A Transcriptome-wide Atlas of RNP Composition Reveals Diverse Classes of mRNAs and lncRNAs

被引:186
作者
Tuck, Alex Charles [1 ]
Tollervey, David [1 ]
机构
[1] Univ Edinburgh, Wellcome Trust Ctr Cell Biol, Edinburgh EH9 3JR, Midlothian, Scotland
基金
英国惠康基金;
关键词
POLY(A) TAIL LENGTH; BINDING PROTEIN; BIDIRECTIONAL PROMOTERS; STRUCTURAL BASIS; NUCLEAR EXOSOME; TERMINATION; DEGRADATION; EXPORT; GENE; SPECIFICITY;
D O I
10.1016/j.cell.2013.07.047
中图分类号
Q5 [生物化学]; Q7 [分子生物学];
学科分类号
071010 ; 081704 ;
摘要
Eukaryotic genomes generate a heterogeneous ensemble of mRNAs and long noncoding RNAs (lncRNAs). LncRNAs and mRNAs are both transcribed by Pol II and acquire 5' caps and poly(A) tails, but only mRNAs are translated into proteins. To address how these classes are distinguished, we identified the transcriptome-wide targets of 13 RNA processing, export, and turnover factors in budding yeast. Comparing the maturation pathways of mRNAs and lncRNAs revealed that transcript fate is largely determined during 3' end formation. Most lncRNAs are targeted for nuclear RNA surveillance, but a subset with 3' cleavage and polyadenylation features resembling the mRNA consensus can be exported to the cytoplasm. The Hrp1 and Nab2 proteins act at this decision point, with dual roles in mRNA cleavage/polyadenylation and lncRNA surveillance. Our data also reveal the dynamic and heterogeneous nature of mRNA maturation, and highlight a subset of "lncRNA-like" mRNAs regulated by the nuclear surveillance machinery.
引用
收藏
页码:996 / 1009
页数:14
相关论文
共 60 条
  • [1] Purification of Nuclear Poly(A)-binding Protein Nab2 Reveals Association with the Yeast Transcriptome and a Messenger Ribonucleoprotein Core Structure
    Batisse, Julien
    Batisse, Claire
    Budd, Aidan
    Boettcher, Bettina
    Hurt, Ed
    [J]. JOURNAL OF BIOLOGICAL CHEMISTRY, 2009, 284 (50) : 34911 - 34917
  • [2] Identification of a regulated pathway for nuclear pre-mRNA turnover
    Bousquet-Antonelli, C
    Presutti, C
    Tollervey, D
    [J]. CELL, 2000, 102 (06) : 765 - 775
  • [3] High-Resolution View of the Yeast Meiotic Program Revealed by Ribosome Profiling
    Brar, Gloria A.
    Yassour, Moran
    Friedman, Nir
    Regev, Aviv
    Ingolia, Nicholas T.
    Weissman, Jonathan S.
    [J]. SCIENCE, 2012, 335 (6068) : 552 - 557
  • [4] Structural Basis for Polyadenosine-RNA Binding by Nab2 Zn Fingers and Its Function in mRNA Nuclear Export
    Brockmann, Christoph
    Soucek, Sharon
    Kuhlmann, Sonja I.
    Mills-Lujan, Katherine
    Kelly, Seth M.
    Yang, Ji-Chun
    Iglesias, Nahid
    Stutz, Francoise
    Corbett, Anita H.
    Neuhaus, David
    Stewart, Murray
    [J]. STRUCTURE, 2012, 20 (06) : 1007 - 1018
  • [5] Trans-acting antisense RNAs mediate transcriptional gene cosuppression in S. cerevisiae
    Camblong, Jurgi
    Beyrouthy, Nissrine
    Guffanti, Elisa
    Schlaepfer, Guillaume
    Steinmetz, Lars M.
    Stutz, Francoise
    [J]. GENES & DEVELOPMENT, 2009, 23 (13) : 1534 - 1545
  • [6] Bimodal expression of PHO84 is modulated by early termination of antisense transcription
    Castelnuovo, Manuele
    Rahman, Samir
    Guffanti, Elisa
    Infantino, Valentina
    Stutz, Francoise
    Zenklusen, Daniel
    [J]. NATURE STRUCTURAL & MOLECULAR BIOLOGY, 2013, 20 (07) : 851 - +
  • [7] Nascent transcript sequencing visualizes transcription at nucleotide resolution
    Churchman, L. Stirling
    Weissman, Jonathan S.
    [J]. NATURE, 2011, 469 (7330) : 368 - +
  • [8] The mRNA encoding the yeast ARE-binding protein Cth2 is generated by a novel 3′ processing pathway
    Ciais, Delphine
    Bohnsack, Markus T.
    Tollervey, David
    [J]. NUCLEIC ACIDS RESEARCH, 2008, 36 (09) : 3075 - 3084
  • [9] Transcriptome-Wide Binding Sites for Components of the Saccharomyces cerevisiae Non-Poly(A) Termination Pathway: Nrd1, Nab3, and Sen1
    Creamer, Tyler J.
    Darby, Miranda M.
    Jamonnak, Nuttara
    Schaughency, Paul
    Hao, Haiping
    Wheelan, Sarah J.
    Corden, Jeffry L.
    [J]. PLOS GENETICS, 2011, 7 (10):
  • [10] A high-resolution map of transcription in the yeast genome
    David, L
    Huber, W
    Granovskaia, M
    Toedling, J
    Palm, CJ
    Bofkin, L
    Jones, T
    Davis, RW
    Steinmetz, LM
    [J]. PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2006, 103 (14) : 5320 - 5325