Regulation of autoreactive B cell responses to endogenous TLR ligands

References

• Wolfowicz CB, Lyons S, Mahon CA, Marshak-Rothstein A, Rothstein TL. Isolation of self-recognizing IgG2a monoclonal rheumatoid factors. Clin Immunol Immunopathol. 1989; 52:313–322.
   PubMedGoogle Scholar
• Hannum LG, Ni D, Haberman AM, Weigert MG, Shlomchik MJ. 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. 1996; 184:1269–1278.
   PubMed Web of Science ®Google Scholar
• Wang H, Shlomchik MJ. Autoantigen-specific B cell activation in Fas-deficient rheumatoid factor immunoglobulin transgenic mice. J Exp Med. 1999; 190:639–649.
   PubMed Web of Science ®Google Scholar
• Leadbetter EA, Rifkin IR, Hohlbaum AM, Beaudette BC, Shlomchik MJ, Marshak-Rothstein A. Chromatin-IgG complexes activate B cells by dual engagement of IgM and toll-like receptors. Nature. 2002; 416:603–607.
   PubMed Web of Science ®Google Scholar
• Viglianti GA, Lau CM, Hanley TM, Miko BA, Shlomchik MJ, Marshak-Rothstein A. Activation of autoreactive B cells by CpG dsDNA. Immunity. 2003; 19:837–847.
   PubMed Web of Science ®Google Scholar
• Lau CM, Broughton C, Tabor AS, Akira S, Flavell RA, Mamula MJ, Christensen SR, Shlomchik MJ, Viglianti GA, Rifkin IR, Marshak-Rothstein A. RNA-associated autoantigens activate B cells by combined B cell antigen receptor/toll-like receptor 7 engagement. J Exp Med. 2005; 202:1171–1177.
   PubMed Web of Science ®Google Scholar
• Hemmi H, Takeuchi O, Kawai T, Kaisho T, Sato S, Sanjo H, Matsumoto M, Hoshino K, Wagner H, Takeda K, Akira S. A toll-like receptor recognizes bacterial DNA. Nature. 2000; 408:740–745.
   PubMed Web of Science ®Google Scholar
• Diebold SS, Kaisho T, Hemmi H, Akira S. Reis e Sousa C. Innate antiviral responses by means of TLR7-mediated recognition of single-stranded RNA. Science. 2004; 303:1529–1531.
   Google Scholar
• Heil F, Hemmi H, Hochrein H, Ampenberger F, Kirschning C, Akira S, Lipford G, Wagner H, Bauer S. Species-specific recognition of single-stranded RNA via toll-like receptor 7 and 8. Science. 2004; 303:1526–1529.
   PubMed Web of Science ®Google Scholar
• Lund JM, Alexopoulou L, Sato A, Karow M, Adams NC, Gale NW, Iwasaki A, Flavell RA. Recognition of single-stranded RNA viruses by toll-like receptor 7. Proc Natl Acad Sci USA. 2004; 101:5598–5603.
   PubMed Web of Science ®Google Scholar
• Chaturvedi A, Dorward D, Pierce SK. The B cell receptor governs the subcellular location of toll-like receptor 9 leading to hyperresponses to DNA-containing antigens. Immunity. 2008; 28:799–809.
   PubMed Web of Science ®Google Scholar
• Boule MW, Broughton C, Mackay F, Akira S, Marshak-Rothstein A, Rifkin IR. Toll-like receptor 9-dependent and -independent dendritic cell activation by chromatin-immunoglobulin G complexes. J Exp Med. 2004; 199:1631–1640 Epub 2004 Jun 14.
   PubMed Web of Science ®Google Scholar
• Means TK, Latz E, Hayashi F, Murali MR, Golenbock DT, Luster AD. Human lupus autoantibody-DNA complexes activate DCs through cooperation of CD32 and TLR9. J Clin Invest. 2005; 115:407–417.
