MicroRNA-146a feedback inhibits RIG-I-dependent type I IFN production in macrophages by targeting TRAF6, IRAK1, and IRAK2

Journal of Immunology

Volumn 183, Issue 3, 2009, Pages 2150-2158

  Hou, Jin ^a,b   Wang, Pin ^b   Lin, Li ^c   Liu, Xingguang ^a   Feng, Ma ^c   An, Huazhang ^a   Wang, Zhugang ^d   Cao, Xuetao ^a,b,c  

^a Tsinghua University   (China)

^b SECOND MILITARY MEDICAL UNIVERSITY   (China)

^c ZHEJIANG UNIVERSITY SCHOOL OF MEDICINE   (China)

^d SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

Author keywords

[No Author keywords available]

Indexed keywords

FAS ASSOCIATED DEATH DOMAIN PROTEIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERFERON; INTERLEUKIN 1 RECEPTOR ASSOCIATED KINASE 1; INTERLEUKIN 1 RECEPTOR ASSOCIATED KINASE 2; MICRORNA; MICRORNA 146A; MYELOID DIFFERENTIATION FACTOR 88; RETINOIC ACID INDUCIBLE PROTEIN I; TOLL LIKE RECEPTOR; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 6; UNCLASSIFIED DRUG; DDX58 PROTEIN, MOUSE; DEAD BOX PROTEIN; INTERLEUKIN 1 RECEPTOR ASSOCIATED KINASE; IRAK1 PROTEIN, MOUSE; MIRN146 MICRORNA, MOUSE;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; EMBRYO; FEEDBACK SYSTEM; GENE EXPRESSION; HUMAN; HUMAN CELL; INTERFERON PRODUCTION; MOUSE; NONHUMAN; PERITONEUM MACROPHAGE; PRIORITY JOURNAL; PROTEIN TARGETING; SIGNAL TRANSDUCTION; UPREGULATION; VESICULAR STOMATITIS VIRUS; VIRUS IMMUNITY; VIRUS INFECTION; VIRUS REPLICATION; ANIMAL; BIOSYNTHESIS; DRUG ANTAGONISM; DRUG EFFECT; GENETICS; IMMUNITY; IMMUNOLOGY; MACROPHAGE; METABOLISM; PHYSIOLOGY; VESICULAR STOMATITIS;

ANIMALS; DEAD-BOX RNA HELICASES; FEEDBACK, BIOCHEMICAL; IMMUNITY; INTERFERON TYPE I; INTERLEUKIN-1 RECEPTOR-ASSOCIATED KINASES; MACROPHAGES; MICE; MICRORNAS; TNF RECEPTOR-ASSOCIATED FACTOR 6; UP-REGULATION; VESICULAR STOMATITIS; VESICULOVIRUS; VIRUS DISEASES; VIRUS REPLICATION;

EID: 68149165370     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.0900707     Document Type: Article

References (46)

