High-throughput determination of RNA structures

RNA performs and regulates a diverse range of cellular processes, with new functional roles being uncovered at a rapid pace. Interest is growing in how these functions are linked to RNA structures that form in the complex cellular environment. A growing suite of technologies that use advances in RNA structural probes, high-throughput sequencing and new computational approaches to interrogate RNA structure at unprecedented throughput are beginning to provide insights into RNA structures at new spatial, temporal and cellular scales.High-throughput sequencing technology is enabling the structures of RNA to be determined on an unprecedented scale, providing insights into the relationship between the structures adopted by RNAs and the functions they perform in the cell.

[1]  Rhiju Das,et al.  Allosteric mechanism of the V. vulnificus adenine riboswitch resolved by four-dimensional chemical mapping , 2018, eLife.

[2]  K. Weeks,et al.  High-throughput SHAPE and hydroxyl radical analysis of RNA structure and ribonucleoprotein assembly. , 2009, Methods in enzymology.

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

[4]  Kevin Y. Yip,et al.  Improved prediction of RNA secondary structure by integrating the free energy model with restraints derived from experimental probing data , 2015, Nucleic acids research.

[5]  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.

[6]  Niranjan Nagarajan,et al.  In Vivo Mapping of Eukaryotic RNA Interactomes Reveals Principles of Higher-Order Organization and Regulation. , 2016, Molecular cell.

[7]  K. Weeks,et al.  The cellular environment stabilizes adenine riboswitch RNA structure. , 2013, Biochemistry.

[8]  S. Oliviero,et al.  Genome-wide profiling of mouse RNA secondary structures reveals key features of the mammalian transcriptome , 2014, Genome Biology.

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

[10]  Kyle E. Watters,et al.  RNA systems biology: uniting functional discoveries and structural tools to understand global roles of RNAs. , 2016, Current opinion in biotechnology.

[11]  James R. Williamson,et al.  The catalytic diversity of RNAs , 2005, Nature Reviews Molecular Cell Biology.

[12]  Kyle E. Watters,et al.  SHAPE-Seq 2.0: systematic optimization and extension of high-throughput chemical probing of RNA secondary structure with next generation sequencing , 2014, Nucleic acids research.

[13]  W. Gilbert Origin of life: The RNA world , 1986, Nature.

[14]  Kyle E. Watters,et al.  Cotranscriptional Folding of a Riboswitch at Nucleotide Resolution , 2016, Nature Structural &Molecular Biology.

[15]  Nils G. Walter,et al.  The Shine-Dalgarno sequence of riboswitch-regulated single mRNAs shows ligand-dependent accessibility bursts , 2016, Nature Communications.

[16]  H. Noller,et al.  Interaction of elongation factors EF-G and EF-Tu with a conserved loop in 23S RNA , 1988, Nature.

[17]  Lior Pachter,et al.  PROBer Provides a General Toolkit for Analyzing Sequencing-Based Toeprinting Assays. , 2017, Cell systems.

[18]  Siqi Tian,et al.  High-throughput mutate-map-rescue evaluates SHAPE-directed RNA structure and uncovers excited states , 2014, bioRxiv.

[19]  Stuart Aitken,et al.  Snapshots of pre-rRNA structural flexibility reveal eukaryotic 40S assembly dynamics at nucleotide resolution , 2014, Nucleic acids research.

[20]  Ge Zhang,et al.  Model-Free RNA Sequence and Structure Alignment Informed by SHAPE Probing Reveals a Conserved Alternate Secondary Structure for 16S rRNA , 2015, PLoS Comput. Biol..

[21]  Kaoru Inoue,et al.  SHAPE reveals transcript-wide interactions, complex structural domains, and protein interactions across the Xist lncRNA in living cells , 2016, Proceedings of the National Academy of Sciences.

[22]  Siqi Tian,et al.  High-throughput mutate-map-rescue evaluates SHAPE-directed RNA structure and uncovers excited states. , 2014, RNA.

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

[24]  Jill P. Mesirov,et al.  RNA Duplex Map in Living Cells Reveals Higher-Order Transcriptome Structure , 2016, Cell.

[25]  Angela M. Yu,et al.  Estimating RNA structure chemical probing reactivities from reverse transcriptase stops and mutations , 2018, bioRxiv.

