Apoptotic marginal zone deletion of anti-Sm/ribonucleoprotein B cells

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

Volumn 109, Issue 20, 2012, Pages 7811-7816

  Kishi, Yusuke ^a   Higuchi, Tetsuya ^a,e   Phoon, Shirly ^a   Sakamaki, Yasuo ^a   Kamiya, Koki ^a   Riemekasten, Gabriela ^b   Akiyoshi, Kazunari ^a,c   Weigert, Martin G ^d   Tsubata, Takeshi ^a  

^a TOKYO MEDICAL AND DENTAL UNIVERSITY   (Japan)

^b CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^c KYOTO UNIVERSITY   (Japan)

^d UNIVERSITY OF CHICAGO   (United States)

^e TOHO UNIVERSITY SAKURA MEDICAL CENTER   (Japan)

Author keywords

Lupus related autoantibody; Marginal zone B cells; Peripheral tolerance

Indexed keywords

CD40 LIGAND; DNA ANTIBODY; IMMUNOGLOBULIN M; RIBONUCLEOPROTEIN ANTIBODY; SM ANTIBODY;

ANIMAL CELL; ANIMAL TISSUE; ANTIBODY PRODUCTION; ANTIGEN EXPRESSION; APOPTOSIS; ARTICLE; B LYMPHOCYTE; B LYMPHOCYTE ACTIVATION; FEMALE; MOUSE; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SYSTEMIC LUPUS ERYTHEMATOSUS;

ANIMALS; ANTIBODIES, ANTINUCLEAR; APOPTOSIS; AUTOANTIBODIES; B-LYMPHOCYTES; CD40 LIGAND; CLODRONIC ACID; CROSSES, GENETIC; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; FLOW CYTOMETRY; IMMUNE TOLERANCE; IMMUNOHISTOCHEMISTRY; INDOLES; LIPOSOMES; LUPUS ERYTHEMATOSUS, SYSTEMIC; MICE; MICE, TRANSGENIC;

MURINAE; MUS; MUS MUSCULUS;

EID: 84861217863     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1204509109     Document Type: Article

References (50)

