Heat shock protein 90 associates with Toll-like receptors 7/9 and mediates self-nucleic acid recognition in SLE

European Journal of Immunology

Volumn 45, Issue 7, 2015, Pages 2028-2041

  Saito, Keita ^a   Kukita, Kazuharu ^a   Kutomi, Goro ^a   Okuya, Koichi ^a   Asanuma, Hiroko ^a   Tabeya, Tetsuya ^a   Naishiro, Yasuka ^a   Yamamoto, Motohisa ^a   Takahashi, Hiroki ^a   Torigoe, Toshihiko ^a   Nakai, Akira ^b   Shinomura, Yasuhisa ^a   Hirata, Koichi ^a   Sato, Noriyuki ^a   Tamura, Yasuaki ^a,c  

^a SAPPORO MEDICAL UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^b YAMAGUCHI UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^c HOKKAIDO UNIVERSITY   (Japan)

Author keywords

Hsp90; IFN ; Plasmacytoid DC; SLE; TLR

Indexed keywords

ALVESPIMYCIN; HEAT SHOCK PROTEIN 90; NUCLEIC ACID; TANESPIMYCIN; TOLL LIKE RECEPTOR 7; TOLL LIKE RECEPTOR 9; ALPHA INTERFERON; ANTINUCLEAR ANTIBODY; AUTOANTIGEN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CLINICAL ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DISEASE ACTIVITY; DNA BINDING; DRUG BINDING; DRUG UPTAKE; ENDOSOME; FEMALE; HUMAN; NONHUMAN; PLASMACYTOID DENDRITIC CELL; PRIORITY JOURNAL; SYSTEMIC LUPUS ERYTHEMATOSUS; ANIMAL; BLOOD; C57BL MOUSE; CONFOCAL MICROSCOPY; DENDRITIC CELL; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; GENE SILENCING; IMMUNOLOGY; IMMUNOPRECIPITATION; INSTITUTE FOR CANCER RESEARCH MOUSE; MOUSE; MURPHY ROTHS LARGE LYMPHOPROLIFERATIVE MOUSE; WESTERN BLOTTING;

ANIMALS; ANTIBODIES, ANTINUCLEAR; AUTOANTIGENS; BLOTTING, WESTERN; DENDRITIC CELLS; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; FLOW CYTOMETRY; GENE KNOCKDOWN TECHNIQUES; HSP90 HEAT-SHOCK PROTEINS; HUMANS; IMMUNOPRECIPITATION; INTERFERON-ALPHA; LUPUS ERYTHEMATOSUS, SYSTEMIC; MICE; MICE, INBRED C57BL; MICE, INBRED ICR; MICE, INBRED MRL LPR; MICROSCOPY, CONFOCAL; NUCLEIC ACIDS; TOLL-LIKE RECEPTOR 7; TOLL-LIKE RECEPTOR 9;

EID: 84935747373     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.201445293     Document Type: Article

References (49)

