Cutting edge: DNase II deficiency prevents activation of autoreactive B cells by double-stranded DNA endogenous ligands

Journal of Immunology

Volumn 194, Issue 4, 2015, Pages 1403-1407

  Pawaria, Sudesh ^a   Moody, Krishna ^a,b   Busto, Patricia ^a   Nundel, Kerstin ^a   Choi, Chee Ho ^c   Ghayur, Tariq ^c   Marshak Rothstein, Ann ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^b BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c Abbvie Bioresearch Center   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AUTOANTIBODY; AUTOANTIGEN; B LYMPHOCYTE RECEPTOR; CPG OLIGODEOXYNUCLEOTIDE; DEOXYRIBONUCLEASE II; DNA DUAL VARIABLE DOMAIN IMMUNOGLOBULIN MOLECULE; DOUBLE STRANDED DNA; IMMUNOGLOBULIN; IMMUNOGLOBULIN M; IMMUNOGLOBULIN M ANTIBODY; LIGAND; TOLL LIKE RECEPTOR 9; UNCLASSIFIED DRUG; DEOXYRIBONUCLEASE; DNA; LYMPHOCYTE ANTIGEN RECEPTOR; TLR9 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY PRODUCTION; ANTIBODY SPECIFICITY; ANTIGEN ANTIBODY COMPLEX; ANTIGEN DETECTION; ARTICLE; B LYMPHOCYTE ACTIVATION; BIOSENSOR; CONTROLLED STUDY; CYTOSOL; DNA DEGRADATION; ENDOSOME; ENZYME DEFICIENCY; GENE INACTIVATION; MOUSE; NONHUMAN; POLYCLONAL ACTIVATION; SPLENOMEGALY; ANIMAL; AUTOIMMUNITY; B LYMPHOCYTE; DEFICIENCY; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; HUMAN; IMMUNOLOGY; KNOCKOUT MOUSE; LYMPHOCYTE ACTIVATION;

ANIMALS; ANTIBODY SPECIFICITY; AUTOANTIBODIES; AUTOANTIGENS; AUTOIMMUNITY; B-LYMPHOCYTES; DNA; ENDODEOXYRIBONUCLEASES; ENZYME-LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; HUMANS; LIGANDS; LYMPHOCYTE ACTIVATION; MICE; MICE, KNOCKOUT; RECEPTORS, ANTIGEN, B-CELL; TOLL-LIKE RECEPTOR 9;

EID: 84922552164     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1402893     Document Type: Article

References (25)

