Chicken STING mediates activation of the IFN gene independently of the RIG-I gene

Journal of Immunology

Volumn 195, Issue 8, 2015, Pages 3922-3936

  Cheng, Yuqiang ^a   Sun, Yingjie ^b   Wang, Hengan ^a   Yan, Yaxian ^a   Ding, Chan ^b   Sun, Jianhe ^a  

^a SHANGHAI JIAO TONG UNIVERSITY   (China)

^b INSTITUTE OF PLANT PROTECTION   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTOR PROTEIN; CHICKEN STIMULATOR OF IFN GENE; CYTOKINE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERFERON; INTERFERON REGULATORY FACTOR 7; INTERLEUKIN 1BETA; INTERLEUKIN 6; INTERLEUKIN 7; INTERLEUKIN 8; MELANOMA DIFFERENTIATION ASSOCIATED GENE 5; MESSENGER RNA; POLY(DEOXYADENYLATE DEOXYTHYMIDYLATE); POLYINOSINIC POLYCYTIDYLIC ACID; PROTEIN MX 1; RETINOIC ACID INDUCIBLE PROTEIN I; SHORT HAIRPIN RNA; UNCLASSIFIED DRUG; AVIAN PROTEIN; BETA INTERFERON; DEAD BOX PROTEIN; MEMBRANE PROTEIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; AVIAN INFLUENZA VIRUS; CELLULAR DISTRIBUTION; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENDOPLASMIC RETICULUM; GENE ACTIVATION; GENE EXPRESSION REGULATION; GENE SILENCING; GENETIC ASSOCIATION; GENETIC CONSERVATION; HUMAN; IFN GENE; IMMUNOPRECIPITATION; IMMUNOREGULATION; INNATE IMMUNITY; INTRACELLULAR SIGNALING; MITOCHONDRIAL MEMBRANE; MOLECULAR CLONING; MOLECULAR DYNAMICS; MOLECULAR EVOLUTION; MOUSE; NEWCASTLE DISEASE VIRUS; NONHUMAN; OUTER MEMBRANE; PHYLOGENETIC TREE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; RIG I GENE; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY; TISSUE SPECIFICITY; UPREGULATION; VIRAL PHENOMENA AND FUNCTIONS; VIRAL YIELD; VIRUS REPLICATION; ANIMAL; AVIAN INFLUENZA; CHICKEN; DRUG EFFECTS; EVOLUTION; GENETICS; IMMUNOLOGY; INFLUENZA A VIRUS (H9N2); SIGNAL TRANSDUCTION;

ANIMALS; AVIAN PROTEINS; BIOLOGICAL EVOLUTION; CHICKENS; DEAD-BOX RNA HELICASES; IMMUNITY, INNATE; INFLUENZA A VIRUS, H9N2 SUBTYPE; INFLUENZA IN BIRDS; INTERFERON-BETA; MEMBRANE PROTEINS; POLY I-C; SIGNAL TRANSDUCTION;

EID: 84943566927     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1500638     Document Type: Article

References (45)