   PubMed Web of Science ®Google Scholar
• Uccellini MB, Busconi L, Green NM, Busto P, Christensen SR, Shlomchik MJ, Marshak-Rothstein A, Viglianti GA. Autoreactive B cells discriminate CpG-rich and CpG-poor DNA and this response is modulated by IFN-alpha. J Immunol. 2008; 181:5875–5884.
   PubMed Web of Science ®Google Scholar
• Dal Porto JM, Gauld SB, Merrell KT, Mills D, Pugh-Bernard AE. Cambier J. B cell antigen receptor signaling 101. Mol Immunol. 2004; 41:599–613.
   PubMed Web of Science ®Google Scholar
• Busconi L, Bauer JW, Tumang JR, Laws A, Perkins-Mesires K, Tabor AS, Lau C, Corley RB, Rothstein TL, Lund FE, Behrens TW, Marshak-Rothstein A. Functional outcome of B cell activation by chromatin immune complex engagement of the B cell receptor and TLR9. J Immunol. 2007; 179:7397–7405.
   PubMed Web of Science ®Google Scholar
• Jun JE, Goodnow CC. Scaffolding of antigen receptors for immunogenic versus tolerogenic signaling. Nat Immunol. 2003; 4:1057–1064.
   PubMed Web of Science ®Google Scholar
• Krieg AM. CpG motifs in bacterial DNA and their immune effects. Annu Rev Immunol. 2002; 20:709–760.
   PubMed Web of Science ®Google Scholar
• O'Neill SK, Veselits ML, Zhang M, Labno C, Cao Y, Finnegan A, Uccellini M, Alegre ML, Cambier JC, Clark MR. Endocytic sequestration of the B cell antigen receptor and toll-like receptor 9 in anergic cells. Proc Natl Acad Sci USA. 2009; 106:6262–6267.
   PubMed Web of Science ®Google Scholar
• Barton GM, Kagan JC, Medzhitov R. Intracellular localization of toll-like receptor 9 prevents recognition of self DNA but facilitates access to viral DNA. Nat Immunol. 2006; 7:49–56.
   PubMed Web of Science ®Google Scholar
• Haas T, Metzger J, Schmitz F, Heit A, Muller T, Latz E, Wagner H. The DNA sugar backbone 2′ deoxyribose determines toll-like receptor 9 activation. Immunity. 2008; 28:315–323.
   PubMed Web of Science ®Google Scholar
• Krieg AM, Yi AK, Matson S, Waldschmidt TJ, Bishop GA, Teasdale R, Koretzky GA, Klinman DM. CpG motifs in bacterial DNA trigger direct B-cell activation. Nature. 1995; 374:546–549.
   PubMed Web of Science ®Google Scholar
• Cross SH, Bird AP. CpG islands and genes. Curr Opin Genet Dev. 1995; 5:309–314.
   PubMed Web of Science ®Google Scholar
• Uccellini MB, Avalos AM, Marshak-Rothstein A, Viglianti GA. Toll-like receptor-dependent immune complex activation of B cells and dendritic cells. Methods Mol Biol. 2009; 517:363–380.
   PubMedGoogle Scholar
• Kariko K, Buckstein M, Ni H, Weissman D. Suppression of RNA recognition by toll-like receptors: The impact of nucleoside modification and the evolutionary origin of RNA. Immunity. 2005; 23:165–175.
   PubMed Web of Science ®Google Scholar
• Baechler EC, Batliwalla FM, Karypis G, Gaffney PM, Ortmann WA, Espe KJ, Shark KB, Grande WJ, Hughes KM, Kapur V, Gregersen PK, Behrens TW. Interferon-inducible gene expression signature in peripheral blood cells of patients with severe lupus. Proc Natl Acad Sci USA. 2003; 100:2610–2615.
   PubMed Web of Science ®Google Scholar
• Jego G, Palucka AK, Blanck JP, Chalouni C, Pascual V, Banchereau J. Plasmacytoid dendritic cells induce plasma cell differentiation through type I interferon and interleukin 6. Immunity. 2003; 19:225–234.
