DDX60 Is Involved in RIG-I-Dependent and Independent Antiviral Responses, and Its Function Is Attenuated by Virus-Induced EGFR Activation

Cell Reports

Volumn 11, Issue 8, 2015, Pages 1193-1207

  Oshiumi, Hiroyuki ^a,b   Miyashita, Moeko ^a,d   Okamoto, Masaaki ^a   Morioka, Yuka ^b   Okabe, Masaru ^c   Matsumoto, Misako ^a   Seya, Tsukasa ^a  

^a HOKKAIDO UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b HOKKAIDO UNIVERSITY   (Japan)

^c OSAKA UNIVERSITY   (Japan)

^d HOKKAIDO INSTITUTE OF TECHNOLOGY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR; INTERFERON; PROTEIN DDX60; RETINOIC ACID INDUCIBLE PROTEIN I; RNA HELICASE; UNCLASSIFIED DRUG; VIRUS RNA; ALPHA INTERFERON; DDX58 PROTEIN, HUMAN; DDX58 PROTEIN, MOUSE; DDX60 PROTEIN, HUMAN; DDX60 PROTEIN, MOUSE; DEAD BOX PROTEIN; SIGNAL TRANSDUCING ADAPTOR PROTEIN; VASCULOTROPIN RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIVIRAL ACTIVITY; ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; EMBRYO; HEPATITIS C VIRUS; IN VIVO STUDY; INFLUENZA VIRUS A; INNATE IMMUNITY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; RNA DEGRADATION; SIGNAL TRANSDUCTION; VIRUS INDUCTION; ANIMAL; GENETICS; HEK293 CELL LINE; HELA CELL LINE; HUMAN; IMMUNOLOGY; KNOCKOUT MOUSE; METABOLISM; VESICULOVIRUS;

MUS;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; DEAD-BOX RNA HELICASES; HEK293 CELLS; HELA CELLS; HUMANS; IMMUNITY, INNATE; INTERFERON-ALPHA; MICE; MICE, KNOCKOUT; RECEPTORS, VASCULAR ENDOTHELIAL GROWTH FACTOR; RNA, VIRAL; SIGNAL TRANSDUCTION; VESICULOVIRUS;

EID: 84929960168     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2015.04.047     Document Type: Article

References (42)

