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Long non-coding RNAs as a source of new peptides

Jorge Ruiz-Orera, Xavier Messeguer, Juan Antonio Subirana and 1 more

eLife · 2014 · CC BY

doi:10.7554/elife.03523

Abstract

Deep transcriptome sequencing has revealed the existence of many transcripts that lack long or conserved open reading frames (ORFs) and which have been termed long non-coding RNAs (lncRNAs). The vast majority of lncRNAs are lineage-specific and do not yet have a known function. In this study, we test the hypothesis that they may act as a repository for the synthesis of new peptides. We find that a large fraction of the lncRNAs expressed in cells from six different species is associated with ribosomes. The patterns of ribosome protection are consistent with the translation of short peptides. lncRNAs show similar coding potential and sequence constraints than evolutionary young protein coding sequences, indicating that they play an important role in de novo protein evolution.

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    Pruitt KD, Brown GR, Hiatt SM, Thibaud-Nissen F, Astashyn A, Ermolaeva O, Farrell CM, Hart J, Landrum MJ, McGarvey KM, Murphy MR, O'Leary NA, Pujar S, Rajput B, Rangwala SH, Riddick LD, Shkeda A, Sun H, Tamez P, Tully RE, Wallin C, Webb D, Weber J, Wu W, DiCuccio M, Kitts P, Maglott DR, Murphy TD, Ostell JM. RefSeq: an update on mammalian reference sequences. Nucleic Acids Research. 2014;42:D756-D763.

    Not in our library10.1093/nar/gkt1114

  73. 73.

    Quinlan AR, Hall IM. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics. 2010;26:841-842.

    Not in our library10.1093/bioinformatics/btq033

  74. 74.

    R Development Core Team. R: a language and environment for statistical computing. R Foundation for statistical computing. 2010.

    Not in our library

  75. 75.
    De Novo ORFs in Drosophila Are Important to Organismal Fitness and Evolved Rapidly from Previously Non-coding Sequences · 2013
    No notice
  76. 76.

    Savard J, Marques-Souza H, Aranda M, Tautz D. A segmentation gene in tribolium produces a polycistronic mRNA that codes for multiple conserved peptides. Cell. 2006;126:559-569.

    Not in our library10.1016/j.cell.2006.05.053

  77. 77.

    Scofield DG, Hong X, Lynch M. Position of the final intron in full-length transcripts: determined by NMD? Molecular Biology and Evolution. 2007;24:896-899.

    Not in our library10.1093/molbev/msm010

  78. 78.

    Sherry ST, Ward MH, Kholodov M, Baker J, Phan L, Smigielski EM, Sirotkin K. dbSNP: the NCBI database of genetic variation. Nucleic Acids Research. 2001;29:308-311.

    Not in our library10.1093/nar/29.1.308

  79. 79.

    Slavoff SA, Heo J, Budnik BA, Hanakahi LA, Saghatelian A. A human short open reading frame (sORF)-encoded polypeptide that stimulates DNA end joining. The Journal of Biological Chemistry. 2014;289:10950-10957.

    Not in our library10.1074/jbc.c113.533968

  80. 80.

    Slavoff SA, Mitchell AJ, Schwaid AG, Cabili MN, Ma J, Levin JZ, Karger AD, Budnik BA, Rinn JL, Saghatelian A. Peptidomic discovery of short open reading frame-encoded peptides in human cells. Nature Chemical Biology. 2013;9:59-64.

    Not in our library10.1038/nchembio.1120

  81. 81.
    ConDeTri - A Content Dependent Read Trimmer for Illumina Data · 2011
    No notice
  82. 82.
    Utilizing sequence intrinsic composition to classify protein-coding and long non-coding transcripts · 2013
    No notice
  83. 83.
    The RNA Degradation Pathway Regulates the Function of GAS5 a Non-Coding RNA in Mammalian Cells · 2013
    No notice
  84. 84.

    Tautz D. Polycistronic peptide coding genes in eukaryotes–how widespread are they? Briefings in Functional Genomics & Proteomics. 2009;8:68-74.

    Not in our library10.1093/bfgp/eln054

  85. 85.

    Tautz D, Domazet-Lošo T. The evolutionary origin of orphan genes. Nature Reviews Genetics. 2011;12:692-702.

    Not in our library10.1038/nrg3053

  86. 86.

    Toll-Riera M, Bosch N, Bellora N, Castelo R, Armengol L, Estivill X, Albà MM. Origin of primate orphan genes: a comparative genomics approach. Molecular Biology and Evolution. 2009;26:603-612.

    Not in our library10.1093/molbev/msn281

  87. 87.

    Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, van Baren MJ, Salzberg SL, Wold BJ, Pachter L. Transcript assembly and quantification by RNA-seq reveals unannotated transcripts and isoform switching during cell differentiation. Nature Biotechnology. 2010;28:511-515.

    Not in our library10.1038/nbt.1621

  88. 88.

    Ulitsky I, Bartel DP. lincRNAs: genomics, evolution, and mechanisms. Cell. 2013;154:26-46.

    Not in our library10.1016/j.cell.2013.06.020

  89. 89.
    Activities at the Universal Protein Resource (UniProt) · 2013
    No notice
  90. 90.
    Extensive localization of long noncoding RNAs to the cytosol and mono- and polyribosomal complexes · 2014
    No notice
  91. 91.
    Direct Detection of Alternative Open Reading Frames Translation Products in Human Significantly Expands the Proteome · 2013
    No notice
  92. 92.
    Comparative ribosome profiling reveals extensive translational complexity in different Trypanosoma brucei life cycle stages · 2014
    No notice
  93. 93.

    Wang L, Park HJ, Dasari S, Wang S, Kocher JP, Li W. CPAT: Coding-Potential Assessment Tool using an alignment-free logistic regression model. Nucleic Acids Research. 2013;41:e74.

    Not in our library10.1093/nar/gkt006

  94. 94.

    Wilson BA, Masel J. Putatively noncoding transcripts show extensive association with ribosomes. Genome Biology and Evolution. 2011;3:1245-1252.

    Not in our library10.1093/gbe/evr099

  95. 95.

    Wissler L, Gadau J, Simola DF, Helmkampf M, Bornberg-Bauer E. Mechanisms and dynamics of orphan gene emergence in insect genomes. Genome Biology and Evolution. 2013;5:439-455.

    Not in our library10.1093/gbe/evt009

  96. 96.
    Hominoid-Specific De Novo Protein-Coding Genes Originating from Long Non-Coding RNAs · 2012
    No notice

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