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Keeping mRNPs in check during assembly and nuclear export

Abstract

The cell nucleus is an intricate organelle that coordinates multiple activities that are associated with DNA replication and gene expression. In all eukaryotes, it stores the genetic information and the machineries that control the production of mature and export-competent messenger ribonucleoproteins (mRNPs), a multistep process that is regulated in a spatial and temporal manner. Recent studies suggest that post-translational modifications play a part in coordinating the co-transcriptional assembly, remodelling and export of mRNP complexes through nuclear pores, adding a new level of regulation to the process of gene expression.

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Figure 1: Co-transcriptional assembly of export-competent mRNPs.
Figure 2: NPC-associated remodelling and surveillance.

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References

  1. Rougemaille, M., Villa, T., Gudipati, R. K. & Libri, D. mRNA journey to the cytoplasm: attire required. Biol. Cell 100, 327–342 (2008).

    Article  CAS  PubMed  Google Scholar 

  2. Iglesias, N. & Stutz, F. Regulation of mRNP dynamics along the export pathway. FEBS Lett. 582, 1987–1996 (2008).

    Article  CAS  PubMed  Google Scholar 

  3. Schmid, M. & Jensen, T. H. Quality control of mRNP in the nucleus. Chromosoma 117, 419–429 (2008).

    Article  CAS  PubMed  Google Scholar 

  4. Houseley, J. & Tollervey, D. The many pathways of RNA degradation. Cell 136, 763–776 (2009).

    Article  CAS  PubMed  Google Scholar 

  5. Du, T. G., Schmid, M. & Jansen, R. P. Why cells move messages: the biological functions of mRNA localization. Semin. Cell Dev. Biol. 18, 171–177 (2007).

    Article  CAS  PubMed  Google Scholar 

  6. Martin, K. C. & Ephrussi, A. mRNA localization: gene expression in the spatial dimension. Cell 136, 719–730 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Deribe, Y. L., Pawson, T. & Dikic, I. Post-translational modifications in signal integration. Nature Struct. Mol. Biol. 17, 666–672 (2010).

    Article  CAS  Google Scholar 

  8. Kim, M., Suh, H., Cho, E. J. & Buratowski, S. Phosphorylation of the yeast Rpb1 C-terminal domain at serines 2, 5, and 7. J. Biol. Chem. 284, 26421–26426 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Egloff, S. & Murphy, S. Cracking the RNA polymerase II CTD code. Trends Genet. 24, 280–288 (2008).

    Article  CAS  PubMed  Google Scholar 

  10. Buratowski, S. Progression through the RNA polymerase II CTD cycle. Mol. Cell 36, 541–546 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Kim, H. et al. Gene-specific RNA polymerase II phosphorylation and the CTD code. Nature Struct. Mol. Biol. 17, 1279–1286 (2010).

    Article  CAS  Google Scholar 

  12. Tietjen, J. R. et al. Chemical-genomic dissection of the CTD code. Nature Struct. Mol. Biol. 17, 1154–1161 (2010).

    Article  CAS  Google Scholar 

  13. Mayer, A. et al. Uniform transitions of the general RNA polymerase II transcription complex. Nature Struct. Mol. Biol. 17, 1272–1278 (2010).

    Article  CAS  Google Scholar 

  14. Hocine, S., Singer, R. H. & Grunwald, D. RNA processing and export. Cold Spring Harb. Perspect. Biol. 2, a000752 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Bentley, D. L. Rules of engagement: co-transcriptional recruitment of pre-mRNA processing factors. Curr. Opin. Cell Biol. 17, 251–256 (2005).

    Article  CAS  PubMed  Google Scholar 

  16. Jiao, X. et al. Identification of a quality-control mechanism for mRNA 5′-end capping. Nature 467, 608–611 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Colot, H. V., Stutz, F. & Rosbash, M. The yeast splicing factor Mud13p is a commitment complex component and corresponds to CBP20, the small subunit of the nuclear cap-binding complex. Genes Dev. 10, 1699–1708 (1996).

    Article  CAS  PubMed  Google Scholar 

  18. Gornemann, J., Kotovic, K. M., Hujer, K. & Neugebauer, K. M. Cotranscriptional spliceosome assembly occurs in a stepwise fashion and requires the cap binding complex. Mol. Cell 19, 53–63 (2005).

