Toward a next-generation atlas of RNA secondary structure

RNA structure plays a crucial role in gene maturation, regulation and function. Determining the form and frequency of RNA folds is essential for a better understanding of how RNA exerts its functions. Low-throughput studies have focused on RNA primary sequences and expression levels, but with an emphasis on relatively small numbers of transcripts. However, with the recent advent of high-throughput technologies, it is realistic to begin analyzing RNA secondary structures on a genome-wide scale. Here, we review genome-wide RNA secondary structure profiles as well as advances in computational structure predictions. We further discuss the novel characteristics of RNA secondary structure across messenger RNAs. Probing RNA secondary structure by high-throughput sequencing will enable us to build atlases of RNA secondary structures, an important step in helping us to understand the versatility of RNA functions in diverse cellular processes.

[1]  B. Gregory,et al.  Global analysis of the RNA-protein interaction and RNA secondary structure landscapes of the Arabidopsis nucleus. , 2015, Molecular cell.

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

[3]  Sean R Eddy,et al.  Computational analysis of conserved RNA secondary structure in transcriptomes and genomes. , 2014, Annual review of biophysics.

[4]  Kevin M Weeks,et al.  RNA secondary structure modeling at consistent high accuracy using differential SHAPE , 2014, RNA.

[5]  J. Doudna,et al.  Insights into RNA structure and function from genome-wide studies , 2014, Nature Reviews Genetics.

[6]  J. Woolford,et al.  Mod-seq: high-throughput sequencing for chemical probing of RNA structure , 2014, RNA.

[7]  Qiangfeng Cliff Zhang,et al.  Landscape and variation of RNA secondary structure across the human transcriptome , 2014, Nature.

[8]  Y. Zhang,et al.  In vivo genome-wide profiling of RNA secondary structure reveals novel regulatory features , 2013, Nature.

[9]  Robert Giegerich,et al.  Introduction to RNA secondary structure comparison. , 2014, Methods in molecular biology.

[10]  Jan Gorodkin,et al.  RNA Sequence, Structure, and Function: Computational and Bioinformatic Methods , 2014, Methods in Molecular Biology.

[11]  Manolis Kellis,et al.  Genome-wide probing of RNA structure reveals active unfolding of mRNA structures in vivo , 2013, Nature.

[12]  J. Plotkin,et al.  Rate-Limiting Steps in Yeast Protein Translation , 2013, Cell.

[13]  B. Gregory,et al.  Arabidopsis mRNA secondary structure correlates with protein function and domains , 2013, Plant signaling & behavior.

[14]  Howard Y. Chang,et al.  Genome-wide mapping of RNA structure using nuclease digestion and high-throughput sequencing , 2013, Nature Protocols.

[15]  K. Weeks,et al.  The genetic code as expressed through relationships between mRNA structure and protein function , 2013, FEBS Letters.

[16]  Alexander Churkin,et al.  RNA dot plots: an image representation for RNA secondary structure analysis and manipulations , 2013, Wiley interdisciplinary reviews. RNA.

[17]  Michael P Snyder,et al.  SeqFold: Genome-scale reconstruction of RNA secondary structure integrating high-throughput sequencing data , 2013, Genome research.

[18]  Michiaki Hamada,et al.  Direct Updating of an RNA Base-Pairing Probability Matrix with Marginal Probability Constraints , 2012, J. Comput. Biol..

[19]  B. Gregory,et al.  PRMD: an integrated database for plant RNA modifications , 2012, Plant Cell.

[20]  Peter Clote,et al.  Integrating Chemical Footprinting Data into RNA Secondary Structure Prediction , 2012, PloS one.

[21]  W. Gu,et al.  Selection on synonymous sites for increased accessibility around miRNA binding sites in plants. , 2012, Molecular biology and evolution.

[22]  F. Narberhaus,et al.  Bacterial RNA thermometers: molecular zippers and switches , 2012, Nature Reviews Microbiology.

[23]  Manolis Kellis,et al.  RNA folding with soft constraints: reconciliation of probing data and thermodynamic secondary structure prediction , 2012, Nucleic acids research.

