1887

Abstract

DExH/D-box helicases are essential nucleic acid and ribonucleoprotein remodelers involved in all aspects of nucleic acid metabolism including replication, gene expression and post-transcriptional modifications. In parallel to their importance in basic cellular functions, DExH/D-box helicases play multiple roles in viral life cycles, with some of them highjacked by viruses or negatively regulating innate immune activation. However, other DExH/D-box helicases have recurrently been highlighted as direct antiviral effectors or as positive regulators of innate immune activation. Innate immunity relies on the ability of Pathogen Recognition Receptors to recognize viral signatures and trigger the production of interferons (IFNs) and pro-inflammatory cytokines. Secreted IFNs interact with their receptors to establish antiviral cellular reprogramming via expression regulation of the interferon-stimulated genes (ISGs). Several DExH/D-box helicases have been reported to act as viral sensors (DDX3, DDX41, DHX9, DDX1/DDX21/DHX36 complex), and others to play roles in innate immune activation (DDX60, DDX60L, DDX23). In contrast, the DDX39A, DDX46, DDX5 and DDX24 helicases act as negative regulators and impede IFN production upon viral infection. Beyond their role in viral sensing, the ISGs DDX60 and DDX60L act as viral inhibitors. Interestingly, the constitutively expressed DEAD-box helicases DDX56, DDX17, DDX42 intrinsically restrict viral replication. Hence, DExH/D-box helicases appear to form a multilayer network of primary and secondary factors involved in both intrinsic and innate antiviral immunity. In this review, we highlight recent findings on the extent of antiviral defences played by helicases and emphasize the need to better understand their immune functions as well as their complex interplay.

Funding
This study was supported by the:
  • European Research Council (Award 759226)
    • Principle Award Recipient: CarolineGoujon
  • Fondation pour la recherche médicale (FRM) (Award FDT201904008024)
    • Principle Award Recipient: BorisBonaventure
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License. The Microbiology Society waived the open access fees for this article.
Loading

Article metrics loading...

/content/journal/jgv/10.1099/jgv.0.001766
2022-08-25
2024-04-20
Loading full text...

Full text loading...

/deliver/fulltext/jgv/103/8/jgv001766.html?itemId=/content/journal/jgv/10.1099/jgv.0.001766&mimeType=html&fmt=ahah

References

  1. Bieniasz PD. Intrinsic immunity: a front-line defense against viral attack. Nat Immunol 2004; 5:1109–1115 [View Article] [PubMed]
    [Google Scholar]
  2. Doyle T, Goujon C, Malim MH. HIV-1 and interferons: who’s interfering with whom?. Nat Rev Microbiol 2015; 13:403–413 [View Article] [PubMed]
    [Google Scholar]
  3. Yan N, Chen ZJ. Intrinsic antiviral immunity. Nat Immunol 2012; 13:214–222 [View Article] [PubMed]
    [Google Scholar]
  4. Kawai T, Akira S. The roles of TLRs, RLRs and NLRs in pathogen recognition. International Immunology 2009; 21:317–337 [View Article] [PubMed]
    [Google Scholar]
  5. Loo Y-M, Gale M. Immune Signaling by RIG-I-like Receptors. Immunity 2011; 34:680–692 [View Article] [PubMed]
    [Google Scholar]
  6. Bermejo-Jambrina M, Eder J, Helgers LC, Hertoghs N, Nijmeijer BM et al. C-type lectin receptors in antiviral immunity and viral escape. Front Immunol 2018; 9:590 [View Article] [PubMed]
    [Google Scholar]
  7. Satoh T, Akira S. Toll-Like Receptor Signaling and Its Inducible Proteins. Microbiol Spectr 2016; 4: [View Article] [PubMed]
    [Google Scholar]
  8. Takeda K, Akira S. Toll-like receptors in innate immunity. Int Immunol 2005; 17:1–14 [View Article] [PubMed]
    [Google Scholar]
  9. Lazear HM, Schoggins JW, Diamond MS. Shared and Distinct Functions of Type I and Type III Interferons. Immunity 2019; 50:907–923 [View Article] [PubMed]
    [Google Scholar]
  10. Schoggins JW. Interferon-Stimulated Genes: What Do They All Do?. Annu Rev Virol 2019; 6:567–584 [View Article] [PubMed]
    [Google Scholar]
  11. Cordin O, Banroques J, Tanner NK, Linder P. The DEAD-box protein family of RNA helicases. Gene 2006; 367:17–37 [View Article] [PubMed]
    [Google Scholar]
  12. Fairman-Williams ME, Guenther U-P, Jankowsky E. SF1 and SF2 helicases: family matters. Curr Opin Struct Biol 2010; 20:313–324 [View Article] [PubMed]
    [Google Scholar]
  13. Singleton MR, Dillingham MS, Wigley DB. Structure and mechanism of helicases and nucleic acid translocases. Annu Rev Biochem 2007; 76:23–50 [View Article] [PubMed]
    [Google Scholar]
  14. Linder P, Jankowsky E. From unwinding to clamping - the DEAD box RNA helicase family. Nat Rev Mol Cell Biol 2011; 12:505–516 [View Article] [PubMed]
    [Google Scholar]
  15. Bernstein DA, Keck JL. Domain mapping of Escherichia coli RecQ defines the roles of conserved N- and C-terminal regions in the RecQ family. Nucleic Acids Research 2003; 31:2778–2785 [View Article] [PubMed]
    [Google Scholar]
  16. He Y, Andersen GR, Nielsen KH. Structural basis for the function of DEAH helicases. EMBO Rep 2010; 11:180–186 [View Article] [PubMed]
    [Google Scholar]
  17. Klostermeier D, Rudolph MG. A novel dimerization motif in the C-terminal domain of the Thermus thermophilus DEAD box helicase Hera confers substantial flexibility †. Nucleic Acids Research 2009; 37:421–430 [View Article] [PubMed]
    [Google Scholar]
  18. Bernstein E, Caudy AA, Hammond SM, Hannon GJ. Role for a bidentate ribonuclease in the initiation step of RNA interference. Nature 2001; 409:363–366 [View Article] [PubMed]
    [Google Scholar]