[26]  Howard Y. Chang,et al.  Detecting riboSNitches with RNA folding algorithms: a genome-wide benchmark , 2015, Nucleic acids research.

[27]  S. Cockroft,et al.  High-throughput RNA structure probing reveals critical folding events during early 60S ribosome assembly in yeast , 2017, Nature Communications.

[28]  Kyle E. Watters,et al.  The centrality of RNA for engineering gene expression , 2013, Biotechnology journal.

[29]  D. Patel,et al.  Adaptive recognition by nucleic acid aptamers. , 2000, Science.

[30]  D. Mathews,et al.  Principles for understanding the accuracy of SHAPE-directed RNA structure modeling. , 2013, Biochemistry.

[31]  Peter F. Stadler,et al.  RNA folding with hard and soft constraints , 2016, Algorithms for Molecular Biology.

[32]  Cole Trapnell,et al.  RNase-mediated protein footprint sequencing reveals protein-binding sites throughout the human transcriptome , 2014, Genome Biology.

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

[34]  Michael F. Sloma,et al.  Base pair probability estimates improve the prediction accuracy of RNA non-canonical base pairs , 2017, PLoS Comput. Biol..

[35]  Quentin Vicens,et al.  Local RNA structural changes induced by crystallization are revealed by SHAPE. , 2007, RNA.

[36]  Rachel M. Mitton-Fry,et al.  SHAPE analysis of the htrA RNA thermometer from Salmonella enterica , 2017, RNA.

[37]  J. Steitz,et al.  The Noncoding RNA Revolution—Trashing Old Rules to Forge New Ones , 2014, Cell.

[38]  Yiliang Ding,et al.  A hybridization-based approach for quantitative and low-bias single-stranded DNA ligation. , 2013, Analytical biochemistry.

[39]  R. Altman,et al.  SAFA: semi-automated footprinting analysis software for high-throughput quantification of nucleic acid footprinting experiments. , 2005, RNA.

[40]  Walter N. Moss,et al.  Probing Xist RNA Structure in Cells Using Targeted Structure-Seq , 2015, PLoS genetics.

[41]  Kyle E. Watters,et al.  Characterizing RNA structures in vitro and in vivo with selective 2'-hydroxyl acylation analyzed by primer extension sequencing (SHAPE-Seq). , 2016, Methods.

[42]  Rhiju Das,et al.  A mutate-and-map strategy accurately infers the base pairs of a 35-nucleotide model RNA. , 2011, RNA.

[43]  T. Saldi,et al.  Transcription elongation rate affects nascent histone pre-mRNA folding and 3′ end processing , 2018, Genes & development.

[44]  Rhiju Das,et al.  Understanding the errors of SHAPE-directed RNA structure modeling. , 2011, Biochemistry.

[45]  Nathan P. Shih,et al.  SEQualyzer: interactive tool for quality control and exploratory analysis of high-throughput RNA structural profiling data. , 2016, Bioinformatics.

[46]  B. Shapiro,et al.  Correlating SHAPE signatures with three-dimensional RNA structures. , 2011, RNA.

[47]  Rhiju Das,et al.  A two-dimensional mutate-and-map strategy for non-coding RNA structure. , 2011, Nature chemistry.

[48]  S. Climie,et al.  In vivo and in vitro structural analysis of the rplJ mRNA leader of Escherichia coli. Protection by bound L10-L7/L12. , 1988, The Journal of biological chemistry.

[49]  J. Bachellerie,et al.  Improved methods for structure probing in large RNAs: a rapid 'heterologous' sequencing approach is coupled to the direct mapping of nuclease accessible sites. Application to the 5' terminal domain of eukaryotic 28S rRNA. , 1983, Nucleic acids research.

[50]  W. Gilbert,et al.  Chemical probes for higher-order structure in RNA. , 1980, Proceedings of the National Academy of Sciences of the United States of America.

[51]  K. Weeks,et al.  Accurate detection of chemical modifications in RNA by mutational profiling (MaP) with ShapeMapper 2 , 2018, RNA.

[52]  Kyle E. Watters,et al.  Using in-cell SHAPE-Seq and simulations to probe structure–function design principles of RNA transcriptional regulators , 2016, RNA.

[53]  Kyle E. Watters,et al.  Simultaneous characterization of cellular RNA structure and function with in-cell SHAPE-Seq , 2015, Nucleic acids research.