1. Chan Y.K., Gack M.U. RIG-I-like receptor regulation in virus infection and immunity. Curr. Opin. Virol. 2015, 12C:7-14.
2. Chen G., Guo X., Lv F., Xu Y., Gao G. p72 DEAD box RNA helicase is required for optimal function of the zinc-finger antiviral protein. Proc. Natl. Acad. Sci. USA 2008, 105:4352-4357.
3. Desmet C.J., Ishii K.J. Nucleic acid sensing at the interface between innate and adaptive immunity in vaccination. Nat. Rev. Immunol. 2012, 12:479-491.
4. Diao J., Pantua H., Ngu H., Komuves L., Diehl L., Schaefer G., Kapadia S.B. Hepatitis C virus induces epidermal growth factor receptor activation via CD81 binding for viral internalization and entry. J.Virol. 2012, 86:10935-10949.
5. Gao D., Wu J., Wu Y.T., Du F., Aroh C., Yan N., Sun L., Chen Z.J. Cyclic GMP-AMP synthase is an innate immune sensor of HIV and other retroviruses. Science 2013, 341:903-906.
6. Guo X., Ma J., Sun J., Gao G. The zinc-finger antiviral protein recruits the RNA processing exosome to degrade the target mRNA. Proc. Natl. Acad. Sci. USA 2007, 104:151-156.
7. Houseley J., LaCava J., Tollervey D. RNA-quality control by the exosome. Nat. Rev. Mol. Cell Biol. 2006, 7:529-539.
8. Jarvius M., Paulsson J., Weibrecht I., Leuchowius K.J., Andersson A.C., Wählby C., Gullberg M., Botling J., Sjöblom T., Markova B., et al. In situ detection of phosphorylated platelet-derived growth factor receptor beta using a generalized proximity ligation method. Mol. Cell. Proteomics 2007, 6:1500-1509.
9. Kingston R.E., Narlikar G.J. ATP-dependent remodeling and acetylation as regulators of chromatin fluidity. Genes Dev. 1999, 13:2339-2352.
10. Kondo T., Kobayashi J., Saitoh T., Maruyama K., Ishii K.J., Barber G.N., Komatsu K., Akira S., Kawai T. DNA damage sensor MRE11 recognizes cytosolic double-stranded DNA and induces type I interferon by regulating STING trafficking. Proc. Natl. Acad. Sci. USA 2013, 110:2969-2974.
11. Koyama S., Ishii K.J., Kumar H., Tanimoto T., Coban C., Uematsu S., Kawai T., Akira S. Differential role of TLR- and RLR-signaling in the immune responses to influenza A virus infection and vaccination. J.Immunol. 2007, 179:4711-4720.
12. Li X.D., Wu J., Gao D., Wang H., Sun L., Chen Z.J. Pivotal roles of cGAS-cGAMP signaling in antiviral defense and immune adjuvant effects. Science 2013, 341:1390-1394.
13. Li Y., Masaki T., Yamane D., McGivern D.R., Lemon S.M. Competing and noncompeting activities of miR-122 and the 5' exonuclease Xrn1 in regulation of hepatitis C virus replication. Proc. Natl. Acad. Sci. USA 2013, 110:1881-1886.
14. Loo Y.M., Gale M. Immune signaling by RIG-I-like receptors. Immunity 2011, 34:680-692.
15. Lupberger J., Zeisel M.B., Xiao F., Thumann C., Fofana I., Zona L., Davis C., Mee C.J., Turek M., Gorke S., et al. EGFR and EphA2 are host factors for hepatitis C virus entry and possible targets for antiviral therapy. Nat. Med. 2011, 17:589-595.
16. Lupberger J., Duong F.H., Fofana I., Zona L., Xiao F., Thumann C., Durand S.C., Pessaux P., Zeisel M.B., Heim M.H., Baumert T.F. Epidermal growth factor receptor signaling impairs the antiviral activity of interferon-alpha. Hepatology 2013, 58:1225-1235.
17. Miyashita M., Oshiumi H., Matsumoto M., Seya T. DDX60, a DEXD/H box helicase, is a novel antiviral factor promoting RIG-I-like receptor-mediated signaling. Mol. Cell. Biol. 2011, 31:3802-3819.
18. Odendall C., Dixit E., Stavru F., Bierne H., Franz K.M., Durbin A.F., Boulant S., Gehrke L., Cossart P., Kagan J.C. Diverse intracellular pathogens activate type III interferon expression from peroxisomes. Nat. Immunol. 2014, 15:717-726.
19. Okamoto M., Oshiumi H., Azuma M., Kato N., Matsumoto M., Seya T. IPS-1 is essential for type III IFN production by hepatocytes and dendritic cells in response to hepatitis C virus infection. J.Immunol. 2014, 192:2770-2777.
20. Onomoto K., Jogi M., Yoo J.S., Narita R., Morimoto S., Takemura A., Sambhara S., Kawaguchi A., Osari S., Nagata K., et al. Critical role of an antiviral stress granule containing RIG-I and PKR in viral detection and innate immunity. PLoS ONE 2012, 7:e43031.
21. Oshiumi H., Matsumoto M., Hatakeyama S., Seya T. Riplet/RNF135, a RING finger protein, ubiquitinates RIG-I to promote interferon-beta induction during the early phase of viral infection. J.Biol. Chem. 2009, 284:807-817.