    Article  PubMed  CAS  Google Scholar 

  19. Cheng, H. et al. Human mRNA export machinery recruited to the 5′ end of mRNA. Cell 127, 1389–1400 (2006).

    Article  CAS  PubMed  Google Scholar 

  20. Lacadie, S. A. & Rosbash, M. Cotranscriptional spliceosome assembly dynamics and the role of U1 snRNA:5′ss base pairing in yeast. Mol. Cell 19, 65–75 (2005).

    Article  CAS  PubMed  Google Scholar 

  21. Kress, T. L., Krogan, N. J. & Guthrie, C. A single SR-like protein, Npl3, promotes pre-mRNA splicing in budding yeast. Mol. Cell 32, 727–734 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Carrillo Oesterreich, F., Preibisch, S. & Neugebauer, K. M. Global analysis of nascent RNA reveals transcriptional pausing in terminal exons. Mol. Cell 40, 571–581 (2010).

    Article  CAS  PubMed  Google Scholar 

  23. Alexander, R. D., Innocente, S. A., Barrass, J. D. & Beggs, J. D. Splicing-dependent RNA polymerase pausing in yeast. Mol. Cell 40, 582–593 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Chavez, S. et al. A protein complex containing Tho2, Hpr1, Mft1 and a novel protein, Thp2, connects transcription elongation with mitotic recombination in Saccharomyces cerevisiae. EMBO J. 19, 5824–5834 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Rodriguez-Navarro, S. & Hurt, E. Linking gene regulation to mRNA production and export. Curr. Opin. Cell Biol. 23, 1–8 (2011).

    Article  CAS  Google Scholar 

  26. Strasser, K. et al. TREX is a conserved complex coupling transcription with messenger RNA export. Nature 417, 304–308 (2002).

    Article  PubMed  CAS  Google Scholar 

  27. Zenklusen, D., Vinciguerra, P., Wyss, J. C. & Stutz, F. Stable mRNP formation and export require cotranscriptional recruitment of the mRNA export factors Yra1p and Sub2p by Hpr1p. Mol. Cell. Biol. 22, 8241–8253 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Johnson, S. A., Cubberley, G. & Bentley, D. L. Cotranscriptional recruitment of the mRNA export factor Yra1 by direct interaction with the 3′ end processing factor Pcf11. Mol. Cell 33, 215–226 (2009).

    Article  CAS  PubMed  Google Scholar 

  29. Dieppois, G., Iglesias, N. & Stutz, F. Cotranscriptional recruitment to the mRNA export receptor Mex67p contributes to nuclear pore anchoring of activated genes. Mol. Cell. Biol. 26, 7858–7870 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Gwizdek, C. et al. Ubiquitin-associated domain of Mex67 synchronizes recruitment of the mRNA export machinery with transcription. Proc. Natl Acad. Sci. USA 103, 16376–16381 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Dias, A. P., Dufu, K., Lei, H. & Reed, R. A role for TREX components in the release of spliced mRNA from nuclear speckle domains. Nature Commun. 1, 97 (2010).

    Article  CAS  Google Scholar 

  32. Masuda, S. et al. Recruitment of the human TREX complex to mRNA during splicing. Genes Dev. 19, 1512–1517 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Valencia, P., Dias, A. P. & Reed, R. Splicing promotes rapid and efficient mRNA export in mammalian cells. Proc. Natl Acad. Sci. USA 105, 3386–3391 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Casolari, J. M. et al. Genome-wide localization of the nuclear transport machinery couples transcriptional status and nuclear organization. Cell 117, 427–439 (2004).

    Article  CAS  PubMed  Google Scholar 

  35. Dieppois, G. & Stutz, F. Connecting the transcription site to the nuclear pore: a multi-tether process that regulates gene expression. J. Cell Sci. 123, 1989–1999 (2010).

    Article  CAS  PubMed  Google Scholar 

  36. Rodriguez-Navarro, S. et al. Sus1, a functional component of the SAGA histone acetylase complex and the nuclear pore-associated mRNA export machinery. Cell 116, 75–86 (2004).

    Article  CAS  PubMed  Google Scholar 

  37. Kohler, A. & Hurt, E. Exporting RNA from the nucleus to the cytoplasm. Nature Rev. Mol. Cell Biol. 8, 761–773 (2007).

    Article  CAS  Google Scholar 

  38. Kurshakova, M. M. et al. SAGA and a novel Drosophila export complex anchor efficient transcription and mRNA export to NPC. EMBO J. 26, 4956–4965 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Wickramasinghe, V. O. et al. mRNA export from mammalian cell nuclei is dependent on GANP. Curr. Biol. 20, 25–31 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Ahmed, S. et al. DNA zip codes control an ancient mechanism for gene targeting to the nuclear periphery. Nature Cell Biol. 12, 111–118 (2010).