[54]  Alain Laederach,et al.  Allele-specific SHAPE-MaP assessment of the effects of somatic variation and protein binding on mRNA structure. , 2018, RNA.

[55]  J. Shendure,et al.  High-throughput determination of RNA structure by proximity ligation , 2015, Nature Biotechnology.

[56]  Kirsten L. Frieda,et al.  Direct Observation of Cotranscriptional Folding in an Adenine Riboswitch , 2012, Science.

[57]  Christopher A. Lavender,et al.  Three-Dimensional RNA Structure Refinement by Hydroxyl Radical Probing , 2012, Nature Methods.

[58]  H. Noller,et al.  Rapid chemical probing of conformation in 16 S ribosomal RNA and 30 S ribosomal subunits using primer extension. , 1986, Journal of molecular biology.

[59]  Nikolay V. Dokholyan,et al.  Comparative Visualization of the RNA Suboptimal Conformational Ensemble In Vivo , 2017, Biophysical journal.

[60]  J. Ebel,et al.  Probing the structure of RNAs in solution. , 1987, Nucleic acids research.

[61]  K. Weeks,et al.  Mapping Local Nucleotide Flexibility by Selective Acylation of 2‘-Amine Substituted RNA , 2000 .

[62]  R. Lease,et al.  Hydroxyl radical footprinting in vivo: mapping macromolecular structures with synchrotron radiation , 2006, Nucleic acids research.

[63]  L. Pachter,et al.  Rational experiment design for sequencing-based RNA structure mapping , 2014, RNA.

[64]  Jan Gorodkin,et al.  The identification and functional annotation of RNA structures conserved in vertebrates , 2017, Genome research.

[65]  Lei Shi,et al.  Updates to the RNA mapping database (RMDB), version 2 , 2018, Nucleic Acids Res..

[66]  K. Zhou,et al.  RNA-guided assembly of Rev-RRE nuclear export complexes , 2014, eLife.

[67]  J. Kieft,et al.  A general strategy to solve the phase problem in RNA crystallography. , 2007, Structure.

[68]  Sarah M. Assmann,et al.  Structure-seq2: sensitive and accurate genome-wide profiling of RNA structure in vivo , 2017, Nucleic acids research.

[69]  Rhiju Das,et al.  Standardization of RNA Chemical Mapping Experiments , 2014, Biochemistry.

[70]  H. Bayley,et al.  Nanopore-based identification of individual nucleotides for direct RNA sequencing. , 2013, Nano letters.

[71]  H. Margalit,et al.  Global Mapping of Small RNA-Target Interactions in Bacteria , 2016, Molecular cell.

[72]  B. Ganem RNA world , 1987, Nature.

[73]  Howard Y. Chang,et al.  Genome regulation by long noncoding RNAs. , 2012, Annual review of biochemistry.

[74]  B. Blencowe,et al.  Global Mapping of Human RNA-RNA Interactions. , 2016, Molecular cell.

[75]  Rhiju Das,et al.  Massively parallel RNA chemical mapping with a reduced bias MAP-seq protocol. , 2013, Methods in molecular biology.

[76]  T. Cech,et al.  Defining the inside and outside of a catalytic RNA molecule. , 1989, Science.

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

[78]  R. Lavery,et al.  A new theoretical index of biochemical reactivity combining steric and electrostatic factors. An application to yeast tRNAPhe. , 1984, Biophysical chemistry.

[79]  K. Weeks,et al.  Multiple conformations are a conserved and regulatory feature of the RB1 5′ UTR , 2015, RNA.

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

[81]  R. F. Luco,et al.  More than a splicing code: integrating the role of RNA, chromatin and non-coding RNA in alternative splicing regulation. , 2011, Current opinion in genetics & development.

[82]  K. Weeks,et al.  Direct identification of base-paired RNA nucleotides by correlated chemical probing , 2017, RNA.

[83]  F. Major,et al.  The MC-Fold and MC-Sym pipeline infers RNA structure from sequence data , 2008, Nature.

[84]  E. Westhof,et al.  Nucleic acids. From self-assembly to induced-fit recognition. , 1997, Current opinion in structural biology.

[85]  Hua Li,et al.  Publisher Correction: Statistical modeling of RNA structure profiling experiments enables parsimonious reconstruction of structure landscapes , 2018, Nature Communications.