  19. Shereda RD, Reiter NJ, Butcher SE, Keck JL. Identification of the SSB binding site on E. coli RecQ reveals a conserved surface for binding SSB’s C terminus. J Mol Biol 2009; 386:612–625 [View Article] [PubMed]
    [Google Scholar]
  20. Trubetskoy D, Proux F, Allemand F, Dreyfus M, Iost I. SrmB, a DEAD-box helicase involved in Escherichia coli ribosome assembly, is specifically targeted to 23S rRNA in vivo. Nucleic Acids Research 2009; 37:6540–6549 [View Article] [PubMed]
    [Google Scholar]
  21. Gorbalenya AE, Koonin EV. Helicases: amino acid sequence comparisons and structure-function relationships. Current Opinion in Structural Biology 1993; 3:419–429 [View Article]
    [Google Scholar]
  22. Ali MAM. DEAD-box RNA helicases: The driving forces behind RNA metabolism at the crossroad of viral replication and antiviral innate immunity. Virus Research 2021; 296:198352 [View Article] [PubMed]
    [Google Scholar]
  23. Taschuk F, Cherry S. DEAD-Box Helicases: Sensors, Regulators, and Effectors for Antiviral Defense. Viruses 2020; 12:181 [View Article] [PubMed]
    [Google Scholar]
  24. Valiente-Echeverría F., Hermoso M.A., Soto-Rifo R. 2015; RNA helicase DDX3: at the crossroad of viral replication and antiviral immunity: DDX3 in viral replication and immunity. Rev. Med. Virol 25:286–299 https://doi.org/10.1002/rmv.1845
    [Google Scholar]
  25. Gitlin L, Barchet W, Gilfillan S, Cella M, Beutler B 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 [View Article] [PubMed]
    [Google Scholar]
  26. Kato H, Sato S, Yoneyama M, Yamamoto M, Uematsu S et al. Cell type-specific involvement of RIG-I in antiviral response. Immunity 2005; 23:19–28 [View Article] [PubMed]
    [Google Scholar]
  27. Yoneyama M, Kikuchi M, Natsukawa T, Shinobu N, Imaizumi T 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 [View Article] [PubMed]
    [Google Scholar]
  28. Pichlmair A, Schulz O, Tan CP, Näslund TI, Liljeström P et al. RIG-I-mediated antiviral responses to single-stranded RNA bearing 5’-phosphates. Science 2006; 314:997–1001 [View Article] [PubMed]
    [Google Scholar]
  29. Wang Y, Ludwig J, Schuberth C, Goldeck M, Schlee M et al. Structural and functional insights into 5’-ppp RNA pattern recognition by the innate immune receptor RIG-I. Nat Struct Mol Biol 2010; 17:781–787 [View Article] [PubMed]
    [Google Scholar]
  30. Saito T, Owen DM, 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 [View Article] [PubMed]
    [Google Scholar]
  31. Kato H, Takeuchi O, Mikamo-Satoh E, Hirai R, Kawai T et al. Length-dependent recognition of double-stranded ribonucleic acids by retinoic acid–inducible gene-I and melanoma differentiation–associated gene 5. Journal of Experimental Medicine 2008; 205:1601–1610 [View Article] [PubMed]
    [Google Scholar]
  32. Takahasi K, Kumeta H, Tsuduki N, Narita R, Shigemoto T et al. Solution structures OF cytosolic RNA sensor MDA5 and LGP2 C-terminal domains: identification of the rna recognition loop in RIG-I-like receptors. J Biol Chem 2009; 284:17465–17474 [View Article] [PubMed]
    [Google Scholar]
  33. Belgnaoui SM, Gosden RG, Semmes OJ, Haoudi A. Human LINE-1 retrotransposon induces DNA damage and apoptosis in cancer cells. Cancer Cell Int 2006; 6:13 [View Article] [PubMed]
    [Google Scholar]
  34. Goubau D, Deddouche S, Reis e Sousa C. Cytosolic sensing of viruses. Immunity 2013; 38:855–869 [View Article] [PubMed]
    [Google Scholar]
  35. Rehwinkel J, Gack MU. RIG-I-like receptors: their regulation and roles in RNA sensing. Nat Rev Immunol 2020; 20:537–551 [View Article] [PubMed]
    [Google Scholar]
  36. Chazal M, Beauclair G, Gracias S, Najburg V, Simon-Lorière E et al. RIG-I Recognizes the 5’ Region of Dengue and Zika Virus Genomes. Cell Rep 2018; 24:320–328 [View Article] [PubMed]
    [Google Scholar]
  37. Fredericksen BL, Gale M. West Nile virus evades activation of interferon regulatory factor 3 through RIG-I-dependent and -independent pathways without antagonizing host defense signaling. J Virol 2006; 80:2913–2923 [View Article] [PubMed]
    [Google Scholar]
  38. Rehwinkel J, Tan CP, Goubau D, Schulz O, Pichlmair A et al. RIG-I Detects Viral Genomic RNA during Negative-Strand RNA Virus Infection. Cell 2010; 140:397–408 [View Article] [PubMed]
    [Google Scholar]
  39. Feng Q, Hato SV, Langereis MA, Zoll J, Virgen-Slane R et al. MDA5 detects the double-stranded RNA replicative form in picornavirus-infected cells. Cell Rep 2012; 2:1187–1196 [View Article] [PubMed]
    [Google Scholar]
  40. Kato H, Takeuchi O, Sato S, Yoneyama M, Yamamoto M et al. Differential roles of MDA5 and RIG-I helicases in the recognition of RNA viruses. Nature 2006; 441:101–105 [View Article] [PubMed]
    [Google Scholar]
  41. Rebendenne A, Chaves Valadão AL, Tauziet M, Maarifi G, Bonaventure B et al. SARS-CoV-2 Triggers an MDA-5-Dependent Interferon Response Which Is Unable To Control Replication in Lung Epithelial Cells. J Virol 2021; 95: [View Article] [PubMed]
    [Google Scholar]
  42. Sampaio NG, Chauveau L, Hertzog J, Bridgeman A, Fowler G et al. The RNA sensor MDA5 detects SARS-CoV-2 infection. Sci Rep 2021; 11:13638 [View Article] [PubMed]
    [Google Scholar]
  43. Yin X, Riva L, Pu Y, Martin-Sancho L, Kanamune J et al. MDA5 Governs the Innate Immune Response to SARS-CoV-2 in Lung Epithelial Cells. Cell Reports 2021; 34:108628 [View Article] [PubMed]
    [Google Scholar]
  44. Zalinger ZB, Elliott R, Rose KM, Weiss SR. MDA5 Is Critical to Host Defense during Infection with Murine Coronavirus. J Virol 2015; 89:12330–12340 [View Article] [PubMed]
    [Google Scholar]
