Mouse superkiller-2-like helicase DDX60 is dispensable for type I IFN induction and immunity to multiple viruses

European Journal of Immunology

Volumn 45, Issue 12, 2015, Pages 3386-3403

  Goubau, Delphine ^a   van der Veen, Annemarthe G ^a   Chakravarty, Probir ^a   Lin, Rongtuan ^b   Rogers, Neil ^a   Rehwinkel, Jan ^a,d   Deddouche, Safia ^a,e   Rosewell, Ian ^a   Hiscott, John ^c   Reis e Sousa, Caetano ^a  

^a THE FRANCIS CRICK INSTITUTE   (United Kingdom)

^b MCGILL UNIVERSITY   (Canada)

^c Cancer Vaccines and Immune Therapies Program   (United States)

^d UNIVERSITY OF OXFORD   (United Kingdom)

^e Université René Descartes   (France)

Author keywords

DDX60; Innate immunity; Interferon; RIG I like helicases

Indexed keywords

ALPHA INTERFERON; BETA INTERFERON; HELICASE; INTERFERON; INTERFERON REGULATORY FACTOR 3; INTERFERON REGULATORY FACTOR 7; NONSTRUCTURAL PROTEIN 1; RETINOIC ACID INDUCIBLE PROTEIN I; SUPERKILLER 2 LIKE HELICASE DDX60; UNCLASSIFIED DRUG; CYTOKINE; DDX60 PROTEIN, MOUSE; DEAD BOX PROTEIN; TOLL LIKE RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BONE MARROW CELL; CONTROLLED STUDY; ENCEPHALOMYOCARDITIS VIRUS; FEMALE; FIBROBLAST; GENE EXPRESSION PROFILING; GENE OVEREXPRESSION; HEK293 CELL LINE; HELA CELL LINE; HEPATITIS C VIRUS; HERPES SIMPLEX VIRUS 1; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; INFLUENZA; INFLUENZA A VIRUS; LISTERIA MONOCYTOGENES; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; RNA VIRUS; SINDBIS VIRUS; UPREGULATION; VACCINIA VIRUS; VIRUS IMMUNITY; VIRUS INFECTION; VIRUS STRAIN; ANIMAL; BIOSYNTHESIS; CELL LINE; IMMUNOLOGY; PHYSIOLOGY;

ANIMALS; CELL LINE; CYTOKINES; DEAD-BOX RNA HELICASES; HUMANS; INTERFERON TYPE I; MICE; TOLL-LIKE RECEPTORS; VIRUS DISEASES;

EID: 84952637644     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.201545794     Document Type: Article

References (57)