1. Takeuchi, O., and S. Akira. 2009. Innate immunity to virus infection. Immunol. Rev. 227:75-86.
2. Palm, N. W., and R. Medzhitov. 2009. Pattern recognition receptors and control of adaptive immunity. Immunol. Rev. 227:221-233.
3. Anilkumar, N., G. San Jose, I. Sawyer, C. X. Santos, C. Sand, A. C. Brewer, D. Warren, and A. M. Shah. 2013. A 28-kDa splice variant of NADPH oxidase-4 is nuclear-localized and involved in redox signaling in vascular cells. Arterioscler. Thromb. Vasc. Biol. 33:e104-e112.
4. Xie, L., M. Liu, L. Fang, X. Su, K. Cai, D. Wang, H. Chen, and S. Xiao. 2010. Molecular cloning and functional characterization of porcine stimulator of interferon genes (STING). Dev. Comp. Immunol. 34:847-854.
5. Akira, S., S. Uematsu, and O. Takeuchi. 2006. Pathogen recognition and innate immunity. Cell 124:783-801.
6. Yoneyama, M., and T. Fujita. 2007. Function of RIG-I-like receptors in antiviral innate immunity. J. Biol. Chem. 282:15315-15318.
7. 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.
8. 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-beta signaling. Mol. Cell 19:727-740.
9. Kawai, T., K. Takahashi, S. Sato, C. Coban, H. Kumar, H. Kato, K. J. Ishii, O. Takeuchi, and S. Akira. 2005. IPS-1, an adaptor triggering RIG-I- and Mda5-mediated type I interferon induction. Nat. Immunol. 6:981-988.
10. Meylan, E., J. Curran, K. Hofmann, D. Moradpour, M. Binder, R. Bartenschlager, and J. Tschopp. 2005. Cardif is an adaptor protein in the RIGI antiviral pathway and is targeted by hepatitis C virus. Nature 437:1167-1172.
11. 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-kappaB and IRF 3. Cell 122:669-682.
12. Fredericksen, B. L., B. C. Keller, J. Fornek, M. G. Katze, and M. Gale, Jr. 2008. Establishment and maintenance of the innate antiviral response toWest Nile Virus involves both RIG-I and MDA5 signaling through IPS-1. J. Virol. 82:609-616.
13. Gitlin, L., L. Benoit, C. Song, M. Cella, S. Gilfillan, M. J. Holtzman, and M. Colonna. 2010. Melanoma differentiation-associated gene 5 (MDA5) is involved in the innate immune response to Paramyxoviridae infection in vivo. PLoS Pathog. 6:e1000734.
14. 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.
15. Liniger, M., A. Summerfield, G. Zimmer, K. C. McCullough, and N. Ruggli. 2012. Chicken cells sense influenza A virus infection through MDA5 and CARDIF signaling involving LGP2. J. Virol. 86:705-717.
16. Zou, J., M. Chang, P. Nie, and C. J. Secombes. 2009. Origin and evolution of the RIG-I like RNA helicase gene family. BMC Evol. Biol. 9:85.
17. Barber, M. R., J. R. Aldridge, Jr., R. G. Webster, and K. E. Magor. 2010. Association of RIG-I with innate immunity of ducks to influenza. [Published erratum appears in 2013 Proc Natl. Acad. Sci. USA 110:7958.] Proc. Natl. Acad. Sci. USA 107:5913-5918.
18. Zeng, W., and Z. J. Chen. 2008. MITAgating viral infection. Immunity 29:513-515.
19. Nakhaei, P., J. Hiscott, and R. Lin. 2010. STING-ing the antiviral pathway. J. Mol. Cell Biol. 2:110-112.
20. Sun, W., Y. Li, L. Chen, H. Chen, F. You, X. Zhou, Y. Zhou, Z. Zhai, D. Chen, and Z. Jiang. 2009. ERIS, an endoplasmic reticulum IFN stimulator, activates innate immune signaling through dimerization. Proc. Natl. Acad. Sci. USA 106:8653-8658.
21. Ishikawa, H., and G. N. Barber. 2008. STING is an endoplasmic reticulum adaptor that facilitates innate immune signalling. Nature 455:674-678.
22. Zhong, B., Y. Yang, S. Li, Y. Y. Wang, Y. Li, F. Diao, C. Lei, X. He, L. Zhang, P. Tien, and H. B. Shu. 2008. The adaptor protein MITA links virus-sensing receptors to IRF3 transcription factor activation. Immunity 29:538-550.
23. Tanaka, Y., and Z. J. Chen. 2012. STING specifies IRF3 phosphorylation by TBK1 in the cytosolic DNA signaling pathway. Sci. Signal. 5:ra20.
24. Chen, H., H. Yuan, R. Gao, J. Zhang, D. Wang, Y. Xiong, G. Fan, F. Yang, X. Li, J. Zhou, et al. 2014. Clinical and epidemiological characteristics of a fatal case of avian influenza A H10N8 virus infection: a descriptive study. Lancet 383:714-721.