[24]  Paul Ryvkin,et al.  Global analysis of RNA secondary structure in two metazoans. , 2012, Cell reports.

[25]  K. Reinert Complete suboptimal folding of RNA and the stability of secondary structures , Biopolymers , 2012 .

[26]  Peter F. Stadler,et al.  ViennaRNA Package 2.0 , 2011, Algorithms for Molecular Biology.

[27]  E. Eyras,et al.  Deciphering 3'ss selection in the yeast genome reveals an RNA thermosensor that mediates alternative splicing. , 2011, Molecular cell.

[28]  Howard Y. Chang,et al.  Understanding the transcriptome through RNA structure , 2011, Nature Reviews Genetics.

[29]  B. Meyers,et al.  Transcriptome dynamics through alternative polyadenylation in developmental and environmental responses in plants revealed by deep sequencing. , 2011, Genome research.

[30]  C Joel McManus,et al.  RNA structure and the mechanisms of alternative splicing. , 2011, Current opinion in genetics & development.

[31]  Cole Trapnell,et al.  Multiplexed RNA structure characterization with selective 2′-hydroxyl acylation analyzed by primer extension sequencing (SHAPE-Seq) , 2011, Proceedings of the National Academy of Sciences.

[32]  Cole Trapnell,et al.  Modeling and automation of sequencing-based characterization of RNA structure , 2011, Proceedings of the National Academy of Sciences.

[33]  Patrick Xuechun Zhao,et al.  psRNATarget: a plant small RNA target analysis server , 2011, Nucleic Acids Res..

[34]  Yongfeng Jin,et al.  New insights into RNA secondary structure in the alternative splicing of pre-mRNAs , 2011, RNA biology.

[35]  Patrick Xuechun Zhao,et al.  Computational analysis of miRNA targets in plants: current status and challenges , 2011, Briefings Bioinform..

[36]  Eric Westhof,et al.  The RNA structurome: high-throughput probing , 2010, Nature Methods.

[37]  Gos Micklem,et al.  Supporting Online Material Materials and Methods Figs. S1 to S50 Tables S1 to S18 References Identification of Functional Elements and Regulatory Circuits by Drosophila Modencode , 2022 .

[38]  D. Haussler,et al.  FragSeq: transcriptome-wide RNA structure probing using high-throughput sequencing , 2010, Nature Methods.

[39]  K. Weeks,et al.  SHAPE-directed RNA secondary structure prediction. , 2010, Methods.

[40]  Howard Y. Chang,et al.  Genome-wide measurement of RNA secondary structure in yeast , 2010, Nature.

[41]  J Andrew Berglund,et al.  Role of RNA structure in regulating pre-mRNA splicing. , 2010, Trends in biochemical sciences.

[42]  M. Metzker Sequencing technologies — the next generation , 2010, Nature Reviews Genetics.

[43]  David H. Mathews,et al.  RNAstructure: software for RNA secondary structure prediction and analysis , 2010, BMC Bioinformatics.

[44]  C. Holt,et al.  Subcellular mRNA Localization in Animal Cells and Why It Matters , 2009, Science.

[45]  F. Bonneau,et al.  The Yeast Exosome Functions as a Macromolecular Cage to Channel RNA Substrates for Degradation , 2009, Cell.

[46]  Kristen K. Dang,et al.  Architecture and Secondary Structure of an Entire HIV-1 RNA Genome , 2009, Nature.

[47]  Kiyoshi Asai,et al.  CentroidFold: a web server for RNA secondary structure prediction , 2009, Nucleic Acids Res..

[48]  Nicholas T. Ingolia,et al.  Genome-Wide Analysis in Vivo of Translation with Nucleotide Resolution Using Ribosome Profiling , 2009, Science.

[49]  K. Martin,et al.  mRNA Localization: Gene Expression in the Spatial Dimension , 2009, Cell.

[50]  Eric Westhof,et al.  The Dynamic Landscapes of RNA Architecture , 2009, Cell.

[51]  Kiyoshi Asai,et al.  Prediction of RNA secondary structure using generalized centroid estimators , 2009, Bioinform..