   PubMed Web of Science ®Google Scholar
• Lau CM, Broughton C, Tabor AS, Akira S, Flavell RA, Mamula MJ, Christensen SR, Shlomchik MJ, Viglianti GA, Rifkin IR, Marshak-Rothstein A. RNA-associated autoantigens activate B cells by combined B cell antigen receptor/toll-like receptor 7 engagement. J Exp Med. 2005; 202:1171–1177.
   PubMed Web of Science ®Google Scholar
• Green NM, Laws A, Kiefer K, Busconi L, Kim YM, Brinkmann MM, Trail EH, Yasuda K, Christensen SR, Shlomchik MJ, Vogel S, Connor JH, Ploegh H, Eilat D, Rifkin IR, van Seventer JM, Marshak-Rothstein A. Murine B cell response to TLR7 ligands depends on an IFN-{beta} Feedback Loop. J Immunol. 2009; 183:1569–1576.
   PubMed Web of Science ®Google Scholar
• Braun D, Caramalho I, Demengeot J. IFN-alpha/beta enhances BCR-dependent B cell responses. Int Immunol. 2002; 14:411–419.
   PubMed Web of Science ®Google Scholar
• Ravetch JV, Bolland S. IgG Fc receptors. Annu Rev Immunol. 2001; 19:275–290.
   PubMed Web of Science ®Google Scholar
• Takai T, Ono M, Hikida M, Ohmori H, Ravetch JV. Augmented humoral and anaphylactic responses in Fc gamma RII-deficient mice. Nature. 1996; 379:346–349.
   PubMed Web of Science ®Google Scholar
• Bolland S, Ravetch JV. Spontaneous autoimmune disease in Fc(gamma)RIIB-deficient mice results from strain-specific epistasis. Immunity. 2000; 13:277–285.
   PubMed Web of Science ®Google Scholar
• Jiang Y, Hirose S, Abe M, Sanokawa-Akakura R, Ohtsuji M, Mi X, Li N, Xiu Y, Zhang D, Shirai J, Hamano Y, Fujii H, Shirai T. Polymorphisms in IgG Fc receptor IIB regulatory regions associated with autoimmune susceptibility. Immunogenetics. 2000; 51:429–435.
   PubMed Web of Science ®Google Scholar
• Isaak A, Gergely PJr, Szekeres Z, Prechl J, Poor G, Erdei A, Gergely J. Physiological up-regulation of inhibitory receptors Fc gamma RII and CR1 on memory B cells is lacking in SLE patients. Int Immunol. 2008; 20:185–192.
   PubMed Web of Science ®Google Scholar
• Mackay M, Stanevsky A, Wang T, Aranow C, Li M, Koenig S, Ravetch JV, Diamond B. Selective dysregulation of the FcgammaIIB receptor on memory B cells in SLE. J Exp Med. 2006; 203:2157–2164.
   PubMed Web of Science ®Google Scholar
• Su K, Yang H, Li X, Gibson AW, Cafardi JM, Zhou T, Edberg JC, Kimberly RP. Expression profile of FcgammaRIIb on leukocytes and its dysregulation in systemic lupus erythematosus. J Immunol. 2007; 178:3272–3280.
   PubMed Web of Science ®Google Scholar
• Phillips NE, Parker DC. Cross-linking of B lymphocyte Fc gamma receptors and membrane immunoglobulin inhibits anti-immunoglobulin-induced blastogenesis. J Immunol. 1984; 132:627–632.
   PubMed Web of Science ®Google Scholar
• Rifkin IR, Leadbetter EA, Beaudette BC, Kiani C, Monestier M, Shlomchik MJ, Marshak-Rothstein A. Immune complexes present in the sera of autoimmune mice activate rheumatoid factor B cells. J Immunol. 2000; 165:1626–1633.
   PubMed Web of Science ®Google Scholar
• Nimmerjahn F, Bruhns P, Horiuchi K, Ravetch JV. FcgammaRIV: A novel FcR with distinct IgG subclass specificity. Immunity. 2005; 23:41–51.
