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Annual Review of Biochemistry

Volume 93, 2024

The Story of RNA Unfolded: The Molecular Function of DEAD- and DExH-Box ATPases and Their Complex Relationship with Membraneless Organelles

Abstract

DEAD- and DExH-box ATPases (DDX/DHXs) are abundant and highly conserved cellular enzymes ubiquitously involved in RNA processing. By remodeling RNA–RNA and RNA–protein interactions, they often function as gatekeepers that control the progression of diverse RNA maturation steps. Intriguingly, most DDX/DHXs localize to membraneless organelles (MLOs) such as nucleoli, nuclear speckles, stress granules, or processing bodies. Recent findings suggest not only that localization to MLOs can promote interaction between DDX/DHXs and their targets but also that DDX/DHXs are key regulators of MLO formation and turnover through their condensation and ATPase activity.

In this review, we describe the molecular function of DDX/DHXs in ribosome biogenesis, messenger RNA splicing, export, translation, and storage or decay as well as their association with prominent MLOs. We discuss how the enzymatic function of DDX/DHXs in RNA processing is linked to DDX/DHX condensation, the accumulation of ribonucleoprotein particles and MLO dynamics. Future research will reveal how these processes orchestrate the RNA life cycle in MLO space and DDX/DHX time.

Keyword(s): DEAD-box ATPases, DExH-box ATPases, membraneless organelles, ribonucleoprotein complexes, RNA processing, RNPs
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/content/journals/10.1146/annurev-biochem-052521-121259
2024-08-02
2025-04-21
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Literature Cited

  1. 1.
    Linder P, Jankowsky E. 2011.. From unwinding to clamping—the DEAD box RNA helicase family. . Nat. Rev. Mol. Cell Biol. 12:(8):505–16
     [Crossref] [Google Scholar]
  2. 2.
    Gilman B, Tijerina P, Russell R. 2017.. Distinct RNA-unwinding mechanisms of DEAD-box and DEAH-box RNA helicase proteins in remodeling structured RNAs and RNPs. . Biochem. Soc. Trans. 45:(6):1313–21
     [Crossref] [Google Scholar]
  3. 3.
    Jarmoskaite I, Russell R. 2014.. RNA helicase proteins as chaperones and remodelers. . Annu. Rev. Biochem. 83::697–725
     [Crossref] [Google Scholar]
  4. 4.
    Weis K, Hondele M. 2022.. The role of DEAD-box ATPases in gene expression and the regulation of RNA–protein condensates. . Annu. Rev. Biochem. 91::197–219
     [Crossref] [Google Scholar]
  5. 5.
    Ozgur S, Gretel B, Falk S, Chakrabarti S, Prabu JR, Conti E. 2015.. The conformational plasticity of eukaryotic RNA-dependent ATPases. . FEBS J. 282:(5):850–63
     [Crossref] [Google Scholar]
  6. 6.
    Hamann F, Enders M, Ficner R. 2019.. Structural basis for RNA translocation by DEAH-box ATPases. . Nucleic Acids Res. 47:(8):4349–62
     [Crossref] [Google Scholar]
  7. 7.
    Bohnsack KE, Ficner R, Bohnsack MT, Jonas S. 2021.. Regulation of DEAH-box RNA helicases by G-patch proteins. . Biol. Chem. 402:(5):561–79
     [Crossref] [Google Scholar]
  8. 8.
    Weis K. 2021.. Dead or alive: DEAD-box ATPases as regulators of ribonucleoprotein complex condensation. . Biol. Chem. 402:(5):653–61
     [Crossref] [Google Scholar]
  9. 9.
    Tauber D, Tauber G, Parker R. 2020.. Mechanisms and regulation of RNA condensation in RNP granule formation. . Trends Biochem. Sci. 45:(9):764–78
     [Crossref] [Google Scholar]
  10. 10.
    Overwijn D, Hondele M. 2023.. DEAD-box ATPases as regulators of biomolecular condensates and membrane-less organelles. . Trends Biochem. Sci. 48:(3):244–58
     [Crossref] [Google Scholar]
  11. 11.
    Shin Y, Brangwynne CP. 2017.. Liquid phase condensation in cell physiology and disease. . Science 357:(6357):eaaf4382
     [Crossref] [Google Scholar]
  12. 12.
    Putnam A, Thomas L, Seydoux G. 2023.. RNA granules: functional compartments or incidental condensates?. Genes Dev. 37:(17–18):354–76
     [Crossref] [Google Scholar]
  13. 13.
    Montpetit B, Thomsen ND, Helmke KJ, Seeliger MA, Berger JM, Weis K. 2011.. A conserved mechanism of DEAD-box ATPase activation by nucleoporins and InsP6 in mRNA export. . Nature 472:(7342):238–42
     [Crossref] [Google Scholar]
  14. 14.
    Dörner K, Ruggeri C, Zemp I, Kutay U. 2023.. Ribosome biogenesis factors—from names to functions. . EMBO J. 42:(7):e112699
     [Crossref] [Google Scholar]
  15. 15.
    Klinge S, Woolford JL. 2019.. Ribosome assembly coming into focus. . Nat. Rev. Mol. Cell Biol. 20:(2):116–31
     [Crossref] [Google Scholar]
  16. 16.
    Shan L, Xu G, Yao R-W, Luan P-F, Huang Y, et al. 2023.. Nucleolar URB1 ensures 3′ ETS rRNA removal to prevent exosome surveillance. . Nature 615:(7952):526–34
     [Crossref] [Google Scholar]
  17. 17.
    Stenström L, Mahdessian D, Gnann C, Cesnik AJ, Ouyang W, et al. 2020.. Mapping the nucleolar proteome reveals a spatiotemporal organization related to intrinsic protein disorder. . Mol. Syst. Biol. 16:(8):e9469
     [Crossref] [Google Scholar]
  18. 18.
    Lin S, Rajan S, Lemberg S, Altawil M, Anderson K, et al. 2022.. Production of nascent ribosome precursors within the nucleolar microenvironment of Saccharomyces cerevisiae. . Genetics 221:(3):iyac070
     [Crossref] [Google Scholar]
  19. 19.
    Tartakoff AM, Chen L, Raghavachari S, Gitiforooz D, Dhinakaran A, et al. 2021.. The nucleolus as a polarized coaxial cable in which the rDNA axis is surrounded by dynamic subunit-specific phases. . Curr. Biol. 31:(12):2507–19.e4
     [Crossref] [Google Scholar]
  20. 20.
    Lafontaine DLJ, Riback JA, Bascetin R, Brangwynne CP. 2021.. The nucleolus as a multiphase liquid condensate. . Nat. Rev. Mol. Cell Biol. 22:(3):165–82
     [Crossref] [Google Scholar]
  21. 21.
    Feric M, Misteli T. 2022.. Function moves biomolecular condensates in phase space. . BioEssays 44:(5):2200001
     [Crossref] [Google Scholar]
  22. 22.
    Yao R-W, Xu G, Wang Y, Shan L, Luan P-F, et al. 2019.. Nascent pre-rRNA sorting via phase separation drives the assembly of dense fibrillar components in the human nucleolus. . Mol. Cell 76:(5):767–83.e11
     [Crossref] [Google Scholar]
  23. 23.