1. Kotzin, B. L., Systemic lupus erythematosus. Cell 1996. 85: 303-306.
2. Hahn, B. H., Antibodies to DNA. N. Engl. J. Med. 1998. 338: 1359-1368.
3. Hooks, J. J., Moutsopoulos, H. M., Geis, S. A., Stahl, N. I., Decker, J. L. and Notkins, A. L., Immune interferon in the circulation of patients with autoimmune disease. N. Engl. J. Med. 1979. 301: 5-8.
4. Ronnblom, L. and Alm, G. V., Systemic lupus erythematosus and the type I interferon system. Arthritis Res. Ther. 2003. 5: 68-75.
5. Baechler, E. C., Batliwalla, F. M., Karypis, G., Gaffney, P. M., Ortmann, W. A., Espe, K. J., Shark, K. B. et al., Interferon-inducible gene expression signature in peripheral blood cells of patients with severe lupus. Proc. Natl. Acad. Sci. USA 2003. 100: 2610-2615.
6. Bennett, L., Palucka, A. K., Arce, E., Cantrell, V., Borvak, J., Banchereau, J. and Pascual, V., Interferon and granulopoiesis signatures in systemic lupus erythematosus blood. J. Exp. Med. 2003. 197: 711-723.
7. Barrat, F. J., Meeker, T., Gregorio, J., Chan, J. H., Uematsu, S., Akira, S., Chang, B. et al., Nucleic acids of mammalian origin can act as endogenous ligands for Toll-like receptors and may promote systemic lupus erythematosus. J. Exp. Med. 2005. 202: 1131-1139.
8. Vollmer, J., Tluk, S., Schmitz, C., Hamm, S., Jurk, M., Forsbach, A., Akira, S. et al., Immune stimulation mediated by autoantigen binding sites within small nuclear RNAs involves Toll-like receptors 7 and 8. J. Exp. Med. 2005. 202: 1575-1585.
9. Marshak-Rothstein, A., Toll-like receptors in systemic autoimmune disease. Nat. Rev. Immunol. 2006. 6: 823-835.
10. Lau, C. M., Broughton, C., Tabor, A. S., Akira, S., Flavell, R. A., Mamula, M. J., Christensen, S. R. 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.
11. Leadbetter, E. A., Rifkin, I. R., Hohlbaum, A. M., Beaudette, B. C., Shlomchik, M. J. and Marshak-Rothstein, A., Chromatin-IgG complexes activate B cells by dual engagement of IgM and Toll-like receptors. Nature 2002. 416: 603-607.
12. Kadowaki, N., Antonenko, S. and Liu, Y. J., Distinct CpG DNA and polyinosinic-polycytidylic acid double-stranded RNA, respectively, stimulate CD11c- type 2 dendritic cell precursors and CD11c+ dendritic cells to produce type I IFN. J. Immunol. 2001. 166: 2291-2295.
13. Hornung, V., Rothenfusser, S., Britsch, S., Krug, A., Jahrsdorfer, B., Giese, T., Endres, 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. Ito, T., Wang, Y. H. and Liu, Y. J., Plasmacytoid dendritic cell precursors/type I interferon-producing cells sense viral infection by Toll-like receptor (TLR) 7 and TLR9. Springer Semin. Immunopathol. 2005. 26: 221-229.
15. Cao, W., Manicassamy, S., Tang, H., Kasturi, S. P., Pirani, A., Murthy, N. and Pulendran, B., Toll-like receptor-mediated induction of type I interferon in plasmacytoid dendritic cells requires the rapamycin-sensitive PI(3)K-mTOR-p70S6K pathway. Nat. Immunol. 2008. 9: 1157-1164.
16. Barton, G. M., Kagan, J. C. and 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.
17. Ganguly, D., Chamilos, G., Lande, R., Gregorio, J., Meller, S., Facchinetti, V., Homey, B. et al., Self-RNA-antimicrobial peptide complexes activate human dendritic cells through TLR7 and TLR8. J. Exp. Med. 2009. 206: 1983-1994.
18. Yanai, H., Ban, T., Wang, Z., Choi, M. K., Kawamura, T., Negishi, H., Nakasato, M. et al., HMGB proteins function as universal sentinels for nucleic-acid-mediated innate immune responses. Nature 2009. 462: 99-103.