1. Akira, S., S. Uematsu, and O. Takeuchi. 2006. Pathogen recognition and innate immunity. Cell 124: 783-801.
2. Beutler, B., C. Eidenschenk, K. Crozat, J. L. Imler, O. Takeuchi, J. A. Hoffmann, and S. Akira. 2007. Genetic analysis of resistance to viral infection. Nat. Rev. Immunol. 7: 753-766.
3. Takeuchi, O., and S. Akira. 2008. MDA5/RIG-I and virus recognition. Curr. Opin. Immunol. 20: 17-22.
4. Vaidya, S. A., and G. Cheng. 2003. Toll-like receptors and innate antiviral responses. Curr. Opin. Immunol. 15: 402-407.
5. Taniguchi, T., and A. Takaoka. 2001. A weak signal for strong responses: interferon-α/β revisited. Nat. Rev. Mol. Cell Biol. 2: 378-386.
6. Honda, K., A. Takaoka, and T. Taniguchi. 2006. Type I interferon gene induction by the interferon regulatory factor family of transcription factors. Immunity 25: 349-360.
7. Liew, F. Y., D. Xu, E. K. Brint, and L. A. O'Neill. 2005. Negative regulation of Toll-like receptor mediated immune responses. Nat. Rev. Immunol. 5: 446-458.
8. Hengel, H., U. H. Koszinowski, and K. K. Conzelmann. 2005. Viruses know it all: new insights into IFN networks. Trends Immunol. 26: 396-401.
9. Iannello, A., O. Debbeche, E. Martin, L. H. Attalah, S. Samarani, and A. Ahmad. 2006. Viral strategies for evading antiviral cellular immune responses of the host. J. Leukocyte Biol. 79: 16-35.
10. Yoneyama, M., M. Kikuchi, T. Natsukawa, N. Shinobu, T. Imaizumi, M. Miyagishi, K. Taira, S. Akira, and T. Fujita. 2004. The RNA helicase RIG-I has an essential function in double-stranded RNA-induced innate antiviral responses. Nat. Immunol. 5: 730-737.
11. 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.
12. Kayagaki, N., Q. Phung, S. Chan, R. Chaudhari, C. Quan, K.M. O'Rourke, M. Eby, E. Pietras, G. Cheng, J.F. Bazan, et al. 2007. DUBA: a deubiquitinase that regulates type I interferon production. Science 318: 1628-1632.
13. Moore, C. B., D. T. BergstralhT, J. A. Duncan, Y. Lei, T. E. Morrison, A. G. Zimmermann, M. A. Accavitti-Loper, V. J. Madden, L. Sun, Z. Ye, et al. 2008. NLRX1 is a regulator of mitochondrial antiviral immunity. Nature 451: 573-577.
14. Bowie, A. G., and L. Unterholzner. 2008. Viral evasion and subversion of pattern-recognition receptor signalling. Nat. Rev. Immunol. 8: 911-922.
15. Gottwein, E., and B. R. Cullen. 2008. Viral and cellular microRNAs as determinants of viral pathogenesis and immunity. Cell Host Microbe 3: 375-387. (Pubitemid 351773098)
16. Bartel, D. P. 2004. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116: 281-297.
17. Bushati, N., and S. M. Cohen. 2007. MicroRNA functions. Annu. Rev. Cell Dev. Biol. 23: 175-205.
18. Taganov, K. D., M. P. Boldin, and D. Baltimore. 2007. MicroRNAs and immunity: tiny players in a big field. Immunity 26: 133-137.
19. Baltimore, D., M. P. Boldin, R. M. O'Connell, D. S. Rao, and K. D. Taganov. 2008. MicroRNAs: new regulators of immune cell development and function. Nat. Immunol. 9: 839-845.
20. Lodish, H. F., B. Zhou, G. Liu, and C. Chen. 2008. Micromanagement of the immune system by microRNAs. Nat. Rev. Immunol. 8: 120-130.
21. Xiao, C., and K. Rajewsky. 2009. MicroRNA control in the immune system: basic principles. Cell 136: 26-36.
22. Taganov, K. D., M. P. Boldin, K. J. Chang, and D. Baltimore. 2006. NF-κB-dependent induction of microRNA miR-146, an inhibitor targeted to signaling proteins of innate immune responses. Proc. Natl. Acad. Sci. USA 103: 12481-12486.
23. Cameron, J. E., Q. Yin, C. Fewell, M. Lacey, J. McBride, X. Wang, Z. Lin, B. C. Schaefer, and E. K. Flemington. 2008. Epstein-Barr virus latent membrane protein 1 induces cellular microRNA miR-146a, a modulator of lymphocyte signaling pathways. J. Virol. 82: 1946-1958.
24. Motsch, N., T. Pfuhl, J. Mrazek, S. Barth, and F. A. Grässer. 2007. Epstein-Barr virus-encoded latent membrane protein 1 (LMP1) induces the expression of the cellular microRNA miR-146a. RNA Biol. 4: 131-137.
25. Perry, M. M., S. A. Moschos, A. E. Williams, N. J. Shepherd, H. M. Larner-Svensson, and M. A. Lindsay. 2008. Rapid changes in microRNA-146a expression negatively regulate the IL-1β-induced inflammatory response in human lung alveolar epithelial cells. J. Immunol. 180: 5689-5698.