    Brangwynne CP, Mitchison TJ, Hyman AA. 2011.. Active liquid-like behavior of nucleoli determines their size and shape in Xenopus laevis oocytes. . PNAS 108:(11):4334–39
     [Crossref] [Google Scholar]
  24. 24.
    Riback JA, Eeftens JM, Lee DSW, Quinodoz SA, Beckers L, et al. 2022.. Viscoelastic RNA entanglement and advective flow underlie nucleolar form and function. . bioRxiv 2021.12.31.474660. https://doi.org/10.1101/2021.12.31.474660
  25. 25.
    LaPeruta AJ, Micic J, Woolford JL Jr. 2022.. Additional principles that govern the release of pre-ribosomes from the nucleolus into the nucleoplasm in yeast. . Nucleic Acids Res. 2022::gkac430
     [Google Scholar]
  26. 26.
    Tartakoff A, DiMario P, Hurt E, McStay B, Panse VG, Tollervey D. 2022.. The dual nature of the nucleolus. . Genes Dev. 36:(13–14):765–69
     [Crossref] [Google Scholar]
  27. 27.
    Mitterer V, Pertschy B. 2022.. RNA folding and functions of RNA helicases in ribosome biogenesis. . RNA Biol. 19:(1):781–810
     [Crossref] [Google Scholar]
  28. 28.
    Martin R, Straub AU, Doebele C, Bohnsack MT. 2013.. DExD/H-box RNA helicases in ribosome biogenesis. . RNA Biol. 10:(1):4–18
     [Crossref] [Google Scholar]
  29. 29.
    Boneberg FM, Brandmann T, Kobel L, van den Heuvel J, Bargsten K, et al. 2019.. Molecular mechanism of the RNA helicase DHX37 and its activation by UTP14A in ribosome biogenesis. . RNA 25:(6):685–701
     [Crossref] [Google Scholar]
  30. 30.
    Choudhury P, Hackert P, Memet I, Sloan KE, Bohnsack MT. 2019.. The human RNA helicase DHX37 is required for release of the U3 snoRNP from pre-ribosomal particles. . RNA Biol. 16:(1):54–68
     [Crossref] [Google Scholar]
  31. 31.
    Jaafar M, Contreras J, Dominique C, Martín-Villanueva S, Capeyrou R, et al. 2021.. Association of snR190 snoRNA chaperone with early pre-60S particles is regulated by the RNA helicase Dbp7 in yeast. . Nat. Commun. 12:(1):6153
     [Crossref] [Google Scholar]
  32. 32.
    Aquino GRR, Hackert P, Krogh N, Pan K-T, Jaafar M, et al. 2021.. The RNA helicase Dbp7 promotes domain V/VI compaction and stabilization of inter-domain interactions during early 60S assembly. . Nat. Commun. 12:(1):6152
     [Crossref] [Google Scholar]
  33. 33.
    Brüning L, Hackert P, Martin R, Gallesio JD, Aquino GRR, et al. 2018.. RNA helicases mediate structural transitions and compositional changes in pre-ribosomal complexes. . Nat. Commun. 9:(1):5383
     [Crossref] [Google Scholar]
  34. 34.
    Cheng J, Lau B, Venuta GL, Ameismeier M, Berninghausen O, et al. 2020.. 90S pre-ribosome transformation into the primordial 40S subunit. . Science 369:(6510):1470–76
     [Crossref] [Google Scholar]
  35. 35.
    Sailer C, Jansen J, Sekulski K, Cruz VE, Erzberger JP, Stengel F. 2022.. A comprehensive landscape of 60S ribosome biogenesis factors. . Cell Rep. 38:(6):110353
     [Crossref] [Google Scholar]
  36. 36.
    Manikas R-G, Thomson E, Thoms M, Hurt E. 2016.. The K+-dependent GTPase Nug1 is implicated in the association of the helicase Dbp10 to the immature peptidyl transferase centre during ribosome maturation. . Nucleic Acids Res. 44:(4):1800–12
     [Crossref] [Google Scholar]
  37. 37.
    Lau B, Huang Z, Kellner N, Niu S, Berninghausen O, et al. 2023.. Mechanism of 5S RNP recruitment and helicase-surveilled rRNA maturation during pre-60S biogenesis. . EMBO Rep. 24::e56910
     [Crossref] [Google Scholar]
  38. 38.
    Cruz VE, Sekulski K, Peddada N, Sailer C, Balasubramanian S, et al. 2022.. Sequence-specific remodeling of a topologically complex RNP substrate by Spb4. . Nat. Struct. Mol. Biol. 29:(12):1228–38
     [Crossref] [Google Scholar]
  39. 39.
    Broeck AV, Klinge S. 2023.. Principles of human pre-60S biogenesis. . Science 381:(6653):eadh3892
     [Crossref] [Google Scholar]
  40. 40.
    Choudhury P, Kretschmer J, Hackert P, Bohnsack KE, Bohnsack MT. 2021.. The DExD box ATPase DDX55 is recruited to domain IV of the 28S ribosomal RNA by its C-terminal region. . RNA Biol. 18:(8):1124–35
     [Crossref] [Google Scholar]
  41. 41.
    Hondele M, Sachdev R, Heinrich S, Wang J, Vallotton P, et al. 2019.. DEAD-box ATPases are global regulators of phase-separated organelles. . Nature 573:(7772):144–48
     [Crossref] [Google Scholar]
  42. 42.
    Gao H, Wei H, Yang Y, Li H, Liang J, et al. 2023.. Phase separation of DDX21 promotes colorectal cancer metastasis via MCM5-dependent EMT pathway. . Oncogene 42:(21):1704–15
     [Crossref] [Google Scholar]
  43. 43.
    Harel I, Chen YR, Ziv I, Singh PP, Negredo PN, et al. 2022.. Identification of protein aggregates in the aging vertebrate brain with prion-like and phase separation properties. . bioRxiv 2022.02.26.482115. https://doi.org/10.1101/2022.02.26.482115
  44. 44.
    Jalal C, Uhlmann-Schiffler H, Stahl H. 2007.. Redundant role of DEAD box proteins p68 (Ddx5) and p72/p82 (Ddx17) in ribosome biogenesis and cell proliferation. . Nucleic Acids Res. 35:(11):3590–601
     [Crossref] [Google Scholar]
  45. 45.
    Srivastava L, Lapik YR, Wang M, Pestov DG. 2010.. Mammalian DEAD box protein Ddx51 acts in 3′ end maturation of 28S rRNA by promoting the release of U8 snoRNA. . Mol. Cell. Biol. 30:(12):2947–56
     [Crossref] [Google Scholar]
  46. 46.
    Wu M, Xu G, Han C, Luan P-F, Xing Y-H, et al. 2021.. lncRNA SLERT controls phase separation of FC/DFCs to facilitate Pol I transcription. . Cell 373:(6554):547–55
     [Google Scholar]
  47. 47.
