ER stress and its regulator X-box-binding protein-1 enhance polyIC-induced innate immune response in dendritic cells

European Journal of Immunology

Volumn 41, Issue 4, 2011, Pages 1086-1097

  Hu, Fanlei ^a,b   Yu, Xiaofei ^b,c,d   Wang, Hongxia ^b,c,d   Zuo, Daming ^b,c,d   Guo, Chunqing ^b,c,d   Yi, Huanfa ^b,c,d   Tirosh, Boaz ^e   Subjeck, John R ^f   Qiu, Xiaoyan ^a   Wang, Xiang Yang ^b,c,d  

^a PEKING UNIVERSITY HEALTH SCIENCE CENTER   (China)

^b VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

^c VIRGINIA COMMONWEALTH UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

^e HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^f ROSWELL PARK CANCER INSTITUTE   (United States)

Author keywords

DCs; ER; Inflammatory response; PolyIC; XBP 1

Indexed keywords

BETA INTERFERON; CYTOKINE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERFERON REGULATORY FACTOR 3; LIGAND; MELANOMA DIFFERENTIATION ASSOCIATED PROTEIN 5; POLYINOSINIC POLYCYTIDYLIC ACID; TOLL LIKE RECEPTOR 3; UNCLASSIFIED DRUG; X BOX BINDING PROTEIN 1;

ANIMAL CELL; ANTIVIRAL ACTIVITY; ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DENDRITIC CELL; ENDOPLASMIC RETICULUM STRESS; GENE SILENCING; IMMUNOSTIMULATION; INFLAMMATION; INNATE IMMUNITY; INTRACELLULAR SIGNALING; MOUSE; NONHUMAN; PRIORITY JOURNAL; RHABDOVIRUS INFECTION; RNA SPLICING; VESICULAR STOMATITIS VIRUS; VIRUS INFECTIVITY;

ANIMALS; CELLS, CULTURED; CRICETINAE; DEAD-BOX RNA HELICASES; DENDRITIC CELLS; DNA-BINDING PROTEINS; ENDOPLASMIC RETICULUM; IMMUNITY, INNATE; INTERFERON-BETA; LIGANDS; MICE; POLY I-C; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTORS; TRANSCRIPTION FACTORS;

EID: 79953034321     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.201040831     Document Type: Article

References (39)