1. Gay D, Saunders T, Camper S, Weigert M (1993) Receptor editing: An approach by autoreactive B cells to escape tolerance. J Exp Med 177:999-1008. (Pubitemid 23097389)
2. Goodnow CC, et al. (1988) Altered immunoglobulin expression and functional silencing of self-reactive B lymphocytes in transgenic mice. Nature 334:676-682.
3. Nemazee DA, Bürki K (1989) Clonal deletion of B lymphocytes in a transgenic mouse bearing anti-MHC class I antibody genes. Nature 337:562-566. (Pubitemid 19045542)
4. Radic MZ, Erikson J, Litwin S, Weigert M (1993) B lymphocytes may escape tolerance by revising their antigen receptors. J Exp Med 177:1165-1173.
5. Goodnow CC, Crosbie J, Jorgensen H, Brink RA, Basten A (1989) Induction of self-tolerance in mature peripheral B lymphocytes. Nature 342:385-391. (Pubitemid 19277513)
6. Hannum LG, Ni D, Haberman AM, Weigert MG, ShlomchikMJ (1996) A disease-related rheumatoid factor autoantibody is not tolerized in a normal mouse: Implications for the origins of autoantibodies in autoimmune disease. J Exp Med 184:1269-1278. (Pubitemid 26354682)
7. Santulli-Marotto S, Retter MW, Gee R, Mamula MJ, Clarke SH (1998) Autoreactive B cell regulation: Peripheral induction of developmental arrest by lupus-associated autoantigens. Immunity 8:209-219. (Pubitemid 28123748)
8. Cyster JG, Goodnow CC (1995) Antigen-induced exclusion from follicles and anergy are separate and complementary processes that influence peripheral B cell fate. Immunity 3:691-701. (Pubitemid 26091145)
9. Mandik-Nayak L, Bui A, Noorchashm H, Eaton A, Erikson J (1997) Regulation of antidouble- stranded DNA B cells in nonautoimmune mice: Localization to the T-B interface of the splenic follicle. J Exp Med 186:1257-1267. (Pubitemid 27469021)
10. Noorchashm H, et al. (1999) Characterization of anergic anti-DNA B cells: B cell anergy is a T cell-independent and potentially reversible process. Int Immunol 11:765-776. (Pubitemid 29237768)
11. Lesley R, et al. (2004) Reduced competitiveness of autoantigen-engaged B cells due to increased dependence on BAFF. Immunity 20:441-453. (Pubitemid 38482122)
12. Thien M, et al. (2004) Excess BAFF rescues self-reactive B cells from peripheral deletion and allows them to enter forbidden follicular and marginal zone niches. Immunity 20: 785-798. (Pubitemid 38757447)
13. Chen C, et al. (1995) The site and stage of anti-DNA B-cell deletion. Nature 373: 252-255.
14. Chen C, et al. (1994) Deletion and editing of B cells that express antibodies to DNA. J Immunol 152:1970-1982. (Pubitemid 24075731)
15. Erikson J, et al. (1991) Expression of anti-DNA immunoglobulin transgenes in nonautoimmune mice. Nature 349:331-334. (Pubitemid 21912076)
16. Fukuyama H, Nimmerjahn F, Ravetch JV (2005) The inhibitory Fcgamma receptor modulates autoimmunity by limiting the accumulation of immunoglobulin G+ anti-DNA plasma cells. Nat Immunol 6:99-106. (Pubitemid 40136701)
17. Li H, Jiang Y, Prak EL, Radic M, Weigert M (2001) Editors and editing of anti-DNA receptors. Immunity 15:947-957. (Pubitemid 34075375)
18. Peters AL, Stunz LL, Bishop GA (2009) CD40 and autoimmunity: The dark side of a great activator. Semin Immunol 21:293-300.
19. Kishi Y, et al. (2010) Augmented antibody response with premature germinal center regression in CD40L transgenic mice. J Immunol 185:211-219.
20. Higuchi T, et al. (2002) Cutting Edge: Ectopic expression of CD40 ligand on B cells induces lupus-like autoimmune disease. J Immunol 168:9-12. (Pubitemid 34014096)
21. Clegg CH, et al. (1997) Thymus dysfunction and chronic inflammatory disease in gp39 transgenic mice. Int Immunol 9:1111-1122. (Pubitemid 27361754)
22. Berland R, et al. (2006) Toll-like receptor 7-dependent loss of B cell tolerance in pathogenic autoantibody knockin mice. Immunity 25:429-440. (Pubitemid 44376724)
23. 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. (Pubitemid 44354217)
24. Brahms H, et al. (2000) The C-terminal RG dipeptide repeats of the spliceosomal Sm proteins D1 and D3 contain symmetrical dimethylarginines, which form a major B-cell epitope for anti-Sm autoantibodies. J Biol Chem 275:17122-17129. (Pubitemid 30398957)
25. Riemekasten G, et al. (1998) A novel epitope on the C-terminus of SmD1 is recognized by the majority of sera from patients with systemic lupus erythematosus. J Clin Invest 102:754-763. (Pubitemid 28399608)