1. Yoshida, H., Y. Okabe, K. Kawane, H. Fukuyama, and S. Nagata. 2005. Lethal anemia caused by interferon-beta produced in mouse embryos carrying undigested DNA. Nat. Immunol. 6: 49-56.
2. Kawane, K., M. Ohtani, K. Miwa, T. Kizawa, Y. Kanbara, Y. Yoshioka, H. Yoshikawa, and S. Nagata. 2006. Chronic polyarthritis caused by mammalian DNA that escapes from degradation in macrophages. Nature 443: 998-1002.
3. Ahn, J., D. Gutman, S. Saijo, and G. N. Barber. 2012. STING manifests self DNA-dependent inflammatory disease. Proc. Natl. Acad. Sci. USA 109: 19386-19391.
4. Leadbetter, E. A., I. R. Rifkin, A. M. Hohlbaum, B. C. Beaudette, M. J. Shlomchik, and A. Marshak-Rothstein. 2002. Chromatin-IgG complexes activate B cells by dual engagement of IgM and Toll-like receptors. Nature 416: 603-607.
5. Plotz, P. H. 2003. The autoantibody repertoire: searching for order. Nat. Rev. Immunol. 3: 73-78.
6. Busconi, L., C. M. Lau, A. S. Tabor, M. B. Uccellini, Z. Ruhe, S. Akira, G. A. Viglianti, I. R. Rifkin, and A. Marshak-Rothstein. 2006. DNA and RNA autoantigens as autoadjuvants. J. Endotoxin Res. 12: 379-384.
7. Lau, C. M., C. Broughton, A. S. Tabor, S. Akira, R. A. Flavell, M. J. Mamula, S. R. Christensen, M. J. Shlomchik, G. A. Viglianti, I. R. Rifkin, and A. MarshakRothstein. 2005. RNA-associated autoantigens activate B cells by combined B cell antigen receptor/Toll-like receptor 7 engagement. J. Exp. Med. 202: 1171-1177.
8. Christensen, S. R., J. Shupe, K. Nickerson, M. Kashgarian, R. A. Flavell, and M. J. Shlomchik. 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.
9. Kono, D. H., M. K. Haraldsson, B. R. Lawson, K. M. Pollard, Y. T. Koh, X. Du, C. N. Arnold, R. Baccala, G. J. Silverman, B. A. Beutler, and A. N. Theofilopoulos. 2009. Endosomal TLR signaling is required for anti-nucleic acid and rheumatoid factor autoantibodies in lupus. Proc. Natl. Acad. Sci. USA 106: 12061-12066.
10. Jackson, S. W., N. E. Scharping, N. S. Kolhatkar, S. Khim, M. A. Schwartz, Q. Z. Li, K. L. Hudkins, C. E. Alpers, D. Liggitt, and D. J. Rawlings. 2014. Opposing impact of B cell-intrinsic TLR7 and TLR9 signals on autoantibody repertoire and systemic inflammation. J. Immunol. 192: 4525-4532.
11. Kawane, K., H. Tanaka, Y. Kitahara, S. Shimaoka, and S. Nagata. 2010. Cytokine-dependent but acquired immunity-independent arthritis caused by DNA escaped from degradation. Proc. Natl. Acad. Sci. USA 107: 19432-19437.
12. Baum, R., S. Sharma, S. Carpenter, Q.-Z. Li, P. Busto, K. A. Fitzgerald, A. Marshak-Rothstein, and E. Gravallese. 2014. Cutting Edge: AIM2 and endosomal TLRs differentially regulate arthritis and autoantibody production in DNase II-deficient mice. J. Immunol. 194: 873-877.
13. Uccellini, M. B., L. Busconi, N. M. Green, P. Busto, S. R. Christensen, M. J. Shlomchik, A. Marshak-Rothstein, and G. A. Viglianti. 2008. Autoreactive B cells discriminate CpG-rich and CpG-poor DNA and this response is modulated by IFN-alpha. J. Immunol. 181: 5875-5884.
14. Julius, M. H., C. H. Heusser, and K. U. Hartmann. 1984. Induction of resting B cells to DNA synthesis by soluble monoclonal anti-immunoglobulin. Eur. J. Immunol. 14: 753-757.
15. Wu, C., H. Ying, S. Bose, R. Miller, L. Medina, L. Santora, and T. Ghayur. 2009. Molecular construction and optimization of anti-human IL-1alpha/beta dual variable domain immunoglobulin (DVD-Ig) molecules. MAbs 1: 339-347.
16. Nündel, K., P. Busto, M. Debatis, and A. Marshak-Rothstein. 2013. The role of Bruton's tyrosine kinase in the development and BCR/TLR-dependent activation of AM14 rheumatoid factor B cells. J. Leukoc. Biol. 94: 865-875.
17. Christensen, S. R., M. Kashgarian, L. Alexopoulou, R. A. Flavell, S. Akira, and M. J. Shlomchik. 2005. Toll-like receptor 9 controls anti-DNA autoantibody production in murine lupus. J. Exp. Med. 202: 321-331.
18. -/-) mice. J. Exp. Med. 195: 1167-1174.
19. Tabeta, K., K. Hoebe, E. M. Janssen, X. Du, P. Georgel, K. Crozat, S. Mudd, N. Mann, S. Sovath, J. Goode, et al. 2006. The Unc93b1 mutation 3d disrupts exogenous antigen presentation and signaling via Toll-like receptors 3, 7 and 9. Nat. Immunol. 7: 156-164.
20. Kina, T., K. Ikuta, E. Takayama, K. Wada, A. S. Majumdar, I. L. Weissman, and Y. Katsura. 2000. The monoclonal antibody TER-119 recognizes a molecule associated with glycophorin A and specifically marks the late stages of murine erythroid lineage. Br. J. Haematol. 109: 280-287.
21. Wu, C., H. Ying, C. Grinnell, S. Bryant, R. Miller, A. Clabbers, S. Bose, D. McCarthy, R. R. Zhu, L. Santora, et al. 2007. Simultaneous targeting of multiple disease mediators by a dual-variable-domain immunoglobulin. Nat. Biotechnol. 25: 1290-1297.
22. Kawane, K., H. Fukuyama, G. Kondoh, J. Takeda, Y. Ohsawa, Y. Uchiyama, and S. Nagata. 2001. Requirement of DNase II for definitive erythropoiesis in the mouse fetal liver. Science 292: 1546-1549.
23. Evans, C. J., and R. J. Aguilera. 2003. DNase II: genes, enzymes and function. Gene 322: 1-15.
24. Yu, P., U. Wellmann, S. Kunder, L. Quintanilla-Martinez, L. Jennen, N. Dear, K. Amann, S. Bauer, T. H. Winkler, and H. Wagner. 2006. Toll-like receptor 9-independent aggravation of glomerulonephritis in a novel model of SLE. Int. Immunol. 18: 1211-1219.
25. Stoehr, A. D., C. T. Schoen, M. M. Mertes, S. Eiglmeier, V. Holecska, A. K. Lorenz, T. Schommartz, A. L. Schoen, C. Hess, A. Winkler, et al. 2011. TLR9 in peritoneal B-1b cells is essential for production of protective self-reactive IgM to control Th17 cells and severe autoimmunity. J. Immunol. 187: 2953-2965.