1. Goubau, D., Deddouche, S. and Reis e Sousa, C. Cytosolic sensing of viruses. Immunity 2013. 38: 855-869.
2. Levy, D. E., Marié, I. J. and Durbin, J. E. Induction and function of type I and III interferon in response to viral infection. Curr. Opin. Virol. 2011. 1: 476-486.
3. Takeuchi, O. and Akira, S. Pattern recognition receptors and inflammation. Cell 2010. 140: 805-820.
4. Yoneyama, M., Onomoto, K., Jogi, M., Akaboshi, T. and Fujita, T. Viral RNA detection by RIG-I-like receptors. Curr. Opin. Immunol. 2015. 32C: 48-53.
5. Ablasser, A., Bauernfeind, F., Hartmann, G., Latz, E., Fitzgerald, K. A. and Hornung, V. RIG-I-dependent sensing of poly(dA:dT) through the induction of an RNA polymerase III-transcribed RNA intermediate. Nat. Immunol. 2009. 10: 1065-1072.
6. Chiu, Y.-H., Macmillan, J. B. and Chen, Z. J. RNA polymerase III detects cytosolic DNA and induces type I interferons through the RIG-I pathway. Cell 2009. 138: 576-591.
7. Cai, X., Chiu, Y.-H., and Chen, Z. J. The cGAS-cGAMP-STING pathway of cytosolic DNA sensing and signaling. Mol. Cell 2014. 54: 289-296.
8. Li, X.-D., Wu, J., Gao, D., Wang, H., Sun, L. and Chen, Z. J. Pivotal roles of cGAS-cGAMP signaling in antiviral defense and immune adjuvant effects. Science 2013. 341: 1390-1394.
9. Schoggins, J. W., MacDuff, D. A., Imanaka, N., Gainey, M. D., Shrestha, B., Eitson, J. L., Mar, K. B. et al., Pan-viral specificity of IFN-induced genes reveals new roles for cGAS in innate immunity. Nature 2014. 505: 691-695.
10. Ishikawa, H., Ma, Z. and Barber, G. N. STING regulates intracellular DNA-mediated, type I interferon-dependent innate immunity. Nature 2009. 461: 788-792.
11. 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.
12. 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.
13. Sun, Q., Sun, L., Liu, H.-H., Chen, X., Seth, R. B., Forman, J. and Chen, Z. J. The specific and essential role of MAVS in antiviral innate immune responses. Immunity 2006. 24: 633-642.
14. Kumar, H., Kawai, T., Kato, H., Sato, S., Takahashi, K., Coban, C., Yamamoto, M. et al., Essential role of IPS-1 in innate immune responses against RNA viruses. J. Exp. Med. 2006. 203: 1795-1803.
15. Kang, D.-C., Gopalkrishnan, R. V., Wu, Q., Jankowsky, E., Pyle, A. M. and Fisher, P. B. MDA-5: an interferon-inducible putative RNA helicase with double-stranded RNA-dependent ATPase activity and melanoma growth-suppressive properties. Proc. Natl. Acad. Sci. 2002. 99: 637-642.
16. Fullam, A. and Schröder, M. DExD/H-box RNA helicases as mediators of anti-viral innate immunity and essential host factors for viral replication. Biochim. Biophys. Acta 2013. 1829: 854-865.
17. Goubau, D., Romieu-Mourez, R., Solis, M., Hernandez, E., Mesplède, T., Lin, R., Leaman, D. et al., Transcriptional re-programming of primary macrophages reveals distinct apoptotic and anti-tumoral functions of IRF-3 and IRF-7. Eur. J. Immunol. 2009. 39: 527-540.
18. Knipe, D. M. and Howley, P. M. In Knipe, D. M., Howley, P. M., Griffin, D. E., Lamb, R. A., Martin, M. A., Straus, B., Roizman, S. E. (Eds.). Fields virology (vol. 1 and 2, 5 ed.). Chapter 22: Viruses and Prions of Yeast, Fungi and Unicellular Organisms. Wolters Kluwer Health/Lippincott Williams & Wilkins, Philadelphia, PA, 2007, pp. 743-744.
19. Wickner, R. B. Double-stranded RNA viruses of Saccharomyces cerevisiae. Microbiol. Rev. 1996. 60: 250-265.
20. Jankowsky, E., Neidle, S., Lilley, D. M. J., Hubbard, R. E., Merrick, W. C., Linder, P., Russell, R. et al., In Jankowsky, E. (Ed.). RNA helicases. Chapter 6: SKi2-Like Proteins: Biology and Mechanism. RSC Biomolecular Sciences, Cambridge, UK, 2012, pp. 149-163.
21. Miyashita, M., Oshiumi, H., Matsumoto, M. and 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.