    Calo E, Flynn RA, Martin L, Spitale RC, Chang HY, Wysocka J. 2015.. RNA helicase DDX21 coordinates transcription and ribosomal RNA processing. . Nature 518:(7538):249–53
     [Crossref] [Google Scholar]
  48. 48.
    Song C, Hotz-Wagenblatt A, Voit R, Grummt I. 2017.. SIRT7 and the DEAD-box helicase DDX21 cooperate to resolve genomic R loops and safeguard genome stability. . Genes Dev. 31:(13):1370–81
     [Crossref] [Google Scholar]
  49. 49.
    Sloan KE, Leisegang MS, Doebele C, Ramírez AS, Simm S, et al. 2015.. The association of late-acting snoRNPs with human pre-ribosomal complexes requires the RNA helicase DDX21. . Nucleic Acids Res. 43:(1):553–64
     [Crossref] [Google Scholar]
  50. 50.
    Koltowska K, Okuda KS, Gloger M, Rondon-Galeano M, Mason E, et al. 2021.. The RNA helicase Ddx21 controls Vegfc-driven developmental lymphangiogenesis by balancing endothelial cell ribosome biogenesis and p53 function. . Nat. Cell Biol. 23:(11):1136–47
     [Crossref] [Google Scholar]
  51. 51.
    Xing Y-H, Yao R-W, Zhang Y, Guo C-J, Jiang S, et al. 2017.. SLERT regulates DDX21 rings associated with Pol I transcription. . Cell 169:(4):664–78.e16
     [Crossref] [Google Scholar]
  52. 52.
    Kim D-S, Camacho CV, Nagari A, Malladi VS, Challa S, Kraus WL. 2019.. Activation of PARP-1 by snoRNAs controls ribosome biogenesis and cell growth via the RNA helicase DDX21. . Mol. Cell 75:(6):1270–85.e14
     [Crossref] [Google Scholar]
  53. 53.
    Miao W, Porter DF, Lopez-Pajares V, Siprashvili Z, Meyers RM, et al. 2023.. Glucose dissociates DDX21 dimers to regulate mRNA splicing and tissue differentiation. . Cell 186:(1):80–97.e26
     [Crossref] [Google Scholar]
  54. 54.
    Hatos A, Tosatto SCE, Vendruscolo M, Fuxreiter M. 2022.. FuzDrop on AlphaFold: visualizing the sequence-dependent propensity of liquid–liquid phase separation and aggregation of proteins. . Nucleic Acids Res. 50:(W1):W337–44
     [Crossref] [Google Scholar]
  55. 55.
    Spector DL, Lamond AI. 2011.. Nuclear speckles. . Cold Spring Harb. Perspect. Biol. 3:(2):a000646
     [Crossref] [Google Scholar]
  56. 56.
    Ilik İA, Malszycki M, Lübke AK, Schade C, Meierhofer D, Aktaş T. 2020.. SON and SRRM2 are essential for nuclear speckle formation. . eLife 9::e60579
     [Crossref] [Google Scholar]
  57. 57.
    Saitoh N, Spahr CS, Patterson SD, Bubulya P, Neuwald AF, Spector DL. 2004.. Proteomic analysis of interchromatin granule clusters. . Mol. Biol. Cell. 15:(8):3876–90
     [Crossref] [Google Scholar]
  58. 58.
    Dopie J, Sweredoski MJ, Moradian A, Belmont AS. 2020.. Tyramide signal amplification mass spectrometry (TSA-MS) ratio identifies nuclear speckle proteins. . J. Cell Biol. 219:(9):e201910207
     [Crossref] [Google Scholar]
  59. 59.
    Campalans A, Amouroux R, Bravard A, Epe B, Radicella JP. 2006.. UVA irradiation induces relocalisation of the DNA repair protein hOGG1 to nuclear speckles. . J. Cell Sci. 120:(1):23–32
     [Crossref] [Google Scholar]
  60. 60.
    Wong A, Zhang S, Mordue D, Wu JM, Zhang Z, et al. 2013.. PDIP38 is translocated to the spliceosomes/nuclear speckles in response to UV-induced DNA damage and is required for UV-induced alternative splicing of MDM2. . Cell Cycle 12:(19):3373–82
     [Crossref] [Google Scholar]
  61. 61.
    Tripathi V, Ellis JD, Shen Z, Song DY, Pan Q, et al. 2010.. The nuclear-retained noncoding RNA MALAT1 regulates alternative splicing by modulating SR splicing factor phosphorylation. . Mol. Cell. 39:(6):925–38
     [Crossref] [Google Scholar]
  62. 62.
    Galganski L, Urbanek MO, Krzyzosiak WJ. 2017.. Nuclear speckles: molecular organization, biological function and role in disease. . Nucleic Acids Res. 45:(18):10350–68
     [Crossref] [Google Scholar]
  63. 63.
    Ilık İA, Aktaş T. 2022.. Nuclear speckles: dynamic hubs of gene expression regulation. . FEBS J. 289:(22):7234–45
     [Crossref] [Google Scholar]
  64. 64.
    Faber GP, Nadav-Eliyahu S, Shav-Tal Y. 2022.. Nuclear speckles—a driving force in gene expression. . J. Cell Sci. 135:(13):jcs259594
     [Crossref] [Google Scholar]
  65. 65.
    Chen Y, Zhang Y, Wang Y, Zhang L, Brinkman EK, et al. 2018.. Mapping 3D genome organization relative to nuclear compartments using TSA-Seq as a cytological ruler. . J. Cell Biol. 217:(11):4025–48
     [Crossref] [Google Scholar]
  66. 66.
    Ding F, Elowitz MB. 2019.. Constitutive splicing and economies of scale in gene expression. . Nat. Struct. Mol. Biol. 26:(6):424–32
     [Crossref] [Google Scholar]
  67. 67.
    Gordon JM, Phizicky DV, Neugebauer KM. 2021.. Nuclear mechanisms of gene expression control: pre-mRNA splicing as a life or death decision. . Curr. Opin. Genet. Dev. 67::67–76
     [Crossref] [Google Scholar]
  68. 68.
    Wilkinson ME, Charenton C, Nagai K. 2020.. RNA splicing by the spliceosome. . Annu. Rev. Biochem. 89::359–88
     [Crossref] [Google Scholar]
  69. 69.
    Plaschka C, Newman AJ, Nagai K. 2019.. Structural basis of nuclear pre-mRNA splicing: lessons from yeast. . Cold Spring Harb. Perspect. Biol. 11:(5):a032391
     [Crossref] [Google Scholar]
  70. 70.
    Kistler AL, Guthrie C. 2001.. Deletion of MUD2, the yeast homolog of U2AF65, can bypass the requirement for Sub2, an essential spliceosomal ATPase. . Genes Dev. 15:(1):42–49
     [Crossref] [Google Scholar]
  71. 71.
    Rodgers ML, Tretbar US, Dehaven A, Alwan AA, Luo G, et al. 2016.. Conformational dynamics of stem II of the U2 snRNA. . RNA 22:(2):225–36
     [Crossref] [Google Scholar]
  72. 72.
    Zhang Z, Will CL, Bertram K, Dybkov O, Hartmuth K, et al. 2020.. Molecular architecture of the human 17S U2 snRNP. . Nature 583:(7815):310–13
     [Crossref] [Google Scholar]
  73. 73.
