The yeast noncoding RNA interaction network

This article describes the creation of the first expert manually curated noncoding RNA interaction networks for S. cerevisiae The RNA-RNA and RNA-protein interaction networks have been carefully extracted from the experimental literature and made available through the IntAct database (www.ebi.ac.uk/intact). We provide an initial network analysis and compare their properties to the much larger protein-protein interaction network. We find that the proteins that bind to ncRNAs in the network contain only a small proportion of classical RNA binding domains. We also see an enrichment of WD40 domains suggesting their direct involvement in ncRNA interactions. We discuss the challenges in collecting noncoding RNA interaction data and the opportunities for worldwide collaboration to fill the unmet need for this data.

[1]  Alex Bateman,et al.  RNAcentral: a comprehensive database of non-coding RNA sequences , 2016, Nucleic acids research.

[2]  Christopher R. Sibley,et al.  CLIPing the brain: Studies of protein–RNA interactions important for neurodegenerative disorders☆☆☆ , 2013, Molecular and Cellular Neuroscience.

[3]  Michel J. Weber,et al.  Mammalian Small Nucleolar RNAs Are Mobile Genetic Elements , 2006, PLoS genetics.

[4]  J. Woolford,et al.  Ribosome Biogenesis in the Yeast Saccharomyces cerevisiae , 2013, Genetics.

[5]  Masayuki Yamamoto,et al.  The long non-coding RNA world in yeasts. , 2016, Biochimica et biophysica acta.

[6]  C. Sander,et al.  The HUPO PSI's Molecular Interaction format—a community standard for the representation of protein interaction data , 2004, Nature Biotechnology.

[7]  S. Loeillet,et al.  XUTs are a class of Xrn1-sensitive antisense regulatory non-coding RNA in yeast , 2011, Nature.

[8]  Christophe Malabat,et al.  Widespread bidirectional promoters are the major source of cryptic transcripts in yeast , 2009, Nature.

[9]  Robert D. Finn,et al.  Rfam 12.0: updates to the RNA families database , 2014, Nucleic Acids Res..

[10]  Ana Kozomara,et al.  miRBase: annotating high confidence microRNAs using deep sequencing data , 2013, Nucleic Acids Res..

[11]  Scott B. Dewell,et al.  Transcriptome-wide Identification of RNA-Binding Protein and MicroRNA Target Sites by PAR-CLIP , 2010, Cell.

[12]  Wei Wu,et al.  NPInter v3.0: an upgraded database of noncoding RNA-associated interactions , 2016, Database J. Biol. Databases Curation.

[13]  Liang-Hu Qu,et al.  Genome-wide analysis of chicken snoRNAs provides unique implications for the evolution of vertebrate snoRNAs , 2009, BMC Genomics.

[14]  P. Khaitovich,et al.  Birth and expression evolution of mammalian microRNA genes , 2013, Genome research.

[15]  Jürgen Brosius,et al.  Retroposed SNOfall--a mammalian-wide comparison of platypus snoRNAs. , 2008, Genome research.

[16]  Yuanfang Guan,et al.  Functional Analysis of Gene Duplications in Saccharomyces cerevisiae , 2007, Genetics.

[17]  Robert D. Finn,et al.  The Pfam protein families database: towards a more sustainable future , 2015, Nucleic Acids Res..

[18]  S. Gerstberger,et al.  A census of human RNA-binding proteins , 2014, Nature Reviews Genetics.

[19]  Peer Bork,et al.  SMART: recent updates, new developments and status in 2015 , 2014, Nucleic Acids Res..

[20]  S. Gerstberger,et al.  Identification of the RNA recognition element of the RBPMS family of RNA-binding proteins and their transcriptome-wide mRNA targets , 2014, RNA.

[21]  Gene W. Yeo,et al.  SONAR Discovers RNA-Binding Proteins from Analysis of Large-Scale Protein-Protein Interactomes. , 2016, Molecular cell.