  45. Soto-Rifo R, Ohlmann T. The role of the DEAD-box RNA helicase DDX3 in mRNA metabolism. WIREs RNA 2013; 4:369–385 [View Article] [PubMed]
    [Google Scholar]
  46. 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-β-inducing potential. Eur J Immunol 2010; 40:940–948 [View Article] [PubMed]
    [Google Scholar]
  47. Gringhuis SI, Hertoghs N, Kaptein TM, Zijlstra-Willems EM, Sarrami-Forooshani R et al. HIV-1 blocks the signaling adaptor MAVS to evade antiviral host defense after sensing of abortive HIV-1 RNA by the host helicase DDX3. Nat Immunol 2017; 18:225–235 [View Article] [PubMed]
    [Google Scholar]
  48. Saha SK, Pietras EM, He JQ, Kang JR, Liu S-Y et al. Regulation of antiviral responses by a direct and specific interaction between TRAF3 and Cardif. EMBO J 2006; 25:3257–3263 [View Article] [PubMed]
    [Google Scholar]
  49. Gu L, Fullam A, McCormack N, Höhn Y, Schröder M. DDX3 directly regulates TRAF3 ubiquitination and acts as a scaffold to co-ordinate assembly of signalling complexes downstream from MAVS. Biochemical Journal 2017; 474:571–587 [View Article] [PubMed]
    [Google Scholar]
  50. Kayagaki N, Phung Q, Chan S, Chaudhari R, Quan C et al. A Deubiquitinase That Regulates Type I Interferon Production. Science 2007; 318:1628–1632 [View Article] [PubMed]
    [Google Scholar]
  51. Tseng P-H, Matsuzawa A, Zhang W, Mino T, Vignali DAA et al. Different modes of ubiquitination of the adaptor TRAF3 selectively activate the expression of type I interferons and proinflammatory cytokines. Nat Immunol 2009; 11:70–75 [View Article] [PubMed]
    [Google Scholar]
  52. Schröder M, Baran M, Bowie AG. Viral targeting of DEAD box protein 3 reveals its role in TBK1/IKKepsilon-mediated IRF activation. EMBO J 2008; 27:2147–2157 [View Article] [PubMed]
    [Google Scholar]
  53. Soulat D, Bürckstümmer T, Westermayer S, Goncalves A, Bauch A et al. 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 [View Article] [PubMed]
    [Google Scholar]
  54. Zhang Z, Kim T, Bao M, Facchinetti V, Jung SY et al. DDX1, DDX21, and DHX36 Helicases Form a Complex with the Adaptor Molecule TRIF to Sense dsRNA in Dendritic Cells. Immunity 2011; 34:866–878 [View Article] [PubMed]
    [Google Scholar]
  55. Bléoo S, Sun X, Hendzel MJ, Rowe JM, Packer M et al. Association of human DEAD box protein DDX1 with a cleavage stimulation factor involved in 3’-end processing of pre-MRNA. Mol Biol Cell 2001; 12:3046–3059 [View Article] [PubMed]
    [Google Scholar]
  56. Germain DR, Li L, Hildebrandt MR, Simmonds AJ, Hughes SC et al. Loss of the Drosophila melanogaster DEAD box protein Ddx1 leads to reduced size and aberrant gametogenesis. Developmental Biology 2015; 407:232–245 [View Article] [PubMed]
    [Google Scholar]
  57. Han C, Liu Y, Wan G, Choi HJ, Zhao L et al. The RNA-Binding Protein DDX1 Promotes Primary MicroRNA Maturation and Inhibits Ovarian Tumor Progression. Cell Reports 2014; 8:1447–1460 [View Article] [PubMed]
    [Google Scholar]
  58. Pérez-González A, Pazo A, Navajas R, Ciordia S, Rodriguez-Frandsen A et al. hCLE/C14orf166 associates with DDX1-HSPC117-FAM98B in a novel transcription-dependent shuttling RNA-transporting complex. PLoS One 2014; 9:e90957 [View Article] [PubMed]
    [Google Scholar]
  59. Zhong W, Li Z, Zhou M, Xu T, Wang Y. DDX1 regulates alternative splicing and insulin secretion in pancreatic β cells. Biochemical and Biophysical Research Communications 2018; 500:751–757 [View Article] [PubMed]
    [Google Scholar]
  60. Calo E, Flynn RA, Martin L, Spitale RC, Chang HY et al. RNA helicase DDX21 coordinates transcription and ribosomal RNA processing. Nature 2015; 518:249–253 [View Article] [PubMed]
    [Google Scholar]
  61. Holmström TH, Mialon A, Kallio M, Nymalm Y, Mannermaa L et al. c-Jun supports ribosomal RNA processing and nucleolar localization of RNA helicase DDX21. J Biol Chem 2008; 283:7046–7053 [View Article] [PubMed]
    [Google Scholar]
  62. Xing Y-H, Yao R-W, Zhang Y, Guo C-J, Jiang S et al. SLERT Regulates DDX21 Rings Associated with Pol I Transcription. Cell 2017; 169:664–678 [View Article] [PubMed]
    [Google Scholar]
  63. Chang-Gu B, Bradburn D, Yangyuoru PM, Russell R. The DHX36-specific-motif (DSM) enhances specificity by accelerating recruitment of DNA G-quadruplex structures. Biol Chem 2021; 402:593–604 [View Article] [PubMed]
    [Google Scholar]
  64. Iwamoto F, Stadler M, Chalupníková K, Oakeley E, Nagamine Y. Transcription-dependent nucleolar cap localization and possible nuclear function of DExH RNA helicase RHAU. Exp Cell Res 2008; 314:1378–1391 [View Article] [PubMed]
    [Google Scholar]
  65. Kim H-N, Lee J-H, Bae S-C, Ryoo H-M, Kim H-H et al. Histone deacetylase inhibitor MS-275 stimulates bone formation in part by enhancing Dhx36-mediated TNAP transcription. J Bone Miner Res 2011; 26:2161–2173 [View Article] [PubMed]
    [Google Scholar]
  66. Murat P, Marsico G, Herdy B, Ghanbarian AT, Portella G et al. RNA G-quadruplexes at upstream open reading frames cause DHX36- and DHX9-dependent translation of human mRNAs. Genome Biol 2018; 19:229 [View Article] [PubMed]
    [Google Scholar]
  67. Sauer M, Juranek SA, Marks J, De Magis A, Kazemier HG et al. DHX36 prevents the accumulation of translationally inactive mRNAs with G4-structures in untranslated regions. Nat Commun 2019; 10:2421 [View Article] [PubMed]
    [Google Scholar]
  68. Tran H, Schilling M, Wirbelauer C, Hess D, Nagamine Y. Facilitation of mRNA deadenylation and decay by the exosome-bound, DExH protein RHAU. Mol Cell 2004; 13:101–111 [View Article] [PubMed]
    [Google Scholar]