   PubMed Web of Science ®Google Scholar
• William J, Euler C, Christensen S, Shlomchik MJ. Evolution of autoantibody responses via somatic hypermutation outside of germinal centers. Science. 2002; 297:2066–2070.
   PubMed Web of Science ®Google Scholar
• Herlands RA, William J, Hershberg U, Shlomchik MJ. Anti-chromatin antibodies drive in vivo antigen-specific activation and somatic hypermutation of rheumatoid factor B cells at extrafollicular sites. Eur J Immunol. 2007; 37:3339–3351.
   PubMed Web of Science ®Google Scholar
• Herlands RA, Christensen SR, Sweet RA, Hershberg U, Shlomchik MJ. T cell-independent and toll-like receptor-dependent antigen-driven activation of autoreactive B cells. Immunity. 2008; 29:249–260.
   PubMed Web of Science ®Google Scholar
• Bolland S, Yim YS, Tus K, Wakeland EK, Ravetch JV. Genetic modifiers of systemic lupus erythematosus in FcgammaRIIB( − / − ) mice. J Exp Med. 2002; 195:1167–1174.
   PubMed Web of Science ®Google Scholar
• Pisitkun P, Deane JA, Difilippantonio MJ, Tarasenko T, Satterthwaite AB, Bolland S. Autoreactive B cell responses to RNA-related antigens due to TLR7 gene duplication. Science. 2006; 312:1669–1672.
   PubMed Web of Science ®Google Scholar
• Subramanian S, Tus K, Li QZ, Wang A, Tian XH, Zhou J, Liang C, Bartov G, McDaniel LD, Zhou XJ, Schultz RA, Wakeland EK. A Tlr7 translocation accelerates systemic autoimmunity in murine lupus. Proc Natl Acad Sci USA. 2006; 103:9970–9975.
   PubMed Web of Science ®Google Scholar
• Deane JA, Pisitkun P, Barrett RS, Feigenbaum L, Town T, Ward JM, Flavell RA, Bolland S. Control of toll-like receptor 7 expression is essential to restrict autoimmunity and dendritic cell proliferation. Immunity. 2007; 27:801–810.
   PubMed Web of Science ®Google Scholar
• Fairhurst AM, Hwang SH, Wang A, Tian XH, Boudreaux C, Zhou XJ, Casco J, Li QZ, Connolly JE, Wakeland EK. Yaa autoimmune phenotypes are conferred by overexpression of TLR7. Eur J Immunol. 2008; 38:1971–1978.
   PubMed Web of Science ®Google Scholar
• Santiago-Raber ML, Kikuchi S, Borel P, Uematsu S, Akira S, Kotzin BL, Izui S. Evidence for genes in addition to Tlr7 in the Yaa translocation linked with acceleration of systemic lupus erythematosus. J Immunol. 2008; 181:1556–1562.
   PubMed Web of Science ®Google Scholar
• Christensen SR, Shupe J, Nickerson K, Kashgarian M, Flavell RA, Shlomchik MJ. Toll-like receptor 7 and TLR9 dictate autoantibody specificity and have opposing inflammatory and regulatory roles in a murine model of lupus. Immunity. 2006; 25:417–428.
   PubMed Web of Science ®Google Scholar
• Lee PY, Kumagai Y, Li Y, Takeuchi O, Yoshida H, Weinstein J, Kellner ES, Nacionales D, Barker T, Kelly-Scumpia K, van Rooijen N, Kumar H, Kawai T, Satoh M, Akira S, Reeves WH. TLR7-dependent and FcgammaR-independent production of type I interferon in experimental mouse lupus. J Exp Med. 2008; 205:2995–3006.
   PubMed Web of Science ®Google Scholar
• Savarese E, Steinberg C, Pawar RD, Reindl W, Akira S, Anders HJ, Krug A. Requirement of toll-like receptor 7 for pristane-induced production of autoantibodies and development of murine lupus nephritis. Arthritis Rheum. 2008; 58:1107–1115.