    Article  CAS  PubMed  Google Scholar 

  41. Brickner, D. G. & Brickner, J. H. Cdk phosphorylation of a nucleoporin controls localization of active genes through the cell cycle. Mol. Biol. Cell 21, 3421–3432 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Saguez, C. et al. Nuclear mRNA surveillance in THO/sub2 mutants is triggered by inefficient polyadenylation. Mol. Cell 31, 91–103 (2008).

    Article  CAS  PubMed  Google Scholar 

  43. Rouge-maille, M. et al. THO/Sub2p functions to coordinate 3′-end processing with gene-nuclear pore association. Cell 135, 308–321 (2008).

    Article  CAS  Google Scholar 

  44. de Almeida, S. F., Garcia-Sacristan, A., Custodio, N. & Carmo-Fonseca, M. A link between nuclear RNA surveillance, the human exosome and RNA polymerase II transcriptional termination. Nucleic Acids Res. 38, 8015–8026 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Qu, X. et al. Assembly of an export-competent mRNP is needed for efficient release of the 3′-end processing complex after polyadenylation. Mol. Cell. Biol. 29, 5327–5338 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Palancade, B. & Doye, V. Sumoylating and desumoylating enzymes at nuclear pores: underpinning their unexpected duties? Trends Cell Biol. 18, 174–183 (2008).

    Article  CAS  PubMed  Google Scholar 

  47. Skruzny, M. et al. An endoribonuclease functionally linked to perinuclear mRNP quality control associates with the nuclear pore complexes. PLoS Biol. 7, e8 (2009).

    Article  PubMed  CAS  Google Scholar 

  48. Vinciguerra, P., Iglesias, N., Camblong, J., Zenklusen, D. & Stutz, F. Perinuclear Mlp proteins downregulate gene expression in response to a defect in mRNA export. EMBO J. 24, 813–823 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Carmody, S. R., Tran, E. J., Apponi, L. H., Corbett, A. H. & Wente, S. R. The mitogen-activated protein kinase Slt2 regulates nuclear retention of non-heat shock mRNAs during heat shock-induced stress. Mol. Cell. Biol. 30, 5168–5179 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Iglesias, N. et al. Ubiquitin-mediated mRNP dynamics and surveillance prior to budding yeast mRNA export. Genes Dev. 24, 1927–1938 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Duncan, K., Umen, J. G. & Guthrie, C. A putative ubiquitin ligase required for efficient mRNA export differentially affects hnRNP transport. Curr. Biol. 10, 687–696 (2000).

    Article  CAS  PubMed  Google Scholar 

  52. Lund, M. K. & Guthrie, C. The DEAD-box protein Dbp5p is required to dissociate Mex67p from exported mRNPs at the nuclear rim. Mol. Cell 20, 645–651 (2005).

    Article  CAS  PubMed  Google Scholar 

  53. Dikic, I., Wakatsuki, S. & Walters, K. J. Ubiquitin-binding domains — from structures to functions. Nature Rev. Mol. Cell Biol. 10, 659–671 (2009).

    Article  CAS  Google Scholar 

  54. Powrie, E. A., Zenklusen, D. & Singer, R. H. A nucleoporin, Nup60p, affects the nuclear and cytoplasmic localization of ASH1 mRNA in S. cerevisiae. RNA 17, 134–144 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Lewis, A., Felberbaum, R. & Hochstrasser, M. A nuclear envelope protein linking nuclear pore basket assembly, SUMO protease regulation, and mRNA surveillance. J. Cell Biol. 178, 813–827 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Hannich, J. T. et al. Defining the SUMO-modified proteome by multiple approaches in Saccharomyces cerevisiae. J. Biol. Chem. 280, 4102–4110 (2005).

    Article  CAS  PubMed  Google Scholar 

  57. Fasken, M. B., Stewart, M. & Corbett, A. H. Functional significance of the interaction between the mRNA-binding protein, Nab2, and the nuclear pore-associated protein, Mlp1, in mRNA export. J. Biol. Chem. 283, 27130–27143 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Grant, R. P. et al. Structure of the N-terminal Mlp1-binding domain of the Saccharomyces cerevisiae mRNA-binding protein, Nab2. J. Mol. Biol. 376, 1048–1059 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Green, D. M., Johnson, C. P., Hagan, H. & Corbett, A. H. The C-terminal domain of myosin-like protein 1 (Mlp1p) is a docking site for heterogeneous nuclear ribonucleoproteins that are required for mRNA export. Proc. Natl Acad. Sci. USA 100, 1010–1015 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Grunwald, D. & Singer, R. H. In vivo imaging of labelled endogenous β-actin mRNA during nucleocytoplasmic transport. Nature 467, 604–607 (2010).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  61. Mor, A. et al. Dynamics of single mRNP nucleocytoplasmic transport and export through the nuclear pore in living cells. Nature Cell Biol. 12, 543–552 (2010).