  69. Pennemann FL, Mussabekova A, Urban C, Stukalov A, Andersen LL et al. Cross-species analysis of viral nucleic acid interacting proteins identifies TAOKs as innate immune regulators. Nat Commun 2021; 12:7009 [View Article] [PubMed]
    [Google Scholar]
  70. Zhang Z, Yuan B, Bao M, Lu N, Kim T et al. The helicase DDX41 senses intracellular DNA mediated by the adaptor STING in dendritic cells. Nat Immunol 2011; 12:959–965 [View Article] [PubMed]
    [Google Scholar]
  71. Hu W, Jain A, Gao Y, Dozmorov IM, Mandraju R et al. Differential outcome of TRIF-mediated signaling in TLR4 and TLR3 induced DC maturation. Proc Natl Acad Sci U S A 2015; 112:13994–13999 [View Article] [PubMed]
    [Google Scholar]
  72. Wu W, Qu Y, Yu S, Wang S, Yin Y et al. Caspase-Dependent Cleavage of DDX21 Suppresses Host Innate Immunity. mBio 2021; 12:e0100521 [View Article] [PubMed]
    [Google Scholar]
  73. Yoo J-S, Takahasi K, Ng CS, Ouda R, Onomoto K et al. DHX36 enhances RIG-I signaling by facilitating PKR-mediated antiviral stress granule formation. PLoS Pathog 2014; 10:e1004012 [View Article] [PubMed]
    [Google Scholar]
  74. Kim T, Pazhoor S, Bao M, Zhang Z, Hanabuchi S et al. Aspartate-glutamate-alanine-histidine box motif (DEAH)/RNA helicase A helicases sense microbial DNA in human plasmacytoid dendritic cells. Proc Natl Acad Sci USA 2010; 107:15181–15186 [View Article] [PubMed]
    [Google Scholar]
  75. Naji S, Ambrus G, Cimermančič P, Reyes JR, Johnson JR et al. Host cell interactome of HIV-1 Rev includes RNA helicases involved in multiple facets of virus production. Mol Cell Proteomics 2012; 11:M111 [View Article] [PubMed]
    [Google Scholar]
  76. Chen G, Liu C-H, Zhou L, Krug RM. Cellular DDX21 RNA helicase inhibits influenza a virus replication but is counteracted by the viral NS1 protein. Cell Host & Microbe 2014; 15:484–493 [View Article] [PubMed]
    [Google Scholar]
  77. McKellar J, Rebendenne A, Wencker M, Moncorgé O, Goujon C. Mammalian and avian host cell influenza a restriction factors. Viruses 2021; 13:522 [View Article] [PubMed]
    [Google Scholar]
  78. Jain A, Bacolla A, Chakraborty P, Grosse F, Vasquez KM. Human DHX9 helicase unwinds triple-helical DNA structures. Biochemistry 2010; 49:6992–6999 [View Article] [PubMed]
    [Google Scholar]
  79. Zhang S, Grosse F. Nuclear DNA Helicase II Unwinds both DNA and RNA. Biochemistry 2002; 33:3906–3912 [View Article] [PubMed]
    [Google Scholar]
  80. Chakraborty P, Grosse F. Human DHX9 helicase preferentially unwinds RNA-containing displacement loops (R-loops) and G-quadruplexes. DNA Repair (Amst) 2011; 10:654–665 [View Article] [PubMed]
    [Google Scholar]
  81. Hartman TR, Qian S, Bolinger C, Fernandez S, Schoenberg DR et al. RNA helicase A is necessary for translation of selected messenger RNAs. Nat Struct Mol Biol 2006; 13:509–516 [View Article] [PubMed]
    [Google Scholar]
  82. Lee T, Pelletier J. The biology of DHX9 and its potential as a therapeutic target. Oncotarget 2016; 7:42716–42739 [View Article] [PubMed]
    [Google Scholar]
  83. Walstrom KM, Schmidt D, Bean CJ, Kelly WG. RNA helicase A is important for germline transcriptional control, proliferation, and meiosis in C. elegans. Mech Dev 2005; 122:707–720 [View Article] [PubMed]
    [Google Scholar]
  84. Huo L, Wang Y-N, Xia W, Hsu S-C, Lai C-C et al. RNA helicase A is A DNA-binding partner for EGFR-mediated transcriptional activation in the nucleus. Proc Natl Acad Sci U S A 2010; 107:16125–16130 [View Article] [PubMed]
    [Google Scholar]
  85. Nakajima T, Uchida C, Anderson SF, Lee C-G, Hurwitz J et al. RNA helicase A mediates association of CBP with RNA polymerase II. Cell 1997; 90:1107–1112 [View Article] [PubMed]
    [Google Scholar]
  86. Fullam A, Schröder M. DExD/H-box RNA helicases as mediators of anti-viral innate immunity and essential host factors for viral replication. Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms 2013; 1829:854–865 [View Article] [PubMed]
    [Google Scholar]
  87. Boeras I, Song Z, Moran A, Franklin J, Brown WC et al. DHX9/RHA Binding to the PBS-Segment of the Genomic RNA during HIV-1 Assembly Bolsters Virion Infectivity. J Mol Biol 2016; 428:2418–2429 [View Article] [PubMed]
    [Google Scholar]
  88. Brady S, Singh G, Bolinger C, Song Z, Boeras I et al. Virion-associated, host-derived DHX9/RNA helicase A enhances the processivity of HIV-1 reverse transcriptase on genomic RNA. J Biol Chem 2019; 294:11473–11485 [View Article] [PubMed]
    [Google Scholar]
  89. Fujii R, Okamoto M, Aratani S, Oishi T, Ohshima T et al. A Role of RNA Helicase A in cis-Acting Transactivation Response Element-mediated Transcriptional Regulation of Human Immunodeficiency Virus Type 1. J Biol Chem 2001; 276:5445–5451 [View Article] [PubMed]
    [Google Scholar]
  90. Zhang Z, Bao M, Lu N, Weng L, Yuan B et al. The E3 ubiquitin ligase TRIM21 negatively regulates the innate immune response to intracellular double-stranded DNA. Nat Immunol 2012; 14:172–178 [View Article] [PubMed]
    [Google Scholar]
  91. Ng YC, Chung W-C, Kang H-R, Cho H-J, Park E-B et al. A DNA-sensing-independent role of A nuclear RNA helicase, DHX9, in stimulation of NF-κB-mediated innate immunity against DNA virus infection. Nucleic Acids Res 2018; 46:9011–9026 [View Article] [PubMed]
    [Google Scholar]
  92. Agafonov DE, Deckert J, Wolf E, Odenwälder P, Bessonov S et al. Semiquantitative Proteomic Analysis of the Human Spliceosome via a Novel Two-Dimensional Gel Electrophoresis Method. Mol Cell Biol 2011; 31:2667–2682 [View Article] [PubMed]
    [Google Scholar]
  93. Irion U, Leptin M. Developmental and cell biological functions of the Drosophila DEAD-box protein abstrakt. Curr Biol 1999; 9:1373–1381 [View Article] [PubMed]
