TLR3-triggered reactive oxygen species contribute to inflammatory responses by activating signal transducer and activator of transcription-1

Journal of Immunology

Volumn 190, Issue 12, 2013, Pages 6368-6377

  Yang, Chul Su ^a   Kim, Jwa Jin ^a   Lee, Sung Joong ^b   Hwang, Jung Hwan ^c   Lee, Chul Ho ^c   Lee, Myung Shik ^d   Jo, Eun Kyeong ^a  

^a Chungnam National University   (South Korea)

^b Seoul National University   (South Korea)

^c Korea Research Institute of Bioscience and Biotechnology (KRIBB)   (South Korea)

^d Sungkyunkwan University School of Medicine   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

BETA INTERFERON; CALCIUM ION; GAMMA INTERFERON INDUCIBLE PROTEIN 10; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERFERON REGULATORY FACTOR 3; NITRIC OXIDE SYNTHASE; PROTEIN P47; PROTEIN TYROSINE KINASE; RANTES; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 2; STAT1 PROTEIN; STAT2 PROTEIN; TOLL LIKE RECEPTOR 3;

ANIMAL CELL; ARTICLE; CELL NUCLEUS; CELL TRANSPORT; CONTROLLED STUDY; FEMALE; INFLAMMATION; INNATE IMMUNITY; MACROPHAGE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION;

ANIMALS; BLOTTING, WESTERN; CELLS, CULTURED; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE; IMMUNITY, INNATE; IMMUNOPRECIPITATION; INFLAMMATION; MACROPHAGES; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICROSCOPY, CONFOCAL; REACTIVE OXYGEN SPECIES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; STAT1 TRANSCRIPTION FACTOR; TOLL-LIKE RECEPTOR 3;

EID: 84879102554     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1202574     Document Type: Article

References (48)

