Home LiteratureArticle Details
PMID: 18096623 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Role of poly (A) tail as an identity element for mRNA nuclear export.

Nucleic acids research ·Vol. 36 ·No. 3 ·2008-02-00 ·Pages 1037-49

Fuke H, Ohno M

Abstract

Different RNA species are rigorously discriminated and exported by distinct export factors, but this discrimination mechanism remains largely unknown. We previously showed, by RNA microinjection experiments, that intronless mRNAs are discriminated from U snRNAs based on their difference in RNA length. However, it was unclear how they are discriminated in the natural situation in which their nascent transcripts emerge progressively during transcription. We hypothesized that transcription from the corresponding promoters is important for this discrimination. Here we show that contrary to our hypothesis, the discrimination process was not significantly influenced by whether transcription occurred from an mRNA- versus a U snRNA-type promoter. Rather, the features of transcribed RNAs determined the RNA identity, consistent with our previous results of RNA microinjection. Moreover, we found that the poly (A) tail can function as an identity element for mRNA export. The presence of a poly (A) tail of an appropriate length committed otherwise short Pol II transcripts to the mRNA export pathway in a dominant manner, indicating that the poly (A) tail either contributes to increasing the RNA length or functions as a platform to recruit mRNA export factors. Our results reveal a novel function of the poly (A) tail in mRNA export.