    Article  CAS  PubMed  Google Scholar 

  62. Alcazar-Roman, A. R., Tran, E. J., Guo, S. & Wente, S. R. Inositol hexakisphosphate and Gle1 activate the DEAD-box protein Dbp5 for nuclear mRNA export. Nature Cell Biol. 8, 711–716 (2006).

    Article  CAS  PubMed  Google Scholar 

  63. Weirich, C. S. et al. Activation of the DExD/H-box protein Dbp5 by the nuclear-pore protein Gle1 and its coactivator InsP6 is required for mRNA export. Nature Cell Biol. 8, 668–676 (2006).

    Article  CAS  PubMed  Google Scholar 

  64. Tran, E. J., Zhou, Y., Corbett, A. H. & Wente, S. R. The DEAD-box protein Dbp5 controls mRNA export by triggering specific RNA:protein remodeling events. Mol. Cell 28, 850–859 (2007).

    Article  CAS  PubMed  Google Scholar 

  65. Bolger, T. A., Folkmann, A. W., Tran, E. J. & Wente, S. R. The mRNA export factor Gle1 and inositol hexakisphosphate regulate distinct stages of translation. Cell 134, 624–633 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Alcazar-Roman, A. R., Bolger, T. A. & Wente, S. R. Control of mRNA export and translation termination by inositol hexakisphosphate requires specific interaction with Gle1. J. Biol. Chem. 285, 16683–16692 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Ives, E. B., Nichols, J., Wente, S. R. & York, J. D. Biochemical and functional characterization of inositol 1,3,4,5,6-pentakisphosphate 2-kinases. J. Biol. Chem. 275, 36575–36583 (2000).

    Article  CAS  PubMed  Google Scholar 

  68. Batisse, J., Batisse, C., Budd, A., Bottcher, B. & Hurt, E. Purification of nuclear poly(A)-binding protein Nab2 reveals association with the yeast transcriptome and a messenger ribonucleoprotein core structure. J. Biol. Chem. 284, 34911–34917 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Kim Guisbert, K., Duncan, K., Li, H. & Guthrie, C. Functional specificity of shuttling hnRNPs revealed by genome-wide analysis of their RNA binding profiles. RNA 11, 383–393 (2005).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  70. Rollenhagen, C., Hodge, C. A. & Cole, C. N. Following temperature stress, export of heat shock mRNA occurs efficiently in cells with mutations in genes normally important for mRNA export. Eukaryot. Cell 6, 505–513 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Krebber, H., Taura, T., Lee, M. S. & Silver, P. A. Uncoupling of the hnRNP Npl3p from mRNAs during the stress-induced block in mRNA export. Genes Dev. 13, 1994–2004 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Mehlin, H., Daneholt, B. & Skoglund, U. Translocation of a specific premessenger ribonucleoprotein particle through the nuclear pore studied with electron microscope tomography. Cell 69, 605–613 (1992).

    Article  CAS  PubMed  Google Scholar 

  73. Tomecki, R., Drazkowska, K. & Dziembowski, A. Mechanisms of RNA degradation by the eukaryotic exosome. Chembiochem 11, 938–945 (2010).

    Article  CAS  PubMed  Google Scholar 

  74. LaCava, J. et al. RNA degradation by the exosome is promoted by a nuclear polyadenylation complex. Cell 121, 713–724 (2005).

    Article  CAS  PubMed  Google Scholar 

  75. Vanacova, S. et al. A new yeast poly(A) polymerase complex involved in RNA quality control. PLoS Biol. 3, e189 (2005).

    Article  PubMed  CAS  Google Scholar 

  76. Wyers, F. et al. Cryptic pol II transcripts are degraded by a nuclear quality control pathway involving a new poly(A) polymerase. Cell 121, 725–737 (2005).