22. Oshiumi, H., Miyashita, M., Okamoto, M., Morioka, Y., Okabe, M., Matsumoto, M. and Seya, T. DDX60 is involved in RIG-I-dependent and independent antiviral responses, and its function is attenuated by virus-induced EGFR activation. Cell Rep. 2015. 11: 1193-1207.
23. Schoggins, J. W., Wilson, S. J., Panis, M., Murphy, M. Y., Jones, C. T., Bieniasz, P. and Rice, C. M. A diverse range of gene products are effectors of the type I interferon antiviral response. Nature 2011. 472: 481-485.
24. Miller, J. C., Brown, B. D., Shay, T., Gautier, E. L., Jojic, V., Cohain, A., Pandey, G. et al., Deciphering the transcriptional network of the dendritic cell lineage. Nat. Immunol. 2012. 13: 888-899.
25. Meylan, E., Curran, J., Hofmann, K., Moradpour, D., Binder, M., Bartenschlager, R. and Tschopp, J. Cardif is an adaptor protein in the RIG-I antiviral pathway and is targeted by hepatitis C virus. Nature 2005. 437: 1167-1172.
26. Seth, R. B., Sun, L., Ea, C.-K. and Chen, Z. J. Identification and characterization of MAVS, a mitochondrial antiviral signaling protein that activates NF-kappaB and IRF 3. Cell. 2005. 122: 669-682.
27. Kawai, T., Takahashi, K., Sato, S., Coban, C., Kumar, H., Kato, H., Ishii, K. J. et al., IPS-1, an adaptor triggering RIG-I- and Mda5-mediated type I interferon induction. Nat. Immunol. 2005. 6: 981-988.
28. Xu, L.-G., Wang, Y.-Y., Han, K.-J., Li, L.-Y., Zhai, Z. and Shu, H.-B. VISA is an adapter protein required for virus-triggered IFN-beta signaling. Mol. Cell 2005. 19: 727-740.
29. Yoneyama, M., Kikuchi, M., Natsukawa, T., Shinobu, N., Imaizumi, T., Miyagishi, M., Taira, K. et al., The RNA helicase RIG-I has an essential function in double-stranded RNA-induced innate antiviral responses. Nat. Immunol. 2004. 5: 730-737.
30. Lin, R., Heylbroeck, C., Pitha, P. M. and Hiscott, J. Virus-dependent phosphorylation of the IRF-3 transcription factor regulates nuclear translocation, transactivation potential, and proteasome-mediated degradation. Mol. Cell. Biol. 1998. 18: 2986-2996.
31. Skarnes, W. C., Rosen, B., West, A. P., Koutsourakis, M., Bushell, W., Iyer, V., Mujica, A. O. et al., A conditional knockout resource for the genome-wide study of mouse gene function. Nature 2011. 474: 337-342.
32. Pichlmair, A., Schulz, O., Tan, C. P., Rehwinkel, J., Kato, H., Takeuchi, O., Akira, S. et al., Activation of MDA5 requires higher-order RNA structures generated during virus infection. J. Virol. 2009. 83: 10761-10769.
33. Goubau, D., Schlee, M., Deddouche, S., Pruijssers, A. J., Zillinger, T., Goldeck, M., Schuberth, C. et al., Antiviral immunity via RIG-I-mediated recognition of RNA bearing 5'' -diphosphates. Nature. 2014. 514: 372-375.
34. Rehwinkel, J., Tan, C. P., Goubau, D., Schulz, O., Pichlmair, A., Bier, K., Robb, N. et al., RIG-I detects viral genomic RNA during negative-strand RNA virus infection. Cell 2010. 140: 397-408.
35. Burdette, D. L., Monroe, K. M., Sotelo-Troha, K., Iwig, J. S., Eckert, B., Hyodo, M., Hayakawa, Y. et al., STING is a direct innate immune sensor of cyclic di-GMP. Nature 2011. 478: 515-518.
36. Kawai, T. and Akira, S. The role of pattern-recognition receptors in innate immunity: update on Toll-like receptors. Nat. Immunol. 2010. 11: 373-384.
37. LeibundGut-Landmann, S., Gross, O., Robinson, M. J., Osorio, F., Slack, E. C., Tsoni, S. V., Schweighoffer, E. et al., Syk- and CARD9-dependent coupling of innate immunity to the induction of T helper cells that produce interleukin 17. Nat. Immunol. 2007. 8: 630-638.
38. Grimm, D., Staeheli, P., Hufbauer, M., Koerner, I., Martínez-Sobrido, L., Solórzano, A., García-Sastre, A. et al., Replication fitness determines high virulence of influenza A virus in mice carrying functional Mx1 resistance gene. Proc. Natl. Acad. Sci. USA 2007. 104: 6806-6811.
