Autoantibody induction by DNA-containing immune complexes requires HMGB1 with the TLR2/MicroRNA-155 pathway

Journal of Immunology

Volumn 190, Issue 11, 2013, Pages 5411-5422

  Wen, Zhenke ^a   Xu, Lin ^a   Chen, Xi ^a   Xu, Wei ^b   Yin, Zhinan ^c   Gao, Xiaoming ^b   Xiong, Sidong ^a,b  

^a FUDAN UNIVERSITY   (China)

^b SOOCHOW UNIVERSITY   (China)

^c NANKAI UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

DOUBLE STRANDED DNA ANTIBODY; HIGH MOBILITY GROUP B1 PROTEIN; MICRORNA 155; TOLL LIKE RECEPTOR 2;

ADULT; ANTIBODY BLOOD LEVEL; ANTIBODY PRODUCTION; ANTIGEN ANTIBODY COMPLEX; ARTICLE; CYTOKINE PRODUCTION; DISEASE ACTIVITY; GENE EXPRESSION; GENE TARGETING; HUMAN; HUMAN CELL; IMMUNOPATHOGENESIS; IMMUNOSTIMULATION; LUPUS ERYTHEMATOSUS NEPHRITIS; MAJOR CLINICAL STUDY; PRIORITY JOURNAL; PROTEIN CONTENT; PROTEIN FUNCTION; SEROLOGY; SYSTEMIC LUPUS ERYTHEMATOSUS; UPREGULATION;

ANTIBODIES, ANTINUCLEAR; ANTIGEN-ANTIBODY COMPLEX; AUTOANTIBODIES; CELLS, CULTURED; DNA; GENE EXPRESSION REGULATION; HMGB1 PROTEIN; HUMANS; LUPUS ERYTHEMATOSUS, SYSTEMIC; MICRORNAS; MODELS, BIOLOGICAL; MYELOID DIFFERENTIATION FACTOR 88; PROTO-ONCOGENE PROTEIN C-ETS-1; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 2;

EID: 84878045716     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1203301     Document Type: Article

References (56)

