DHX36 Enhances RIG-I Signaling by Facilitating PKR-Mediated Antiviral Stress Granule Formation

PLoS Pathogens

Volumn 10, Issue 3, 2014, Pages

  Yoo, Ji Seung ^a   Takahasi, Kiyohiro ^a   Ng, Chen Seng ^a   Ouda, Ryota ^a   Onomoto, Koji ^b   Yoneyama, Mitsutoshi ^b   Lai, Janice Ching ^c   Lattmann, Simon ^c   Nagamine, Yoshikuni ^c   Matsui, Tadashi ^d   Iwabuchi, Kuniyoshi ^d   Kato, Hiroki ^a   Fujita, Takashi ^a  

^a KYOTO UNIVERSITY   (Japan)

^b CHIBA UNIVERSITY   (Japan)

^c FRIEDRICH MIESCHER INSTITUTE FOR BIOMEDICAL RESEARCH   (Switzerland)

^d KANAZAWA MEDICAL UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BETA INTERFERON; HELICASE; HELICASE 36; INTERFERON; PROTEIN KINASE; UNCLASSIFIED DRUG; VIRUS RNA;

ARTICLE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DIMERIZATION; ENZYME ACTIVITY; ENZYME LINKED IMMUNOSORBENT ASSAY; GENE ACTIVATION; GENETIC TRANSFECTION; HUMAN CELL; IMMUNOBLOTTING; IMMUNOFLUORESCENCE MICROSCOPY; IMMUNOPRECIPITATION; INNATE IMMUNITY; PHENOTYPE; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; PROTEIN PURIFICATION; REAL TIME POLYMERASE CHAIN REACTION; RNA INTERFERENCE; SIGNAL TRANSDUCTION; VIRUS INFECTION; WESTERN BLOTTING;

CYTOPLASMIC GRANULES; DEAD-BOX RNA HELICASES; EIF-2 KINASE; ENZYME-LINKED IMMUNOSORBENT ASSAY; FLUORESCENT ANTIBODY TECHNIQUE; GENE KNOCKOUT TECHNIQUES; HEK293 CELLS; HELA CELLS; HUMANS; IMMUNOPRECIPITATION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA VIRUS INFECTIONS; RNA VIRUSES; RNA, DOUBLE-STRANDED; RNA, SMALL INTERFERING; RNA, VIRAL; SIGNAL TRANSDUCTION; STRESS, PHYSIOLOGICAL; TRANSFECTION;

EID: 84897407806     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1004012     Document Type: Article

References (43)