   PubMed Web of Science ®Google Scholar
• Christensen SR, Kashgarian M, Alexopoulou L, Flavell RA, Akira S, Shlomchik MJ. Toll-like receptor 9 controls anti-DNA autoantibody production in murine lupus. J Exp Med. 2005; 202:321–331.
   PubMed Web of Science ®Google Scholar
• Sadik CD, Bachmann M, Pfeilschifter J, Muhl H. Activation of interferon regulatory factor-3 via toll-like receptor 3 and immunomodulatory functions detected in A549 lung epithelial cells exposed to misplaced U1-snRNA. Nucleic Acids Res. 2009; 37:5041–5056.
   PubMed Web of Science ®Google Scholar
• Wu X, Peng SL. Toll-like receptor 9 signaling protects against murine lupus. Arthritis Rheum. 2006; 54:336–342.
   PubMed Web of Science ®Google Scholar
• Yu P, Wellmann U, Kunder S, Quintanilla-Martinez L, Jennen L, Dear N, Amann K, Bauer S, Winkler TH, Wagner H. Toll-like receptor 9-independent aggravation of glomerulonephritis in a novel model of SLE. Int Immunol. 2006; 18:1211–1219.
   PubMed Web of Science ®Google Scholar
• Kono DH, Haraldsson MK, Lawson BR, Pollard KM, Koh YT, Du X, Arnold CN, Baccala R, Silverman GJ, Beutler BA, Theofilopoulos AN. Endosomal TLR signaling is required for anti-nucleic acid and rheumatoid factor autoantibodies in lupus. Proc Natl Acad Sci USA. 2009; 106:12061–12066.
   PubMed Web of Science ®Google Scholar
• Ehlers M, Fukuyama H, McGaha TL, Aderem A, Ravetch JV. TLR9/MyD88 signaling is required for class switching to pathogenic IgG2a and 2b autoantibodies in SLE. J Exp Med. 2006; 203:553–561.
   PubMed Web of Science ®Google Scholar
• Eckl-Dorna J, Batista FD. BCR-mediated uptake of antigen linked to TLR9 ligand stimulates B-cell proliferation and antigen-specific plasma cell formation. Blood. 2009; 113:3969–3977.
   PubMed Web of Science ®Google Scholar
• Baudino L, Azeredo da Silveira S, Nakata M, Izui S. Molecular and cellular basis for pathogenicity of autoantibodies: Lessons from murine monoclonal autoantibodies. Springer Semin Immunopathol. 2006; 28:175–184.
   PubMed Web of Science ®Google Scholar
• Dhodapkar KM, Banerjee D, Connolly J, Kukreja A, Matayeva E, Veri MC, Ravetch JV, Steinman RM, Dhodapkar MV. Selective blockade of the inhibitory Fcgamma receptor (FcgammaRIIB) in human dendritic cells and monocytes induces a type I interferon response program. J Exp Med. 2007; 204:1359–1369.
   PubMed Web of Science ®Google Scholar
• Blanco P, Palucka AK, Gill M, Pascual V, Banchereau J. Induction of dendritic cell differentiation by IFN-alpha in systemic lupus erythematosus. Science. 2001; 294:1540–1543.
   PubMed Web of Science ®Google Scholar
• Hron JD, Peng SL. Type IIFN protects against murine lupus. J Immunol. 2004; 173:2134–2142.
   PubMed Web of Science ®Google Scholar
• Nacionales DC, Kelly-Scumpia KM, Lee PY, Weinstein JS, Lyons R, Sobel E, Satoh M, Reeves WH. Deficiency of the type I interferon receptor protects mice from experimental lupus. Arthritis Rheum. 2007; 56:3770–3783.
   PubMed Web of Science ®Google Scholar
• Jorgensen TN, Roper E, Thurman JM, Marrack P, Kotzin BL. Type I interferon signaling is involved in the spontaneous development of lupus-like disease in B6.Nba2 and (B6.Nba2 x NZW)F(1) mice. Genes Immun. 2007; 8:653–662.
   PubMed Web of Science ®Google Scholar