1. Chung, S. A., K. E. Taylor, R. R. Graham, J. Nititham, A. T. Lee, W. A. Ortmann, C. O. Jacob, M. E. Alarcón-Riquelme, B. P. Tsao, J. B. Harley, et al SLEGEN. 2011. Differential genetic associations for systemic lupus erythematosus based on anti-dsDNA autoantibody production. PLoS Genet. 7: e1001323.
2. Ching, K. H., P. D. Burbelo, C. Tipton, C. Wei, M. Petri, I. Sanz, and M. J. Iadarola. 2012. Two major autoantibody clusters in systemic lupus erythematosus. PLoS ONE 7: e32001.
3. Arbuckle, M. R., M. T. McClain, M. V. Rubertone, R. H. Scofield, G. J. Dennis, J. A. James, and J. B. Harley. 2003. Development of autoantibodies before the clinical onset of systemic lupus erythematosus. N. Engl. J. Med. 349: 1526-1533. (Pubitemid 37255038)
4. Isenberg, D. A., J. J. Manson, M. R. Ehrenstein, and A. Rahman. 2007. Fifty years of anti-ds DNA antibodies: are we approaching journey's end? Rheumatology (Oxford) 46: 1052-1056. (Pubitemid 47050602)
5. Swaak, A. J., J. Groenwold, L. A. Aarden, L. W. Statius van Eps, and E. W. Feltkamp. 1982. Prognostic value of anti-dsDNA in SLE. Ann. Rheum. Dis. 41: 388-395. (Pubitemid 12038906)
6. von Mühlen, C. A., and E. M. Tan. 1995. Autoantibodies in the diagnosis of systemic rheumatic diseases. Semin. Arthritis Rheum. 24: 323-358.
7. Rahman, A., and D. A. Isenberg. 2008. Systemic lupus erythematosus. N. Engl. J. Med. 358: 929-939. (Pubitemid 351397092)
8. Sanz, I., and F. E. Lee. 2010. B cells as therapeutic targets in SLE. Nat Rev Rheumatol 6: 326-337.
9. Wen, Z., L. Xu, W. Xu, and S. Xiong. 2012. Production of anti-double-stranded DNA antibodies in activated lymphocyte derived DNA induced lupus model was dependent on CD4+ T cells. Lupus 21: 508-516.
10. Atamaniuk, J., Y. Y. Hsiao, M. Mustak, D. Bernhard, L. Erlacher, M. Fodinger, B. Tiran, and K. M. Stuhlmeier. 2011. Analysing cell-free plasma DNA and SLE disease activity. Eur. J. Clin. Invest. 41: 579-583.
11. Means, T. K., E. Latz, F. Hayashi, M. R. Murali, D. T. Golenbock, and A. D. Luster. 2005. Human lupus autoantibody-DNA complexes activate DCs through cooperation of CD32 and TLR9. J. Clin. Invest. 115: 407-417. (Pubitemid 40385482)
12. Barrat, F. J., T. Meeker, J. Gregorio, J. H. Chan, S. Uematsu, S. Akira, B. Chang, O. Duramad, and R. L. Coffman. 2005. Nucleic acids of mammalian origin can act as endogenous ligands for Toll-like receptors and may promote systemic lupus erythematosus. J. Exp. Med. 202: 1131-1139. (Pubitemid 41464506)
13. Marshak-Rothstein, A. 2006. Toll-like receptors in systemic autoimmune disease. Nat. Rev. Immunol. 6: 823-835. (Pubitemid 44631651)
14. 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. (Pubitemid 34406754)
15. Viglianti, G. A., C. M. Lau, T. M. Hanley, B. A. Miko, M. J. Shlomchik, and A. Marshak-Rothstein. 2003. Activation of autoreactive B cells by CpG dsDNA. Immunity 19: 837-847. (Pubitemid 37542304)
16. 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. Marshak-Rothstein. 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)
17. Blanco, P., A. K. Palucka, M. Gill, V. Pascual, and J. Banchereau. 2001. Induction of dendritic cell differentiation by IFN-alpha in systemic lupus erythematosus. Science 294: 1540-1543. (Pubitemid 33063928)
18. Gill, M. A., P. Blanco, E. Arce, V. Pascual, J. Banchereau, and A. K. Palucka. 2002. Blood dendritic cells and DC-poietins in systemic lupus erythematosus. Hum. Immunol. 63: 1172-1180. (Pubitemid 36025992)
19. Joo, H., C. Coquery, Y. Xue, I. Gayet, S. R. Dillon, M. Punaro, G. Zurawski, J. Banchereau, V. Pascual, and S. Oh. 2012. Serum from patients with SLE instructs monocytes to promote IgG and IgA plasmablast differentiation. J. Exp. Med. 209: 1335-1348.
20. Lin, Y., L. Zhang, A. X. Cai, M. Lee, W. Zhang, D. Neuberg, C. M. Canning, R. J. Soiffer, E. P. Alyea, J. Ritz, et al. 2011. Effective posttransplant antitumor immunity is associated with TLR-stimulating nucleic acid-immunoglobulin complexes in humans. J. Clin. Invest. 121: 1574-1584.