[86]  Yin Tang,et al.  Protein Structure Is Related to RNA Structural Reactivity In Vivo. , 2016, Journal of molecular biology.

[87]  William H Coldren,et al.  Light-Activated Chemical Probing of Nucleobase Solvent Accessibility Inside Cells , 2018, Nature chemical biology.

[88]  Bo Li,et al.  Metrics for rapid quality control in RNA structure probing experiments , 2016, Bioinform..

[89]  D. Turner,et al.  Incorporating chemical modification constraints into a dynamic programming algorithm for prediction of RNA secondary structure. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

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

[91]  Pablo Cordero,et al.  Rich RNA Structure Landscapes Revealed by Mutate-and-Map Analysis , 2015, PLoS Comput. Biol..

[92]  Nikolay V. Dokholyan,et al.  Single-molecule correlated chemical probing of RNA , 2014, Proceedings of the National Academy of Sciences.

[93]  K. Weeks,et al.  The mechanisms of RNA SHAPE chemistry. , 2012, Journal of the American Chemical Society.

[94]  X. Wang,et al.  Hydroxyl radical "footprinting" of RNA: application to pre-mRNA splicing complexes. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[95]  D. Mathews,et al.  Accurate SHAPE-directed RNA secondary structure modeling, including pseudoknots , 2013, Proceedings of the National Academy of Sciences.

[96]  Steven Busan,et al.  RNA motif discovery by SHAPE and mutational profiling (SHAPE-MaP) , 2014, Nature Methods.

[97]  Morgan C. Giddings,et al.  Influence of nucleotide identity on ribose 2'-hydroxyl reactivity in RNA. , 2009, RNA.

[98]  David S. Goodsell,et al.  The RCSB protein data bank: integrative view of protein, gene and 3D structural information , 2016, Nucleic Acids Res..

[99]  Kevin M Weeks,et al.  Quantitative analysis of RNA solvent accessibility by N-silylation of guanosine. , 2009, Biochemistry.

[100]  C. Brooks,et al.  Hierarchy of RNA functional dynamics. , 2014, Annual review of biochemistry.

[101]  Jakob Skou Pedersen,et al.  ProbFold: a probabilistic method for integration of probing data in RNA secondary structure prediction , 2016, Bioinform..

[102]  Howard Y. Chang,et al.  Structural imprints in vivo decode RNA regulatory mechanisms , 2015, Nature.

[103]  T. Pan,et al.  Single-molecule studies highlight conformational heterogeneity in the early folding steps of a large ribozyme. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[104]  Michael F. Sloma,et al.  Improving RNA secondary structure prediction with structure mapping data. , 2015, Methods in enzymology.

[105]  K. Weeks,et al.  Slow conformational dynamics at C2'-endo nucleotides in RNA. , 2008, Journal of the American Chemical Society.

[106]  Rhiju Das,et al.  RNA structure inference through chemical mapping after accidental or intentional mutations , 2017, Proceedings of the National Academy of Sciences.

[107]  R. Altman,et al.  High-throughput single-nucleotide structural mapping by capillary automated footprinting analysis , 2008, Nucleic acids research.

[108]  K. Weeks,et al.  Detection of RNA-Protein Interactions in Living Cells with SHAPE. , 2015, Biochemistry.

[109]  David H Mathews,et al.  Modeling RNA secondary structure folding ensembles using SHAPE mapping data , 2017, Nucleic acids research.

[110]  H. Noller,et al.  Functional modification of 16S ribosomal RNA by kethoxal. , 1972, Proceedings of the National Academy of Sciences of the United States of America.

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

[112]  P. Bevilacqua,et al.  Glyoxals as in vivo RNA structural probes of guanine base-pairing. , 2018, RNA.

[113]  Christopher A. Lavender,et al.  In-cell SHAPE reveals that free 30S ribosome subunits are in the inactive state , 2015, Proceedings of the National Academy of Sciences.

[114]  Robert D. Finn,et al.  Rfam 13.0: shifting to a genome-centric resource for non-coding RNA families , 2017, Nucleic Acids Res..

[115]  Janusz M Bujnicki,et al.  Computational modeling of RNA 3D structures, with the aid of experimental restraints , 2014, RNA biology.

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

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

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

[119]  R R Breaker,et al.  Relationship between internucleotide linkage geometry and the stability of RNA. , 1999, RNA.