    Xu Y-Z, Query CC. 2007.. Competition between the ATPase Prp5 and branch region-U2 snRNA pairing modulates the fidelity of spliceosome assembly. . Mol. Cell 28:(5):838–49
     [Crossref] [Google Scholar]
  74. 74.
    Zhang X, Zhan X, Bian T, Yang F, Li P, et al. 2022.. Structural insights into branch site proofreading by human spliceosome. . bioRxiv 2022.11.07.515429. https://doi.org/10.1101/2022.11.07.515429
  75. 75.
    Zhang Z, Rigo N, Dybkov O, Fourmann J-B, Will CL, et al. 2021.. Structural insights into how Prp5 proofreads the pre-mRNA branch site. . Nature 596:(7871):296–300
     [Crossref] [Google Scholar]
  76. 76.
    Staley JP, Guthrie C. 1999.. An RNA switch at the 5′ splice site requires ATP and the DEAD box protein Prp28p. . Mol. Cell 3:(1):55–64
     [Crossref] [Google Scholar]
  77. 77.
    Plaschka C, Lin P-C, Charenton C, Nagai K. 2018.. Prespliceosome structure provides insights into spliceosome assembly and regulation. . Nature 559:(7714):419–22
     [Crossref] [Google Scholar]
  78. 78.
    Boesler C, Rigo N, Anokhina MM, Tauchert MJ, Agafonov DE, et al. 2016.. A spliceosome intermediate with loosely associated tri-snRNP accumulates in the absence of Prp28 ATPase activity. . Nat. Commun. 7:(1):11997
     [Crossref] [Google Scholar]
  79. 79.
    Warkocki Z, Schneider C, Mozaffari-Jovin S, Schmitzová J, Höbartner C, et al. 2015.. The G-patch protein Spp2 couples the spliceosome-stimulated ATPase activity of the DEAH-box protein Prp2 to catalytic activation of the spliceosome. . Genes Dev. 29:(1):94–107
     [Crossref] [Google Scholar]
  80. 80.
    Rauhut R, Fabrizio P, Dybkov O, Hartmuth K, Pena V, et al. 2016.. Molecular architecture of the Saccharomyces cerevisiae activated spliceosome. . Science 353:(6306):1399–405
     [Crossref] [Google Scholar]
  81. 81.
    Yan C, Wan R, Bai R, Huang G, Shi Y. 2016.. Structure of a yeast activated spliceosome at 3.5 Å resolution. . Science 353:(6302):904–11
     [Crossref] [Google Scholar]
  82. 82.
    Fica SM, Oubridge C, Galej WP, Wilkinson ME, Bai X-C, et al. 2017.. Structure of a spliceosome remodelled for exon ligation. . Nature 542:(7641):377–80
     [Crossref] [Google Scholar]
  83. 83.
    Strittmatter LM, Capitanchik C, Newman AJ, Hallegger M, Norman CM, et al. 2021.. psiCLIP reveals dynamic RNA binding by DEAH-box helicases before and after exon ligation. . Nat. Commun. 12:(1):1488
     [Crossref] [Google Scholar]
  84. 84.
    Mayas RM, Maita H, Staley JP. 2006.. Exon ligation is proofread by the DExD/H-box ATPase Prp22p. . Nat. Struct. Mol. Biol. 13:(6):482–90
     [Crossref] [Google Scholar]
  85. 85.
    Wilkinson ME, Fica SM, Galej WP, Norman CM, Newman AJ, Nagai K. 2017.. Postcatalytic spliceosome structure reveals mechanism of 3′-splice site selection. . Science 358:(6368):1283–88
     [Crossref] [Google Scholar]
  86. 86.
    Schwer B, Gross CH. 1998.. Prp22, a DExH-box RNA helicase, plays two distinct roles in yeast pre-mRNA splicing. . EMBO J. 17:(7):2086–94
     [Crossref] [Google Scholar]
  87. 87.
    Wagner JDO, Jankowsky E, Company M, Pyle AM, Abelson JN. 1998.. The DEAH-box protein PRP22 is an ATPase that mediates ATP-dependent mRNA release from the spliceosome and unwinds RNA duplexes. . EMBO J. 17:(10):2926–37
     [Crossref] [Google Scholar]
  88. 88.
    Tsai R-T, Tseng C-K, Lee P-J, Chen H-C, Fu R-H, et al. 2007.. Dynamic interactions of Ntr1-Ntr2 with Prp43 and with U5 govern the recruitment of Prp43 to mediate spliceosome disassembly. . Mol. Cell. Biol. 27:(23):8027–37
     [Crossref] [Google Scholar]
  89. 89.
    Studer MK, Ivanović L, Weber ME, Marti S, Jonas S. 2020.. Structural basis for DEAH-helicase activation by G-patch proteins. . PNAS 117:(13):7159–70
     [Crossref] [Google Scholar]
  90. 90.
    Toroney R, Nielsen KH, Staley JP. 2019.. Termination of pre-mRNA splicing requires that the ATPase and RNA unwindase Prp43p acts on the catalytic snRNA U6. . Genes Dev. 33:(21–22):1555–74
     [Crossref] [Google Scholar]
  91. 91.
    Zhang X, Zhan X, Yan C, Zhang W, Liu D, et al. 2019.. Structures of the human spliceosomes before and after release of the ligated exon. . Cell Res. 29:(4):274–85
     [Crossref] [Google Scholar]
  92. 92.
    Maul-Newby HM, Amorello AN, Sharma T, Kim JH, Modena MS, et al. 2022.. A model for DHX15 mediated disassembly of A-complex spliceosomes. . RNA 28:(4):583–95
     [Crossref] [Google Scholar]
  93. 93.
    Fourmann J-B, Dybkov O, Agafonov DE, Tauchert MJ, Urlaub H, et al. 2016.. The target of the DEAH-box NTP triphosphatase Prp43 in Saccharomyces cerevisiae spliceosomes is the U2 snRNP-intron interaction. . eLife 5::e15564
     [Crossref] [Google Scholar]
  94. 94.
    Ilagan JO, Chalkley RJ, Burlingame AL, Jurica MS. 2013.. Rearrangements within human spliceosomes captured after exon ligation. . RNA 19:(3):400–12
     [Crossref] [Google Scholar]
  95. 95.
    Bessonov S, Anokhina M, Krasauskas A, Golas MM, Sander B, et al. 2010.. Characterization of purified human Bact spliceosomal complexes reveals compositional and morphological changes during spliceosome activation and first step catalysis. . RNA 16:(12):2384–403
     [Crossref] [Google Scholar]
  96. 96.
    Shinriki S, Hirayama M, Nagamachi A, Yokoyama A, Kawamura T, et al. 2022.. DDX41 coordinates RNA splicing and transcriptional elongation to prevent DNA replication stress in hematopoietic cells. . Leukemia 36:(11):2605–20
     [Crossref] [Google Scholar]
  97. 97.
