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Structural and functional analysis of mRNA export regulation by the nuclear pore complex.

Lin DH, Correia AR, Cai SW, Huber FM, Jette CA, Hoelz A
Nat Commun 9 2319 (2018)
Related entries: 6b4e, 6b4f, 6b4g, 6b4h, 6b4i, 6b4k

Cited: 27 times
EuropePMC logo PMID: 29899397

Abstract

The nuclear pore complex (NPC) controls the passage of macromolecules between the nucleus and cytoplasm, but how the NPC directly participates in macromolecular transport remains poorly understood. In the final step of mRNA export, the DEAD-box helicase DDX19 is activated by the nucleoporins Gle1, Nup214, and Nup42 to remove Nxf1•Nxt1 from mRNAs. Here, we report crystal structures of Gle1•Nup42 from three organisms that reveal an evolutionarily conserved binding mode. Biochemical reconstitution of the DDX19 ATPase cycle establishes that human DDX19 activation does not require IP6, unlike its fungal homologs, and that Gle1 stability affects DDX19 activation. Mutations linked to motor neuron diseases cause decreased Gle1 thermostability, implicating nucleoporin misfolding as a disease determinant. Crystal structures of human Gle1•Nup42•DDX19 reveal the structural rearrangements in DDX19 from an auto-inhibited to an RNA-binding competent state. Together, our results provide the foundation for further mechanistic analyses of mRNA export in humans.

Reviews - 6b4j mentioned but not cited (2)

  1. The Structure of the Nuclear Pore Complex (An Update). Lin DH, Hoelz A. Annu Rev Biochem 88 725-783 (2019)
  2. Host DDX Helicases as Possible SARS-CoV-2 Proviral Factors: A Structural Overview of Their Hijacking Through Multiple Viral Proteins. Squeglia F, Romano M, Ruggiero A, Maga G, Berisio R. Front Chem 8 602162 (2020)

Articles - 6b4j mentioned but not cited (1)

  1. Structural and functional analysis of mRNA export regulation by the nuclear pore complex. Lin DH, Correia AR, Cai SW, Huber FM, Jette CA, Hoelz A. Nat Commun 9 2319 (2018)


Reviews citing this publication (13)

  1. Mechanisms of nuclear mRNA export: A structural perspective. Xie Y, Ren Y. Traffic 20 829-840 (2019)
  2. NUP214 in Leukemia: It's More than Transport. Mendes A, Fahrenkrog B. Cells 8 E76 (2019)
  3. The coming-of-age of nucleocytoplasmic transport in motor neuron disease and neurodegeneration. Ferreira PA. Cell Mol Life Sci 76 2247-2273 (2019)
  4. Melatonin: Regulation of Biomolecular Condensates in Neurodegenerative Disorders. Loh D, Reiter RJ. Antioxidants (Basel) 10 1483 (2021)
  5. Strength in Diversity: Nuclear Export of Viral RNAs. Gales JP, Kubina J, Geldreich A, Dimitrova M. Viruses 12 E1014 (2020)
  6. RNA transport from transcription to localized translation: a single molecule perspective. Basyuk E, Rage F, Bertrand E. RNA Biol 18 1221-1237 (2021)
  7. Nuclear mRNA maturation and mRNA export control: from trypanosomes to opisthokonts. Kramer S. Parasitology 148 1196-1218 (2021)
  8. Emerging molecular functions and novel roles for the DEAD-box protein Dbp5/DDX19 in gene expression. Arul Nambi Rajan A, Montpetit B. Cell Mol Life Sci 78 2019-2030 (2021)
  9. Evolution and diversification of the nuclear pore complex. Makarov AA, Padilla-Mejia NE, Field MC. Biochem Soc Trans 49 1601-1619 (2021)
  10. Gonadotropin Regulation Testicular RNA Helicase, Two Decades of Studies on Its Structure Function and Regulation From Its Discovery Opens a Window for Development of a Non-hormonal Oral Male Contraceptive. Dufau ML, Kavarthapu R. Front Endocrinol (Lausanne) 10 576 (2019)
  11. Melatonin: Regulation of Viral Phase Separation and Epitranscriptomics in Post-Acute Sequelae of COVID-19. Loh D, Reiter RJ. Int J Mol Sci 23 8122 (2022)
  12. Nuclear envelope, chromatin organizers, histones, and DNA: The many achilles heels exploited across cancers. Balaji AK, Saha S, Deshpande S, Poola D, Sengupta K. Front Cell Dev Biol 10 1068347 (2022)
  13. Nuclear transport proteins: structure, function, and disease relevance. Yang Y, Guo L, Chen L, Gong B, Jia D, Sun Q. Signal Transduct Target Ther 8 425 (2023)