25. Neumann, G., C. A. Macken, and Y. Kawaoka. 2014. Identification of amino acid changes that may have been critical for the genesis of A (H7N9) influenza viruses. J. Virol. 88:4877-4896.
26. Centers for Disease Control and Prevention (CDC). 2013. Emergence of avian influenza A (H7N9) virus causing severe human illness - China, February-April 2013. MMWR Morb. Mortal. Wkly. Rep. 62:366-371.
27. Gao, R., B. Cao, Y. Hu, Z. Feng, D. Wang, W. Hu, J. Chen, Z. Jie, H. Qiu, K. Xu, et al. 2013. Human infection with a novel avian-origin influenza A (H7N9) virus. N. Engl. J. Med. 368:1888-1897.
28. Kageyama, T., S. Fujisaki, E. Takashita, H. Xu, S. Yamada, Y. Uchida, G. Neumann, T. Saito, Y. Kawaoka, and M. Tashiro. 2013. Genetic analysis of novel avian A (H7N9) influenza viruses isolated from patients in China, February to April 2013. Euro Surveill. 18:20453.
29. Liu, D., W. Shi, and G. F. Gao. 2014. Poultry carrying H9N2 act as incubators for novel human avian influenza viruses. Lancet 383:869.
30. Schaefer-Klein, J., I. Givol, E. V. Barsov, J. M. Whitcomb, M. Van Brocklin, D. N. Foster, M. J. Federspiel, and S. H. Hughes. 1998. The EV-O-derived cell line DF-1 supports the efficient replication of avian leukosis-sarcoma viruses and vectors. Virology 248:305-311.
31. Sick, C., U. Schultz, U. Münster, J. Meier, B. Kaspers, and P. Staeheli. 1998. Promoter structures and differential responses to viral and nonviral inducers of chicken type I interferon genes. J. Biol. Chem. 273:9749-9754.
32. Ouyang, S., X. Song, Y. Wang, H. Ru, N. Shaw, Y. Jiang, F. Niu, Y. Zhu, W. Qiu, K. Parvatiyar, et al. 2012. Structural analysis of the STING adaptor protein reveals a hydrophobic dimer interface and mode of cyclic di-GMP binding. Immunity 36:1073-1086.
33. Biacchesi, S., E. Mérour, A. Lamoureux, J. Bernard, and M. Brémont. 2012. Both STING and MAVS fish orthologs contribute to the induction of interferon mediated by RIG-I. PLoS One 7:e47737.
34. Pelham, H. R. 2000. Using sorting signals to retain proteins in endoplasmic reticulum. Methods Enzymol. 327:279-283.
35. Teasdale, R. D., and M. R. Jackson. 1996. Signal-mediated sorting of membrane proteins between the endoplasmic reticulum and the golgi apparatus. Annu. Rev. Cell Dev. Biol. 12:27-54.
36. Zerangue, N., B. Schwappach, Y. N. Jan, and L. Y. Jan. 1999. A new ER trafficking signal regulates the subunit stoichiometry of plasma membrane K (ATP) channels. Neuron 22:537-548.
37. Huang, Z., X. Chen, B. Yu, and D. Chen. 2012. Cloning and functional characterization of rat stimulator of interferon genes (STING) regulated by miR-24. Dev. Comp. Immunol. 37:414-420.
38. Blaauboer, S. M., V. D. Gabrielle, and L. Jin. 2014. MPYS/STING-mediated TNF-a, not type I IFN, is essential for the mucosal adjuvant activity of (39-59) - cyclic-di-guanosine-monophosphate in vivo. J. Immunol. 192:492-502.
39. Yie, J., K. Senger, and D. Thanos. 1999. Mechanism by which the IFN-beta enhanceosome activates transcription. Proc. Natl. Acad. Sci. USA 96:13108-13113.
40. Cormican, P., A. T. Lloyd, T. Downing, S. J. Connell, D. Bradley, and C. O'Farrelly. 2009. The avian Toll-Like receptor pathway-subtle differences amidst general conformity. Dev. Comp. Immunol. 33:967-973.
41. Barber, M. R., J. R. Aldridge, Jr., X. Fleming-Canepa, Y. D. Wang, R. G. Webster, and K. E. Magor. 2013. Identification of avian RIG-I responsive genes during influenza infection. Mol. Immunol. 54:89-97.
42. Ishikawa, H., Z. Ma, and G. N. Barber. 2009. STING regulates intracellular DNAmediated, type I interferon-dependent innate immunity. Nature 461:788-792.
43. Sun, F., Y. B. Zhang, T. K. Liu, J. Shi, B. Wang, and J. F. Gui. 2011. Fish MITA serves as a mediator for distinct fish IFN gene activation dependent on IRF3 or IRF7. J. Immunol. 187:2531-2539.
44. Ran, Y., H. B. Shu, and Y. Y. Wang. 2014. MITA/STING: a central and multifaceted mediator in innate immune response. Cytokine Growth Factor Rev. 25:631-639.
45. Karpala, A. J., C. Stewart, J. McKay, J. W. Lowenthal, and A. G. D. Bean. 2011. Characterization of chicken Mda5 activity: regulation of IFN-β in the absence of RIG-I functionality. J. Immunol. 186:5397-5405.