Endocytosis-free DNA sensing by cell surface TLR9 in neutrophils: Rapid defense with autoimmune risks

European Journal of Immunology

Volumn 43, Issue 8, 2013, Pages 2006-2009

  Miyake, Kensuke ^a   Onji, Masahiro ^b  

^a UNIVERSITY OF TOKYO   (Japan)

^b OKAYAMA UNIVERSITY   (Japan)

Author keywords

DNA sensing; Neutrophils; TLR9

Indexed keywords

BACTERIAL DNA; TOLL LIKE RECEPTOR 9;

ANTIGEN EXPRESSION; ARTICLE; AUTOIMMUNITY; CELL SURFACE; DEGRANULATION; DNA SENSING; ENDOCYTOSIS; GENETIC PROCEDURES; HUMAN; INFLAMMATION; INNATE IMMUNITY; NEUTROPHIL; NONHUMAN; PRIORITY JOURNAL;

DNA SENSING; NEUTROPHILS; TLR9;

ANIMALS; HUMANS; NEUTROPHIL ACTIVATION; NEUTROPHILS; TOLL-LIKE RECEPTOR 9;

EID: 84881501517     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.201343882     Document Type: Article

References (29)

1. Beutler, B., Jiang, Z., Georgel, P., Crozat, K., Croker, B., Rutschmann, S., Du, X. and Hoebe, K., Genetic analysis of host resistance: Toll-like receptor signaling and immunity at large. Annu. Rev. Immunol. 2006. 24: 353-389.
2. Kaisho, T. and Akira, S., Toll-like receptor function and signaling. J. Allergy Clin. Immunol. 2006. 117: 979-987; quiz 988.
3. Kawai, T. and Akira, S., The role of pattern-recognition receptors in innate immunity: update on Toll-like receptors. Nat. Immunol. 2010. 11: 373-384.
4. Krieg, A. M., CpG motifs in bacterial DNA and their immune effects. Annu. Rev. Immunol. 2002. 20: 709-760.
5. Heil, F., Hemmi, H., Hochrein, H., Ampenberger, F., Kirschning, C., Akira, S., Lipford, G. et al., Species-specific recognition of single-stranded RNA via Toll-like receptor 7 and 8. Science 2004. 303: 1526-1529.
6. Hemmi, H., Takeuchi, O., Kawai, T., Kaisho, T., Sato, S., Sanjo, H., Matsumoto, M. et al., A Toll-like receptor recognizes bacterial DNA. Nature 2000. 408: 740-745.
7. Yasuda, K., Rutz, M., Schlatter, B., Metzger, J., Luppa, P. B., Schmitz, F., Haas, T. et al., CpG motif-independent activation of TLR9 upon endosomal translocation of "natural" phosphodiester DNA. Eur. J. Immunol. 2006. 36: 431-436.
8. 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.
9. Lande, R., Gregorio, J., Facchinetti, V., Chatterjee, B., Wang, Y. H., Homey, B., Cao, W. et al., Plasmacytoid dendritic cells sense self-DNA coupled with antimicrobial peptide. Nature 2007. 449: 564-569.
10. 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.
11. Ewald, S. E., Lee, B. L., Lau, L., Wickliffe, K. E., Shi, G. P., Chapman, H. A. and Barton, G. M., The ectodomain of Toll-like receptor 9 is cleaved to generate a functional receptor. Nature 2008. 456: 658-662.
12. Park, B., Brinkmann, M. M., Spooner, E., Lee, C. C., Kim, Y. M. and Ploegh, H. L., Proteolytic cleavage in an endolysosomal compartment is required for activation of Toll-like receptor 9. Nat. Immunol. 2008. 9: 1407-1414.
13. Ewald, S. E., Engel, A., Lee, J., Wang, M., Bogyo, M. and Barton, G. M., Nucleic acid recognition by Toll-like receptors is coupled to stepwise processing by cathepsins and asparagine endopeptidase. J. Exp. Med. 2011. 208: 643-651.
14. Sepulveda, F. E., Maschalidi, S., Colisson, R., Heslop, L., Ghirelli, C., Sakka, E., Lennon-Duménil, A. M. et al., Critical role for asparagine endopeptidase in endocytic Toll-like receptor signaling in dendritic cells. Immunity 2009. 31: 737-748.