    [Google Scholar]
  94. Polprasert C, Schulze I, Sekeres MA, Makishima H, Przychodzen B et al. Inherited and Somatic Defects in DDX41 in Myeloid Neoplasms. Cancer Cell 2015; 27:658–670 [View Article] [PubMed]
    [Google Scholar]
  95. Liu J, Huang Y, Huang X, Li C, Ni S wei et al. Grouper DDX41 exerts antiviral activity against fish iridovirus and nodavirus infection. Fish & Shellfish Immunology 2019; 91:40–49 [View Article]
    [Google Scholar]
  96. Ma J, Li J, Fan D, Feng W, Lin A et al. Identification of DEAD-Box RNA Helicase DDX41 as a Trafficking Protein That Involves in Multiple Innate Immune Signaling Pathways in a Zebrafish Model. Front Immunol 2018; 9:1327 [View Article] [PubMed]
    [Google Scholar]
  97. Soponpong S, Amparyup P, Kawai T, Tassanakajon A. A Cytosolic Sensor, PmDDX41, Binds Double Stranded-DNA and Triggers the Activation of an Innate Antiviral Response in the Shrimp Penaeus monodon via the STING-Dependent Signaling Pathway. Front Immunol 2019; 10:2069 [View Article] [PubMed]
    [Google Scholar]
  98. Moriyama M, Koshiba T, Ichinohe T. Influenza A virus M2 protein triggers mitochondrial DNA-mediated antiviral immune responses. Nat Commun 2019; 10:4624 [View Article] [PubMed]
    [Google Scholar]
  99. Stavrou S, Blouch K, Kotla S, Bass A, Ross SR. Nucleic acid recognition orchestrates the anti-viral response to retroviruses. Cell Host Microbe 2015; 17:478–488 [View Article] [PubMed]
    [Google Scholar]
  100. Stavrou S, Aguilera AN, Blouch K, Ross SR. DDX41 Recognizes RNA/DNA Retroviral Reverse Transcripts and Is Critical for In Vivo Control of Murine Leukemia Virus Infection. mBio 2018; 9:e00923-18 [View Article] [PubMed]
    [Google Scholar]
  101. Lee K-G, Kim SS-Y, Kui L, Voon DC-C, Mauduit M et al. Bruton’s tyrosine kinase phosphorylates DDX41 and activates its binding of dsDNA and STING to initiate type 1 interferon response. Cell Rep 2015; 10:1055–1065 [View Article] [PubMed]
    [Google Scholar]
  102. Mitoma H, Hanabuchi S, Kim T, Bao M, Zhang Z et al. The DHX33 RNA helicase senses cytosolic RNA and activates the NLRP3 inflammasome. Immunity 2013; 39:123–135 [View Article] [PubMed]
    [Google Scholar]
  103. Duan Y, Zeng J, Fan S, Liao Y, Feng M et al. Herpes Simplex Virus Type 1-Encoded miR-H2-3p Manipulates Cytosolic DNA-Stimulated Antiviral Innate Immune Response by Targeting DDX41. Viruses 2019; 11:756 [View Article] [PubMed]
    [Google Scholar]
  104. 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 [View Article] [PubMed]
    [Google Scholar]
  105. Goubau D, van der Veen AG, Chakravarty P, Lin R, Rogers N et al. Mouse superkiller-2-like helicase DDX60 is dispensable for type I IFN induction and immunity to multiple viruses. Eur J Immunol 2015; 45:3386–3403 [View Article] [PubMed]
    [Google Scholar]
  106. Oshiumi H, Miyashita M, Okamoto M, Morioka Y, Okabe M et al. DDX60 Is Involved in RIG-I-Dependent and Independent Antiviral Responses, and Its Function Is Attenuated by Virus-Induced EGFR Activation. Cell Reports 2015; 11:1193–1207 [View Article] [PubMed]
    [Google Scholar]
  107. Dlakić M, Mushegian A. Prp8, the pivotal protein of the spliceosomal catalytic center, evolved from a retroelement-encoded reverse transcriptase. RNA 2011; 17:799–808 [View Article] [PubMed]
    [Google Scholar]
  108. Strauss EJ, Guthrie C. PRP28, a “DEAD-box” protein, is required for the first step of mRNA splicing in vitro. Nucleic Acids Res 1994; 22:3187–3193 [View Article] [PubMed]
    [Google Scholar]
  109. Ruan J, Cao Y, Ling T, Li P, Wu S et al. DDX23, an Evolutionary Conserved dsRNA Sensor, Participates in Innate Antiviral Responses by Pairing With TRIF or MAVS. Front Immunol 2019; 10:2202 [View Article] [PubMed]
    [Google Scholar]
  110. Yoshimoto R, Kataoka N, Okawa K, Ohno M. Isolation and characterization of post-splicing lariat-intron complexes. Nucleic Acids Res 2009; 37:891–902 [View Article] [PubMed]
    [Google Scholar]
  111. Inesta-Vaquera F, Chaugule VK, Galloway A, Chandler L, Rojas-Fernandez A et al. DHX15 regulates CMTR1-dependent gene expression and cell proliferation. Life Sci Alliance 2018; 1:e201800092 [View Article] [PubMed]
    [Google Scholar]
  112. Memet I, Doebele C, Sloan KE, Bohnsack MT. The G-patch protein NF-κB-repressing factor mediates the recruitment of the exonuclease XRN2 and activation of the RNA helicase DHX15 in human ribosome biogenesis. Nucleic Acids Res 2017; 45:5359–5374 [View Article] [PubMed]
    [Google Scholar]
  113. Lu H, Lu N, Weng L, Yuan B, Liu Y et al. DHX15 Senses Double-Stranded RNA in Myeloid Dendritic Cells. JI 2014; 193:1364–1372 [View Article] [PubMed]
    [Google Scholar]
  114. Mosallanejad K, Sekine Y, Ishikura-Kinoshita S, Kumagai K, Nagano T et al. The DEAH-Box RNA Helicase DHX15 Activates NF-κB and MAPK Signaling Downstream of MAVS During Antiviral Responses. Sci Signal 2014; 7:ra40 [View Article] [PubMed]
    [Google Scholar]
  115. Pattabhi S, Knoll ML, Gale M, Loo Y-M. DHX15 Is a Coreceptor for RLR Signaling That Promotes Antiviral Defense Against RNA Virus Infection. Journal of Interferon & Cytokine Research 2019; 39:331–346 [View Article] [PubMed]
    [Google Scholar]
  116. Xing J, Zhou X, Fang M, Zhang E, Minze LJ et al. DHX15 is required to control RNA virus-induced intestinal inflammation. Cell Rep 2021; 35:109205 [View Article] [PubMed]
    [Google Scholar]
  117. Mosallanejad K, Sekine Y, Ishikura-Kinoshita S, Kumagai K, Nagano T et al. The DEAH-Box RNA Helicase DHX15 Activates NF-κB and MAPK Signaling Downstream of MAVS During Antiviral Responses. Sci Signal 2014; 7: [View Article] [PubMed]