    Article  CAS  PubMed  Google Scholar 

  77. Gilbert, W., Siebel, C. W. & Guthrie, C. Phosphorylation by Sky1p promotes Npl3p shuttling and mRNA dissociation. RNA 7, 302–313 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. McBride, A. E., Conboy, A. K., Brown, S. P., Ariyachet, C. & Rutledge, K. L. Specific sequences within arginine–glycine-rich domains affect mRNA-binding protein function. Nucleic Acids Res. 37, 4322–4330 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. McBride, A. E. et al. Arginine methylation of yeast mRNA-binding protein Npl3 directly affects its function, nuclear export, and intranuclear protein interactions. J. Biol. Chem. 280, 30888–30898 (2005).

    Article  CAS  PubMed  Google Scholar 

  80. Siebel, C. W. & Guthrie, C. The essential yeast RNA binding protein Np13p is methylated. Proc. Natl Acad. Sci. USA 93, 13641–13646 (1996).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. Bucheli, M. E. & Buratowski, S. Npl3 is an antagonist of mRNA 3′ end formation by RNA polymerase II. EMBO J. 24, 2150–2160 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Bucheli, M. E., He, X., Kaplan, C. D., Moore, C. L. & Buratowski, S. Polyadenylation site choice in yeast is affected by competition between Npl3 and polyadenylation factor CFI. RNA 13, 1756–1764 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Dermody, J. L. et al. Unphosphorylated SR-like protein Npl3 stimulates RNA polymerase II elongation. PLoS ONE 3, e3273 (2008).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  84. Lund, M. K., Kress, T. L. & Guthrie, C. Autoregulation of Npl3, a yeast SR protein, requires a novel downstream region and serine phosphorylation. Mol. Cell. Biol. 28, 3873–3881 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Gilbert, W. & Guthrie, C. The Glc7p nuclear phosphatase promotes mRNA export by facilitating association of Mex67p with mRNA. Mol. Cell 13, 201–212 (2004).

    Article  CAS  PubMed  Google Scholar 

  86. Huang, Y. & Steitz, J. A. SRprises along a messenger's journey. Mol. Cell 17, 613–615 (2005).

    Article  CAS  PubMed  Google Scholar 

  87. Estrella, L. A., Wilkinson, M. F. & Gonzalez, C. I. The shuttling protein Npl3 promotes translation termination accuracy in Saccharomyces cerevisiae. J. Mol. Biol. 394, 410–422 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Windgassen, M. et al. Yeast shuttling SR proteins Npl3p, Gbp2p, and Hrb1p are part of the translating mRNPs, and Npl3p can function as a translational repressor. Mol. Cell. Biol. 24, 10479–10491 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. Henry, M. F. & Silver, P. A. A novel methyltransferase (Hmt1p) modifies poly(A)+-RNA-binding proteins. Mol. Cell. Biol. 16, 3668–3678 (1996).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  90. Yu, M. C. et al. Arginine methyltransferase affects interactions and recruitment of mRNA processing and export factors. Genes Dev. 18, 2024–2035 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. Shen, E. C. et al. Arginine methylation facilitates the nuclear export of hnRNP proteins. Genes Dev. 12, 679–691 (1998).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Chen, Y. C. et al. Protein arginine methylation facilitates cotranscriptional recruitment of pre-mRNA splicing factors. Mol. Cell. Biol. 30, 5245–5256 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Wong, C. M. et al. Yeast arginine methyltransferase Hmt1p regulates transcription elongation and termination by methylating Npl3p. Nucleic Acids Res. 38, 2217–2228 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Hung., M. L., Hautbergue, G. M., Snijders, A. P., Dickman, M. J. & Wilson, S. A. Arginine methylation of REF/ALY promotes efficient handover of mRNA to TAP/NXF1. Nucleic Acids Res. 38, 3351–3361 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. Montpetit, B. et al. A conserved mechanism of DEAD-box ATPase activation by nucleoporins and InsP6 in mRNA export. Nature 472, 238–242 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  96. Shuman, S. What messenger RNA capping tells us about eukaryotic evolution. Nature Rev. Mol. Cell Biol. 3, 619–625 (2002).

    Article  CAS  Google Scholar 

  97. Green, D. M. et al. Nab2p is required for poly(A) RNA export in Saccharomyces cerevisiae and is regulated by arginine methylation via Hmt1p. J. Biol. Chem. 277, 7752–7760 (2002).

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We are grateful to our anonymous reviewers for their comments and suggestions to improve this manuscript and apologize to many colleagues whose work could not be cited because of lack of space.

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Tutucci, E., Stutz, F. Keeping mRNPs in check during assembly and nuclear export. Nat Rev Mol Cell Biol 12, 377–384 (2011). https://doi.org/10.1038/nrm3119

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