MeSH Terms
3' Untranslated Regions/chemistry Active Transport, Cell Nucleus Animals Cell Nucleus/metabolism Humans Poly A/chemistry,metabolism Polyadenylation Promoter Regions, Genetic RNA Transport RNA, Messenger/chemistry,metabolism RNA, Small Nuclear/chemistry,metabolism Regulatory Sequences, Ribonucleic Acid Transcription, Genetic Xenopus laevis
Chemicals
3' Untranslated Regions RNA, Messenger RNA, Small Nuclear Regulatory Sequences, Ribonucleic Acid Poly A
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Fuke Hiroyuki
Institute for Virus Research, Kyoto University, Kyoto 606-8507, Japan.
Ohno Mutsuhito
References (64)
64 references, click to expand
  1. Human mRNA export machinery recruited to the 5' end of mRNA.
    Cell. 2006 Dec 29;127(7):1389-400 PMID: 17190602
  2. Biochemical analysis of TREX complex recruitment to intronless and intron-containing yeast genes.
    EMBO J. 2004 Jul 7;23(13):2620-31 PMID: 15192704
  3. A molecular link between SR protein dephosphorylation and mRNA export.
    Proc Natl Acad Sci U S A. 2004 Jun 29;101(26):9666-70 PMID: 15210956
  4. A synthetic A tail rescues yeast nuclear accumulation of a ribozyme-terminated transcript.
    RNA. 2004 Dec;10(12):1888-99 PMID: 15547135
  5. Strange bedfellows: polyadenylation factors at the promoter.
    Genes Dev. 2003 Jun 1;17(11):1321-7 PMID: 12782649
  6. Nuclear export of the yeast mRNA-binding protein Nab2 is linked to a direct interaction with Gfd1 and to Gle1 function.
    J Biol Chem. 2004 Aug 20;279(34):35384-91 PMID: 15208322
  7. Dynamic nuclear pore complexes: life on the edge.
    Cell. 2006 Jun 16;125(6):1041-53 PMID: 16777596
  8. New perspectives on connecting messenger RNA 3' end formation to transcription.
    Curr Opin Cell Biol. 2004 Jun;16(3):272-8 PMID: 15145351
  9. Integrator, a multiprotein mediator of small nuclear RNA processing, associates with the C-terminal repeat of RNA polymerase II.
    Cell. 2005 Oct 21;123(2):265-76 PMID: 16239144
  10. Dual requirement for yeast hnRNP Nab2p in mRNA poly(A) tail length control and nuclear export.
    EMBO J. 2002 Apr 2;21(7):1800-10 PMID: 11927564
  11. Tap and NXT promote translation of unspliced mRNA.
    Genes Dev. 2003 Dec 15;17(24):3075-86 PMID: 14701875
  12. A cap-binding protein complex mediating U snRNA export.
    Nature. 1995 Aug 24;376(6542):709-12 PMID: 7651522
  13. PHAX, a mediator of U snRNA nuclear export whose activity is regulated by phosphorylation.
    Cell. 2000 Apr 14;101(2):187-98 PMID: 10786834
  14. Nuclear RNA export.
    J Cell Sci. 2003 Feb 15;116(Pt 4):587-97 PMID: 12538759
  15. Evidence that poly(A) binding protein has an evolutionarily conserved function in facilitating mRNA biogenesis and export.
    RNA. 2003 Dec;9(12):1476-90 PMID: 14624004
  16. Yeast poly(A)-binding protein Pab1 shuttles between the nucleus and the cytoplasm and functions in mRNA export.
    RNA. 2005 Apr;11(4):517-31 PMID: 15769879
  17. Mex67p, a novel factor for nuclear mRNA export, binds to both poly(A)+ RNA and nuclear pores.
    EMBO J. 1997 Jun 2;16(11):3256-71 PMID: 9214641
  18. NXF-2, REF-1, and REF-2 affect the choice of nuclear export pathway for tra-2 mRNA in C. elegans.
    Mol Cell. 2004 Jun 4;14(5):599-610 PMID: 15175155
  19. The simian retrovirus-1 constitutive transport element, unlike the HIV-1 RRE, uses factors required for cellular mRNA export.
    Curr Biol. 1997 Sep 1;7(9):619-28 PMID: 9285715
  20. Splicing enhances translation in mammalian cells: an additional function of the exon junction complex.
    Genes Dev. 2004 Jan 15;18(2):210-22 PMID: 14752011
  21. Quality control of messenger ribonucleoprotein particles in the nucleus and at the pore.
    Curr Opin Cell Biol. 2005 Jun;17(3):294-301 PMID: 15901500
  22. REF proteins mediate the export of spliced and unspliced mRNAs from the nucleus.
    Proc Natl Acad Sci U S A. 2001 Jan 30;98(3):1030-5 PMID: 11158589
  23. Spliceosomal UsnRNP biogenesis, structure and function.
    Curr Opin Cell Biol. 2001 Jun;13(3):290-301 PMID: 11343899
  24. Poly(A)-binding proteins: multifunctional scaffolds for the post-transcriptional control of gene expression.
    Genome Biol. 2003;4(7):223 PMID: 12844354
  25. The 3' ends of human pre-snRNAs are produced by RNA polymerase II CTD-dependent RNA processing.
    EMBO J. 2003 Sep 1;22(17):4544-54 PMID: 12941705
  26. SR proteins preferentially associate with mRNAs in the nucleus and facilitate their export to the cytoplasm.
    Genes Cells. 2004 Oct;9(10):959-65 PMID: 15461666
  27. Yeast poly(A)-binding protein, Pab1, and PAN, a poly(A) nuclease complex recruited by Pab1, connect mRNA biogenesis to export.
    Genes Dev. 2005 Jan 1;19(1):90-103 PMID: 15630021
  28. RNA length defines RNA export pathway.
    Genes Dev. 2004 Sep 1;18(17):2074-85 PMID: 15314030
  29. Nuclear export of different classes of RNA is mediated by specific factors.
    J Cell Biol. 1994 Mar;124(5):627-35 PMID: 7509815
  30. REF, an evolutionary conserved family of hnRNP-like proteins, interacts with TAP/Mex67p and participates in mRNA nuclear export.