1. Fujita T, (2009) A nonself RNA pattern: tri-p to panhandle. Immunity 31: 4-5.
2. Schlee M, Hartmann G, (2010) The chase for the RIG-I ligand-recent advances. Molecular therapy: the journal of the American Society of Gene Therapy 18: 1254-1262.
3. Kato H, Takahasi K, Fujita T, (2011) RIG-I-like receptors: cytoplasmic sensors for non-self RNA. Immunological reviews 243: 91-98.
4. Balachandran S, Barber GN, (2007) PKR in innate immunity, cancer, and viral oncolysis. Methods in molecular biology 383: 277-301.
5. Gilfoy FD, Mason PW, (2007) West Nile virus-induced interferon production is mediated by the double-stranded RNA-dependent protein kinase PKR. Journal of virology 81: 11148-11158.
6. McAllister CS, Toth AM, Zhang P, Devaux P, Cattaneo R, et al. (2010) Mechanisms of protein kinase PKR-mediated amplification of beta interferon induction by C protein-deficient measles virus. Journal of virology 84: 380-386.
7. Pindel A, Sadler A, (2011) The role of protein kinase R in the interferon response. Journal of interferon & cytokine research: the official journal of the International Society for Interferon and Cytokine Research 31: 59-70.
8. Schulz O, Pichlmair A, Rehwinkel J, Rogers NC, Scheuner D, et al. (2010) Protein kinase R contributes to immunity against specific viruses by regulating interferon mRNA integrity. Cell host & microbe 7: 354-361.
9. Sen A, Pruijssers AJ, Dermody TS, Garcia-Sastre A, Greenberg HB, (2011) The early interferon response to rotavirus is regulated by PKR and depends on MAVS/IPS-1, RIG-I, MDA-5, and IRF3. Journal of virology 85: 3717-3732.
10. Nallagatla SR, Hwang J, Toroney R, Zheng X, Cameron CE, et al. (2007) 5′-triphosphate-dependent activation of PKR by RNAs with short stem-loops. Science 318: 1455-1458.
11. Ng CS, Jogi M, Yoo JS, Onomoto K, Koike S, et al. (2013) EMCV Disrupts Stress Granules, the Critical Platform for Triggering Antiviral Innate Immune Responses. Journal of virology 87: 9511-9522.
12. Okonski KM, Samuel CE, (2013) Stress granule formation induced by measles virus is protein kinase PKR dependent and impaired by RNA adenosine deaminase ADAR1. Journal of virology 87: 756-766.
13. Onomoto K, Jogi M, Yoo JS, Narita R, Morimoto S, et al. (2012) Critical role of an antiviral stress granule containing RIG-I and PKR in viral detection and innate immunity. PloS one 7: e43031.
14. Simpson-Holley M, Kedersha N, Dower K, Rubins KH, Anderson P, et al. (2011) Formation of antiviral cytoplasmic granules during orthopoxvirus infection. Journal of virology 85: 1581-1593.
15. Valiente-Echeverria F, Melnychuk L, Mouland AJ, (2012) Viral modulation of stress granules. Virus research 169: 430-437.
16. White JP, Lloyd RE, (2012) Regulation of stress granules in virus systems. Trends in microbiology 20: 175-183.
17. Fullam A, Schroder M, (2013) DExD/H-box RNA helicases as mediators of anti-viral innate immunity and essential host factors for viral replication. Biochimica et biophysica acta 1829: 854-865.
18. Tran H, Schilling M, Wirbelauer C, Hess D, Nagamine Y, (2004) Facilitation of mRNA deadenylation and decay by the exosome-bound, DExH protein RHAU. Molecular cell 13: 101-111.
19. Creacy SD, Routh ED, Iwamoto F, Nagamine Y, Akman SA, et al. (2008) G4 resolvase 1 binds both DNA and RNA tetramolecular quadruplex with high affinity and is the major source of tetramolecular quadruplex G4-DNA and G4-RNA resolving activity in HeLa cell lysates. The Journal of biological chemistry 283: 34626-34634.
20. Lattmann S, Giri B, Vaughn JP, Akman SA, Nagamine Y, (2010) Role of the amino terminal RHAU-specific motif in the recognition and resolution of guanine quadruplex-RNA by the DEAH-box RNA helicase RHAU. Nucleic acids research 38: 6219-6233.
21. Kim T, Pazhoor S, Bao M, Zhang Z, Hanabuchi S, et al. (2010) Aspartate-glutamate-alanine-histidine box motif (DEAH)/RNA helicase A helicases sense microbial DNA in human plasmacytoid dendritic cells. Proceedings of the National Academy of Sciences of the United States of America 107: 15181-15186.
22. Zhang Z, Kim T, Bao M, Facchinetti V, Jung SY, et al. (2011) DDX1, DDX21, and DHX36 helicases form a complex with the adaptor molecule TRIF to sense dsRNA in dendritic cells. Immunity 34: 866-878.