[22]  D. Ingber,et al.  High-Betweenness Proteins in the Yeast Protein Interaction Network , 2005, Journal of biomedicine & biotechnology.

[23]  Wayne A. Decatur,et al.  Genome-wide searching for pseudouridylation guide snoRNAs: analysis of the Saccharomyces cerevisiae genome. , 2004, Nucleic acids research.

[24]  Rafael C. Jimenez,et al.  Merging and scoring molecular interactions utilising existing community standards: tools, use-cases and a case study , 2015, Database J. Biol. Databases Curation.

[25]  Timothy R. Hughes,et al.  High-throughput characterization of protein–RNA interactions , 2014, Briefings in functional genomics.

[26]  Richard Bonneau,et al.  The mRNA-bound proteome and its global occupancy profile on protein-coding transcripts. , 2012, Molecular cell.

[27]  E. Laing,et al.  Conserved mRNA-binding proteomes in eukaryotic organisms , 2015, Nature Structural &Molecular Biology.

[28]  Peter F. Stadler,et al.  tRNAdb 2009: compilation of tRNA sequences and tRNA genes , 2008, Nucleic Acids Res..

[29]  Fred Winston,et al.  Intergenic transcription is required to repress the Saccharomyces cerevisiae SER3 gene , 2004, Nature.

[30]  Wayne A. Decatur,et al.  New bioinformatic tools for analysis of nucleotide modifications in eukaryotic rRNA. , 2007, RNA.

[31]  Martin Kuiper,et al.  BiNGO: a Cytoscape plugin to assess overrepresentation of Gene Ontology categories in Biological Networks , 2005, Bioinform..

[32]  Rafael C. Jimenez,et al.  The MIntAct project—IntAct as a common curation platform for 11 molecular interaction databases , 2013, Nucleic Acids Res..

[33]  S. Janga,et al.  Dissecting the expression relationships between RNA-binding proteins and their cognate targets in eukaryotic post-transcriptional regulatory networks , 2016, Scientific Reports.

[34]  Paulo P. Amaral,et al.  The Reality of Pervasive Transcription , 2011, PLoS biology.

[35]  C. Mungall,et al.  Gene Ontology Consortium : going forward The Gene Ontology , 2015 .

[36]  Johannes Goll,et al.  Protein interaction data curation: the International Molecular Exchange (IMEx) consortium , 2012, Nature Methods.

[37]  Christian von Mering,et al.  RAIN: RNA–protein Association and Interaction Networks , 2017, Database J. Biol. Databases Curation.

[38]  Hui Zhou,et al.  starBase v2.0: decoding miRNA-ceRNA, miRNA-ncRNA and protein–RNA interaction networks from large-scale CLIP-Seq data , 2013, Nucleic Acids Res..

[39]  Jeroen Krijgsveld,et al.  The RNA-binding proteomes from yeast to man harbour conserved enigmRBPs , 2015, Nature Communications.

[40]  G. Storz.  An Expanding Universe of Noncoding RNAs , 2002, Science.

[41]  Gabriele Varani,et al.  RNA is rarely at a loss for companions; as soon as RNA , 2008 .

[42]  Yi-Tao Yu,et al.  U2 snRNA is inducibly pseudouridylated at novel sites by Pus7p and snR81 RNP , 2011, The EMBO journal.

[43]  Henning Hermjakob,et al.  Shared resources, shared costs—leveraging biocuration resources , 2015, Database J. Biol. Databases Curation.

[44]  M. Gillespie,et al.  Guidelines for the functional annotation of microRNAs using the Gene Ontology , 2016, RNA.

[45]  Christoph Steinbeck,et al.  ChEBI in 2016: Improved services and an expanding collection of metabolites , 2015, Nucleic Acids Res..

[46]  Norman E. Davey,et al.  Insights into RNA Biology from an Atlas of Mammalian mRNA-Binding Proteins , 2012, Cell.

[47]  Gábor Csárdi,et al.  The igraph software package for complex network research , 2006 .