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

[121]  Kyle E. Watters,et al.  Probing of RNA structures in a positive sense RNA virus reveals selection pressures for structural elements , 2017, Nucleic acids research.

[122]  Rhiju Das,et al.  Consistent global structures of complex RNA states through multidimensional chemical mapping , 2015, eLife.

[123]  H. Al‐Hashimi,et al.  RNA dynamics: it is about time. , 2008, Current opinion in structural biology.

[124]  J. Weissman,et al.  DMS-MaPseq for genome-wide or targeted RNA structure probing in vivo , 2016, Nature Methods.

[125]  A. Krogh,et al.  SHAPE Selection (SHAPES) enrich for RNA structure signal in SHAPE sequencing-based probing data. , 2015, RNA.

[126]  Yiliang Ding,et al.  Determination of in vivo RNA structure in low-abundance transcripts , 2013, Nature Communications.

[127]  A. L. Mackay,et al.  Crystallography , 1976, Nature.

[128]  Julius B. Lucks,et al.  An RNA Mapping DataBase for curating RNA structure mapping experiments , 2012, Bioinform..

[129]  Gabriele Varani,et al.  Strong correlation between SHAPE chemistry and the generalized NMR order parameter (S2) in RNA. , 2008, Journal of the American Chemical Society.

[130]  Morgan C. Giddings,et al.  High-Throughput SHAPE Analysis Reveals Structures in HIV-1 Genomic RNA Strongly Conserved across Distinct Biological States , 2008, PLoS biology.

[131]  B Lucks Julius,et al.  プライマー伸長塩基配列決定法(SHAPE‐Seq)を用いて分析した選択的2′‐ヒドロキシルアシル化による多重RNA構造の特徴化 , 2011 .

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

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

[134]  Gaurav Sharma,et al.  Modeling RNA Secondary Structure with Sequence Comparison and Experimental Mapping Data. , 2017, Biophysical journal.

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

[136]  Feng Ding,et al.  Native-like RNA tertiary structures using a sequence-encoded cleavage agent and refinement by discrete molecular dynamics. , 2009, Journal of the American Chemical Society.

[137]  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.

[138]  J. Tyson About time , 1996, Nature.

[139]  Viviana Gradinaru,et al.  Single-molecule RNA detection at depth by hybridization chain reaction and tissue hydrogel embedding and clearing , 2016, Development.

[140]  Peter F. Stadler,et al.  SHAPE directed RNA folding , 2015, bioRxiv.

[141]  Craig L. Zirbel,et al.  Sharing and archiving nucleic acid structure mapping data. , 2011, RNA.

[142]  K. Weeks,et al.  C2′-endo nucleotides as molecular timers suggested by the folding of an RNA domain , 2009, Proceedings of the National Academy of Sciences.

[143]  S. Luo,et al.  RNA-ligase-dependent biases in miRNA representation in deep-sequenced small RNA cDNA libraries. , 2011, RNA.

[144]  Jernej Ule,et al.  hiCLIP reveals the in vivo atlas of mRNA secondary structures recognized by Staufen 1 , 2015, Nature.

[145]  Lior Pachter,et al.  RNA structure characterization from chemical mapping experiments , 2011, 2011 49th Annual Allerton Conference on Communication, Control, and Computing (Allerton).

[146]  Kevin M Weeks,et al.  RNA SHAPE chemistry reveals nonhierarchical interactions dominate equilibrium structural transitions in tRNA(Asp) transcripts. , 2005, Journal of the American Chemical Society.

[147]  Paul D. Carlson,et al.  Characterizing the Structure-Function Relationship of a Naturally Occurring RNA Thermometer. , 2017, Biochemistry.

[148]  A. Krainer,et al.  Antisense-oligonucleotide-directed inhibition of nonsense-mediated mRNA decay , 2015, Nature Biotechnology.

[149]  Manolis Kellis,et al.  Best practices for genome-wide RNA structure analysis: combination of mutational profiles and drop-off information , 2017, bioRxiv.

[150]  D. Bartel,et al.  RNA G-quadruplexes are globally unfolded in eukaryotic cells and depleted in bacteria , 2016, Science.

[151]  G. Storz,et al.  Bacterial small RNA regulators: versatile roles and rapidly evolving variations. , 2011, Cold Spring Harbor perspectives in biology.

[152]  Robert Tibshirani,et al.  Genome-wide measurement of RNA folding energies. , 2012, Molecular cell.

