Sharing and archiving nucleic acid structure mapping data.

Nucleic acids are particularly amenable to structural characterization using chemical and enzymatic probes. Each individual structure mapping experiment reveals specific information about the structure and/or dynamics of the nucleic acid. Currently, there is no simple approach for making these data publically available in a standardized format. We therefore developed a standard for reporting the results of single nucleotide resolution nucleic acid structure mapping experiments, or SNRNASMs. We propose a schema for sharing nucleic acid chemical probing data that uses generic public servers for storing, retrieving, and searching the data. We have also developed a consistent nomenclature (ontology) within the Ontology of Biomedical Investigations (OBI), which provides unique identifiers (termed persistent URLs, or PURLs) for classifying the data. Links to standardized data sets shared using our proposed format along with a tutorial and links to templates can be found at http://snrnasm.bio.unc.edu.

[1]  Donald F. Senear,et al.  [9] Quantitative DNase footprint titration: A method for studying protein-DNA interactions , 1986 .

[2]  M. Chance,et al.  Monovalent cations mediate formation of native tertiary structure of the Tetrahymena thermophila ribozyme , 2002, Nature Structural Biology.

[3]  Cathy H. Wu,et al.  Framework for a Protein Ontology , 2006, TMBIO '06.

[4]  Nan Yu,et al.  The Comparative RNA Web (CRW) Site: an online database of comparative sequence and structure information for ribosomal, intron, and other RNAs , 2002, BMC Bioinformatics.

[5]  N. Walter,et al.  Probing non-selective cation binding in the hairpin ribozyme with Tb(III). , 2000, Journal of molecular biology.

[6]  D. Turner,et al.  Secondary structure model of the RNA recognized by the reverse transcriptase from the R2 retrotransposable element. , 1997, RNA.

[7]  A. Laederach,et al.  Evaluation of the information content of RNA structure mapping data for secondary structure prediction. , 2010, RNA.

[8]  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.

[9]  Todd A. Anderson,et al.  Computational identification of microRNAs and their targets , 2006, Comput. Biol. Chem..

[10]  A. Maxam,et al.  Structure mapping of 5'-32P-labeled RNA with S1 nuclease. , 1978, Biochemistry.

[11]  M. A. Shea,et al.  Quantitative DNase footprint titration: a method for studying protein-DNA interactions. , 1986, Methods in enzymology.

[12]  D. Herschlag,et al.  Probing the folding landscape of the Tetrahymena ribozyme: commitment to form the native conformation is late in the folding pathway. , 2001, Journal of molecular biology.

[13]  Prachi Shah,et al.  The ENCODEdb portal: simplified access to ENCODE Consortium data. , 2007, Genome research.

[14]  J. Barton,et al.  Rh(DIP)3(3+): a shape-selective metal complex which targets cruciforms. , 1988, Nucleic acids research.

[15]  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.

[16]  Jian Zhang,et al.  The Protein Ontology: a structured representation of protein forms and complexes , 2010, Nucleic Acids Res..

[17]  Samson W. Tu,et al.  Protégé-2000: An Open-Source Ontology-Development and Knowledge-Acquisition Environment: AMIA 2003 Open Source Expo , 2003, AMIA.

[18]  Chris F. Taylor,et al.  Development of FuGO: an ontology for functional genomics investigations. , 2006, Omics : a journal of integrative biology.

[19]  Jessica A. Turner,et al.  Modeling biomedical experimental processes with OBI , 2010, J. Biomed. Semant..

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

[21]  K. Weeks,et al.  Toward global RNA structure analysis , 2010, Nature Biotechnology.

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

[23]  S. Woodson,et al.  RNA folding and ribosome assembly. , 2008, Current opinion in chemical biology.

[24]  J. Barton,et al.  Metals and DNA: molecular left-handed complements , 1986, Science.

[25]  E. Westhof,et al.  Analysis of RNA motifs. , 2003, Current opinion in structural biology.