15. Onji, M., Kanno, A., Saitoh, S., Fukui, R., Motoi, Y., Shibata, T., Matsumoto, F. et al., An essential role for the N-terminal fragment of Toll-like receptor 9 in DNA sensing. Nat. Commun. 2013. 4: 1949.
16. Tabeta, K., Hoebe, K., Janssen, E. M., Du, X., Georgel, P., Crozat, K., Mudd, S. 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.
17. Kim, Y. M., Brinkmann, M. M., Paquet, M. E. and Ploegh, H. L., UNC93B1 delivers nucleotide-sensing Toll-like receptors to endolysosomes. Nature 2008. 452: 234-238.
18. Takahashi, K., Shibata, T., Akashi-Takamura, S., Kiyokawa, T., Wakabayashi, Y., Tanimura, N., Kobayashi, T. et al., A protein associated with Toll-like receptor (TLR) 4 (PRAT4A) is required for TLR-dependent immune responses. J. Exp. Med. 2007. 204: 2963-2976.
19. Fukui, R., Saitoh, S., Kanno, A., Onji, M., Shibata, T., Ito, A., Matsumoto, M. et al., Unc93B1 restricts systemic lethal inflammation by orchestrating Toll-like receptor 7 and 9 trafficking. Immunity 2011. 35: 69-81.
20. Mouchess, M. L., Arpaia, N., Souza, G., Barbalat, R., Ewald, S. E., Lau, L. and Barton, G. M., Transmembrane mutations in Toll-like receptor 9 bypass the requirement for ectodomain proteolysis and induce fatal inflammation. Immunity 2011. 35: 721-732.
21. Lindau, D., Mussard, J., Wagner, B. J., Ribon, M., Rönnefarth, V. M., Quettier, M., Jelcic, I. et al., Primary blood neutrophils express a functional cell surface Toll-like receptor 9. Eur. J. Immunol. 2013. 43: 2101-2113.
22. Hacker, H., Redecke, V., Blagoev, B., Kratchmarova, I., Hsu, L. C., Wang, G. G., Kamps, M. P. et al., Specificity in Toll-like receptor signalling through distinct effector functions of TRAF3 and TRAF6. Nature 2006. 439: 204-207.
23. Peter, M. E., Kubarenko, A. V., Weber, A. N. and Dalpke, A. H., Identification of an N-terminal recognition site in TLR9 that contributes to CpG-DNA-mediated receptor activation. J. Immunol. 2009. 182: 7690-7697.
24. Lee, B. L., Moon, J. E., Shu, J. H., Yuan, L., Newman, Z. R., Schekman, R. and Barton, G. M., UNC93B1 mediates differential trafficking of endosomal TLRs. Elife 2013. 2: e00291.
25. Sasai, M., Linehan, M. M. and Iwasaki, A., Bifurcation of Toll-like receptor 9 signaling by adaptor protein 3. Science 2010. 329: 1530-1534.
26. Blasius, A. L., Arnold, C. N., Georgel, P., Rutschmann, S., Xia, Y., Lin, P., Ross, C. et al., Slc15a4, AP-3, and Hermansky-Pudlak syndrome proteins are required for Toll-like receptor signaling in plasmacytoid dendritic cells. Proc. Natl. Acad. Sci. USA 2010. 107: 19973-19978.
27. Fontana, S., Parolini, S., Vermi, W., Booth, S., Gallo, F., Donini, M., Benassi, M. et al., Innate immunity defects in Hermansky-Pudlak type 2 syndrome. Blood 2006. 107: 4857-4864.
28. Lande, R., Ganguly, D., Facchinetti, V., Frasca, L., Conrad, C., Gregorio, J., Meller, S. et al., Neutrophils activate plasmacytoid dendritic cells by releasing self-DNA-peptide complexes in systemic lupus erythematosus. Sci. Transl. Med. 2011. 3: 73ra19.
29. Garcia-Romo, G. S., Caielli, S., Vega, B., Connolly, J., Allantaz, F., Xu, Z., Punaro, M. et al., Netting neutrophils are major inducers of type I IFN production in pediatric systemic lupus erythematosus. Sci. Transl. Med. 2011. 3: 73ra20.