26. Dai, R., R. A. Phillips, Y. Zhang, D. Khan, O. Crasta, and S. A. Ahmed. 2008. Suppression of LPS-induced Interferon-γ and nitric oxide in splenic lymphocytes by select estrogen-regulated microRNAs: a novel mechanism of immune modulation. Blood 112: 4591-4597.
27. -/- mice develop colitis associated with downregulation of Gαi2. Cell Res. 17: 858-868.
28. Zhang, N., S. Shen, L. Jiang, W. Zhang, H. Zhang, Y. Sun, X. Li, Q. Huang, B. Ge, S. Chen, et al. 2008. RIG-I plays a critical role in negatively regulating granulocytic proliferation. Proc. Natl. Acad. Sci. USA 105: 10553-10558.
29. Liu, X., M. Yao, N. Li, C. Wang, Y. Zheng, and X. Cao. 2008. CaMKII promotes TLR-triggered proinflammatory cytokine and type I interferon production by directly binding and activating TAK1 and IRF3 in macrophages. Blood 112: 4961-4970.
30. An, H., J. Hou, J. Zhou, W. Zhao, H. Xu, Y. Zheng, Y. Yu, S. Liu, and X. Cao. 2008. Phosphatase SHP-1 promotes TLR- and RIG-I-activated production of type I interferon by inhibiting the kinase IRAK1. Nat. Immunol. 9: 542-550.
31. Otsuka, M., Q. Jing, P. Georgel, L. New, J. Chen, J. Mols, Y.J. Kang, Z. Jiang, X. Du, R. Cook, et al. 2007. Hypersusceptibility to vesicular stomatitis virus infection in Dicer1-deficient mice is due to impaired miR24 and miR93 expression. Immunity 27: 123-134.
32. Zhang, M., H. Tang, Z. Guo, H. An, X. Zhu, W. Song, J. Guo, X. Huang, T. Chen, J. Wang, and X. Cao. 2004. Splenic stroma drives mature dendritic cells to differentiate into regulatory dendritic cells. Nat. Immunol. 5: 1124-1133.
33. Gao, X., E. Gulari, and X. Zhou. 2004. In situ synthesis of oligonucleotide microarrays. Biopolymers 73: 579-596.
34. ΔΔCt method. Methods 25: 402-408.
35. Gitlin, L., W Barchet, S. Gilfillan, M. Cella, B. Beutler, R.A. Flavell, M. S. Diamond, and M. Colonna. 2006. Essential role of mda-5 in type I IFN responses to polyriboinosinic:polyribocytidylic acid and encephalomyocarditis picornavirus. Proc. Natl. Acad. Sci. USA 103: 8459-8464.
36. Yoshida, R., G. Takaesu, H. Yoshida, F. Okamoto, T. Yoshioka, Y. Choi, S. Akira, T. Kawai, A. Yoshimura, and T. Kobayashi. 2008. TNF receptor-associated factor (TRAF) 6 and MEK kinase (MEKK) 1 play a pivotal role in the retinoic-acid-inducible gene-I (RIG-I)-like helicase antiviral pathway. J. Biol. Chem. 283: 36211-36220.
37. Xu, L. G., Y. Y. Wang, K. J. Han, L. Y. Li, Z. Zhai, and H. B. Shu. 2005. VISA is an adapter protein required for virus-triggered IFN-β signaling. Mol. Cell 19: 727-740.
38. Balachandran, S., E. Thomas, and G. N. Barber. 2004. A FADD-dependent innate immune mechanism in mammalian cells. Nature 432: 401-405.
39. Balachandran, S., T. Venkataraman, P. B. Fisher, and G. N. Barber. 2007. Fas-associated death domain-containing protein-mediated antiviral innate immune signaling involves the regulation of Irf7. J. Immunol. 178: 2429-2439.
40. Komuro, A., D. Bamming, and C. M. Horvath. 2008. Negative regulation of cytoplasmic RNA-mediated antiviral signaling. Cytokine 43: 350-358.
41. Seth, R. B., L. Sun, C. K. Ea, and Z. J. Chen. 2005. Identification and characterization of MAVS, a mitochondrial antiviral signaling protein that activates NF-κB and IRF3. Cell 122: 669-682.
42. Kawagoe, T., S. Sato, K. Matsushita, H. Kato, K. Matsui, Y. Kumagai, T. Saitoh, T. Kawai, O. Takeuchi, and S. Akira. 2008. Sequential control of Toll-like receptor-dependent responses by IRAK1 and IRAK2. Nat. Immunol. 9: 684-691.
43. Akira, S., and K. Takeda. 2004. Toll-like receptor signalling. Nat. Rev. Immunol. 4: 499-511.
44. Keating, S. E., G. M. Maloney, E. M. Moran, and A. G. Bowie. 2007. IRAK-2 participates in multiple Toll-like receptor signaling pathways to NF-κB via activation of TRAF6 ubiquitination. J. Biol. Chem. 282: 33435-33443.
45. Zhande, R., S. M. Dauphinee, J. A. Thomas, M. Yamamoto, S. Akira, and A. Karsan. 2007. FADD negatively regulates lipopolysaccharide signaling by impairing interleukin-1 receptor-associated kinase 1-MyD88 interaction. Mol. Cell Biol. 27: 7394-7404.
46. Selbach, M., B. Schwanhäusser, N. Thierfelder, Z. Fang, R. Khanin, and N. Rajewsky. 2008. Widespread changes in protein synthesis induced by microRNAs. Nature 455: 58-63.