    Yang F, Bian T, Zhan X, Chen Z, Xing Z, et al. 2023.. Mechanisms of the RNA helicases DDX42 and DDX46 in human U2 snRNP assembly. . Nat. Commun. 14:(1):897
     [Crossref] [Google Scholar]
  98. 98.
    Will CL, Urlaub H, Achsel T, Gentzel M, Wilm M, Lührmann R. 2002.. Characterization of novel SF3b and 17S U2 snRNP proteins, including a human Prp5p homologue and an SF3b DEAD-box protein. . EMBO J. 21:(18):4978–88
     [Crossref] [Google Scholar]
  99. 99.
    Zhao B, Li Z, Qian R, Liu G, Fan M, et al. 2022.. Cancer-associated mutations in SF3B1 disrupt the interaction between SF3B1 and DDX42. . J. Biochem. 172:(2):117–26
     [Crossref] [Google Scholar]
  100. 100.
    Xu K, Sun S, Yan M, Cui J, Yang Y, et al. 2022.. DDX5 and DDX17—multifaceted proteins in the regulation of tumorigenesis and tumor progression. . Front. Oncol. 12::943032
     [Crossref] [Google Scholar]
  101. 101.
    Dardenne E, Polay Espinoza M, Fattet L, Germann S, Lambert M-P, et al. 2014.. RNA helicases DDX5 and DDX17 dynamically orchestrate transcription, miRNA, and splicing programs in cell differentiation. . Cell Rep. 7:(6):1900–13
     [Crossref] [Google Scholar]
  102. 102.
    Saha S, Yang X, Huang SN, Agama K, Baechler SA, et al. 2022.. Resolution of R-loops by topoisomerase III-β (TOP3B) in coordination with the DEAD-box helicase DDX5. . Cell Rep. 40:(2):111067
     [Crossref] [Google Scholar]
  103. 103.
    Lambert M-P, Terrone S, Giraud G, Benoit-Pilven C, Cluet D, et al. 2018.. The RNA helicase DDX17 controls the transcriptional activity of REST and the expression of proneural microRNAs in neuronal differentiation. . Nucleic Acids Res. 46:(15):7686–700
     [Crossref] [Google Scholar]
  104. 104.
    Lin C, Yang L, Yang JJ, Huang Y, Liu Z-R. 2005.. ATPase/helicase activities of p68 RNA helicase are required for pre-mRNA splicing but not for assembly of the spliceosome. . Mol. Cell. Biol. 25:(17):7484–93
     [Crossref] [Google Scholar]
  105. 105.
    Kar A, Fushimi K, Zhou X, Ray P, Shi C, et al. 2011.. RNA helicase p68 (DDX5) regulates tau exon 10 splicing by modulating a stem-loop structure at the 5′ splice site. . Mol. Cell. Biol. 31:(9):1812–21
     [Crossref] [Google Scholar]
  106. 106.
    Camats M, Guil S, Kokolo M, Bach-Elias M. 2008.. P68 RNA helicase (DDX5) alters activity of cis- and trans-acting factors of the alternative splicing of H-Ras. . PLOS ONE 3:(8):e2926
     [Crossref] [Google Scholar]
  107. 107.
    Chen Z, Hou C, Wang L, Yu C, Chen T, et al. 2022.. Screening membraneless organelle participants with machine-learning models that integrate multimodal features. . PNAS 119:(24):e2115369119
     [Crossref] [Google Scholar]
  108. 108.
    Huang H, Zhang J, Harvey SE, Hu X, Cheng C. 2017.. RNA G-quadruplex secondary structure promotes alternative splicing via the RNA-binding protein hnRNPF. . Genes Dev. 31:(22):2296–309
     [Crossref] [Google Scholar]
  109. 109.
    Georgakopoulos-Soares I, Parada GE, Wong HY, Medhi R, Furlan G, et al. 2022.. Alternative splicing modulation by G-quadruplexes. . Nat. Commun. 13:(1):2404
     [Crossref] [Google Scholar]
  110. 110.
    Caterino M, Paeschke K. 2022.. Action and function of helicases on RNA G-quadruplexes. . Methods 204::110–25
     [Crossref] [Google Scholar]
  111. 111.
    Yangyuoru PM, Bradburn DA, Liu Z, Xiao TS, Russell R. 2018.. The G-quadruplex (G4) resolvase DHX36 efficiently and specifically disrupts DNA G4s via a translocation-based helicase mechanism. . J. Biol. Chem. 293:(6):1924–32
     [Crossref] [Google Scholar]
  112. 112.
    Chen MC, Tippana R, Demeshkina NA, Murat P, Balasubramanian S, et al. 2018.. Structural basis of G-quadruplex unfolding by the DEAH/RHA helicase DHX36. . Nature 558:(7710):465–69
     [Crossref] [Google Scholar]
  113. 113.
    Berchtold D, Battich N, Pelkmans L. 2018.. A systems-level study reveals regulators of membrane-less organelles in human cells. . Mol. Cell 72:(6):1035–49.e5
     [Crossref] [Google Scholar]
  114. 114.
    Boehm V, Gehring NH. 2016.. Exon junction complexes: supervising the gene expression assembly line. . Trends Genet. 32:(11):724–35
     [Crossref] [Google Scholar]
  115. 115.
    Hir HL, Izaurralde E, Maquat LE, Moore MJ. 2000.. The spliceosome deposits multiple proteins 20–24 nucleotides upstream of mRNA exon–exon junctions. . EMBO J. 19:(24):6860–69
     [Crossref] [Google Scholar]
  116. 116.
    Busetto V, Barbosa I, Basquin J, Marquenet É, Hocq R, et al. 2020.. Structural and functional insights into CWC27/CWC22 heterodimer linking the exon junction complex to spliceosomes. . Nucleic Acids Res. 48:(10):5670–83
     [Crossref] [Google Scholar]
  117. 117.
    Merz C, Urlaub H, Will CL, Lührmann R. 2007.. Protein composition of human mRNPs spliced in vitro and differential requirements for mRNP protein recruitment. . RNA 13:(1):116–28
     [Crossref] [Google Scholar]
  118. 118.
    Schlautmann LP, Gehring NH. 2020.. A day in the life of the exon junction complex. . Biomolecules 10:(6):866
     [Crossref] [Google Scholar]
  119. 119.
    Buchwald G, Schüssler S, Basquin C, Hir HL, Conti E. 2013.. Crystal structure of the human eIF4AIII–CWC22 complex shows how a DEAD-box protein is inhibited by a MIF4G domain. . PNAS 110:(48):E4611–18
     [Crossref] [Google Scholar]
  120. 120.
    Bono F, Ebert J, Lorentzen E, Conti E. 2006.. The crystal structure of the exon junction complex reveals how it maintains a stable grip on mRNA. . Cell 126:(4):713–25
     [Crossref] [Google Scholar]
  121. 121.
    Andersen CBF, Ballut L, Johansen JS, Chamieh H, Nielsen KH, et al. 2006.. Structure of the exon junction core complex with a trapped DEAD-box ATPase bound to RNA. . Science 313:(5795):1968–72
     [Crossref] [Google Scholar]
  122. 122.