19. Okuya, K., Tamura, Y., Saito, K., Kutomi, G., Torigoe, T., Hirata, K. and Sato, N., Spatiotemporal regulation of heat shock protein 90-chaperoned self-DNA and CpG-oligodeoxynucleotide for type I IFN induction via targeting to static early endosome. J. Immunol. 2010. 184: 7092-7099.
20. Ochel, H. J., Eichhorn, K. and Gademann, G., Geldanamycin: the prototype of a class of antitumor drugs targeting the heat shock protein 90 family of molecular chaperones. Cell Stress Chaperones 2001. 6: 105-112.
21. Sausville, E. A., Tomaszewski, J. E. and Ivy, P., Clinical development of 17-allylamino, 17-demethoxygeldanamycin. Curr. Cancer Drug Targets 2003. 3: 377-383.
22. Shimp, S. K., 3rd, Chafin, C. B., Regna, N. L., Hammond, S. E., Read, M. A., Caudell, D. L., Rylander, M. et al., Heat shock protein 90 inhibition by 17-DMAG lessens disease in the MRL/lpr mouse model of systemic lupus erythematosus. Cell Mol. Immunol. 2012. 9: 255-266.
23. Zheng, H. and Li, Z., Cutting edge: cross-presentation of cell-associated antigens to MHC class I molecule is regulated by a major transcription factor for heat shock proteins. J. Immunol. 2004. 173: 5929-5933.
24. Ichiyanagi, T., Imai, T., Kajiwara, C., Mizukami, S., Nakai, A., Nakayama, T. and Udono, H., Essential role of endogenous heat shock protein 90 of dendritic cells in antigen cross-presentation. J. Immunol. 2010. 185: 2693-2700.
25. Xu, W., Mimnaugh, E. G., Kim, J. S., Trepel, J. B. and Neckers, L. M., Hsp90, not Grp94, regulates the intracellular trafficking and stability of nascent ErbB2. Cell Stress Chaperones 2002. 7: 91-96.
26. Yang, Y., Liu, B., Dai, J., Srivastava, P. K., Zammit, D. J., Lefrancois, L. and Li, Z., Heat shock protein gp96 is a master chaperone for toll-like receptors and is important in the innate function of macrophages. Immunity 2007. 26: 215-226.
27. Liu, B., Yang, Y., Qiu, Z., Staron, M., Hong, F., Li, Y., Wu, S. et al., Folding of Toll-like receptors by the HSP90 paralogue gp96 requires a substrate-specific cochaperone. Nat. Commun. 2010. 1: 79.
28. Honda, K., Yanai, H., Negishi, H., Asagiri, M., Sato, M., Mizutani, T., Shimada, N. et al., IRF-7 is the master regulator of type-I interferon-dependent immune responses. Nature 2005. 434: 772-777.
29. Sato, M., Suemori, H., Hata, N., Asagiri, M., Ogasawara, K., Nakao, K., Nakaya, T. et al., Distinct and essential roles of transcription factors IRF-3 and IRF-7 in response to viruses for IFN-alpha/beta gene induction. Immunity 2000. 13: 539-548.
30. Marie, I., Smith, E., Prakash, A. and Levy, D. E., Phosphorylation-induced dimerization of interferon regulatory factor 7 unmasks DNA binding and a bipartite transactivation domain. Mol. Cell Biol. 2000. 20: 8803-8814.
31. Andrews, B. S., Eisenberg, R. A., Theofilopoulos, A. N., Izui, S., Wilson, C. B., McConahey, P. J., Murphy, E. D. et al., Spontaneous murine lupus-like syndromes. Clinical and immunopathological manifestations in several strains. J. Exp. Med. 1978. 148: 1198-1215.
32. Waza, M., Adachi, H., Katsuno, M., Minamiyama, M., Sang, C., Tanaka, F., Inukai, A. et al., 17-AAG, an Hsp90 inhibitor, ameliorates polyglutamine-mediated motor neuron degeneration. Nat. Med. 2005. 11: 1088-1095.
33. Waza, M., Adachi, H., Katsuno, M., Minamiyama, M., Tanaka, F. and Sobue, G., Alleviating neurodegeneration by an anticancer agent: an Hsp90 inhibitor (17-AAG). Ann. NY Acad. Sci. 2006. 1086: 21-34.
34. Latchman, D. S. and Isenberg, D. A., The role of hsp90 in SLE. Autoimmunity 1994. 19: 211-218.