21. Tian, J., A. M. Avalos, S. Y. Mao, B. Chen, K. Senthil, H. Wu, P. Parroche, S. Drabic, D. Golenbock, C. Sirois, et al. 2007. Toll-like receptor 9-dependent activation by DNA-containing immune complexes is mediated by HMGB1 and RAGE. Nat. Immunol. 8: 487-496. (Pubitemid 46605917)
22. Van Beek, J. P., L. Kennedy, J. S. Rockel, S. M. Bernier, and A. Leask. 2006. The induction of CCN2 by TGFbeta1 involves Ets-1. Arthritis Res. Ther. 8: R36.
23. Wang, C., G. Fei, Z. Liu, Q. Li, Z. Xu, and T. Ren. 2012. HMGB1 was a pivotal synergistic effecor for CpG oligonucleotide to enhance the progression of human lung cancer cells. Cancer Biol. Ther. 13: 727-736.
24. Taki, M., K. Verschueren, K. Yokoyama, M. Nagayama, and N. Kamata. 2006. Involvement of Ets-1 transcription factor in inducing matrix metalloproteinase-2 expression by epithelial-mesenchymal transition in human squamous carcinoma cells. Int. J. Oncol. 28: 487-496.
25. Huang, Z., S. Huang, Q. Wang, L. Liang, S. Ni, L. Wang, W. Sheng, X. He, and X. Du. 2011. MicroRNA-95 promotes cell proliferation and targets sorting Nexin 1 in human colorectal carcinoma. Cancer Res. 71: 2582-2589.
26. Urbonaviciute, V., and R. E. Voll. 2011. High-mobility group box 1 represents a potential marker of disease activity and novel therapeutic target in systemic lupus erythematosus. J. Intern. Med. 270: 309-318.
27. Kokkola, R., A. Andersson, G. Mullins, T. Ostberg, C. J. Treutiger, B. Arnold, P. Nawroth, U. Andersson, R. A. Harris, and H. E. Harris. 2005. RAGE is the major receptor for the proinflammatory activity of HMGB1 in rodent macrophages. Scand. J. Immunol. 61: 1-9. (Pubitemid 40188342)
28. Park, J. S., F. Gamboni-Robertson, Q. He, D. Svetkauskaite, J. Y. Kim, D. Strassheim, J. W. Sohn, S. Yamada, I. Maruyama, A. Banerjee, et al. 2006. High mobility group box 1 protein interacts with multiple Toll-like receptors. Am. J. Physiol. Cell Physiol. 290: C917-C924.
29. Leng, R. X., H. F. Pan, W. Z. Qin, G. M. Chen, and D. Q. Ye. 2011. Role of microRNA-155 in autoimmunity. Cytokine Growth Factor Rev. 22: 141-147.
30. Teng, G., P. Hakimpour, P. Landgraf, A. Rice, T. Tuschl, R. Casellas, and F. N. Papavasiliou. 2008. MicroRNA-155 is a negative regulator of activation-induced cytidine deaminase. Immunity 28: 621-629.
31. Rodriguez, A., E. Vigorito, S. Clare, M. V. Warren, P. Couttet, D. R. Soond, S. van Dongen, R. J. Grocock, P. P. Das, E. A. Miska, et al. 2007. Requirement of bic/microRNA-155 for normal immune function. Science 316: 608-611. (Pubitemid 46683148)
32. Thai, T. H., D. P. Calado, S. Casola, K. M. Ansel, C. Xiao, Y. Xue, A. Murphy, D. Frendewey, D. Valenzuela, J. L. Kutok, et al. 2007. Regulation of the germinal center response by microRNA-155. Science 316: 604-608. (Pubitemid 46683147)
33. Vigorito, E., K. L. Perks, C. Abreu-Goodger, S. Bunting, Z. Xiang, S. Kohlhaas, P. P. Das, E. A. Miska, A. Rodriguez, A. Bradley, et al. 2007. microRNA-155 regulates the generation of immunoglobulin class-switched plasma cells. Immunity 27: 847-859. (Pubitemid 350258623)
34. O'Connell, R. M., K. D. Taganov, M. P. Boldin, G. Cheng, and D. Baltimore. 2007. MicroRNA-155 is induced during the macrophage inflammatory response. Proc. Natl. Acad. Sci. USA 104: 1604-1609. (Pubitemid 46214637)
35. Romania, P., V. Lulli, E. Pelosi, M. Biffoni, C. Peschle, and G. Marziali. 2008. MicroRNA 155 modulates megakaryopoiesis at progenitor and precursor level by targeting Ets-1 and Meis1 transcription factors. Br. J. Haematol. 143: 570-580.
36. Liu, Z., and A. Davidson. 2012. Taming lupus-a new understanding of pathogenesis is leading to clinical advances. Nat. Med. 18: 871-882.
37. Flesher, D. L., X. Sun, T. W. Behrens, R. R. Graham, and L. A. Criswell. 2010. Recent advances in the genetics of systemic lupus erythematosus. Expert Rev. Clin. Immunol. 6: 461-479.
38. Sessa, L., and M. E. Bianchi. 2007. The evolution of High Mobility Group Box (HMGB) chromatin proteins in multicellular animals. Gene 387: 133-140. (Pubitemid 44959570)
39. Sims, G. P., D. C. Rowe, S. T. Rietdijk, R. Herbst, and A. J. Coyle. 2010. HMGB1 and RAGE in inflammation and cancer. Annu. Rev. Immunol. 28: 367-388.