26. Witsch EJ, Cao H, Fukuyama H, Weigert M (2006) Light chain editing generates polyreactive antibodies in chronic graft-versus-host reaction. J Exp Med 203:1761-1772. (Pubitemid 44036281)
27. Li Y, Li H, Weigert M (2002) Autoreactive B cells in the marginal zone that express dual receptors. J Exp Med 195:181-188. (Pubitemid 34461262)
28. Sekiguchi DR, et al. (2006) Development and selection of edited B cells in B6.56R mice. J Immunol 176:6879-6887. (Pubitemid 43787869)
29. Tsubata T, Wu J, Honjo T (1993) B-cell apoptosis induced by antigen receptor crosslinking is blocked by a T-cell signal through CD40. Nature 364:645-648. (Pubitemid 23274724)
30. Lesley R, Kelly LM, Xu Y, Cyster JG (2006) Naive CD4 T cells constitutively express CD40L and augment autoreactive B cell survival. Proc Natl Acad Sci USA 103: 10717-10722. (Pubitemid 44078043)
31. Van Rooijen N, Sanders A (1994) Liposome mediated depletion of macrophages: Mechanism of action, preparation of liposomes and applications. J Immunol Methods 174:83-93.
32. Witsch EJ, Bettelheim E (2008) Allelic and isotypic light chain inclusion in peripheral B cells from anti-DNA antibody transgenic C57BL/6 and BALB/c mice. J Immunol 180: 3708-3718.
33. Hanayama R, et al. (2002) Identification of a factor that links apoptotic cells to phagocytes. Nature 417:182-187. (Pubitemid 34506799)
34. Khan SN, et al. (2008) Editing and escape from editing in anti-DNA B cells. Proc Natl Acad Sci USA 105:3861-3866. (Pubitemid 351723490)
35. Mandik-Nayak L, Racz J, Sleckman BP, Allen PM (2006) Autoreactive marginal zone B cells are spontaneously activated but lymph node B cells require T cell help. J Exp Med 203:1985-1998. (Pubitemid 44188472)
36. Qian Y, Wang H, Clarke SH (2004) Impaired clearance of apoptotic cells induces the activation of autoreactive anti-Sm marginal zone and B-1 B cells. J Immunol 172: 625-635. (Pubitemid 38020521)
37. Thorn M, Lewis RH, Mumbey-Wafula A, Kantrowitz S, Spatz LA (2010) BAFF overexpression promotes anti-dsDNA B-cell maturation and antibody secretion. Cell Immunol 261:9-22.
38. 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. (Pubitemid 41586947)
39. Oliver AM, Martin F, Gartland GL, Carter RH, Kearney JF (1997) Marginal zone B cells exhibit unique activation, proliferative and immunoglobulin secretory responses. Eur J Immunol 27:2366-2374. (Pubitemid 27404323)
40. Ekland EH, Forster R, Lipp M, Cyster JG (2004) Requirements for follicular exclusion and competitive elimination of autoantigen-binding B cells. J Immunol 172: 4700-4708. (Pubitemid 38456390)
41. Pillai S, Cariappa A, Moran ST (2005) Marginal zone B cells. Annu Rev Immunol 23: 161-196. (Pubitemid 40563168)
42. Bianchi ME (2007) DAMPs, PAMPs and alarmins: All we need to know about danger. J Leukoc Biol 81:1-5.
43. Borrero M, Clarke SH (2002) Low-affinity anti-Smith antigen B cells are regulated by anergy as opposed to developmental arrest or differentiation to B-1. J Immunol 168: 13-21. (Pubitemid 34014097)
44. Huse WD, et al. (1989) Generation of a large combinatorial library of the immunoglobulin repertoire in phage lambda. Science 246:1275-1281. (Pubitemid 20066710)
45. Prak EL, Trounstine M, Huszar D, Weigert M (1994) Light chain editing in kappa-deficient animals: A potential mechanism of B cell tolerance. J Exp Med 180:1805-1815. (Pubitemid 24328571)
46. Ramsden DA, Paige CJ, Wu GE (1994) Kappa light chain rearrangement in mouse fetal liver. J Immunol 153:1150-1160. (Pubitemid 24228506)
47. Retter MW, Nemazee D (1998) Receptor editing occurs frequently during normal B cell development. J Exp Med 188:1231-1238. (Pubitemid 28478011)
48. Schlissel MS, Baltimore D (1989) Activation of immunoglobulin kappa gene rearrangement correlates with induction of germline kappa gene transcription. Cell 58: 1001-1007. (Pubitemid 19227905)
49. Asano K, et al. (2004) Masking of phosphatidylserine inhibits apoptotic cell engulfment and induces autoantibody production in mice. J Exp Med 200:459-467. (Pubitemid 39121903)
50. Carsetti R, Köhler G, Lamers MC (1995) Transitional B cells are the target of negative selection in the B cell compartment. J Exp Med 181:2129-2140.