[52]  Phillip A Sharp,et al.  The Centrality of RNA , 2009, Cell.

[53]  D. Moazed Small RNAs in transcriptional gene silencing and genome defence , 2009, Nature.

[54]  D. Mathews,et al.  Accurate SHAPE-directed RNA structure determination , 2009, Proceedings of the National Academy of Sciences.

[55]  D. Herschlag,et al.  Metal ion-based RNA cleavage as a structural probe. , 2009, Methods in enzymology.

[56]  Charles J H Jang,et al.  Selective mRNA translation coordinates energetic and metabolic adjustments to cellular oxygen deprivation and reoxygenation in Arabidopsis thaliana. , 2008, The Plant journal : for cell and molecular biology.

[57]  K. Weeks,et al.  Time-resolved RNA SHAPE chemistry. , 2008, Journal of the American Chemical Society.

[58]  Eran Segal,et al.  Computational prediction of RNA structural motifs involved in posttranscriptional regulatory processes , 2008, Proceedings of the National Academy of Sciences.

[59]  I. Hofacker,et al.  Beyond energy minimization: approaches to the kinetic folding of RNA , 2008 .

[60]  T. Rapoport,et al.  The Signal Sequence Coding Region Promotes Nuclear Export of mRNA , 2007, PLoS biology.

[61]  P. Tomançak,et al.  Global Analysis of mRNA Localization Reveals a Prominent Role in Organizing Cellular Architecture and Function , 2007, Cell.

[62]  Michael Kertesz,et al.  The role of site accessibility in microRNA target recognition , 2007, Nature Genetics.

[63]  K. Weeks,et al.  A fast-acting reagent for accurate analysis of RNA secondary and tertiary structure by SHAPE chemistry. , 2007, Journal of the American Chemical Society.

[64]  T. Kouzarides Chromatin Modifications and Their Function , 2007, Cell.

[65]  Jeffrey Wilusz,et al.  The highways and byways of mRNA decay , 2007, Nature Reviews Molecular Cell Biology.

[66]  K. Weeks,et al.  Selective 2′-hydroxyl acylation analyzed by primer extension (SHAPE): quantitative RNA structure analysis at single nucleotide resolution , 2006, Nature Protocols.

[67]  E. Nudler,et al.  Gene Control by Large Noncoding RNAs , 2006, Science's STKE.

[68]  Serafim Batzoglou,et al.  CONTRAfold: RNA secondary structure prediction without physics-based models , 2006, ISMB.

[69]  David H Mathews,et al.  Revolutions in RNA secondary structure prediction. , 2006, Journal of molecular biology.

[70]  Aleksey Y. Ogurtsov,et al.  A periodic pattern of mRNA secondary structure created by the genetic code , 2006, Nucleic acids research.

[71]  E. Kandel,et al.  RNA-mediated response to heat shock in mammalian cells , 2006, Nature.

[72]  Robert Giegerich,et al.  RNAshapes: an integrated RNA analysis package based on abstract shapes. , 2006, Bioinformatics.

[73]  R. Giegerich,et al.  Complete probabilistic analysis of RNA shapes , 2006, BMC Biology.

[74]  Torsten Waldminghaus,et al.  RNA thermometers are common in α- and γ-proteobacteria , 2005 .

[75]  Alain Xayaphoummine,et al.  Kinefold web server for RNA/DNA folding path and structure prediction including pseudoknots and knots , 2005, Nucleic Acids Res..

[76]  R. Russell,et al.  Principles of MicroRNA–Target Recognition , 2005, PLoS biology.

[77]  Torsten Waldminghaus,et al.  RNA thermometers are common in alpha- and gamma-proteobacteria. , 2005, Biological chemistry.

[78]  Christian W. Cobaugh,et al.  Evaluation of the suitability of free-energy minimization using nearest-neighbor energy parameters for RNA secondary structure prediction , 2004, BMC Bioinformatics.

[79]  Hélène Touzet,et al.  CARNAC: folding families of related RNAs , 2004, Nucleic Acids Res..