[153]  B. Wold,et al.  Sequence census methods for functional genomics , 2008, Nature Methods.

[154]  Kang Zhang,et al.  Mapping RNA–RNA interactome and RNA structure in vivo by MARIO , 2016, Nature Communications.

[155]  Howard Y. Chang,et al.  Comparison of SHAPE reagents for mapping RNA structures inside living cells , 2017, RNA.

[156]  Risa Kawaguchi,et al.  Parallel computation of genome-scale RNA secondary structure to detect structural constraints on human genome , 2016, BMC Bioinformatics.

[157]  D. Bartel,et al.  Widespread Influence of 3′-End Structures on Mammalian mRNA Processing and Stability , 2017, Cell.

[158]  David Evans,et al.  Overview of methods , 2008 .

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

[160]  Howard Y. Chang,et al.  RNA SHAPE analysis in living cells. , 2013, Nature chemical biology.

[161]  K. Weeks,et al.  RNA structure analysis at single nucleotide resolution by selective 2'-hydroxyl acylation and primer extension (SHAPE). , 2005, Journal of the American Chemical Society.

[162]  David H Burkhardt,et al.  Operon mRNAs are organized into ORF-centric structures that predict translation efficiency , 2017, eLife.

[163]  J. T. Madison,et al.  Structure of a Ribonucleic Acid , 1965, Science.

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

[165]  K. Weeks,et al.  Selective 2'-hydroxyl acylation analyzed by protection from exoribonuclease. , 2010, Journal of the American Chemical Society.

[166]  K. Weeks,et al.  Fingerprinting noncanonical and tertiary RNA structures by differential SHAPE reactivity. , 2012, Journal of the American Chemical Society.

[167]  Fei Deng,et al.  SEQualyzer: interactive tool for quality control and exploratory analysis of high‐throughput RNA structural profiling data , 2017, Bioinform..

[168]  J. Rinn,et al.  Localization and abundance analysis of human lncRNAs at single-cell and single-molecule resolution , 2015, Genome Biology.

[169]  Razvan Nutiu,et al.  Pervasive Regulatory Functions of mRNA Structure Revealed by High-Resolution SHAPE Probing , 2018, Cell.

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

[171]  A. Pardi,et al.  NMR Methods for Studying the Structure and Dynamics of RNA , 2005, Chembiochem : a European journal of chemical biology.

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

[173]  Chuan-Tien Hung,et al.  Control of the negative IRES trans-acting factor KHSRP by ubiquitination , 2016, Nucleic acids research.

[174]  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.

[175]  R. Finkel,et al.  Treatment of infantile-onset spinal muscular atrophy with nusinersen: a phase 2, open-label, dose-escalation study , 2016, The Lancet.

[176]  Giovanni Bussi,et al.  Molecular Dynamics Simulations Reveal an Interplay between SHAPE Reagent Binding and RNA Flexibility , 2017, The journal of physical chemistry letters.

[177]  T. Cech,et al.  The Ribosome Is a Ribozyme , 2000, Science.

[178]  K. Weeks,et al.  Functionally conserved architecture of hepatitis C virus RNA genomes , 2015, Proceedings of the National Academy of Sciences.

[179]  Michael T. Wolfinger,et al.  Predicting RNA secondary structures from sequence and probing data. , 2016, Methods.

[180]  P. Ryvkin,et al.  Genome-Wide Double-Stranded RNA Sequencing Reveals the Functional Significance of Base-Paired RNAs in Arabidopsis , 2010, PLoS genetics.

[181]  R. Russell,et al.  DMS footprinting of structured RNAs and RNA–protein complexes , 2007, Nature Protocols.

[182]  J. Lucks,et al.  Characterizing the structure-function relationship of a naturally-occurring RNA thermometer , 2017, bioRxiv.

[183]  Kyle E. Watters,et al.  Distributed biotin–streptavidin transcription roadblocks for mapping cotranscriptional RNA folding , 2017, Nucleic acids research.

[184]  David H Mathews,et al.  RNA structure prediction: an overview of methods. , 2012, Methods in molecular biology.

[185]  M. Rutenberg-Schoenberg,et al.  Interpreting Reverse Transcriptase Termination and Mutation Events for Greater Insight into the Chemical Probing of RNA. , 2017, Biochemistry.