1. Alexopoulou, L., A. C. Holt, R. A. Medzhitov, and R. A. Flavell. 2001. Recognition of double-stranded RNA and activation of NF-κB by Toll-like receptor 3. Nature 413: 732-738. (Pubitemid 33009951)
2. Akira, S., K. Takeda, and T. Kaisho. 2001. Toll-like receptors: critical proteins linking innate and acquired immunity. Nat. Immunol. 2: 675-680. (Pubitemid 32747155)
3. Yamamoto, M., S. Sato, H. Hemmi, K. Hoshino, T. Kaisho, H. Sanjo, O. Takeuchi, M. Sugiyama, M. Okabe, K. Takeda, and S. Akira. 2003. Role of adaptor TRIF in the MyD88-independent Toll-like receptor signaling pathway. Science 301: 640-643. (Pubitemid 36927946)
4. Takeuchi, O., and S. Akira. 2009. Innate immunity to virus infection. Immunol. Rev. 227: 75-86.
5. Weighardt, H., G. Jusek, J. Mages, R. Lang, K. Hoebe, B. Beutler, and B. Holzmann. 2004. Identification of a TLR4- and TRIF-dependent activation program of dendritic cells. Eur. J. Immunol. 34: 558-564. (Pubitemid 39255965)
6. Akira, S., S. Uematsu, and O. Takeuchi. 2006. Pathogen recognition and innate immunity. Cell 124: 783-801.
7. van Boxel-Dezaire, A. H., M. R. Rani, and G. R. Stark. 2006. Complex modulation of cell type-specific signaling in response to type I interferons. Immunity 25: 361-372.
8. Gao, J. J., M. B. Filla, M. J. Fultz, S. N. Vogel, S. W. Russell, and W. J. Murphy. 1998. Autocrine/paracrine IFN-αβ mediates the lipopolysaccharide-induced activation of transcription factor Stat1α in mouse macrophages: pivotal role of Stat1α in induction of the inducible nitric oxide synthase gene. J. Immunol. 161: 4803-4810. (Pubitemid 28492057)
9. Kim, H. S., and M. S. Lee. 2005. Essential role of STAT1 in caspase-independent cell death of activated macrophages through the p38 mitogen-activated protein kinase/STAT1/reactive oxygen species pathway. Mol. Cell. Biol. 25: 6821-6833. (Pubitemid 41023252)
10. Schindler, C., and J. E. Darnell, Jr. 1995. Transcriptional responses to polypeptide ligands: the JAK-STAT pathway. Annu. Rev. Biochem. 64: 621-651.
11. Saha, B., S. Jyothi Prasanna, B. Chandrasekar, and D. Nandi. 2010. Gene modulation and immunoregulatory roles of interferon γ. Cytokine 50: 1-14.
12. Najjar, I., F. Baran-Marszak, C. Le Clorennec, C. Laguillier, O. Schischmanoff, I. Youlyouz-Marfak, M. Schlee, G. W. Bornkamm, M. Raphaë l, J. Feuillard, and R. Fagard. 2005. Latent membrane protein 1 regulates STAT1 through NF-κB-dependent interferon secretion in Epstein-Barr virus-immortalized B cells. J. Virol. 79: 4936-4943. (Pubitemid 40464244)
13. Forman, H. J., and M. Torres. 2002. Reactive oxygen species and cell signaling: respiratory burst in macrophage signaling. Am. J. Respir. Crit. Care Med. 166: S4-S8. (Pubitemid 36015930)
14. Lam, G. Y., J. Huang, and J. H. Brumell. 2010. The many roles of NOX2 NADPH oxidase-derived ROS in immunity. Semin. Immunopathol. 32: 415-430.
15. Bae, Y. S., H. Oh, S. G. Rhee, and Y. D. Yoo. 2011. Regulation of reactive oxygen species generation in cell signaling. Mol. Cells 32: 491-509.
16. Yang, C. S., D. M. Shin, K. H. Kim, Z. W. Lee, C. H. Lee, S. G. Park, Y. S. Bae, and E. K. Jo. 2009. NADPH oxidase 2 interaction with TLR2 is required for efficient innate immune responses to mycobacteria via cathelicidin expression. J. Immunol. 182: 3696-3705.
17. Matsuzawa, A., K. Saegusa, T. Noguchi, C. Sadamitsu, H. Nishitoh, S. Nagai, S. Koyasu, K. Matsumoto, K. Takeda, and H. Ichijo. 2005. ROS-dependent activation of the TRAF6-ASK1-p38 pathway is selectively required for TLR4-mediated innate immunity. Nat. Immunol. 6: 587-592. (Pubitemid 41710729)
18. Yang, C. S., D. S. Lee, C. H. Song, S. J. An, S. Li, J. M. Kim, C. S. Kim, D. G. Yoo, B. H. Jeon, H. Y. Yang, et al. 2007. Roles of peroxiredoxin II in the regulation of proinflammatory responses to LPS and protection against endotoxin-induced lethal shock. J. Exp. Med. 204: 583-594. (Pubitemid 46457081)
19. Yang, C. S., D. M. Shin, H. M. Lee, J. W. Son, S. J. Lee, S. Akira, M. A. Gougerot-Pocidalo, J. El-Benna, H. Ichijo, and E. K. Jo. 2008. ASK1-p38 MAPK-p47phox activation is essential for inflammatory responses during tuberculosis via TLR2-ROS signalling. Cell Microbiol. 10: 741-754. (Pubitemid 351194099)
20. Kato, H., O. Takeuchi, S. Sato, M. Yoneyama, M. Yamamoto, K. Matsui, S. Uematsu, A. Jung, T. Kawai, K. J. Ishii, et al. 2006. Differential roles of MDA5 and RIG-I helicases in the recognition of RNA viruses. Nature 441: 101-105.
21. Johnsen, I. B., T. T. Nguyen, M. Ringdal, A. M. Tryggestad, O. Bakke, E. Lien, T. Espevik, and M. W. Anthonsen. 2006. Toll-like receptor 3 associates with c-Src tyrosine kinase on endosomes to initiate antiviral signaling. EMBO J. 25: 3335-3346. (Pubitemid 44141791)
22. 2+-dependent signaling by TLR2. J. Immunol. 177: 1330-1337.
23. phox, the phagocyte NADPH oxidase/NOX2 organizer: structure, phosphorylation and implication in diseases. Exp. Mol. Med. 41: 217-225.
24. Durbin, J. E., T. R. Johnson, R. K. Durbin, S. E. Mertz, R. A. Morotti, R. S. Peebles, and B. S. Graham. 2002. The role of IFN in respiratory syncytial virus pathogenesis. J. Immunol. 168: 2944-2952.