    Sträßer K, Masuda S, Mason P, Pfannstiel J, Oppizzi M, et al. 2002.. TREX is a conserved complex coupling transcription with messenger RNA export. . Nature 417:(6886):304–8
     [Crossref] [Google Scholar]
  123. 123.
    Schuller SK, Schuller JM, Prabu JR, Baumgärtner M, Bonneau F, et al. 2020.. Structural insights into the nucleic acid remodeling mechanisms of the yeast THO-Sub2 complex. . eLife 9::e61467
     [Crossref] [Google Scholar]
  124. 124.
    Ren Y, Schmiege P, Blobel G. 2017.. Structural and biochemical analyses of the DEAD-box ATPase Sub2 in association with THO or Yra1. . eLife 6::e20070
     [Crossref] [Google Scholar]
  125. 125.
    Chen C, Tan M, Wu Z, Zhang Y, He F, et al. 2021.. Structural and functional insights into R-loop prevention and mRNA export by budding yeast THO-Sub2 complex. . Sci. Bull. 66:(23):2347–52
     [Crossref] [Google Scholar]
  126. 126.
    Sträßer K, Hurt E. 2001.. Splicing factor Sub2p is required for nuclear mRNA export through its interaction with Yra1p. . Nature 413:(6856):648–52
     [Crossref] [Google Scholar]
  127. 127.
    Viphakone N, Sudbery I, Griffith L, Heath CG, Sims D, Wilson SA. 2019.. Co-transcriptional loading of RNA export factors shapes the human transcriptome. . Mol. Cell 75:(2):310–23.e8
     [Crossref] [Google Scholar]
  128. 128.
    Gromadzka AM, Steckelberg A-L, Singh KK, Hofmann K, Gehring NH. 2016.. A short conserved motif in ALYREF directs cap- and EJC-dependent assembly of export complexes on spliced mRNAs. . Nucleic Acids Res. 44:(5):2348–61
     [Crossref] [Google Scholar]
  129. 129.
    Cordiner RA, Dou Y, Thomsen R, Bugai A, Granneman S, Jensen TH. 2023.. Temporal-iCLIP captures co-transcriptional RNA-protein interactions. . Nat. Commun. 14:(1):696
     [Crossref] [Google Scholar]
  130. 130.
    Pacheco-Fiallos B, Vorländer MK, Riabov-Bassat D, Fin L, O'Reilly FJ, et al. 2023.. mRNA recognition and packaging by the human transcription–export complex. . Nature 616:(7958):828–35
     [Crossref] [Google Scholar]
  131. 131.
    Dufu K, Livingstone MJ, Seebacher J, Gygi SP, Wilson SA, Reed R. 2010.. ATP is required for interactions between UAP56 and two conserved mRNA export proteins, Aly and CIP29, to assemble the TREX complex. . Genes Dev. 24:(18):2043–53
     [Crossref] [Google Scholar]
  132. 132.
    Pühringer T, Hohmann U, Fin L, Pacheco-Fiallos B, Schellhaas U, et al. 2020.. Structure of the human core transcription-export complex reveals a hub for multivalent interactions. . eLife 9::e61503
     [Crossref] [Google Scholar]
  133. 133.
    Chang C, Hautbergue GM, Walsh MJ, Viphakone N, van Dijk TB, et al. 2013.. Chtop is a component of the dynamic TREX mRNA export complex. . EMBO J. 32:(3):473–86
     [Crossref] [Google Scholar]
  134. 134.
    Taniguchi I, Ohno M. 2008.. ATP-dependent recruitment of export factor Aly/REF onto intronless mRNAs by RNA helicase UAP56. . Mol. Cell. Biol. 28:(2):601–8
     [Crossref] [Google Scholar]
  135. 135.
    Bonneau F, Basquin J, Steigenberger B, Schäfer T, Schäfer IB, Conti E. 2023.. Nuclear mRNPs are compact particles packaged with a network of proteins promoting RNA–RNA interactions. . Genes Dev. 37::505–17
     [Crossref] [Google Scholar]
  136. 136.
    Rajan AAN, Montpetit B. 2021.. Emerging molecular functions and novel roles for the DEAD-box protein Dbp5/DDX19 in gene expression. . Cell. Mol. Life Sci. 78:(5):2019–30
     [Crossref] [Google Scholar]
  137. 137.
    Folkmann AW, Noble KN, Cole CN, Wente SR. 2011.. Dbp5, Gle1-IP6 and Nup159. . Nucleus 2:(6):540–48
     [Crossref] [Google Scholar]
  138. 138.
    Lin DH, Correia AR, Cai SW, Huber FM, Jette CA, Hoelz A. 2018.. Structural and functional analysis of mRNA export regulation by the nuclear pore complex. . Nat. Commun. 9:(1):2319
     [Crossref] [Google Scholar]
  139. 139.
    Weirich CS, Erzberger JP, Flick JS, Berger JM, Thorner J, Weis K. 2006.. Activation of the DExD/H-box protein Dbp5 by the nuclear-pore protein Gle1 and its coactivator InsP6 is required for mRNA export. . Nat. Cell Biol. 8:(7):668–76
     [Crossref] [Google Scholar]
  140. 140.
    Alcázar-Román AR, Tran EJ, Guo S, Wente SR. 2006.. Inositol hexakisphosphate and Gle1 activate the DEAD-box protein Dbp5 for nuclear mRNA export. . Nat. Cell Biol. 8:(7):711–16
     [Crossref] [Google Scholar]
  141. 141.
    Lund MK, Guthrie C. 2005.. The DEAD-box protein Dbp5p is required to dissociate Mex67p from exported mRNPs at the nuclear rim. . Mol. Cell 20:(4):645–51
     [Crossref] [Google Scholar]
  142. 142.
    Tran EJ, Zhou Y, Corbett AH, Wente SR. 2007.. The DEAD-Box protein Dbp5 controls mRNA export by triggering specific RNA:protein remodeling events. . Mol. Cell 28:(5):850–59
     [Crossref] [Google Scholar]
  143. 143.
    Heinrich S, Hondele M, Marchand D, Derrer CP, Zedan M, et al. 2022.. Condensation of a nuclear mRNA export factor regulates mRNA transport during stress. . bioRxiv 2022.01.30.478372. https://doi.org/10.1101/2022.01.30.478372
  144. 144.
    Gehring NH, Lamprinaki S, Kulozik AE, Hentze MW. 2009.. Disassembly of exon junction complexes by PYM. . Cell 137:(3):536–48
     [Crossref] [Google Scholar]
  145. 145.
    Diem MD, Chan CC, Younis I, Dreyfuss G. 2007.. PYM binds the cytoplasmic exon-junction complex and ribosomes to enhance translation of spliced mRNAs. . Nat. Struct. Mol. Biol. 14:(12):1173–79
     [Crossref] [Google Scholar]
  146. 146.
    Andreou AZ, Klostermeier D. 2013.. The DEAD-box helicase eIF4A. . RNA Biol. 10:(1):19–32
     [Crossref] [Google Scholar]
  147. 147.
    Linder P. 2003.. Yeast RNA helicases of the DEAD-box family involved in translation initiation. . Biol. Cell 95:(3–4):157–67
     [Crossref] [Google Scholar]
  148. 148.