40. Rovere-Querini, P., A. Capobianco, P. Scaffidi, B. Valentinis, F. Catalanotti, M. Giazzon, I. E. Dumitriu, S. Müller, M. Iannacone, C. Traversari, et al. 2004. HMGB1 is an endogenous immune adjuvant released by necrotic cells. EMBO Rep. 5: 825-830. (Pubitemid 39199174)
41. Dumitriu, I. E., P. Baruah, B. Valentinis, R. E. Voll, M. Herrmann, P. P. Nawroth, B. Arnold, M. E. Bianchi, A. A. Manfredi, and P. Rovere-Querini. 2005. Release of high mobility group box 1 by dendritic cells controls T cell activation via the receptor for advanced glycation end products. J. Immunol. 174: 7506-7515. (Pubitemid 40806253)
42. Qing, X., M. Pitashny, D. B. Thomas, F. J. Barrat, M. P. Hogarth, and C. Putterman. 2008. Pathogenic anti-DNA antibodies modulate gene expression in mesangial cells: involvement of HMGB1 in anti-DNA antibody-induced renal injury. Immunol. Lett. 121: 61-73.
43. Urbonaviciute, V., B. G. Fürnrohr, S. Meister, L. Munoz, P. Heyder, F. De Marchis, M. E. Bianchi, C. Kirschning, H. Wagner, A. A. Manfredi, et al. 2008. Induction of inflammatory and immune responses by HMGB1-nucleosome complexes: implications for the pathogenesis of SLE. J. Exp. Med. 205: 3007-3018.
44. Tam, W., D. Ben-Yehuda, and W. S. Hayward. 1997. bic, a novel gene activated by proviral insertions in avian leukosis virus-induced lymphomas, is likely to function through its noncoding RNA. Mol. Cell. Biol. 17: 1490-1502. (Pubitemid 27097379)
45. Lagos-Quintana, M., R. Rauhut, A. Yalcin, J. Meyer, W. Lendeckel, and T. Tuschl. 2002. Identification of tissue-specific microRNAs from mouse. Curr. Biol. 12: 735-739. (Pubitemid 34455427)
46. John, S. A., J. L. Clements, L. M. Russell, and L. A. Garrett-Sinha. 2008. Ets-1 regulates plasma cell differentiation by interfering with the activity of the transcription factor Blimp-1. J. Biol. Chem. 283: 951-962.
47. Urbonaviciute, V., B. G. Fürnrohr, C. Weber, M. Haslbeck, S. Wilhelm, M. Herrmann, and R. E. Voll. 2007. Factors masking HMGB1 in human serum and plasma. J. Leukoc. Biol. 81: 67-74. (Pubitemid 46021254)
48. Jiang, W., and D. S. Pisetsky. 2008. Expression of high mobility group protein 1 in the sera of patients and mice with systemic lupus erythematosus. Ann. Rheum. Dis. 67: 727-728. (Pubitemid 351571946)
49. Li, J., H. Xie, T. Wen, H. Liu, W. Zhu, and X. Chen. 2010. Expression of high mobility group box chromosomal protein 1 and its modulating effects on downstream cytokines in systemic lupus erythematosus. J. Rheumatol. 37: 766-775.
50. Abdulahad, D. A., J. Westra, J. Bijzet, P. C. Limburg, C. G. Kallenberg, and M. Bijl. 2011. High mobility group box 1 (HMGB1) and anti-HMGB1 antibodies and their relation to disease characteristics in systemic lupus erythematosus. Arthritis Res. Ther. 13: R71.
51. Dai, R., Y. Zhang, D. Khan, B. Heid, D. Caudell, O. Crasta, and S. A. Ahmed. 2010. Identification of a common lupus disease-associated microRNA expression pattern in three different murine models of lupus. PLoS ONE 5: e14302.
52. O'Connell, R. M., D. Kahn, W. S. Gibson, J. L. Round, R. L. Scholz, A. A. Chaudhuri, M. E. Kahn, D. S. Rao, and D. Baltimore. 2010. MicroRNA-155 promotes autoimmune inflammation by enhancing inflammatory T cell development. Immunity 33: 607-619.
53. Blüml, S., M. Bonelli, B. Niederreiter, A. Puchner, G. Mayr, S. Hayer, M. I. Koenders, W. B. van den Berg, J. Smolen, and K. Redlich. 2011. Essential role of microRNA-155 in the pathogenesis of autoimmune arthritis in mice. Arthritis Rheum. 63: 1281-1288.
54. Leng, R. X., H. F. Pan, G. M. Chen, C. C. Feng, Y. G. Fan, D. Q. Ye, and X. P. Li. 2011. The dual nature of Ets-1: focus to the pathogenesis of systemic lupus erythematosus. Autoimmun. Rev. 10: 439-443.
55. Slifka, M. K., and R. Ahmed. 1998. Long-lived plasma cells: a mechanism for maintaining persistent antibody production. Curr. Opin. Immunol. 10: 252-258. (Pubitemid 28286950)
56. Pone, E. J., J. Zhang, T. Mai, C. A. White, G. Li, J. K. Sakakura, P. J. Patel, A. Al-Qahtani, H. Zan, Z. Xu, and P. Casali. 2012. BCR-signalling synergizes with TLR-signalling for induction of AID and immunoglobulin class-switching through the non-canonical NF-κB pathway. Nat. Commun. 3: 767.