35. Ripley, B. J., Isenberg, D. A. and Latchman, D. S., Elevated levels of the 90 kDa heat shock protein (hsp90) in SLE correlate with levels of IL-6 and autoantibodies to hsp90. J. Autoimmun. 2001. 17: 341-346.
36. Bombardier, C., Gladman, D. D., Urowitz, M. B., Caron, D. and Chang, C. H., Derivation of the SLEDAI. A disease activity index for lupus patients. The Committee on Prognosis Studies in SLE. Arthritis Rheum. 1992. 35: 630-640.
37. Olesinska, M., Wiesik-Szewczyk, E. and Chwalinska-Sadowska, H., [Evaluation of systemic lupus erythematosus activity during pregnancy]. Pol. Arch. Med. Wewn 2007. 117: 312-316.
38. Hua, J., Kirou, K., Lee, C. and Crow, M. K., Functional assay of type I interferon in systemic lupus erythematosus plasma and association with anti-RNA binding protein autoantibodies. Arthritis Rheum. 2006. 54: 1906-1916.
39. Lovgren, T., Eloranta, M. L., Bave, U., Alm, G. V. and Ronnblom, L., Induction of interferon-alpha production in plasmacytoid dendritic cells by immune complexes containing nucleic acid released by necrotic or late apoptotic cells and lupus IgG. Arthritis Rheum. 2004. 50: 1861-1872.
40. Fukui, R., Saitoh, S., Matsumoto, F., Kozuka-Hata, H., Oyama, M., Tabeta, K., Beutler, B. et al., Unc93B1 biases Toll-like receptor responses to nucleic acid in dendritic cells toward DNA- but against RNA-sensing. J. Exp. Med. 2009. 206: 1339-1350.
41. Kamal, A., Thao, L., Sensintaffar, J., Zhang, L., Boehm, M. F., Fritz, L. C. and Burrows, F. J., A high-affinity conformation of Hsp90 confers tumour selectivity on Hsp90 inhibitors. Nature 2003. 425: 407-410.
42. Workman, P., Altered states: selectively drugging the Hsp90 cancer chaperone. Trends Mol. Med. 2004. 10: 47-51.
43. Linker-Israeli, M., Deans, R. J., Wallace, D. J., Prehn, J., Ozeri-Chen, T. and Klinenberg, J. R., Elevated levels of endogenous IL-6 in systemic lupus erythematosus. A putative role in pathogenesis. J. Immunol. 1991. 147: 117-123.
44. Linker-Israeli, M., Wallace, D. J., Prehn, J., Michael, D., Honda, M., Taylor, K. D., Paul-Labrador, M. et al., Association of IL-6 gene alleles with systemic lupus erythematosus (SLE) and with elevated IL-6 expression. Genes Immun. 1999. 1: 45-52.
45. Stephanou, A., Amin, V., Isenberg, D. A., Akira, S., Kishimoto, T. and Latchman, D. S., Interleukin 6 activates heat-shock protein 90 beta gene expression. Biochem. J. 1997. 321(Pt 1): 103-106.
46. Stephanou, A., Conroy, S., Isenberg, D. A., Maione, D., Poli, V., Ciliberto, G. and Latchman, D. S., Elevation of IL-6 in transgenic mice results in increased levels of the 90 kDa heat shock protein (hsp90) and the production of anti-hsp90 antibodies. J. Autoimmun. 1998. 11: 249-253.
47. Stephanou, A., Isenberg, D. A., Akira, S., Kishimoto, T. and Latchman, D. S., The nuclear factor interleukin-6 (NF-IL6) and signal transducer and activator of transcription-3 (STAT-3) signalling pathways co-operate to mediate the activation of the hsp90beta gene by interleukin-6 but have opposite effects on its inducibility by heat shock. Biochem. J. 1998. 330(Pt 1): 189-195.
48. Dong, L., Ito, S., Ishii, K. J. and Klinman, D. M., Suppressive oligodeoxynucleotides delay the onset of glomerulonephritis and prolong survival in lupus-prone NZB x NZW mice. Arthritis Rheum. 2005. 52: 651-658.
49. Hochberg, M. C., Updating the American College of Rheumatology revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum. 1997. 40: 1725.