22. Oshiumi H., Miyashita M., Inoue N., Okabe M., Matsumoto M., Seya T. The ubiquitin ligase Riplet is essential for RIG-I-dependent innate immune responses to RNA virus infection. Cell Host Microbe 2010, 8:496-509.
23. Oshiumi H., Sakai K., Matsumoto M., Seya T. DEAD/H BOX 3 (DDX3) helicase binds the RIG-I adaptor IPS-1 to up-regulate IFN-beta inducing potential. Eur. J. Immunol. 2010, 40:940-948.
24. Oshiumi H., Miyashita M., Matsumoto M., Seya T. A distinct role of Riplet-mediated K63-Linked polyubiquitination of the RIG-I repressor domain in human antiviral innate immune responses. PLoS Pathog. 2013, 9:e1003533.
25. Saito T., Hirai R., Loo Y.M., Owen D., Johnson C.L., Sinha S.C., Akira S., Fujita T., Gale M. Regulation of innate antiviral defenses through a shared repressor domain in RIG-I and LGP2. Proc. Natl. Acad. Sci. USA 2007, 104:582-587.
26. Saito T., Owen D.M., Jiang F., Marcotrigiano J., Gale M. Innate immunity induced by composition-dependent RIG-I recognition of hepatitis C virus RNA. Nature 2008, 454:523-527.
27. Schmid M., Jensen T.H. The exosome: a multipurpose RNA-decay machine. Trends Biochem. Sci. 2008, 33:501-510.
28. Schoggins J.W., Wilson S.J., Panis M., Murphy M.Y., Jones C.T., Bieniasz P., Rice C.M. A diverse range of gene products are effectors of the type I interferon antiviral response. Nature 2011, 472:481-485.
29. Schröder M., Baran M., Bowie A.G. Viral targeting of DEAD box protein 3 reveals its role in TBK1/IKKepsilon-mediated IRF activation. EMBO J. 2008, 27:2147-2157.
30. Schulz O., Diebold S.S., Chen M., Näslund T.I., Nolte M.A., Alexopoulou L., Azuma Y.T., Flavell R.A., Liljeström P., Reis e Sousa C. Toll-likereceptor 3 promotes cross-priming to virus-infected cells. Nature 2005, 433:887-892.
31. Sedano C.D., Sarnow P. Hepatitis C virus subverts liver-specific miR-122 to protect the viral genome from exoribonuclease Xrn2. Cell Host Microbe 2014, 16:257-264.
32. Shurin G.V., Yurkovetsky Z.R., Chatta G.S., Tourkova I.L., Shurin M.R., Lokshin A.E. Dynamic alteration of soluble serum biomarkers in healthy aging. Cytokine 2007, 39:123-129.
33. Solinger J.A., Kiianitsa K., Heyer W.D. Rad54, a Swi2/Snf2-like recombinational repair protein, disassembles Rad51:dsDNA filaments. Mol. Cell 2002, 10:1175-1188.
34. Soulat D., Bürckstümmer T., Westermayer S., Goncalves A., Bauch A., Stefanovic A., Hantschel O., Bennett K.L., Decker T., Superti-Furga G. The DEAD-box helicase DDX3X is a critical component of the TANK-binding kinase 1-dependent innate immune response. EMBO J. 2008, 27:2135-2146.
35. Sugimoto N., Mitoma H., Kim T., Hanabuchi S., Liu Y.J. Helicase proteins DHX29 and RIG-I cosense cytosolic nucleic acids in the human airway system. Proc. Natl. Acad. Sci. USA 2014, 111:7747-7752.
36. Sun L., Wu J., Du F., Chen X., Chen Z.J. Cyclic GMP-AMP synthase is a cytosolic DNA sensor that activates the type I interferon pathway. Science 2013, 339:786-791.
37. Takahasi K., Yoneyama M., Nishihori T., Hirai R., Kumeta H., Narita R., Gale M., Inagaki F., Fujita T. Nonself RNA-sensing mechanism of RIG-I helicase and activation of antiviral immune responses. Mol. Cell 2008, 29:428-440.
38. Tong J., Taylor P., Jovceva E., St-Germain J.R., Jin L.L., Nikolic A., Gu X., Li Z.H., Trudel S., Moran M.F. Tandem immunoprecipitation of phosphotyrosine-mass spectrometry (TIPY-MS) indicates C19ORF19 becomes tyrosine-phosphorylated and associated with activated epidermal growth factor receptor. J.Proteome Res. 2008, 7:1067-1077.
39. Ueki I.F., Min-Oo G., Kalinowski A., Ballon-Landa E., Lanier L.L., Nadel J.A., Koff J.L. Respiratory virus-induced EGFR activation suppresses IRF1-dependent interferon λ and antiviral defense in airway epithelium. J.Exp. Med. 2013, 210:1929-1936.
40. Yamashita M., Chattopadhyay S., Fensterl V., Saikia P., Wetzel J.L., Sen G.C. Epidermal growth factor receptor is essential for Toll-like receptor 3 signaling. Sci. Signal. 2012, 5:ra50.
41. Yanai H., Ban T., Wang Z., Choi M.K., Kawamura T., Negishi H., Nakasato M., Lu Y., Hangai S., Koshiba R., et al. HMGB proteins function as universal sentinels for nucleic-acid-mediated innate immune responses. Nature 2009, 462:99-103.
42. Yoo J.S., Takahasi K., Ng C.S., Ouda R., Onomoto K., Yoneyama M., Lai J.C., Lattmann S., Nagamine Y., Matsui T., et al. DHX36 enhances RIG-I signaling by facilitating PKR-mediated antiviral stress granule formation. PLoS Pathog. 2014, 10:e1004012.