    [Google Scholar]
  118. Liu Y, Lu N, Yuan B, Weng L, Wang F et al. The interaction between the helicase DHX33 and IPS-1 as a novel pathway to sense double-stranded RNA and RNA viruses in myeloid dendritic cells. Cell Mol Immunol 2013; 11:49–57 [View Article] [PubMed]
    [Google Scholar]
  119. Zhang Z, Yuan B, Lu N, Facchinetti V, Liu Y-J. DHX9 Pairs with IPS-1 To Sense Double-Stranded RNA in Myeloid Dendritic Cells. JI 2011; 187:4501–4508 [View Article] [PubMed]
    [Google Scholar]
  120. Pisareva VP, Pisarev AV, Komar AA, Hellen CUT, Pestova TV. Translation initiation on mammalian mRNAs with structured 5’UTRs requires DExH-box protein DHX29. Cell 2008; 135:1237–1250 [View Article] [PubMed]
    [Google Scholar]
  121. Sweeney TR, Dhote V, Guca E, Hellen CUT, Hashem Y et al. Functional role and ribosomal position of the unique N-terminal region of DHX29, a factor required for initiation on structured mammalian mRNAs. Nucleic Acids Res 2021; 49:12955–12969 [View Article] [PubMed]
    [Google Scholar]
  122. 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 U S A 2014; 111:7747–7752 [View Article] [PubMed]
    [Google Scholar]
  123. Zhu Q, Tan P, Li Y, Lin M, Li C et al. DHX29 functions as an RNA co-sensor for MDA5-mediated EMCV-specific antiviral immunity. PLoS Pathog 2018; 14:e1006886 [View Article] [PubMed]
    [Google Scholar]
  124. Gencheva M, Kato M, Newo ANS, Lin R-J. Contribution of DEAH-box protein DHX16 in human pre-mRNA splicing. Biochemical Journal 2010; 429:25–32 [View Article] [PubMed]
    [Google Scholar]
  125. Kim SH, Lin RJ. Spliceosome activation by PRP2 ATPase prior to the first transesterification reaction of pre-mRNA splicing. Mol Cell Biol 1996; 16:6810–6819 [View Article] [PubMed]
    [Google Scholar]
  126. Hage A, Bharaj P, van Tol S, Giraldo MI, Gonzalez-Orozco M et al. The RNA helicase DHX16 recognizes specific viral RNA to trigger RIG-I-dependent innate antiviral immunity. Cell Reports 2022; 38:110434 [View Article] [PubMed]
    [Google Scholar]
  127. Rajsbaum R, Versteeg GA, Schmid S, Maestre AM, Belicha-Villanueva A et al. Unanchored K48-linked polyubiquitin synthesized by the E3-ubiquitin ligase TRIM6 stimulates the interferon-IKKε kinase-mediated antiviral response. Immunity 2014; 40:880–895 [View Article] [PubMed]
    [Google Scholar]
  128. Will CL, Urlaub H, Achsel T, Gentzel M, Wilm M et al. Characterization of novel SF3b and 17S U2 snRNP proteins, including a human Prp5p homologue and an SF3b DEAD-box protein. EMBO J 2002; 21:4978–4988 [View Article] [PubMed]
    [Google Scholar]
  129. Xu Y-Z, Newnham CM, Kameoka S, Huang T, Konarska MM et al. Prp5 bridges U1 and U2 snRNPs and enables stable U2 snRNP association with intron RNA. EMBO J 2004; 23:376–385 [View Article] [PubMed]
    [Google Scholar]
  130. Admoni-Elisha L, Nakdimon I, Shteinfer A, Prezma T, Arif T et al. Novel biomarker proteins in chronic lymphocytic leukemia: impact on diagnosis, prognosis and treatment. PLoS ONE 2016; 11:e0148500 [View Article] [PubMed]
    [Google Scholar]
  131. Li B, Li Y-M, He W-T, Chen H, Zhu H-W et al. Knockdown of DDX46 inhibits proliferation and induces apoptosis in esophageal squamous cell carcinoma cells. Oncol Rep 2016; 36:223–230 [View Article] [PubMed]
    [Google Scholar]
  132. Li M, Ma Y, Huang P, Du A, Yang X et al. Lentiviral DDX46 knockdown inhibits growth and induces apoptosis in human colorectal cancer cells. Gene 2015; 560:237–244 [View Article] [PubMed]
    [Google Scholar]
  133. Fleckner J, Zhang M, Valcárcel J, Green MR. U2AF65 recruits a novel human DEAD box protein required for the U2 snRNP-branchpoint interaction. Genes Dev 1997; 11:1864–1872 [View Article] [PubMed]
    [Google Scholar]
  134. Masuda T, Kuroda MJ, Harada S. Specific and Independent Recognition of U3 and U5 att Sites by Human Immunodeficiency Virus Type 1 Integrase In Vivo. J Virol 1998; 72:8396–8402 [View Article]
    [Google Scholar]
  135. Nakata D, Nakao S, Nakayama K, Araki S, Nakayama Y et al. The RNA helicase DDX39B and its paralog DDX39A regulate androgen receptor splice variant AR-V7 generation. Biochem Biophys Res Commun 2017; 483:271–276 [View Article] [PubMed]
    [Google Scholar]
  136. Pryor A, Tung L, Yang Z, Kapadia F, Chang T-H et al. Growth-regulated expression and G0-specific turnover of the mRNA that encodes URH49, a mammalian DExH/D box protein that is highly related to the mRNA export protein UAP56. Nucleic Acids Research 2004; 32:1857–1865 [View Article] [PubMed]
    [Google Scholar]
  137. Saleem I, Mirza S, Sarkar A, Raza M, Mohapatra B et al. The Mammalian Ecdysoneless Protein Interacts with RNA Helicase DDX39A To Regulate Nuclear mRNA Export. Mol Cell Biol 2021; 41:e0010321 [View Article] [PubMed]
    [Google Scholar]
  138. Shi P, Guo Y, Su Y, Zhu M, Fu Y et al. SUMOylation of DDX39A Alters Binding and Export of Antiviral Transcripts to Control Innate Immunity. J Immunol 2020; 205:168–180 [View Article] [PubMed]
    [Google Scholar]
  139. Zheng Q, Hou J, Zhou Y, Li Z, Cao X. The RNA helicase DDX46 inhibits innate immunity by entrapping m6A-demethylated antiviral transcripts in the nucleus. Nat Immunol 2017; 18:1094–1103 [View Article] [PubMed]
    [Google Scholar]
  140. Ma Z, Moore R, Xu X, Barber GN, Heise MT. DDX24 Negatively Regulates Cytosolic RNA-Mediated Innate Immune Signaling. PLoS Pathog 2013; 9:e1003721 [View Article] [PubMed]
    [Google Scholar]
  141. Balachandran S, Thomas E, Barber GN. A FADD-dependent innate immune mechanism in mammalian cells. Nature 2004; 432:401–405 [View Article] [PubMed]
    [Google Scholar]