25. Hu, X., S. D. Chakravarty, and L. B. Ivashkiv. 2008. Regulation of interferon and Toll-like receptor signaling during macrophage activation by opposing feedforward and feedback inhibition mechanisms. Immunol. Rev. 226: 41-56.
26. Stempelj, M., M. Kedinger, L. Augenlicht, and L. Klampfer. 2007. Essential role of the JAK/STAT1 signaling pathway in the expression of inducible nitric-oxide synthase in intestinal epithelial cells and its regulation by butyrate. J. Biol. Chem. 282: 9797-9804. (Pubitemid 47104628)
27. Oshiumi, H., M. Matsumoto, K. Funami, T. Akazawa, and T. Seya. 2003. TICAM-1, an adaptor molecule that participates in Toll-like receptor 3-mediated interferon-beta induction. Nat. Immunol. 4: 161-167. (Pubitemid 36193018)
28. Seleme, M. C., W. Lei, A. R. Burg, K. Y. Goh, A. Metz, C. Steele, and H. M. Tse. 2012. Dysregulated TLR3-dependent signaling and innate immune activation in superoxide-deficient macrophages from nonobese diabetic mice. Free Radic. Biol. Med. 52: 2047-2056.
29. Yuk, J. M., and E. K. Jo. 2011. Toll-like receptors and innate immunity. J. Bacteriol. Virol. 41: 225-235.
30. Imai, Y., K. Kuba, G. G. Neely, R. Yaghubian-Malhami, T. Perkmann, G. van Loo, M. Ermolaeva, R. Veldhuizen, Y. H. Leung, H. Wang, et al. 2008. Identification of oxidative stress and Toll-like receptor 4 signaling as a key pathway of acute lung injury. Cell 133: 235-249. (Pubitemid 351512299)
31. Ichikawa, S., M. Miyake, R. Fujii, and Y. Konishi. 2012. MyD88 associated ROS generation is crucial for Lactobacillus induced IL-12 production in macrophage. PLoS ONE 7: e35880.
32. Jendrysik, M. A., S. Vasilevsky, L. Yi, A. Wood, N. Zhu, Y. Zhao, S. M. Koontz, and S. H. Jackson. 2011. NADPH oxidase-2 derived ROS dictates murine DC cytokine-mediated cell fate decisions during CD4 T helper-cell commitment. PLoS ONE 6: e28198.
33. Soucy-Faulkner, A., E. Mukawera, K. Fink, A. Martel, L. Jouan, Y. Nzengue, D. Lamarre, C. Vande Velde, and N. Grandvaux. 2010. Requirement of NOX2 and reactive oxygen species for efficient RIG-I-mediated antiviral response through regulation of MAVS expression. PLoS Pathog. 6: e1000930.
34. Joo, J. H., J. H. Ryu, C. H. Kim, H. J. Kim, M. S. Suh, J. O. Kim, S. Y. Chung, S. N. Lee, H. M. Kim, Y. S. Bae, and J. H. Yoon. 2012. Dual oxidase 2 is essential for the Toll-like receptor 5-mediated inflammatory response in airway mucosa. Antioxid. Redox Signal. 16: 57-70.
35. Tang, H., W. Cao, S. P. Kasturi, R. Ravindran, H. I. Nakaya, K. Kundu, N. Murthy, T. B. Kepler, B. Malissen, and B. Pulendran. 2010. The T helper type 2 response to cysteine proteases requires dendritic cell-basophil cooperation via ROS-mediated signaling. Nat. Immunol. 11: 608-617.
36. West, A. P., I. E. Brodsky, C. Rahner, D. K. Woo, H. Erdjument-Bromage, P. Tempst, M. C. Walsh, Y. Choi, G. S. Shadel, and S. Ghosh. 2011. TLR signalling augments macrophage bactericidal activity through mitochondrial ROS. Nature 472: 476-480.
37. Medvedev, A. E., W. Piao, J. Shoenfelt, S. H. Rhee, H. Chen, S. Basu, L. M. Wahl, M. J. Fenton, and S. N. Vogel. 2007. Role of TLR4 tyrosine phosphorylation in signal transduction and endotoxin tolerance. J. Biol. Chem. 282: 16042-16053. (Pubitemid 47100380)
38. Gardner, P. 1989. Calcium and T lymphocyte activation. Cell 59: 15-20. (Pubitemid 19248554)
39. Gallo, E. M., K. Canté-Barrett, and G. R. Crabtree. 2006. Lymphocyte calcium signaling from membrane to nucleus. Nat. Immunol. 7: 25-32. (Pubitemid 41823865)
40. 2+ signaling in airway epithelial cells facilitates leukocyte recruitment and transepithelial migration. J. Leukoc. Biol. 86: 1135-1144.
41. Stark, G. R., and J. E. Darnell, Jr. 2012. The JAK-STAT pathway at twenty. Immunity 36: 503-514.
42. Wagner, A. H., I. Wittjen, T. Stojanovic, P. Middel, J. G. Meingassner, and M. Hecker. 2008. Signal transducer and activator of transcription 1 decoy oligodeoxynucleotide suppression of contact hypersensitivity. J. Allergy Clin. Immunol. 121: 158-165, e5.
43. Kaur, T., D. Mukherjea, K. Sheehan, S. Jajoo, L. P. Rybak, and V. Ramkumar. 2011. Short interfering RNA against STAT1 attenuates cisplatin-induced ototoxicity in the rat by suppressing inflammation. Cell Death Dis. 2: e180.
44. Koff, J. L., M. X. Shao, I. F. Ueki, and J. A. Nadel. 2008. Multiple TLRs activate EGFR via a signaling cascade to produce innate immune responses in airway epithelium. Am. J. Physiol. Lung Cell. Mol. Physiol. 294: L1068-L1075.
45. Heyworth, P. G., A. R. Cross, and J. T. Curnutte. 2003. Chronic granulomatous disease. Curr. Opin. Immunol. 15: 578-584. (Pubitemid 37130200)
46. Assari, T. 2006. Chronic granulomatous disease; fundamental stages in our understanding of CGD. Med. Immunol. 5: 4.
47. Moir, S., S. S. De Ravin, B. H. Santich, J. Y. Kim, J. G. Posada, J. Ho, C. M. Buckner, W. Wang, L. Kardava, M. Garofalo, et al. 2012. Humans with chronic granulomatous disease maintain humoral immunologic memory despite low frequencies of circulating memory B cells. Blood 120: 4850-4858.
48. Shatynski, K. E., H. Chen, J. Kwon, and M. S. Williams. 2012. Decreased STAT5 phosphorylation and GATA-3 expression in NOX2-deficient T cells: role in T helper development. Eur. J. Immunol. 42: 3202-3211.