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Nuclear export of different classes of RNA is mediated by specific factors.

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  • 1. European Molecular Biology Laboratory, Heidelberg, Germany.
      Authors
    • Jarmolowski A 1
    (1 author)

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The Journal of Cell Biology, 01 Mar 1994, 124(5):627-635
https://doi.org/10.1083/jcb.124.5.627 PMID: 7509815 PMCID: PMC2119953

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Abstract 

Various classes of RNA are exported from the nucleus to the cytoplasm, including transcripts of RNA polymerase I (large ribosomal RNAs), II (U-rich small nuclear RNAs [U snRNAs], mRNAs), and III (tRNAs, 5S RNA). Here, evidence is presented that some steps in the export of various classes of nuclear RNA are mediated by specific rather than common factors. Using microinjection into Xenopus oocytes, it is shown that a tRNA, a U snRNA, and an mRNA competitively inhibit their own export at concentrations at which they have no effect on the export of heterologous RNAs. While the export of both U snRNAs and mRNAs is enhanced by their 7-methyl guanosine cap structures, factors recognizing this structure are found to be limiting in concentration only in the case of U snRNAs. In addition to the specific factors, evidence for steps in the export process that may be common to at least some classes of RNA are provided by experiments in which synthetic homopolymeric RNAs are used as inhibitors.

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J Cell Biol. 1994 Mar 1; 124(5): 627–635.
PMCID: PMC2119953
PMID: 7509815

Nuclear export of different classes of RNA is mediated by specific factors

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Abstract

Various classes of RNA are exported from the nucleus to the cytoplasm, including transcripts of RNA polymerase I (large ribosomal RNAs), II (U- rich small nuclear RNAs [U snRNAs], mRNAs), and III (tRNAs, 5S RNA). Here, evidence is presented that some steps in the export of various classes of nuclear RNA are mediated by specific rather than common factors. Using microinjection into Xenopus oocytes, it is shown that a tRNA, a U snRNA, and an mRNA competitively inhibit their own export at concentrations at which they have no effect on the export of heterologous RNAs. While the export of both U snRNAs and mRNAs is enhanced by their 7-methyl guanosine cap structures, factors recognizing this structure are found to be limiting in concentration only in the case of U snRNAs. In addition to the specific factors, evidence for steps in the export process that may be common to at least some classes of RNA are provided by experiments in which synthetic homopolymeric RNAs are used as inhibitors.