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

[27]  E. Westhof,et al.  Binding of Escherichia coli ribosomal protein S8 to 16 S rRNA. A model for the interaction and the tertiary structure of the RNA binding site. , 1987, Journal of molecular biology.

[28]  R. E. Lockard,et al.  Mapping tRNA structure in solution using double-strand-specific ribonuclease V1 from cobra venom. , 1981, Nucleic acids research.

[29]  G J Williams,et al.  The Protein Data Bank: a computer-based archival file for macromolecular structures. , 1977, Journal of molecular biology.

[30]  T. N. Bhat,et al.  The Protein Data Bank , 2000, Nucleic Acids Res..

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

[32]  J. Ebel,et al.  The tRNA‐like structure of turnip yellow mosaic virus RNA: structural organization of the last 159 nucleotides from the 3′ OH terminus , 1982, The EMBO journal.

[33]  Oliver Hofmann,et al.  ISA software suite: supporting standards-compliant experimental annotation and enabling curation at the community level , 2010, Bioinform..

[34]  RNA structure analysis using T2 ribonuclease: detection of pH and metal ion induced conformational changes in yeast tRNAPhe. , 1984, Nucleic acids research.

[35]  Daniel Herschlag,et al.  Semiautomated and rapid quantification of nucleic acid footprinting and structure mapping experiments , 2008, Nature Protocols.

[36]  D. Thirumalai,et al.  RNA and protein folding: common themes and variations. , 2005, Biochemistry.

[37]  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.

[38]  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.

[39]  A. Tranguch,et al.  Structure-sensitive RNA footprinting of yeast nuclear ribonuclease P. , 1994, Biochemistry.

[40]  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.

[41]  R. Breaker,et al.  In-line probing analysis of riboswitches. , 2008, Methods in molecular biology.

[42]  Sebastian Doniach,et al.  Principles of RNA compaction: insights from the equilibrium folding pathway of the P4-P6 RNA domain in monovalent cations. , 2004, Journal of molecular biology.

[43]  H. Noller,et al.  Directed hydroxyl radical probing of 16S rRNA using Fe(II) tethered to ribosomal protein S4. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[44]  James W. Brown,et al.  The RNA Ontology Consortium: an open invitation to the RNA community. , 2006, RNA.

[45]  D. Thirumalai,et al.  Role of counterion condensation in folding of the Tetrahymena ribozyme. I. Equilibrium stabilization by cations. , 2001, Journal of molecular biology.

[46]  X. Zhuang,et al.  Exploring the folding landscape of a structured RNA , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[47]  V. Vlassov,et al.  The tertiary structure of yeast tRNAPhe in solution studied by phosphodiester bond modification with ethylnitrosourea , 1980, FEBS letters.

[48]  Morgan C. Giddings,et al.  ShapeFinder: a software system for high-throughput quantitative analysis of nucleic acid reactivity information resolved by capillary electrophoresis. , 2008, RNA.

[49]  J. Doudna,et al.  Ribozyme structures and mechanisms. , 2000, Annual review of biochemistry.

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

[51]  Sean R. Eddy,et al.  Rfam: an RNA family database , 2003, Nucleic Acids Res..

[52]  D. Herschlag,et al.  The paradoxical behavior of a highly structured misfolded intermediate in RNA folding. , 2006, Journal of molecular biology.

[53]  James W. Brown,et al.  The RNA structure alignment ontology. , 2009, RNA.

[54]  M. Brenowitz,et al.  Monitoring structural changes in nucleic acids with single residue spatial and millisecond time resolution by quantitative hydroxyl radical footprinting , 2008, Nature Protocols.

[55]  Karen Eilbeck,et al.  The RNA Ontology (RNAO): An ontology for integrating RNA sequence and structure data , 2009, Appl. Ontology.

[56]  A. Rich,et al.  Chemical probes of DNA conformation: detection of Z-DNA at nucleotide resolution , 1985, Cell.