[80]  Xing Xu,et al.  A graph theoretical approach for predicting common RNA secondary structure motifs including pseudoknots in unaligned sequences , 2004, Bioinform..

[81]  Sean R. Eddy,et al.  Evaluation of several lightweight stochastic context-free grammars for RNA secondary structure prediction , 2004, BMC Bioinformatics.

[82]  C. Lawrence,et al.  A statistical sampling algorithm for RNA secondary structure prediction. , 2003, Nucleic acids research.

[83]  Michael Zuker,et al.  Mfold web server for nucleic acid folding and hybridization prediction , 2003, Nucleic Acids Res..

[84]  Ivo L. Hofacker,et al.  Vienna RNA secondary structure server , 2003, Nucleic Acids Res..

[85]  P. Stadler,et al.  Secondary structure prediction for aligned RNA sequences. , 2002, Journal of molecular biology.

[86]  R. Gutell,et al.  The accuracy of ribosomal RNA comparative structure models. , 2002, Current opinion in structural biology.

[87]  Michael T. Wolfinger,et al.  Barrier Trees of Degenerate Landscapes , 2002 .

[88]  S. Birken,et al.  Preparation and analysis of the common urinary forms of human chorionic gonadotropin. , 2000, Methods.

[89]  P. Romby,et al.  Probing RNA structure and RNA-ligand complexes with chemical probes. , 2000, Methods in enzymology.

[90]  I. Tinoco,et al.  How RNA folds. , 1999, Journal of molecular biology.

[91]  J. Sabina,et al.  Expanded sequence dependence of thermodynamic parameters improves prediction of RNA secondary structure. , 1999, Journal of molecular biology.

[92]  P. Schuster,et al.  Complete suboptimal folding of RNA and the stability of secondary structures. , 1999, Biopolymers.

[93]  S. Peltz,et al.  ATP is a cofactor of the Upf1 protein that modulates its translation termination and RNA binding activities. , 1998, RNA.

[94]  Wien,et al.  Kinetic Folding of RNA , 1998 .

[95]  E. Westhof,et al.  Hierarchy and dynamics of RNA folding. , 1997, Annual review of biophysics and biomolecular structure.

[96]  M. Zuker,et al.  "Well-determined" regions in RNA secondary structure prediction: analysis of small subunit ribosomal RNA. , 1995, Nucleic acids research.

[97]  R. Durbin,et al.  RNA sequence analysis using covariance models. , 1994, Nucleic acids research.

[98]  Walter Fontana,et al.  Fast folding and comparison of RNA secondary structures , 1994 .

[99]  J. McCaskill The equilibrium partition function and base pair binding probabilities for RNA secondary structure , 1990, Biopolymers.

[100]  M. Zuker On finding all suboptimal foldings of an RNA molecule. , 1989, Science.

[101]  J. Ebel,et al.  Use of lead(II) to probe the structure of large RNA's. Conformation of the 3' terminal domain of E. coli 16S rRNA and its involvement in building the tRNA binding sites. , 1989, Journal of biomolecular structure & dynamics.

[102]  G. Knapp Enzymatic approaches to probing of RNA secondary and tertiary structure. , 1989, Methods in enzymology.

[103]  D. Sankoff Simultaneous Solution of the RNA Folding, Alignment and Protosequence Problems , 1985 .

[104]  D. Sankoff,et al.  RNA secondary structures and their prediction , 1984 .

[105]  A. Rich,et al.  Comparison of transfer ribonucleic acid structures using cobra venom and S1 endonucleases. , 1982, Biochemistry.

[106]  Michael Zuker,et al.  Optimal computer folding of large RNA sequences using thermodynamics and auxiliary information , 1981, Nucleic Acids Res..

[107]  M. Waterman,et al.  RNA secondary structure: a complete mathematical analysis , 1978 .

[108]  Jerrold R. Griggs,et al.  Algorithms for Loop Matchings , 1978 .

[109]  C. Woese,et al.  5S RNA secondary structure , 1975, Nature.

[110]  I. Tinoco,et al.  Estimation of Secondary Structure in Ribonucleic Acids , 1971, Nature.