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Selected References

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  • Amberg DC, Goldstein AL, Cole CN. Isolation and characterization of RAT1: an essential gene of Saccharomyces cerevisiae required for the efficient nucleocytoplasmic trafficking of mRNA. Genes Dev. 1992 Jul;6(7):1173–1189. [Abstract] [Google Scholar]
  • Amberg DC, Fleischmann M, Stagljar I, Cole CN, Aebi M. Nuclear PRP20 protein is required for mRNA export. EMBO J. 1993 Jan;12(1):233–241. [Europe PMC free article] [Abstract] [Google Scholar]
  • Bataillé N, Helser T, Fried HM. Cytoplasmic transport of ribosomal subunits microinjected into the Xenopus laevis oocyte nucleus: a generalized, facilitated process. J Cell Biol. 1990 Oct;111(4):1571–1582. [Europe PMC free article] [Abstract] [Google Scholar]
  • Dargemont C, Kühn LC. Export of mRNA from microinjected nuclei of Xenopus laevis oocytes. J Cell Biol. 1992 Jul;118(1):1–9. [Europe PMC free article] [Abstract] [Google Scholar]
  • De Robertis EM, Lienhard S, Parisot RF. Intracellular transport of microinjected 5S and small nuclear RNAs. Nature. 1982 Feb 18;295(5850):572–577. [Abstract] [Google Scholar]
  • Dingwall C, Laskey R. The nuclear membrane. Science. 1992 Nov 6;258(5084):942–947. [Abstract] [Google Scholar]
  • Dreyfuss G, Matunis MJ, Piñol-Roma S, Burd CG. hnRNP proteins and the biogenesis of mRNA. Annu Rev Biochem. 1993;62:289–321. [Abstract] [Google Scholar]
  • Dworetzky SI, Feldherr CM. Translocation of RNA-coated gold particles through the nuclear pores of oocytes. J Cell Biol. 1988 Mar;106(3):575–584. [Europe PMC free article] [Abstract] [Google Scholar]
  • Eckner R, Ellmeier W, Birnstiel ML. Mature mRNA 3' end formation stimulates RNA export from the nucleus. EMBO J. 1991 Nov;10(11):3513–3522. [Europe PMC free article] [Abstract] [Google Scholar]
  • Featherstone C, Darby MK, Gerace L. A monoclonal antibody against the nuclear pore complex inhibits nucleocytoplasmic transport of protein and RNA in vivo. J Cell Biol. 1988 Oct;107(4):1289–1297. [Europe PMC free article] [Abstract] [Google Scholar]
  • Fischer U, Lührmann R. An essential signaling role for the m3G cap in the transport of U1 snRNP to the nucleus. Science. 1990 Aug 17;249(4970):786–790. [Abstract] [Google Scholar]
  • Fischer U, Darzynkiewicz E, Tahara SM, Dathan NA, Lührmann R, Mattaj IW. Diversity in the signals required for nuclear accumulation of U snRNPs and variety in the pathways of nuclear transport. J Cell Biol. 1991 May;113(4):705–714. [Europe PMC free article] [Abstract] [Google Scholar]
  • Fischer U, Sumpter V, Sekine M, Satoh T, Lührmann R. Nucleo-cytoplasmic transport of U snRNPs: definition of a nuclear location signal in the Sm core domain that binds a transport receptor independently of the m3G cap. EMBO J. 1993 Feb;12(2):573–583. [Europe PMC free article] [Abstract] [Google Scholar]
  • Forrester W, Stutz F, Rosbash M, Wickens M. Defects in mRNA 3'-end formation, transcription initiation, and mRNA transport associated with the yeast mutation prp20: possible coupling of mRNA processing and chromatin structure. Genes Dev. 1992 Oct;6(10):1914–1926. [Abstract] [Google Scholar]
  • Garcia-Bustos J, Heitman J, Hall MN. Nuclear protein localization. Biochim Biophys Acta. 1991 Mar 7;1071(1):83–101. [Abstract] [Google Scholar]
  • Gerace L. Molecular trafficking across the nuclear pore complex. Curr Opin Cell Biol. 1992 Aug;4(4):637–645. [Abstract] [Google Scholar]
  • Goldfarb DS, Gariépy J, Schoolnik G, Kornberg RD. Synthetic peptides as nuclear localization signals. Nature. 1986 Aug 14;322(6080):641–644. [Abstract] [Google Scholar]
  • Guddat U, Bakken AH, Pieler T. Protein-mediated nuclear export of RNA: 5S rRNA containing small RNPs in xenopus oocytes. Cell. 1990 Feb 23;60(4):619–628. [Abstract] [Google Scholar]
  • Hamm J, Mattaj IW. Monomethylated cap structures facilitate RNA export from the nucleus. Cell. 1990 Oct 5;63(1):109–118. [Abstract] [Google Scholar]
  • Hamm J, Kazmaier M, Mattaj IW. In vitro assembly of U1 snRNPs. EMBO J. 1987 Nov;6(11):3479–3485. [Europe PMC free article] [Abstract] [Google Scholar]
  • Hamm J, Dathan NA, Mattaj IW. Functional analysis of mutant Xenopus U2 snRNAs. Cell. 1989 Oct 6;59(1):159–169. [Abstract] [Google Scholar]
  • Izaurralde E, Mattaj IW. Transport of RNA between nucleus and cytoplasm. Semin Cell Biol. 1992 Aug;3(4):279–288. [Abstract] [Google Scholar]
  • Izaurralde E, Stepinski J, Darzynkiewicz E, Mattaj IW. A cap binding protein that may mediate nuclear export of RNA polymerase II-transcribed RNAs. J Cell Biol. 1992 Sep;118(6):1287–1295. [Europe PMC free article] [Abstract] [Google Scholar]
  • Jarmolowski A, Mattaj IW. The determinants for Sm protein binding to Xenopus U1 and U5 snRNAs are complex and non-identical. EMBO J. 1993 Jan;12(1):223–232. [Europe PMC free article] [Abstract] [Google Scholar]
