T., Corcoran L.M., et al. Fas ligand-mediated immune surveillance by Tcells is essential for the control of spontaneous B cell lymphomas. Nat. Med. 2014, 20:283-290.
2. Aït-Azzouzene D., Kono D.H., Gonzalez-Quintial R., McHeyzer-Williams L.J., Lim M., Wickramarachchi D., Gerdes T., Gavin A.L., Skog P., McHeyzer-Williams M.G., et al. Deletion of IgG-switched autoreactive B cells and defects in Fas(lpr) lupus mice. J.Immunol. 2010, 185:1015-1027.
3. Alabyev B., Vuyyuru R., Manser T. Influence of Fas on the regulation of the response of an anti-nuclear antigen B cell clonotype to foreign antigen. Int. Immunol. 2008, 20:1279-1287.
4. Andrews B.S., Eisenberg R.A., Theofilopoulos A.N., Izui S., Wilson C.B., McConahey P.J., Murphy E.D., Roths J.B., Dixon F.J. Spontaneous murine lupus-like syndromes. Clinical and immunopathological manifestations in several strains. J.Exp. Med. 1978, 148:1198-1215.
5. Brink R. The imperfect control of self-reactive germinal center B cells. Curr. Opin. Immunol. 2014, 28:97-101.
6. Chan T.D., Gatto D., Wood K., Camidge T., Basten A., Brink R. Antigen affinity controls rapid T-dependent antibody production by driving the expansion rather than the differentiation or extrafollicular migration of early plasmablasts. J.Immunol. 2009, 183:3139-3149.
7. Chan T.D., Wood K., Hermes J.R., Butt D., Jolly C.J., Basten A., Brink R. Elimination of germinal-center-derived self-reactive B cells is governed by the location and concentration of self-antigen. Immunity 2012, 37:893-904.
8. Dahlke I., Nott D.J., Ruhno J., Sewell W.A., Collins A.M. Antigen selection in the IgE response of allergic and nonallergic individuals. J.Allergy Clin. Immunol. 2006, 117:1477-1483.
9. Dema B., Charles N., Pellefigues C., Ricks T.K., Suzuki R., Jiang C., Scheffel J., Hasni S., Hoffman V., Jablonski M., et al. Immunoglobulin E plays an immunoregulatory role in lupus. J.Exp. Med. 2014, 211:2159-2168.
10. Dema B., Pellefigues C., Hasni S., Gault N., Jiang C., Ricks T.K., Bonelli M.M., Scheffel J., Sacré K., Jablonski M., et al. Autoreactive IgE is prevalent in systemic lupus erythematosus and is associated with increased disease activity and nephritis. PLoS ONE 2014, 9:e90424.
11. Erazo A., Kutchukhidze N., Leung M., Christ A.P., Urban J.F., Curotto de Lafaille M.A., Lafaille J.J. Unique maturation program of the IgE response invivo. Immunity 2007, 26:191-203.
12. Fisher G.H., Rosenberg F.J., Straus S.E., Dale J.K., Middleton L.A., Lin A.Y., Strober W., Lenardo M.J., Puck J.M. Dominant interfering Fas gene mutations impair apoptosis in a human autoimmune lymphoproliferative syndrome. Cell 1995, 81:935-946.
13. Garrone P., Neidhardt E.M., Garcia E., Galibert L., van Kooten C., Banchereau J. Fas ligation induces apoptosis of CD40-activated human B lymphocytes. J.Exp. Med. 1995, 182:1265-1273.
14. Hahne M., Renno T., Schroeter M., Irmler M., French L., Bornard T., MacDonald H.R., Tschopp J. Activated B cells express functional Fas ligand. Eur. J. Immunol. 1996, 26:721-724.
15. Han S., Hathcock K., Zheng B., Kepler T.B., Hodes R., Kelsoe G. Cellular interaction in germinal centers. Roles of CD40 ligand and B7-2 in established germinal centers. J.Immunol. 1995, 155:556-567.
16. Han S., Zheng B., Dal Porto J., Kelsoe G. In situ studies of the primary immune response to (4-hydroxy-3-nitrophenyl)acetyl. IV. Affinity-dependent, antigen-driven B cell apoptosis in germinal centers as a mechanism for maintaining self-tolerance. J.Exp. Med. 1995, 182:1635-1644.
17. Hao Z., Duncan G.S., Seagal J., Su Y.W., Hong C., Haight J., Chen N.J., Elia A., Wakeham A., Li W.Y., et al. Fas receptor expression in germinal-center B cells is essential for T and B lymphocyte homeostasis. Immunity 2008, 29:615-627.
18. Herlands R.A., Christensen S.R., Sweet R.A., Hershberg U., Shlomchik M.J. T cell-independent and toll-like receptor-dependent antigen-driven activation of autoreactive B cells. Immunity 2008, 29:249-260.
19. Hoch S., Boyd M., Malone B., Gonye G., Schwaber J., Schwaber J. Fas-mediated apoptosis eliminates B cells that acquire self-reactivity during the germinal center response to NP. Cell. Immunol. 2000, 203:103-110.
20. Liu Y.J., Barthélémy C., de Bouteiller O., Arpin C., Durand I., Banchereau J. Memory B cells from human tonsils colonize mucosal epithelium and directly present antigen to Tcells by rapid up-regulation of B7-1 and B7-2. Immunity 1995, 2:239-248.
21. Messingham K.A., Holahan H.M., Fairley J.A. Unraveling the significance of IgE autoantibodies in organ-specific autoimmunity: lessons learned from bullous pemphigoid. Immunol. Res. 2014, 59:273-278.