    Krause L, Willing F, Andreou AZ, Klostermeier D. 2022.. The domains of yeast eIF4G, eIF4E and the cap fine-tune eIF4A activities through an intricate network of stimulatory and inhibitory effects. . Nucleic Acids Res. 50:(11):6497–510
     [Crossref] [Google Scholar]
  149. 149.
    Izidoro MS, Sokabe M, Villa N, Merrick WC, Fraser CS. 2022.. Human eukaryotic initiation factor 4E (eIF4E) and the nucleotide-bound state of eIF4A regulate eIF4F binding to RNA. . J. Biol. Chem. 298:(10):102368
     [Crossref] [Google Scholar]
  150. 150.
    Wang J, Shin B-S, Alvarado C, Kim J-R, Bohlen J, et al. 2022.. Rapid 40S scanning and its regulation by mRNA structure during eukaryotic translation initiation. . Cell 185:(24):4474–87.e17
     [Crossref] [Google Scholar]
  151. 151.
    O'Sullivan MH, Fraser CS. 2023.. Monitoring RNA restructuring in a human cell-free extract reveals eIF4A-dependent and eIF4A-independent unwinding activity. . J. Biol. Chem. 299:(7):104936
     [Crossref] [Google Scholar]
  152. 152.
    Ryan CS, Schröder M. 2022.. The human DEAD-box helicase DDX3X as a regulator of mRNA translation. . Front. Cell Dev. Biol. 10::1033684
     [Crossref] [Google Scholar]
  153. 153.
    Shen H, Yanas A, Owens MC, Zhang C, Fritsch C, et al. 2022.. Sexually dimorphic RNA helicases DDX3X and DDX3Y differentially regulate RNA metabolism through phase separation. . Mol. Cell 82:(14):2588–603.e9
     [Crossref] [Google Scholar]
  154. 154.
    Putnam AA, Gao Z, Liu F, Jia H, Yang Q, Jankowsky E. 2015.. Division of labor in an oligomer of the DEAD-box RNA helicase Ded1p. . Mol. Cell 59:(4):541–52
     [Crossref] [Google Scholar]
  155. 155.
    Oh S, Flynn RA, Floor SN, Purzner J, Martin L, et al. 2016.. Medulloblastoma-associated DDX3 variant selectively alters the translational response to stress. . Oncotarget 7:(19):28169–82
     [Crossref] [Google Scholar]
  156. 156.
    Valentin-Vega YA, Wang Y-D, Parker M, Patmore DM, Kanagaraj A, et al. 2016.. Cancer-associated DDX3X mutations drive stress granule assembly and impair global translation. . Sci. Rep. 6:(1):25996
     [Crossref] [Google Scholar]
  157. 157.
    Guenther U-P, Weinberg DE, Zubradt MM, Tedeschi FA, Stawicki BN, et al. 2018.. The helicase Ded1p controls use of near-cognate translation initiation codons in 5′ UTRs. . Nature 559:(7712):130–34
     [Crossref] [Google Scholar]
  158. 158.
    Calviello L, Venkataramanan S, Rogowski KJ, Wyler E, Wilkins K, et al. 2021.. DDX3 depletion represses translation of mRNAs with complex 5′ UTRs. . Nucleic Acids Res. 49:(9):5336–50
     [Crossref] [Google Scholar]
  159. 159.
    Ishigaki Y, Li X, Serin G, Maquat LE. 2001.. Evidence for a pioneer round of mRNA translation: mRNAs subject to nonsense-mediated decay in mammalian cells are bound by CBP80 and CBP20. . Cell 106:(5):607–17
     [Crossref] [Google Scholar]
  160. 160.
    Schweingruber C, Soffientini P, Ruepp M-D, Bachi A, Mühlemann O. 2016.. Identification of interactions in the NMD complex using proximity-dependent biotinylation (BioID). . PLOS ONE 11:(3):e0150239
     [Crossref] [Google Scholar]
  161. 161.
    Shih J-W, Wang W-T, Tsai T-Y, Kuo C-Y, Li H-K, Wu Lee Y-H. 2011.. Critical roles of RNA helicase DDX3 and its interactions with eIF4E/PABP1 in stress granule assembly and stress response. . Biochem. J. 441:(1):119–29
     [Crossref] [Google Scholar]
  162. 162.
    Hilliker A, Gao Z, Jankowsky E, Parker R. 2011.. The DEAD-box protein Ded1 modulates translation by the formation and resolution of an eIF4F-mRNA complex. . Mol. Cell 43:(6):962–72
     [Crossref] [Google Scholar]
  163. 163.
    Soto-Rifo R, Rubilar PS, Limousin T, de Breyne S, Décimo D, Ohlmann T. 2012.. DEAD-box protein DDX3 associates with eIF4F to promote translation of selected mRNAs. . EMBO J. 31:(18):3745–56
     [Crossref] [Google Scholar]
  164. 164.
    Gulay S, Gupta N, Lorsch JR, Hinnebusch AG. 2020.. Distinct interactions of eIF4A and eIF4E with RNA helicase Ded1 stimulate translation in vivo. . eLife 9::e58243
     [Crossref] [Google Scholar]
  165. 165.
    Chuang R-Y, Weaver PL, Liu Z, Chang T-H. 1997.. Requirement of the DEAD-box protein Ded1p for messenger RNA translation. . Science 275:(5305):1468–71
     [Crossref] [Google Scholar]
  166. 166.
    Ostareck DH, Vries ISN, Ostareck-Lederer A. 2014.. DDX6 and its orthologs as modulators of cellular and viral RNA expression. . WIREs RNA 5:(5):659–78
     [Crossref] [Google Scholar]
  167. 167.
    Stefano BD, Luo E-C, Haggerty C, Aigner S, Charlton J, et al. 2019.. The RNA helicase DDX6 controls cellular plasticity by modulating P-body homeostasis. . Cell Stem Cell 25:(5):622–38.e13
     [Crossref] [Google Scholar]
  168. 168.
    Kim J, Muraoka M, Okada H, Toyoda A, Ajima R, Saga Y. 2022.. The RNA helicase DDX6 controls early mouse embryogenesis by repressing aberrant inhibition of BMP signaling through miRNA-mediated gene silencing. . PLOS Genet. 18:(10):e1009967
     [Crossref] [Google Scholar]
  169. 169.
    Ernoult-Lange M, Baconnais S, Harper M, Minshall N, Souquere S, et al. 2012.. Multiple binding of repressed mRNAs by the P-body protein Rck/p54. . RNA 18:(9):1702–15
     [Crossref] [Google Scholar]
  170. 170.
    Radhakrishnan A, Chen Y-H, Martin S, Alhusaini N, Green R, Coller J. 2016.. The DEAD-box protein Dhh1p couples mRNA decay and translation by monitoring codon optimality. . Cell 167:(1):122–32.e9
     [Crossref] [Google Scholar]
  171. 171.
    Mathys H, Basquin J, Ozgur S, Czarnocki-Cieciura M, Bonneau F, et al. 2014.. Structural and biochemical insights to the role of the CCR4-NOT complex and DDX6 ATPase in microRNA repression. . Mol. Cell 54:(5):751–65
     [Crossref] [Google Scholar]
  172. 172.