Articles citing this publication (11)

  1. Architecture of the cytoplasmic face of the nuclear pore. Bley CJ, Nie S, Mobbs GW, Petrovic S, Gres AT, Liu X, Mukherjee S, Harvey S, Huber FM, Lin DH, Brown B, Tang AW, Rundlet EJ, Correia AR, Chen S, Regmi SG, Stevens TA, Jette CA, Dasso M, Patke A, Palazzo AF, Kossiakoff AA, Hoelz A. Science 376 eabm9129 (2022)
  2. Architecture of the linker-scaffold in the nuclear pore. Petrovic S, Samanta D, Perriches T, Bley CJ, Thierbach K, Brown B, Nie S, Mobbs GW, Stevens TA, Liu X, Tomaleri GP, Schaus L, Hoelz A. Science 376 eabm9798 (2022)
  3. Imaging within single NPCs reveals NXF1's role in mRNA export on the cytoplasmic side of the pore. Ben-Yishay R, Mor A, Shraga A, Ashkenazy-Titelman A, Kinor N, Schwed-Gross A, Jacob A, Kozer N, Kumar P, Garini Y, Shav-Tal Y. J Cell Biol 218 2962-2981 (2019)
  4. Nuclear RNA binding regulates TDP-43 nuclear localization and passive nuclear export. Duan L, Zaepfel BL, Aksenova V, Dasso M, Rothstein JD, Kalab P, Hayes LR. Cell Rep 40 111106 (2022)
  5. Translation mediated by the nuclear cap-binding complex is confined to the perinuclear region via a CTIF-DDX19B interaction. Park Y, Park J, Hwang HJ, Kim L, Jeong K, Song HK, Rufener SC, Mühlemann O, Kim YK. Nucleic Acids Res 49 8261-8276 (2021)
  6. The nucleoporin Gle1 activates DEAD-box protein 5 (Dbp5) by promoting ATP binding and accelerating rate limiting phosphate release. Gray S, Cao W, Montpetit B, De La Cruz EM. Nucleic Acids Res 50 3998-4011 (2022)
  7. Functions of Gle1 are governed by two distinct modes of self-association. Mason AC, Wente SR. J Biol Chem 295 16813-16825 (2020)
  8. Nuclear export mechanisms of circular RNAs: size does matter. Azmi AS. Noncoding RNA Investig 2 52 (2018)
  9. Dynamics of nuclear export of pre-ribosomal subunits revealed by high-speed single-molecule microscopy in live cells. Junod SL, Tingey M, Kelich JM, Goryaynov A, Herbine K, Yang W. iScience 26 107445 (2023)
  10. Quantitative comparison of nuclear transport inhibition by SARS coronavirus ORF6 reveals the importance of oligomerization. Yoo TY, Mitchison TJ. Proc Natl Acad Sci U S A 121 e2307997121 (2024)
  11. SE translation mRNA overexpression: a potential prognostic predictor in breast cancer. Du Q, Hao R, Liu L, Liu Y, Chen S, You H, Zhang Y, Dong Y. Transl Cancer Res 8 2044-2052 (2019)


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