  142. Kawai T, Takahashi K, Sato S, Coban C, Kumar H et al. IPS-1, an adaptor triggering RIG-I- and Mda5-mediated type I interferon induction. Nat Immunol 2005; 6:981–988 [View Article] [PubMed]
    [Google Scholar]
  143. Michallet M-C, Meylan E, Ermolaeva MA, Vazquez J, Rebsamen M et al. TRADD protein is an essential component of the RIG-like helicase antiviral pathway. Immunity 2008; 28:651–661 [View Article] [PubMed]
    [Google Scholar]
  144. Jalal C, Uhlmann-Schiffler H, Stahl H. Redundant role of DEAD box proteins p68 (Ddx5) and p72/p82 (Ddx17) in ribosome biogenesis and cell proliferation. Nucleic Acids Res 2007; 35:3590–3601 [View Article] [PubMed]
    [Google Scholar]
  145. Liu Z-R. p68 RNA helicase is an essential human splicing factor that acts at the U1 snRNA-5’ splice site duplex. Mol Cell Biol 2002; 22:5443–5450 [View Article] [PubMed]
    [Google Scholar]
  146. Wilson BJ, Bates GJ, Nicol SM, Gregory DJ, Perkins ND et al. The p68 and p72 DEAD box RNA helicases interact with HDAC1 and repress transcription in a promoter-specific manner. BMC Mol Biol 2004; 5:11 [View Article] [PubMed]
    [Google Scholar]
  147. Zonta E, Bittencourt D, Samaan S, Germann S, Dutertre M et al. The RNA helicase DDX5/p68 is a key factor promoting c-fos expression at different levels from transcription to mRNA export. Nucleic Acids Research 2013; 41:554–564 [View Article] [PubMed]
    [Google Scholar]
  148. Chen J-Y, Chen W-N, Poon K-MV, Zheng B-J, Lin X et al. Interaction between SARS-CoV helicase and a multifunctional cellular protein (Ddx5) revealed by yeast and mammalian cell two-hybrid systems. Arch Virol 2009; 154:507–512 [View Article] [PubMed]
    [Google Scholar]
  149. Sithole N, Williams CA, Abbink TEM, Lever AML. DDX5 potentiates HIV-1 transcription as a co-factor of Tat. Retrovirology 2020; 17:6 [View Article] [PubMed]
    [Google Scholar]
  150. Zhou X, Luo J, Mills L, Wu S, Pan T et al. DDX5 Facilitates HIV-1 Replication as a Cellular Co-Factor of Rev. PLoS ONE 2013; 8:e65040 [View Article] [PubMed]
    [Google Scholar]
  151. Bortz E, Westera L, Maamary J, Steel J, Albrecht RA et al. Host- and strain-specific regulation of influenza virus polymerase activity by interacting cellular proteins. mBio 2011; 2:e00151-11 [View Article] [PubMed]
    [Google Scholar]
  152. Li C, Ge L, Li P, Wang Y, Sun M et al. The DEAD-box RNA helicase DDX5 acts as a positive regulator of Japanese encephalitis virus replication by binding to viral 3’ UTR. Antiviral Res 2013; 100:487–499 [View Article] [PubMed]
    [Google Scholar]
  153. Goh P-Y, Tan Y-J, Lim SP, Tan YH, Lim SG et al. Cellular RNA helicase p68 relocalization and interaction with the hepatitis C virus (HCV) NS5B protein and the potential role of p68 in HCV RNA replication. J Virol 2004; 78:5288–5298 [View Article] [PubMed]
    [Google Scholar]
  154. Xu J, Cai Y, Ma Z, Jiang B, Liu W et al. The RNA helicase DDX5 promotes viral infection via regulating N6-methyladenosine levels on the DHX58 and NFκB transcripts to dampen antiviral innate immunity. PLoS Pathog 2021; 17:e1009530 [View Article] [PubMed]
    [Google Scholar]
  155. Zan J, Xu R, Tang X, Lu M, Xie S et al. RNA helicase DDX5 suppresses IFN-I antiviral innate immune response by interacting with PP2A-Cβ to deactivate IRF3. Experimental Cell Research 2020; 396:112332 [View Article] [PubMed]
    [Google Scholar]
  156. Long L, Deng Y, Yao F, Guan D, Feng Y et al. Recruitment of Phosphatase PP2A by RACK1 Adaptor Protein Deactivates Transcription Factor IRF3 and Limits Type I Interferon Signaling. Immunity 2014; 40:515–529 [View Article] [PubMed]
    [Google Scholar]
  157. Peng D, Wang Z, Huang A, Zhao Y, Qin FX-F. A Novel Function of F-Box Protein FBXO17 in Negative Regulation of Type I IFN Signaling by Recruiting PP2A for IFN Regulatory Factor 3 Deactivation. JI 2017; 198:808–819 [View Article] [PubMed]
    [Google Scholar]
  158. Zaccara S, Jaffrey SR. A Unified Model for the Function of YTHDF Proteins in Regulating m6A-Modified mRNA. Cell 2020; 181:1582–1595 [View Article] [PubMed]
    [Google Scholar]
  159. Feng T, Sun T, Li G, Pan W, Wang K et al. DEAD-Box Helicase DDX25 Is a Negative Regulator of Type I Interferon Pathway and Facilitates RNA Virus Infection. Front Cell Infect Microbiol 2017; 7:356 [View Article] [PubMed]
    [Google Scholar]
  160. Zhang K, Zhang Y, Xue J, Meng Q, Liu H et al. DDX19 Inhibits Type I Interferon Production by Disrupting TBK1-IKKε-IRF3 Interactions and Promoting TBK1 and IKKε Degradation. Cell Reports 2019; 26:1258–1272 [View Article] [PubMed]
    [Google Scholar]
  161. Jones EL, Laidlaw SM, Dustin LB. TRIM21/Ro52 - Roles in Innate Immunity and Autoimmune Disease. Front Immunol 2021; 12:3538 [View Article] [PubMed]
    [Google Scholar]
  162. Kurata R, Tajima A, Yonezawa T, Inoko H. TRIM39R, but not TRIM39B, regulates type I interferon response. Biochemical and Biophysical Research Communications 2013; 436:90–95 [View Article] [PubMed]
    [Google Scholar]
  163. Schoggins JW, Wilson SJ, Panis M, Murphy MY, Jones CT et al. A diverse range of gene products are effectors of the type I interferon antiviral response. Nature 2011; 472:481–485 [View Article] [PubMed]
    [Google Scholar]
  164. Grünvogel O, Esser-Nobis K, Reustle A, Schult P, Müller B et al. DDX60L Is an Interferon-Stimulated Gene Product Restricting Hepatitis C Virus Replication in Cell Culture. J Virol 2015; 89:10548–10568 [View Article] [PubMed]
    [Google Scholar]
  165. Moy RH, Cole BS, Yasunaga A, Gold B, Shankarling G et al. Stem-Loop Recognition by DDX17 Facilitates miRNA Processing and Antiviral Defense. Cell 2014; 158:764–777 [View Article] [PubMed]