[57]  D. Galas,et al.  DNAse footprinting: a simple method for the detection of protein-DNA binding specificity. , 1978, Nucleic acids research.

[58]  Andrea Barta,et al.  Strategies for RNA folding and assembly , 2004, Nature Reviews Molecular Cell Biology.

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

[60]  P. Wrede,et al.  Conformational changes of yeast tRNAPhe and E. coli tRNA2Glu as indicated by different nuclease digestion patterns. , 1979, The Journal of biological chemistry.

[61]  S. Woodson.  Recent insights on RNA folding mechanisms from catalytic RNA , 2000, Cellular and Molecular Life Sciences CMLS.

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

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

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

[65]  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.

[66]  Rapid quantification and analysis of kinetic •OH radical footprinting data using SAFA. , 2009, Methods in enzymology.

[67]  M. Chance,et al.  Multiple monovalent ion-dependent pathways for the folding of the L-21 Tetrahymena thermophila ribozyme. , 2003, Journal of molecular biology.

[68]  G J Williams,et al.  The Protein Data Bank: a computer-based archival file for macromolecular structures. , 1978, Archives of biochemistry and biophysics.

[69]  K. Weeks.  Advances in RNA structure analysis by chemical probing. , 2010, Current opinion in structural biology.

[70]  Sean R. Eddy,et al.  Rfam: annotating non-coding RNAs in complete genomes , 2004, Nucleic Acids Res..

[71]  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.

[72]  M A Musen,et al.  BioPortal: ontologies and data resources with the click of a mouse. , 2008, AMIA ... Annual Symposium proceedings. AMIA Symposium.

[73]  D. Thirumalai,et al.  Counterion charge density determines the position and plasticity of RNA folding transition states. , 2006, Journal of molecular biology.

[74]  C. Ralston,et al.  Folding mechanism of the Tetrahymena ribozyme P4-P6 domain. , 2000, Biochemistry.

[75]  Magdalena A. Jonikas,et al.  Distinct contribution of electrostatics, initial conformational ensemble, and macromolecular stability in RNA folding , 2007, Proceedings of the National Academy of Sciences.

[76]  K. Coffman,et al.  Secondary , 2020, Definitions.

[77]  D. Baker,et al.  Atomic accuracy in predicting and designing non-canonical RNA structure , 2010, Nature Methods.

[78]  D. Thirumalai,et al.  Role of counterion condensation in folding of the Tetrahymena ribozyme. II. Counterion-dependence of folding kinetics. , 2001, Journal of molecular biology.

[79]  Kirill Degtyarenko,et al.  ChEBI: An Open Bioinformatics and Cheminformatics Resource , 2009, Current protocols in bioinformatics.

[80]  Magdalena A. Jonikas,et al.  Structural inference of native and partially folded RNA by high-throughput contact mapping , 2008, Proceedings of the National Academy of Sciences.

[81]  Changbong Hyeon,et al.  Charge density of divalent metal cations determines RNA stability. , 2007, Journal of the American Chemical Society.

[82]  Mark A. Musen,et al.  OBO to OWL: a protégé OWL tab to read/save OBO ontologies , 2007, Bioinform..

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

[84]  T. Cech,et al.  Visualizing the higher order folding of a catalytic RNA molecule. , 1991, Science.

[85]  David L. Wheeler,et al.  GenBank , 2015, Nucleic Acids Res..

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

[87]  T. Tullius.  Probing DNA Structure with Hydroxyl Radicals , 2001, Current protocols in nucleic acid chemistry.

[88]  Michael Darsow,et al.  ChEBI: a database and ontology for chemical entities of biological interest , 2007, Nucleic Acids Res..

[89]  J. Vournakis,et al.  RNA structure analysis using methidiumpropyl-EDTA.Fe(II): a base-pair-specific RNA structure probe. , 1984, Proceedings of the National Academy of Sciences of the United States of America.