[48]  Chao Xu,et al.  Structural insights into Gemin5-guided selection of pre-snRNAs for snRNP assembly , 2016, Genes & development.

[49]  Jeroen Krijgsveld,et al.  Comprehensive Identification of RNA-Binding Domains in Human Cells , 2016, Molecular cell.

[50]  B. Dujon.  Yeast evolutionary genomics , 2010, Nature Reviews Genetics.

[51]  Marcel E. Dinger,et al.  lncRNAdb v2.0: expanding the reference database for functional long noncoding RNAs , 2014, Nucleic Acids Res..

[52]  Naoya Kenmochi,et al.  snOPY: a small nucleolar RNA orthological gene database , 2013, BMC Research Notes.

[53]  Robin D. Dowell,et al.  Toggle involving cis-interfering noncoding RNAs controls variegated gene expression in yeast , 2009, Proceedings of the National Academy of Sciences.

[54]  A. Morillon,et al.  Pervasive transcription - Lessons from yeast. , 2011, Biochimie.

[55]  Boqin Hu,et al.  CLIPdb: a CLIP-seq database for protein-RNA interactions , 2015, BMC Genomics.

[56]  David Tollervey,et al.  Cross-linking, ligation, and sequencing of hybrids reveals RNA–RNA interactions in yeast , 2011, Proceedings of the National Academy of Sciences.

[57]  Jeroen Krijgsveld,et al.  Comprehensive Identification of RNA-Binding Proteins by RNA Interactome Capture. , 2016, Methods in molecular biology.

[58]  María Martín,et al.  UniProt: A hub for protein information , 2015 .

[59]  The Uniprot Consortium,et al.  UniProt: a hub for protein information , 2014, Nucleic Acids Res..

[60]  David Tollervey,et al.  Identification of protein binding sites on U3 snoRNA and pre-rRNA by UV cross-linking and high-throughput analysis of cDNAs , 2009, Proceedings of the National Academy of Sciences.

[61]  Edith D. Wong,et al.  Saccharomyces Genome Database: the genomics resource of budding yeast , 2011, Nucleic Acids Res..

[62]  John S. Mattick,et al.  lncRNAdb: a reference database for long noncoding RNAs , 2010, Nucleic Acids Res..

[63]  Patricia P. Chan,et al.  GtRNAdb: a database of transfer RNA genes detected in genomic sequence , 2008, Nucleic Acids Res..

[64]  Michael Primig,et al.  Transcription of Two Long Noncoding RNAs Mediates Mating-Type Control of Gametogenesis in Budding Yeast , 2012, Cell.

[65]  David Tollervey,et al.  A Transcriptome-wide Atlas of RNP Composition Reveals Diverse Classes of mRNAs and lncRNAs , 2013, Cell.

[66]  Roy Parker,et al.  Global Analysis of Yeast mRNPs , 2012, Nature Structural &Molecular Biology.

[67]  Yi-Tao Yu,et al.  Pseudouridylation of yeast U2 snRNA is catalyzed by either an RNA‐guided or RNA‐independent mechanism , 2005, The EMBO journal.

[68]  Hsien-Da Huang,et al.  RNAcentral: an international database of ncRNA sequences , 2014, Nucleic Acids Res..

[69]  P. Shannon,et al.  Cytoscape: a software environment for integrated models of biomolecular interaction networks. , 2003, Genome research.

[70]  Johannes Söding,et al.  Transcriptome maps of mRNP biogenesis factors define pre-mRNA recognition. , 2014, Molecular cell.

[71]  Gabriele Varani,et al.  The structure and function of small nucleolar ribonucleoproteins , 2007, Nucleic acids research.

[72]  A. Barabasi,et al.  Lethality and centrality in protein networks , 2001, Nature.

[73]  Henning Hermjakob,et al.  A visual review of the interactome of LRRK2: Using deep-curated molecular interaction data to represent biology , 2015, Proteomics.