B-cell receptor for antigen modulates B-cell responses to complex TLR9 agonists and antagonists: Implications for systemic lupus erythematosus

Lupus

Volumn 19, Issue 11, 2010, Pages 1290-1301

  Goeken, J A ^a   Layer, T ^a   Fleenor, S ^a   Laccheo, M ^a   Lenert, Petar ^a  

^a UNIVERSITY OF IOWA   (United States)

Author keywords

B lymphocytes; B cell receptor for antigen; systemic lupus erythematosus; Toll like receptor 9

Indexed keywords

B LYMPHOCYTE RECEPTOR; INTERLEUKIN 6; OLIGONUCLEOTIDE PHOSPHOROTHIOATE; TOLL LIKE RECEPTOR 9; TOLL LIKE RECEPTOR 9 AGONIST; TOLL LIKE RECEPTOR 9 ANTAGONIST; TOLL LIKE RECEPTOR AGONIST; UNCLASSIFIED DRUG;

ANIMAL CELL; APOPTOSIS; ARTICLE; B LYMPHOCYTE ACTIVATION; CONTROLLED STUDY; DRUG EFFECT; DRUG POTENCY; FEMALE; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; SYSTEMIC LUPUS ERYTHEMATOSUS;

ANIMALS; AUTOANTIBODIES; B-LYMPHOCYTES; CELL CYCLE; HUMANS; IMMUNOGLOBULIN M; LUPUS ERYTHEMATOSUS, SYSTEMIC; LYMPHOCYTE ACTIVATION; MICE; MICE, KNOCKOUT; NUCLEIC ACID CONFORMATION; OLIGODEOXYRIBONUCLEOTIDES; RECEPTORS, ANTIGEN, B-CELL; TOLL-LIKE RECEPTOR 9;

EID: 78649742705     PISSN: 09612033     EISSN: None     Source Type: Journal    
DOI: 10.1177/0961203310371157     Document Type: Article

References (43)