23. Chalupnikova K, Lattmann S, Selak N, Iwamoto F, Fujiki Y, et al. (2008) Recruitment of the RNA helicase RHAU to stress granules via a unique RNA-binding domain. The Journal of biological chemistry 283: 35186-35198.
24. Lai JC, Ponti S, Pan D, Kohler H, Skoda RC, et al. (2012) The DEAH-box helicase RHAU is an essential gene and critical for mouse hematopoiesis. Blood 119: 4291-4300.
25. Schlee M, Roth A, Hornung V, Hagmann CA, Wimmenauer V, et al. (2009) Recognition of 5′ triphosphate by RIG-I helicase requires short blunt double-stranded RNA as contained in panhandle of negative-strand virus. Immunity 31: 25-34.
26. Schmidt A, Schwerd T, Hamm W, Hellmuth JC, Cui S, et al. (2009) 5′-triphosphate RNA requires base-paired structures to activate antiviral signaling via RIG-I. Proceedings of the National Academy of Sciences of the United States of America 106: 12067-12072.
27. Gack MU, Shin YC, Joo CH, Urano T, Liang C, et al. (2007) TRIM25 RING-finger E3 ubiquitin ligase is essential for RIG-I-mediated antiviral activity. Nature 446: 916-920.
28. Anderson P, Kedersha N, (2008) Stress granules: the Tao of RNA triage. Trends in biochemical sciences 33: 141-150.
29. Dey M, Cao C, Dar AC, Tamura T, Ozato K, et al. (2005) Mechanistic link between PKR dimerization, autophosphorylation, and eIF2alpha substrate recognition. Cell 122: 901-913.
30. Lu J, O'Hara EB, Trieselmann BA, Romano PR, Dever TE, (1999) The interferon-induced double-stranded RNA-activated protein kinase PKR will phosphorylate serine, threonine, or tyrosine at residue 51 in eukaryotic initiation factor 2alpha. The Journal of biological chemistry 274: 32198-32203.
31. Kato H, Takeuchi O, Sato S, Yoneyama M, Yamamoto M, et al. (2006) Differential roles of MDA5 and RIG-I helicases in the recognition of RNA viruses. Nature 441: 101-105.
32. White JP, Cardenas AM, Marissen WE, Lloyd RE, (2007) Inhibition of cytoplasmic mRNA stress granule formation by a viral proteinase. Cell host & microbe 2: 295-305.
33. Booy EP, Meier M, Okun N, Novakowski SK, Xiong S, et al. (2012) The RNA helicase RHAU (DHX36) unwinds a G4-quadruplex in human telomerase RNA and promotes the formation of the P1 helix template boundary. Nucleic acids research 40: 4110-4124.
34. Giri B, Smaldino PJ, Thys RG, Creacy SD, Routh ED, et al. (2011) G4 resolvase 1 tightly binds and unwinds unimolecular G4-DNA. Nucleic acids research 39: 7161-7178.
35. Takahasi K, Yoneyama M, Nishihori T, Hirai R, Kumeta H, et al. (2008) Nonself RNA-sensing mechanism of RIG-I helicase and activation of antiviral immune responses. Molecular cell 29: 428-440.
36. Hornung V, Ellegast J, Kim S, Brzozka K, Jung A, et al. (2006) 5′-Triphosphate RNA is the ligand for RIG-I. Science 314: 994-997.
37. Kato H, Takeuchi O, Mikamo-Satoh E, Hirai R, Kawai T, et al. (2008) Length-dependent recognition of double-stranded ribonucleic acids by retinoic acid-inducible gene-I and melanoma differentiation-associated gene 5. The Journal of experimental medicine 205: 1601-1610.
38. Iwamoto F, Stadler M, Chalupnikova K, Oakeley E, Nagamine Y, (2008) Transcription-dependent nucleolar cap localization and possible nuclear function of DExH RNA helicase RHAU. Experimental cell research 314: 1378-1391.
39. Kageyama M, Takahasi K, Narita R, Hirai R, Yoneyama M, et al. (2011) 55 Amino acid linker between helicase and carboxyl terminal domains of RIG-I functions as a critical repression domain and determines inter-domain conformation. Biochemical and biophysical research communications 415: 75-81.
40. Yoneyama M, Kikuchi M, Natsukawa T, Shinobu N, Imaizumi T, et al. (2004) The RNA helicase RIG-I has an essential function in double-stranded RNA-induced innate antiviral responses. Nature immunology 5: 730-737.
41. Iwamura T, Yoneyama M, Yamaguchi K, Suhara W, Mori W, et al. (2001) Induction of IRF-3/-7 kinase and NF-kappaB in response to double-stranded RNA and virus infection: common and unique pathways. Genes to cells: devoted to molecular & cellular mechanisms 6: 375-388.
42. Momose F, Kikuchi Y, Komase K, Morikawa Y, (2007) Visualization of microtubule-mediated transport of influenza viral progeny ribonucleoprotein. Microbes and infection/Institut Pasteur 9: 1422-1433.
43. Matsui T, Tanihara K, Date T, (2001) Expression of unphosphorylated form of human double-stranded RNA-activated protein kinase in Escherichia coli. Biochemical and biophysical research communications 284: 798-807.