    Mugler CF, Hondele M, Heinrich S, Sachdev R, Vallotton P, et al. 2016.. ATPase activity of the DEAD-box protein Dhh1 controls processing body formation. . eLife 5::e18746
     [Crossref] [Google Scholar]
  173. 173.
    Chen Y, Boland A, Kuzuoğlu-Öztürk D, Bawankar P, Loh B, et al. 2014.. A DDX6-CNOT1 complex and W-binding pockets in CNOT9 reveal direct links between miRNA target recognition and silencing. . Mol. Cell 54:(5):737–50
     [Crossref] [Google Scholar]
  174. 174.
    Rouya C, Siddiqui N, Morita M, Duchaine TF, Fabian MR, Sonenberg N. 2014.. Human DDX6 effects miRNA-mediated gene silencing via direct binding to CNOT1. . RNA 20:(9):1398–409
     [Crossref] [Google Scholar]
  175. 175.
    Kamenska A, Simpson C, Vindry C, Broomhead H, Bénard M, et al. 2016.. The DDX6–4E-T interaction mediates translational repression and P-body assembly. . Nucleic Acids Res. 44:(13):6318–34
     [Crossref] [Google Scholar]
  176. 176.
    Ozgur S, Basquin J, Kamenska A, Filipowicz W, Standart N, Conti E. 2015.. Structure of a human 4E-T/DDX6/CNOT1 complex reveals the different interplay of DDX6-binding proteins with the CCR4-NOT complex. . Cell Rep. 13:(4):703–11
     [Crossref] [Google Scholar]
  177. 177.
    Räsch F, Weber R, Izaurralde E, Igreja C. 2020.. 4E-T-bound mRNAs are stored in a silenced and deadenylated form. . Genes Dev. 34:(11–12):847–60
     [Crossref] [Google Scholar]
  178. 178.
    Riggs CL, Kedersha N, Ivanov P, Anderson P. 2020.. Mammalian stress granules and P bodies at a glance. . J. Cell Sci. 133:(16):jcs242487
     [Crossref] [Google Scholar]
  179. 179.
    Hubstenberger A, Courel M, Bénard M, Souquere S, Ernoult-Lange M, et al. 2017.. P-body purification reveals the condensation of repressed mRNA regulons. . Mol. Cell 68:(1):144–57.e5
     [Crossref] [Google Scholar]
  180. 180.
    Jain S, Wheeler JR, Walters RW, Agrawal A, Barsic A, Parker R. 2016.. ATPase-modulated stress granules contain a diverse proteome and substructure. . Cell 164:(3):487–98
     [Crossref] [Google Scholar]
  181. 181.
    Sanders DW, Kedersha N, Lee DSW, Strom AR, Drake V, et al. 2020.. Competing protein-RNA interaction networks control multiphase intracellular organization. . Cell 181:(2):306–24.e28
     [Crossref] [Google Scholar]
  182. 182.
    Ripin N, Parker R. 2022.. Are stress granules the RNA analogs of misfolded protein aggregates?. RNA 28:(1):67–75
     [Crossref] [Google Scholar]
  183. 183.
    Mateju D, Eichenberger B, Voigt F, Eglinger J, Roth G, Chao JA. 2020.. Single-molecule imaging reveals translation of mRNAs localized to stress granules. . Cell 183:(7):1801–12.e13
     [Crossref] [Google Scholar]
  184. 184.
    Youn J-Y, Dyakov BJA, Zhang J, Knight JDR, Vernon RM, et al. 2019.. Properties of stress granule and P-body proteomes. . Mol. Cell 76:(2):286–94
     [Crossref] [Google Scholar]
  185. 185.
    Tauber D, Tauber G, Khong A, Treeck BV, Pelletier J, Parker R. 2020.. Modulation of RNA condensation by the DEAD-box protein eIF4A. . Cell 180:(3):411–26.e16
     [Crossref] [Google Scholar]
  186. 186.
    Li L, Garg M, Wang Y, Wang W, Godbout R. 2022.. DEAD box 1 (DDX1) protein binds to and protects cytoplasmic stress response mRNAs in cells exposed to oxidative stress. . J. Biol. Chem. 298:(8):102180
     [Crossref] [Google Scholar]
  187. 187.
    Aryanpur PP, Mittelmeier TM, Bolger TA. 2021.. The RNA helicase Ded1 regulates translation and granule formation during multiple phases of cellular stress responses. . Mol. Cell. Biol. 42:(1):e00244-21
     [Google Scholar]
  188. 188.
    Minshall N, Kress M, Weil D, Standart N. 2009.. Role of p54 RNA helicase activity and its C-terminal domain in translational repression, P-body localization and assembly. . Mol. Biol. Cell 20:(9):2464–72
     [Crossref] [Google Scholar]
  189. 189.
    Currie SL, Xing W, Muhlrad D, Decker CJ, Parker R, Rosen MK. 2023.. Quantitative reconstitution of yeast RNA processing bodies. . PNAS 120:(14):e2214064120
     [Crossref] [Google Scholar]
  190. 190.
    Coller J, Parker R. 2005.. General translational repression by activators of mRNA decapping. . Cell 122:(6):875–86
     [Crossref] [Google Scholar]
  191. 191.
    Pushpalatha KV, Solyga M, Nakamura A, Besse F. 2022.. RNP components condense into repressive RNP granules in the aging brain. . Nat. Commun. 13:(1):2782
     [Crossref] [Google Scholar]
  192. 192.
    Iserman C, Altamirano CD, Jegers C, Friedrich U, Zarin T, et al. 2020.. Condensation of Ded1p promotes a translational switch from housekeeping to stress protein production. . Cell 181:(4):818–31.e19
     [Crossref] [Google Scholar]
  193. 193.
    Saito M, Hess D, Eglinger J, Fritsch AW, Kreysing M, et al. 2019.. Acetylation of intrinsically disordered regions regulates phase separation. . Nat. Chem. Biol. 15:(1):51–61
     [Crossref] [Google Scholar]
  194. 194.
    Hubstenberger A, Cameron C, Noble SL, Keenan S, Evans TC. 2015.. Modifiers of solid RNP granules control normal RNP dynamics and mRNA activity in early development. . J. Cell Biol. 211:(3):703–16
     [Crossref] [Google Scholar]
  195. 195.
    Majerciak V, Zhou T, Kruhlak MJ, Zheng Z-M. 2023.. RNA helicase DDX6 and scaffold protein GW182 in P-bodies promote biogenesis of stress granules. . Nucleic Acids Res. 51:(17):9337–55
     [Crossref] [Google Scholar]
/content/journals/10.1146/annurev-biochem-052521-121259
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The Story of RNA Unfolded: The Molecular Function of DEAD- and DExH-Box ATPases and Their Complex Relationship with Membraneless Organelles
Annual Review of Biochemistry 93, 79 (2024); https://doi.org/10.1146/annurev-biochem-052521-121259
/content/journals/10.1146/annurev-biochem-052521-121259
/content/journals/10.1146/annurev-biochem-052521-121259
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