39. Kochs, G., Martínez-Sobrido, L., Lienenklaus, S., Weiss, S., García-Sastre, A. and Staeheli, P. Strong interferon-inducing capacity of a highly virulent variant of influenza A virus strain PR8 with deletions in the NS1 gene. J. Gen. Virol. 2009. 90: 2990-2994.
40. Everitt, A. R., Clare, S., Pertel, T., John, S. P., Wash, R. S., Smith, S. E., Chin, C. R. et al., IFITM3 restricts the morbidity and mortality associated with influenza. Nature 2012. 484: 519-523.
41. Doi, K. Experimental encephalomyocarditis virus infection in small laboratory rodents. J. Comp. Pathol. 2011. 144: 25-40.
42. Gitlin, L., Barchet, W., Gilfillan, S., Cella, M., Beutler, B., Flavell, R. A., Diamond, M. S. et al., 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.
43. Ryman, K. D., Klimstra, W. B., Nguyen, K. B., Biron, C. A. and Johnston, R. E. Alpha/beta interferon protects adult mice from fatal Sindbis virus infection and is an important determinant of cell and tissue tropism. J. Virol. 2000. 74: 3366-3378.
44. Weisswange, I., Newsome, T. P., Schleich, S. and Way, M. The rate of N-WASP exchange limits the extent of ARP2/3-complex-dependent actin-based motility. Nature 2009. 458: 87-91.
45. Wallace, M. E., Keating, R., Heath, W. R. and Carbone, F. R. The cytotoxic T-cell response to herpes simplex virus type 1 infection of C57BL/6 mice is almost entirely directed against a single immunodominant determinant. J. Virol. 1999. 73: 7619-7626.
46. Mangan, N. E. and Fung, K. Y. Type I interferons in regulation of mucosal immunity. Immunol. Cell Biol. 2012. 90: 510-519.
47. O'Connell, R. M., Saha, S. K., Vaidya, S. A., Bruhn, K. W., Miranda, G. A., Zarnegar, B., Perry, A. K. et al., Type I interferon production enhances susceptibility to Listeria monocytogenes infection. J. Exp. Med. 2004. 200: 437-445.
48. Auerbuch, V., Brockstedt, D. G., Meyer-Morse, N., O'Riordan, M. and Portnoy, D. A. Mice lacking the type I interferon receptor are resistant to Listeria monocytogenes. J. Exp. Med. 2004. 200: 527-533.
49. Eckard, S. C., Rice, G. I., Fabre, A., Badens, C., Gray, E. E., Hartley, J. L., Crow, Y. J. et al., The SKIV2L RNA exosome limits activation of the RIG-I-like receptors. Nat. Immunol. 2014. 15: 839-845.
50. Zhao, T., Yang, L., Sun, Q., Arguello, M., Ballard, D. W., Hiscott, J. and Lin, R. The NEMO adaptor bridges the nuclear factor-kappaB and interferon regulatory factor signaling pathways. Nat. Immunol. 2007. 8: 592-600.
51. Inaba, K., Inaba, M., Romani, N., Aya, H., Deguchi, M., Ikehara, S., Muramatsu, S. et al., 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.
52. Schraml, B. U., van Blijswijk, J., Zelenay, S., Whitney, P. G., Filby, A., Acton, S. E., Rogers, N. C. et al., Genetic tracing via DNGR-1 expression history defines dendritic cells as a hematopoietic lineage. Cell 2013. 154: 843-858.
53. Busch, D. H., Vijh, S. and Pamer, E. G. Current protocols in immunology: animal model for infection with Listeria monocytogenes, John Willey & Sons, Inc., 2000, 19.9.1-19.9.9.
54. Diebold, S. S., Montoya, M., Unger, H., Alexopoulou, L., Roy, P., Haswell, L. E., Al-Shamkhani, A. et al., Viral infection switches non-plasmacytoid dendritic cells into high interferon producers. Nature 2003. 424: 324-328.
55. Huson, D. H., Richter, D. C., Rausch, C., Dezulian, T., Franz, M. and Rupp, R. Dendroscope: an interactive viewer for large phylogenetic trees. BMC Bioinformatics 2007. 8: 460.
56. Karolchik, D., Baertsch, R., Diekhans, M., Furey, T. S., Hinrichs, A., Lu, Y. T., Roskin, K. M. et al., The UCSC genome browser database. Nucleic Acids Res. 2003. 31: 51-54.
57. Rice, P., Longden, I. and Bleasby, A. EMBOSS: the European molecular biology open software suite. Trends Genet. 2000. 16: 276-277.