1. Anelli, T. and Sitia, R., Protein quality control in the early secretory pathway. EMBO J. 2008. 27: 315-327.
2. Marciniak, S. J. and Ron, D., Endoplasmic reticulum stress signaling in disease. Physiol. Rev. 2006. 86: 1133-1149.
3. Malhotra, J. D. and Kaufman, R. J., The endoplasmic reticulum and the unfolded protein response. Semin. Cell Dev. Biol. 2007. 18: 716-731.
4. Yoshida, H., ER stress and diseases. FEBS J. 2007. 274: 630-658.
5. Schroder, M. and Kaufman, R. J., ER stress and the unfolded protein response. Mutat. Res. 2005. 569: 29-63.
6. Ron, D. and Walter, P., Signal integration in the endoplasmic reticulum unfolded protein response. Nat. Rev. Mol. Cell Biol. 2007. 8: 519-529.
7. Yoshida, H., Matsui, T., Yamamoto, A., Okada, T. and Mori, K., XBP1 mRNA is induced by ATF6 and spliced by IRE1 in response to ER stress to produce a highly active transcription factor. Cell 2001. 107: 881-891.
8. Lee, K., Tirasophon, W., Shen, X., Michalak, M., Prywes, R., Okada, T., Yoshida, H. et al., IRE1-mediated unconventional mRNA splicing and S2P-mediated ATF6 cleavage merge to regulate XBP1 in signaling the unfolded protein response. Genes Dev. 2002. 16: 452-466.
9. Harding, H. P., Novoa, I., Zhang, Y., Zeng, H., Wek, R., Schapira, M. and Ron, D., Regulated translation initiation controls stress-induced gene expression in mammalian cells. Mol. Cell 2000. 6: 1099-1108.
10. Szegezdi, E., Logue, S. E., Gorman, A. M. and Samali, A., Mediators of endoplasmic reticulum stress-induced apoptosis. EMBO Rep. 2006. 7: 880-885.
11. Smith, J. A., Turner, M. J., DeLay, M. L., Klenk, E. I., Sowders, D. P. and Colbert, R. A., Endoplasmic reticulum stress and the unfolded protein response are linked to synergistic IFN-beta induction via X-box binding protein 1. Eur. J. Immunol. 2008. 38: 1194-1203.
12. Medzhitov, R. and Janeway, C. A., Jr., Decoding the patterns of self and nonself by the innate immune system. Science 2002. 296: 298-300.
13. Akira, S. and Takeda, K., Toll-like receptor signalling. Nat. Rev. Immunol. 2004. 4: 499-511.
14. Akira, S., Uematsu, S. and Takeuchi, O., Pathogen recognition and innate immunity. Cell 2006. 124: 783-801.
15. Alexopoulou, L., Holt, A. C., Medzhitov, R. and Flavell, R. A., Recognition of double-stranded RNA and activation of NF-κB by Toll-like receptor 3. Nature 2001. 413: 732-738.
16. Gitlin, L., Barchet, W., Gilfillan, S., Cella, M., Beutler, B., Flavell, R. A., Diamond, M. S. and Colonna, M., Essential role of mda-5 in type I IFN responses to polyriboinosinic:polyribocytidylic acid and encephalomyocarditis picornavirus. Proc. Natl. Acad. Sci. USA 2006. 103: 8459-8464.
17. Perrot, I., Deauvieau, F., Massacrier, C., Hughes, N., Garrone, P., Durand, I., Demaria, O. et al., TLR3 and Rig-like receptor on myeloid dendritic cells and Rig-like receptor on human NK cells are both mandatory for production of IFN-gamma in response to double-stranded RNA. J. Immunol. 2010. 185: 2080-2088.
18. Boonstra, A., Asselin-Paturel, C., Gilliet, M., Crain, C., Trinchieri, G., Liu, Y.-J. and O'Garra, A., Flexibility of mouse classical and plasmacytoid-derived dendritic cells in directing T helper type 1 and 2 cell development. J. Exp. Med. 2003. 197: 101-109.
19. Honda, K., Takaoka, A. and Taniguchi, T., Type I interferon gene induction by the interferon regulatory factor family of transcription factors. Immunity 2006. 25: 349-360.
20. Kawai, T. and Akira, S., Toll-like receptor and RIG-I-like receptor signaling. Ann. N. Y. Acad. Sci. 2008. 1143: 1-20.
21. Malmgaard, L., Salazar-Mather, T. P., Lewis, C. A. and Biron, C. A., Promotion of alpha/beta interferon induction during in vivo viral infection through alpha/beta interferon receptor/STAT1 system-dependent and -independent pathways. J. Virol. 2002. 76: 4520-4525.