    RNA. 2000 Apr;6(4):638-50 PMID: 10786854
  31. Small nuclear RNA genes: a model system to study fundamental mechanisms of transcription.
    J Biol Chem. 2001 Jul 20;276(29):26733-6 PMID: 11390411
  32. The spliceosome deposits multiple proteins 20-24 nucleotides upstream of mRNA exon-exon junctions.
    EMBO J. 2000 Dec 15;19(24):6860-9 PMID: 11118221
  33. Formation of the 3' end of U1 snRNA requires compatible snRNA promoter elements.
    Cell. 1986 Oct 24;47(2):249-58 PMID: 3768956
  34. Monomethylated cap structures facilitate RNA export from the nucleus.
    Cell. 1990 Oct 5;63(1):109-18 PMID: 2208274
  35. Schizosaccharomyces pombe spPABP, a homologue of Saccharomyces cerevisiae Pab1p, is a non-essential, shuttling protein that facilitates mRNA export.
    Yeast. 2002 Jun 30;19(9):803-10 PMID: 12112233
  36. Exon junction complexes mediate the enhancing effect of splicing on mRNA expression.
    Proc Natl Acad Sci U S A. 2003 Sep 30;100(20):11327-32 PMID: 12972633
  37. A nuclear cap binding protein from HeLa cells.
    Nucleic Acids Res. 1990 Dec 11;18(23):6989-95 PMID: 2148205
  38. Splicing factors SRp20 and 9G8 promote the nucleocytoplasmic export of mRNA.
    Mol Cell. 2001 Apr;7(4):899-905 PMID: 11336712
  39. The interaction between cap-binding complex and RNA export factor is required for intronless mRNA export.
    J Biol Chem. 2007 May 25;282(21):15645-51 PMID: 17363367
  40. CRM1 is an export receptor for leucine-rich nuclear export signals.
    Cell. 1997 Sep 19;90(6):1051-60 PMID: 9323133
  41. Structure and function of poly(A) binding proteins.
    Biochim Biophys Acta. 2004 May 25;1678(2-3):67-84 PMID: 15157733
  42. TAP, the human homolog of Mex67p, mediates CTE-dependent RNA export from the nucleus.
    Mol Cell. 1998 Apr;1(5):649-59 PMID: 9660949
  43. CRM1 is responsible for intracellular transport mediated by the nuclear export signal.
    Nature. 1997 Nov 20;390(6657):308-11 PMID: 9384386
  44. Exportin 1 (Crm1p) is an essential nuclear export factor.
    Cell. 1997 Sep 19;90(6):1041-50 PMID: 9323132
  45. TREX is a conserved complex coupling transcription with messenger RNA export.
    Nature. 2002 May 16;417(6886):304-8 PMID: 11979277
  46. Recruitment of the human TREX complex to mRNA during splicing.
    Genes Dev. 2005 Jul 1;19(13):1512-7 PMID: 15998806
  47. Characterization and subcellular localization of ribonuclease H activities from Xenopus laevis oocytes.
    J Biol Chem. 1994 Oct 7;269(40):25185-92 PMID: 7929207
  48. SR splicing factors serve as adapter proteins for TAP-dependent mRNA export.
    Mol Cell. 2003 Mar;11(3):837-43 PMID: 12667464
  49. New perspectives on nuclear transport.
    Annu Rev Genet. 2001;35:341-64 PMID: 11700287
  50. Early formation of mRNP: license for export or quality control?
    Mol Cell. 2003 May;11(5):1129-38 PMID: 12769839
  51. Cotranscriptional coupling of splicing factor recruitment and precursor messenger RNA splicing in mammalian cells.
    Nat Struct Mol Biol. 2006 Sep;13(9):815-22 PMID: 16921380
  52. The Y14 protein communicates to the cytoplasm the position of exon-exon junctions.
    EMBO J. 2001 Apr 17;20(8):2062-8 PMID: 11296238
  53. 3' end formation of U1 snRNA precursors is coupled to transcription from snRNA promoters.
    Cell. 1986 Oct 24;47(2):259-66 PMID: 3021336
  54. Hypophosphorylated ASF/SF2 binds TAP and is present in messenger ribonucleoproteins.
    J Biol Chem. 2004 Jul 23;279(30):31745-9 PMID: 15184380
  55. Yra1p, a conserved nuclear RNA-binding protein, interacts directly with Mex67p and is required for mRNA export.
    EMBO J. 2000 Feb 1;19(3):410-20 PMID: 10722314
  56. Identity elements used in export of mRNAs.
    Mol Cell. 2002 Mar;9(3):659-71 PMID: 11931772
  57. Rules of engagement: co-transcriptional recruitment of pre-mRNA processing factors.
    Curr Opin Cell Biol. 2005 Jun;17(3):251-6 PMID: 15901493
  58. SR proteins function in coupling RNAP II transcription to pre-mRNA splicing.
    Mol Cell. 2007 Jun 22;26(6):867-81 PMID: 17588520
  59. The protein Aly links pre-messenger-RNA splicing to nuclear export in metazoans.
    Nature. 2000 Sep 21;407(6802):401-5 PMID: 11014198
  60. The Mex67p-mediated nuclear mRNA export pathway is conserved from yeast to human.
    EMBO J. 1999 May 4;18(9):2593-609 PMID: 10228171
  61. Formation of export-competent mRNP: escaping nuclear destruction.
    Curr Opin Cell Biol. 2005 Jun;17(3):287-93 PMID: 15901499
  62. Identification of the factors that interact with NCBP, an 80 kDa nuclear cap binding protein.
    Nucleic Acids Res. 1995 Sep 25;23(18):3638-41 PMID: 7478990
  63. The human U1 snRNA promoter and enhancer do not direct synthesis of messenger RNA.
    Nucleic Acids Res. 1988 Jul 11;16(13):5827-40 PMID: 2456520
  64. 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 U S A. 2003 Feb 4;100(3):1010-5 PMID: 12531921
Article Info
Journal
Nucleic acids research
Abbr.
Nucleic Acids Res
ISSN
1362-4962
Published
2008-02-00
Epub
2007-00-20
Pages
1037-49
Language
English
Region
England
NLM ID
0411011
PMCID
PMC2241894
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com