    [Google Scholar]
  166. Taschuk F, Tapescu I, Moy RH, Cherry S. DDX56 Binds to Chikungunya Virus RNA To Control Infection. mBio 2020; 11:e02623-20 [View Article] [PubMed]
    [Google Scholar]
  167. Lamm GM, Nicol SM, Fuller-Pace FV, Lamond AI. p72: a human nuclear DEAD box protein highly related to p68. Nucleic Acids Res 1996; 24:3739–3747 [View Article] [PubMed]
    [Google Scholar]
  168. Ogilvie VC, Wilson BJ, Nicol SM, Morrice NA, Saunders LR et al. The highly related DEAD box RNA helicases p68 and p72 exist as heterodimers in cells. Nucleic Acids Res 2003; 31:1470–1480 [View Article] [PubMed]
    [Google Scholar]
  169. Björk P, Wieslander L. Mechanisms of mRNA export. Semin Cell Dev Biol 2014; 32:47–54 [View Article] [PubMed]
    [Google Scholar]
  170. Geißler V, Altmeyer S, Stein B, Uhlmann-Schiffler H, Stahl H. The RNA helicase Ddx5/p68 binds to hUpf3 and enhances NMD of Ddx17/p72 and Smg5 mRNA. Nucleic Acids Research 2013; 41:7875–7888 [View Article] [PubMed]
    [Google Scholar]
  171. Zhou Z, Licklider LJ, Gygi SP, Reed R. Comprehensive proteomic analysis of the human spliceosome. Nature 2002; 419:182–185 [View Article] [PubMed]
    [Google Scholar]
  172. Lorgeoux R-P, Pan Q, Le Duff Y, Liang C. DDX17 promotes the production of infectious HIV-1 particles through modulating viral RNA packaging and translation frameshift. Virology 2013; 443:384–392 [View Article] [PubMed]
    [Google Scholar]
  173. Sithole N, Williams CA, Vaughan AM, Kenyon JC, Lever AML. DDX17 Specifically, and Independently of DDX5, Controls Use of the HIV A4/5 Splice Acceptor Cluster and Is Essential for Efficient Replication of HIV. Journal of Molecular Biology 2018; 430:3111–3128 [View Article] [PubMed]
    [Google Scholar]
  174. Sabin LR, Zheng Q, Thekkat P, Yang J, Hannon GJ et al. Dicer-2 Processes Diverse Viral RNA Species. PLoS ONE 2013; 8:e55458 [View Article] [PubMed]
    [Google Scholar]
  175. 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 [View Article] [PubMed]
    [Google Scholar]
  176. Bick MJ, Carroll J-WN, Gao G, Goff SP, Rice CM et al. Expression of the Zinc-Finger Antiviral Protein Inhibits Alphavirus Replication. J Virol 2003; 77:11555–11562 [View Article] [PubMed]
    [Google Scholar]
  177. Xuan Y, Gong D, Qi J, Han C, Deng H et al. ZAP Inhibits Murine Gammaherpesvirus 68 ORF64 Expression and Is Antagonized by RTA. J Virol 2013; 87:2735–2743 [View Article] [PubMed]
    [Google Scholar]
  178. Zhu Y, Chen G, Lv F, Wang X, Ji X et al. Zinc-finger antiviral protein inhibits HIV-1 infection by selectively targeting multiply spliced viral mRNAs for degradation. Proc Natl Acad Sci USA 2011; 108:15834–15839 [View Article] [PubMed]
    [Google Scholar]
  179. 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 [View Article] [PubMed]
    [Google Scholar]
  180. Moudry P, Chroma K, Bursac S, Volarevic S, Bartek J. RNA-interference screen for p53 regulators unveils a role of WDR75 in ribosome biogenesis. Cell Death Differ 2021; 29:687–696 [View Article] [PubMed]
    [Google Scholar]
  181. Wang J, Liu J, Ye M, Liu F, Wu S et al. Ddx56 maintains proliferation of mouse embryonic stem cells via ribosome assembly and interaction with the Oct4/Sox2 complex. Stem Cell Res Ther 2020; 11:314 [View Article] [PubMed]
    [Google Scholar]
  182. Reid CR, Hobman TC. The nucleolar helicase DDX56 redistributes to West Nile virus assembly sites. Virology 2017; 500:169–177 [View Article] [PubMed]
    [Google Scholar]
  183. Xu Z, Anderson R, Hobman TC. The Capsid-Binding Nucleolar Helicase DDX56 Is Important for Infectivity of West Nile Virus. J Virol 2011; 85:5571–5580 [View Article] [PubMed]
    [Google Scholar]
  184. Fu S-Z, Yang W-P, Ru Y, Zhang K-S, Wang Y et al. DDX56 cooperates with FMDV 3A to enhance FMDV replication by inhibiting the phosphorylation of IRF3. Cell Signal 2019; 64:109393 [View Article] [PubMed]
    [Google Scholar]
  185. Pirinçal A, Turan K. Human DDX56 protein interacts with influenza A virus NS1 protein and stimulates the virus replication. Genet Mol Biol 2021; 44:e20200158 [View Article]
    [Google Scholar]
  186. Treffers EE, Tas A, Scholte FEM, Van MN, Heemskerk MT et al. Temporal SILAC-based quantitative proteomics identifies host factors involved in chikungunya virus replication. Proteomics 2015; 15:2267–2280 [View Article] [PubMed]
    [Google Scholar]
  187. Li D, Fu S, Wu Z, Yang W, Ru Y et al. DDX56 inhibits type I interferon by disrupting assembly of IRF3-IPO5 to inhibit IRF3 nucleus import. J Cell Sci 2019; 133:jcs230409 [View Article] [PubMed]
    [Google Scholar]
  188. Uhlmann-Schiffler H, Jalal C, Stahl H. Ddx42p--a human DEAD box protein with RNA chaperone activities. Nucleic Acids Research 2006; 34:10–22 [View Article] [PubMed]
    [Google Scholar]
  189. Zyner KG, Mulhearn DS, Adhikari S, Martínez Cuesta S, Di Antonio M et al. Genetic interactions of G-quadruplexes in humans. eLife 2019; 8:e46793 [View Article] [PubMed]
    [Google Scholar]
  190. Bonaventure B, Rebendenne A, de Gracia FG, McKellar J, Gracias S et al. The DEAD box RNA helicase DDX42 is an intrinsic inhibitor of positive-strand RNA viruses. Microbiology 2020 [View Article]
    [Google Scholar]
  191. Yoneyama M, Kikuchi M, Matsumoto K, Imaizumi T, Miyagishi M et al. Shared and unique functions of the DExD/H-box helicases RIG-I, MDA5, and LGP2 in antiviral innate immunity. J Immunol 2005; 175:2851–2858 [View Article] [PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/jgv.0.001766
Loading
/content/journal/jgv/10.1099/jgv.0.001766
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error