1. Takeda K., Kaisho T., Akira S. Toll-like receptors. Annu Rev Immunol 2003 ; 21: 335-376.
2. Hemmi H., Takeuchi O., Kawai T., et al. A toll-like receptor recognizes bacterial DNA. Nature 2000 ; 408: 740-745.
3. Alexopoulou L., Holt AC, Medzhitov R., Flavell RA Recognition of double-stranded RNA and activation of NF-kappaB by Toll-like receptor 3. Nature 2001 ; 413: 732-738.
4. Hemmi H., Kaisho T., Takeuchi O., et al. Small anti-viral compounds activate immune cells via the TLR7 MyD88-dependent signaling pathway. Nat Immunol 2002 ; 3: 196-200.
5. Rifkin IR, Leadbetter EA, Busconi L., Viglianti G., Marshak-Rothstein A. Toll-like receptors, endogenous ligands, and systemic autoimmune disease. Immunol Rev 2005 ; 204: 27-42. (Pubitemid 40460491)
6. Latz E., Schoenemeyer A., Visintin A., et al. TLR9 signals after translocating from the ER to CpG DNA in the lysosome. Nat Immunol 2004 ; 5: 190-198.
7. Tabeta K., Hoebe K., Janssen EM, et al. The Unc93b1 mutation 3d disrupts exogenous antigen presentation and signaling via Toll-like receptors 3, 7 and 9. Nat Immunol 2006 ; 7: 156-164.
8. Kim Y-M., Brinkmann MM, Paquet M-E., Ploegh HL UNC93B1 delivers nucleotide-sensing toll-like receptors to endolysosomes. Nature 2008 ; 452: 234-238.
9. Kono DH, Haraldsson MK, Lawson BR, et al. Endosomal TLR signaling is required for anti-nucleic acid and rheumatoid factor autoantibodies in lupus. Proc Natl Acad Sci U S A 2009 ; 106: 12061-12066.
10. Krug A., Rothenfusser S., Hornung V., et al. Identification of CpG oligonucleotide sequences with high induction of IFN-alpha/beta in plasmocytoid dendritic cells. Eur J Immunol 2001 ; 31: 2154-2163.
11. Verthelyi D., Ishii KJ, Gursel M., Takeshita F., Klinman DM Human peripheral blood cells differentially recognize and respond to two distinct CpG motifs. J Immunol 2001 ; 166: 2372-2377.
12. Kerkmann M., Costa LT, Richter C., et al. Spontaneous formation of nucleic acid-based nanoparticles is responsible for high interferon-a induction by CpG-A in plasmacytoid dendritic cells. J Biol Chem 2005 ; 280: 8086-8093.
13. Hornung V., Rothenfusser S., Britsch S., et al. Quantitative expression of toll-like receptor 1-10 mRNA in cellular subsets of human peripheral blood mononuclear cells and sensitivity to CpG oligodeoxynucleotides. J Immunol 2002 ; 168: 4531-4537.
14. Brummel R., Roberts TL, Stacey KJ, Lenert P. Higher-order CpGDNA stimulation reveals distinct activation requirements for marginal zone and follicular B cells in lupus mice. Eur J Immunol 2006 ; 36: 1951-1962.
15. Ruprecht CR, Lanzavecchia A. Toll-like receptor stimulation as a third signal required for activation of human naive B cells. Eur J Immunol 2006 ; 36: 810-816.
16. Honda K., Ohba Y., Yannai H., et al. Spatiotemporal regulation of MyD88-IRF-7 signaling for robust type-I interferon induction. Nature 2005 ; 434: 1035-1040.
17. Guiducci C., Ott G., Chan JH, et al. Properties regulating the nature of the plasmacytoid dendritic cell response to Toll-like receptor 9 activation. J Exp Med 2006 ; 203: 1999-2008.
18. Lenert P., Yasuda K., Busconi L., et al. DNA-like Class R inhibitory oligonucleotides (INH-ODNs) preferentially block autoantigeninduced B-cell and dendritic cell activation in vitro and autoantibody production in lupus-prone MRL-Faslpr/lpr mice in vivo. Arthritis Res Ther 2009 ; 11: R79.
19. 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.
20. Busconi L., Bauer JW, Tumang JR, et al. Functional outcome of B cell activation by chromatin immune complex engagement of the B cell receptor and TLR9. J Immunol 2007 ; 179: 7397-7405.
21. Poeck H., Wagner M., Battiany J., et al. Plasmacytoid dendritic cells, antigen, and CpG-C license human B cells for plasma cell differentiation and immunoglobulin production in the absence of T-cell help. Blood 2004 ; 103: 3058-3064.
22. 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 ; 5: 49-56.
23. Lenert P. Targeting Toll-like receptor signaling in plasmacytoid dendritic cells and autoreactive B cells as a therapy for lupus. Arthritis Res Ther 2006 ; 8: 203.
24. Ewald SE, Lee BL, Lau L., et al. The ectodomain of Toll-like receptor 9 is cleaved to generate a functional receptor. Nature 2008 ; 456: 658-662.
25. Lenert P., Stunz L., Yi AK, Krieg AM, Ashman RF CpG stimulation of primary mouse B cells is blocked by inhibitory oligodeoxyribonucleotides at a site proximal to NF-κB activation. Antisense Nucleic Acid Drug Dev 2001 ; 11: 247-256.
26. Stunz LL, Lenert P., Peckham D., et al. Inhibitory oligonucleotides specifically block effects of stimulatory CpG oligonucleotides in B cells. Eur J Immunol 2002 ; 32: 1212-1222.
27. Gursel I., Gursel M., Yamada H., Ishii KJ, Takeshita F., Klinman DM Repetitive elements in mammalian telomeres suppress bacterial DNA-induced immune activation. J Immunol 2003 ; 171: 1393-1400.
28. Stacey K., Young GR, Clark F., et al. The molecular basis for the lack of immunostimulatory activity of vertebrate DNA. J Immunol 2003 ; 170: 3614-3620.
29. Duramad O., Fearon KL, Chang B., et al. Inhibitors of TLR-9 act on multiple cell subsets in mouse and man in vitro and prevent death in vivo from systemic inflammation. J Immunol 2005 ; 174: 5193-5200.
30. Lenert P., Rasmussen W., Ashman RF, Ballas ZK Structural characterization of the inhibitory DNA motif for the type A[D]-CpGinduced cytokine secretion and NK-cell lytic activity in mouse spleen cells. DNA Cell Biol 2003 ; 22: 621-631.
31. Leadbetter EA, Rifkin IR, Hohlbaum AM, Beaudette BC, Schlomchik MJ, Marshak-Rothstein A. Chromatin-IgG complexes activate B cells by dual engagement of IgM and Toll-like receptors. Nature 2002 ; 416: 603-607.
32. Lau CM, Broughton C., Tabor AS, et al. RNA-associated autoantigens activate B cells by combined B cell antigen receptor/Toll-like receptor 7 engagement. J Exp Med 2005 ; 202: 1171-1177.
33. Lenert P. Inhibitory oligodeoxynucleotides - therapeutic promise for systemic autoimmune diseases? Clin Exp Immunol 2005 ; 140: 1-10.
34. Brummel R., Lenert P. Activation of marginal zone B cells from lupus mice with type A(D) CpG-oligodeoxynucleotides. J Immunol 2005 ; 174: 2429-2434. (Pubitemid 40223993)
35. Avalos AM, Latz E., Mousseau B., et al. Differential cytokine production and bystander activation of autoreactive B cells in response to CpG-A and CpG-B oligonucleotides. J Immunol 2009 ; 183: 6262-6268.
36. Lenert P., Goeken A., Handwerger B., Ashman RF Innate immune responses in lupus-prone Palmerston North mice: Differential responses to LPS and bacterial-DNA/CpG-oligonucleotides. J Clin Immunol 2003 ; 23: 202-213.
37. Lenert P., Brummel R., Field EH, Ashman RF TLR-9 activation of marginal zone B cells in lupus mice regulates immunity through increased IL-10 production. J Clin Immunol 2005 ; 25: 29-40.
38. Lian ZX, Kikuchi K., Yang GX, Ansari AA, Ikehara S., Gershwin ME Expansion of bone marrow IFN-alpha-producing dendritic cells in New Zealand Black (NZB) mice: high level expression of TLR9 and secretion of IFN-alpha in NZB bone marrow. J Immunol 2004 ; 173: 5283-5289.
39. Anders HJ, Vielhauer V., Eis V., et al. Activation of toll-like receptor-9 induces progression of renal disease in MRL-Fas(lpr) mice. FASEB J 2004 ; 18: 534-536.
40. Shlomchik MJ, Zharhary D., Camper S., Saunders T., Weigert MP A rheumatoid factor transgenic mouse model of autoantibody regulation. Int Immunol 1993 ; 5: 1329-1341.
41. 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.
42. 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.
43. Pons-Estel GJ, Alarcón GS, McGwin Jr G., et al. Protective effect of hydroxychloroquine on renal damage in patients with lupus nephritis: LXV, data from a multiethnic US cohort. Arthritis Rheum 2009 ; 61: 830-839.