22. Nossal G.J. Somatic mutations in B lymphocytes: new perspectives in tolerance research?. Immunol. Cell Biol. 1988, 66:105-110.
23. O' Reilly L.A., Tai L., Lee L., Kruse E.A., Grabow S., Fairlie W.D., Haynes N.M., Tarlinton D.M., Zhang J.G., Belz G.T., et al. Membrane-bound Fas ligand only is essential for Fas-induced apoptosis. Nature 2009, 461:659-663.
24. Paus D., Phan T.G., Chan T.D., Gardam S., Basten A., Brink R. Antigen recognition strength regulates the choice between extrafollicular plasma cell and germinal center B cell differentiation. J.Exp. Med. 2006, 203:1081-1091.
25. Permin H., Wiik A. The prevalence of IgE antinuclear antibodies in rheumatoid arthritis and systemic lupus erythematosus. Acta Pathol. Microbiol. Scand. [C] 1978, 86C:245-249.
26. Phan T.G., Amesbury M., Gardam S., Crosbie J., Hasbold J., Hodgkin P.D., Basten A., 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. 2003, 197:845-860.
27. Phan T.G., Paus D., Chan T.D., Turner M.L., Nutt S.L., Basten A., Brink R. High affinity germinal center B cells are actively selected into the plasma cell compartment. J.Exp. Med. 2006, 203:2419-2424.
28. Price S., Shaw P.A., Seitz A., Joshi G., Davis J., Niemela J.E., Perkins K., Hornung R.L., Folio L., Rosenberg P.S., et al. Natural history of autoimmune lymphoproliferative syndrome associated with FAS gene mutations. Blood 2014, 123:1989-1999.
29. Provost T.T., Tomasi T.B. Immunopathology of bullous pemphigoid. Basement membrane deposition of IgE, alternate pathway components and fibrin. Clin. Exp. Immunol. 1974, 18:193-200.
30. Rathmell J.C., Cooke M.P., Ho W.Y., Grein J., Townsend S.E., Davis M.M., Goodnow C.C. CD95 (Fas)-dependent elimination of self-reactive B cells upon interaction with CD4+ Tcells. Nature 1995, 376:181-184.
31. Rieux-Laucat F., Le Deist F., Hivroz C., Roberts I.A., Debatin K.M., Fischer A., de Villartay J.P. Mutations in Fas associated with human lymphoproliferative syndrome and autoimmunity. Science 1995, 268:1347-1349.
32. Smith K.G., Nossal G.J., Tarlinton D.M. FAS is highly expressed in the germinal center but is not required for regulation of the B-cell response to antigen. Proc. Natl. Acad. Sci. USA 1995, 92:11628-11632.
33. Suan D., Nguyen A., Moran I., Bourne K., Hermes J.R., Arshi M., Hampton H.R., Tomura M., Miwa Y., Kelleher A.D., et al. T follicular helper cells have distinct modes of migration and molecular signatures in naive and memory immune responses. Immunity 2015, 42:704-718.
34. Takahashi T., Tanaka M., Brannan C.I., Jenkins N.A., Copeland N.G., Suda T., Nagata S. Generalized lymphoproliferative disease in mice, caused by a point mutation in the Fas ligand. Cell 1994, 76:969-976.
35. Takahashi Y., Ohta H., Takemori T. Fas is required for clonal selection in germinal centers and the subsequent establishment of the memory B cell repertoire. Immunity 2001, 14:181-192.
36. Takahashi S., Futatsugi-Yumikura S., Fukuoka A., Yoshimoto T., Nakanishi K., Yonehara S. Fas deficiency in mice with the Balb/c background induces blepharitis with allergic inflammation and hyper-IgE production in conjunction with severe autoimmune disease. Int. Immunol. 2013, 25:287-293.
37. Thaunat O., Granja A.G., Barral P., Filby A., Montaner B., Collinson L., Martinez-Martin N., Harwood N.E., Bruckbauer A., Batista F.D. Asymmetric segregation of polarized antigen on B cell division shapes presentation capacity. Science 2012, 335:475-479.
38. Verbeke C.S., Wenthe U., Zentgraf H. Fas ligand expression in the germinal centre. J.Pathol. 1999, 189:155-160.
39. Victora G.D., Nussenzweig M.C. Germinal centers. Annu. Rev. Immunol. 2012, 30:429-457.
40. Wang Y., Jackson K.J., Davies J., Chen Z., Gaeta B.A., Rimmer J., Sewell W.A., Collins A.M. IgE-associated IGHV genes from venom and peanut allergic individuals lack mutational evidence of antigen selection. PLoS ONE 2014, 9:e89730.
41. Watanabe-Fukunaga R., Brannan C.I., Copeland N.G., Jenkins N.A., Nagata S. Lymphoproliferation disorder in mice explained by defects in Fas antigen that mediates apoptosis. Nature 1992, 356:314-317.
42. William J., Euler C., Christensen S., Shlomchik M.J. Evolution of autoantibody responses via somatic hypermutation outside of germinal centers. Science 2002, 297:2066-2070.
43. Wu J., Wilson J., He J., Xiang L., Schur P.H., Mountz J.D. Fas ligand mutation in a patient with systemic lupus erythematosus and lymphoproliferative disease. J.Clin. Invest. 1996, 98:1107-1113.
44. Xiong H., Dolpady J., Wabl M., Curotto de Lafaille M.A., Lafaille J.J. Sequential class switching is required for the generation of high affinity IgE antibodies. J.Exp. Med. 2012, 209:353-364.
45. Yang Z., Sullivan B.M., Allen C.D. Fluorescent invivo detection reveals that IgE(+) B cells are restrained by an intrinsic cell fate predisposition. Immunity 2012, 36:857-872.