  • Kadowaki T, Zhao Y, Tartakoff AM. A conditional yeast mutant deficient in mRNA transport from nucleus to cytoplasm. Proc Natl Acad Sci U S A. 1992 Mar 15;89(6):2312–2316. [Europe PMC free article] [Abstract] [Google Scholar]
  • Kadowaki T, Goldfarb D, Spitz LM, Tartakoff AM, Ohno M. Regulation of RNA processing and transport by a nuclear guanine nucleotide release protein and members of the Ras superfamily. EMBO J. 1993 Jul;12(7):2929–2937. [Europe PMC free article] [Abstract] [Google Scholar]
  • Khanna-Gupta A, Ware VC. Nucleocytoplasmic transport of ribosomes in a eukaryotic system: is there a facilitated transport process? Proc Natl Acad Sci U S A. 1989 Mar;86(6):1791–1795. [Europe PMC free article] [Abstract] [Google Scholar]
  • Maquat LE. Nuclear mRNA export. Curr Opin Cell Biol. 1991 Dec;3(6):1004–1012. [Abstract] [Google Scholar]
  • Mattaj IW, De Robertis EM. Nuclear segregation of U2 snRNA requires binding of specific snRNP proteins. Cell. 1985 Jan;40(1):111–118. [Abstract] [Google Scholar]
  • Mehlin H, Daneholt B, Skoglund U. Translocation of a specific premessenger ribonucleoprotein particle through the nuclear pore studied with electron microscope tomography. Cell. 1992 May 15;69(4):605–613. [Abstract] [Google Scholar]
  • Michaud N, Goldfarb DS. Multiple pathways in nuclear transport: the import of U2 snRNP occurs by a novel kinetic pathway. J Cell Biol. 1991 Jan;112(2):215–223. [Europe PMC free article] [Abstract] [Google Scholar]
  • Michaud N, Goldfarb D. Microinjected U snRNAs are imported to oocyte nuclei via the nuclear pore complex by three distinguishable targeting pathways. J Cell Biol. 1992 Feb;116(4):851–861. [Europe PMC free article] [Abstract] [Google Scholar]
  • Neuman de Vegvar HE, Dahlberg JE. Nucleocytoplasmic transport and processing of small nuclear RNA precursors. Mol Cell Biol. 1990 Jul;10(7):3365–3375. [Europe PMC free article] [Abstract] [Google Scholar]
  • Newmeyer DD. The nuclear pore complex and nucleocytoplasmic transport. Curr Opin Cell Biol. 1993 Jun;5(3):395–407. [Abstract] [Google Scholar]
  • Nigg EA, Baeuerle PA, Lührmann R. Nuclear import-export: in search of signals and mechanisms. Cell. 1991 Jul 12;66(1):15–22. [Abstract] [Google Scholar]
  • Ohno M, Kataoka N, Shimura Y. A nuclear cap binding protein from HeLa cells. Nucleic Acids Res. 1990 Dec 11;18(23):6989–6995. [Europe PMC free article] [Abstract] [Google Scholar]
  • Piñol-Roma S, Dreyfuss G. Transcription-dependent and transcription-independent nuclear transport of hnRNP proteins. Science. 1991 Jul 19;253(5017):312–314. [Abstract] [Google Scholar]
  • Piñol-Roma S, Dreyfuss G. Shuttling of pre-mRNA binding proteins between nucleus and cytoplasm. Nature. 1992 Feb 20;355(6362):730–732. [Abstract] [Google Scholar]
  • Piñol-Roma S, Dreyfuss G. hnRNP proteins: localization and transport between the nucleus and the cytoplasm. Trends Cell Biol. 1993 May;3(5):151–155. [Abstract] [Google Scholar]
  • Scherly D, Boelens W, Dathan NA, van Venrooij WJ, Mattaj IW. Major determinants of the specificity of interaction between small nuclear ribonucleoproteins U1A and U2B'' and their cognate RNAs. Nature. 1990 Jun 7;345(6275):502–506. [Abstract] [Google Scholar]
  • Sillekens PT, Habets WJ, Beijer RP, van Venrooij WJ. cDNA cloning of the human U1 snRNA-associated A protein: extensive homology between U1 and U2 snRNP-specific proteins. EMBO J. 1987 Dec 1;6(12):3841–3848. [Europe PMC free article] [Abstract] [Google Scholar]
  • Silver PA. How proteins enter the nucleus. Cell. 1991 Feb 8;64(3):489–497. [Abstract] [Google Scholar]
  • Singh R, Green MR. Sequence-specific binding of transfer RNA by glyceraldehyde-3-phosphate dehydrogenase. Science. 1993 Jan 15;259(5093):365–368. [Abstract] [Google Scholar]
  • Stevens BJ, Swift H. RNA transport from nucleus to cytoplasm in Chironomus salivary glands. J Cell Biol. 1966 Oct;31(1):55–77. [Europe PMC free article] [Abstract] [Google Scholar]
  • Terns MP, Dahlberg JE, Lund E. Multiple cis-acting signals for export of pre-U1 snRNA from the nucleus. Genes Dev. 1993 Oct;7(10):1898–1908. [Abstract] [Google Scholar]
  • Tobian JA, Drinkard L, Zasloff M. tRNA nuclear transport: defining the critical regions of human tRNAimet by point mutagenesis. Cell. 1985 Dec;43(2 Pt 1):415–422. [Abstract] [Google Scholar]
  • Wickens MP, Gurdon JB. Post-transcriptional processing of simian virus 40 late transcripts in injected frog oocytes. J Mol Biol. 1983 Jan 5;163(1):1–26. [Abstract] [Google Scholar]
  • Zasloff M. tRNA transport from the nucleus in a eukaryotic cell: carrier-mediated translocation process. Proc Natl Acad Sci U S A. 1983 Nov;80(21):6436–6440. [Europe PMC free article] [Abstract] [Google Scholar]
  • Zasloff M, Rosenberg M, Santos T. Impaired nuclear transport of a human variant tRNAiMet. Nature. 1982 Nov 4;300(5887):81–84. [Abstract] [Google Scholar]
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