22. Iwakoshi, N. N., Pypaert, M. and Glimcher, L. H., The transcription factor XBP-1 is essential for the development and survival of dendritic cells. J. Exp. Med. 2007. 204: 2267-2275.
23. Deng, J., Lu, P. D., Zhang, Y., Scheuner, D., Kaufman, R. J., Sonenberg, N., Harding, H. P. and Ron, D., Translational repression mediates activation of nuclear factor kappa B by phosphorylated translation initiation factor 2. Mol. Cell. Biol. 2004. 24: 10161-10168.
24. Deniaud, A., Sharaf el dein, O., Maillier, E., Poncet, D., Kroemer, G., Lemaire, C. and Brenner, C., Endoplasmic reticulum stress induces calcium-dependent permeability transition, mitochondrial outer membrane permeabilization and apoptosis. Oncogene 2008. 27: 285-299.
25. Yamamoto, M., Sato, S., Hemmi, H., Hoshino, K., Kaisho, T., Sanjo, H., Takeuchi, O. et al., Role of adaptor TRIF in the MyD88-independent toll-like receptor signaling pathway. Science 2003. 301: 640-643.
26. Fitzgerald, K. A., McWhirter, S. M., Faia, K. L., Rowe, D. C., Latz, E., Golenbock, D. T., Coyle, A. J. et al., IKKepsilon and TBK1 are essential components of the IRF3 signaling pathway. Nat. Immunol. 2003. 4: 491-496.
27. Sharma, S., tenOever, B. R., Grandvaux, N., Zhou, G. P., Lin, R. and Hiscott, J., Triggering the interferon antiviral response through an IKK-related pathway. Science 2003. 300: 1148-1151.
28. Alexopoulou, L., Holt, A. C., Medzhitov, R. and Flavell, R. A., Recognition of double-stranded RNA and activation of NF-κB by Toll-like receptor 3. Nature 2001. 413: 732-738.
29. Kato, H., Takeuchi, O., Sato, S., Yoneyama, M., Yamamoto, M., Matsui, K., Uematsu, S. et al., Differential roles of MDA5 and RIG-I helicases in the recognition of RNA viruses. Nature 2006. 441: 101-105.
30. Lee, A. H., Iwakoshi, N. N. and Glimcher, L. H., XBP-1 regulates a subset of endoplasmic reticulum resident chaperone genes in the unfolded protein response. Mol. Cell. Biol. 2003. 23: 7448-7459.
31. Zeng, L., Liu, Y. P., Sha, H., Chen, H., Qi, L. and Smith, J. A., XBP-1 couples endoplasmic reticulum stress to augmented IFN-beta induction via a cis-acting enhancer in macrophages. J. Immunol. 2010. 185: 2324-2330.
32. Martinon, F., Chen, X., Lee, A. H. and Glimcher, L. H., TLR activation of the transcription factor XBP1 regulates innate immune responses in macrophages. Nat. Immunol. 2010. 11: 411-418.
33. Lund, J. M., Alexopoulou, L., Sato, A., Karow, M., Adams, N. C., Gale, N. W., Iwasaki, A. and Flavell, R. A., Recognition of single-stranded RNA viruses by Toll-like receptor 7. Proc. Natl. Acad. Sci. USA 2004. 101: 5598-5603.
34. Le Blanc, I., Luyet, P. P., Pons, V., Ferguson, C., Emans, N., Petiot, A., Mayran, N. et al., Endosome-to-cytosol transport of viral nucleocapsids. Nat. Cell. Biol. 2005. 7: 653-664.
35. Kato, H., Sato, S., Yoneyama, M., Yamamoto, M., Uematsu, S., Matsui, K., Tsujimura, T. et al., Cell type-specific involvement of RIG-I in antiviral response. Immunity 2005. 23: 19-28.
36. Shen, Z., Reznikoff, G., Dranoff, G. and Rock, K. L., Cloned dendritic cells can present exogenous antigens on both MHC class I and class II molecules. J. Immunol. 1997. 158: 2723-2730.
37. Inaba, K., Inaba, M., Romani, N., Aya, H., Deguchi, M., Ikehara, S., Muramatsu, S. and Steinman, R. M., Generation of large numbers of dendritic cells from mouse bone marrow cultures supplemented with granulocyte/macrophage colony-stimulating factor. J. Exp. Med. 1992. 176: 1693-1702.
38. Yi, H., Yu, X., Gao, P., Wang, Y., Baek, S. H., Chen, X., Kim, H. L. et al., Pattern recognition scavenger receptor SRA/CD204 down-regulates Toll-like receptor 4 signaling-dependent CD8 T-cell activation. Blood 2009. 113: 5819-5828.
39. Renn, C. N., Sanchez, D. J., Ochoa, M. T., Legaspi, A. J., Oh, C. K., Liu, P. T., Krutzik, S. R. et al., TLR activation of Langerhans cell-like dendritic cells triggers an antiviral immune response. J. Immunol. 2006. 177: 298-305.