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PMID: 29426922 Published · epublish English Evaluation Study Journal Article Research Support, N.I.H., Extramural

Statistical modeling of RNA structure profiling experiments enables parsimonious reconstruction of structure landscapes.

Nature communications ·Vol. 9 ·No. 1 ·2018-00-09 ·Pages 606

Li H, Aviran S

Abstract

RNA plays key regulatory roles in diverse cellular processes, where its functionality often derives from folding into and converting between structures. Many RNAs further rely on co-existence of alternative structures, which govern their response to cellular signals. However, characterizing heterogeneous landscapes is difficult, both experimentally and computationally. Recently, structure profiling experiments have emerged as powerful and affordable structure characterization methods, which improve computational structure prediction. To date, efforts have centered on predicting one optimal structure, with much less progress made on multiple-structure prediction. Here, we report a probabilistic modeling approach that predicts a parsimonious set of co-existing structures and estimates their abundances from structure profiling data. We demonstrate robust landscape reconstruction and quantitative insights into structural dynamics by analyzing numerous data sets. This work establishes a framework for data-directed characterization of structure landscapes to aid experimentalists in performing structure-function studies.

MeSH Terms
Models, Chemical Models, Statistical Molecular Structure RNA/chemistry Riboswitch
Chemicals
Riboswitch RNA
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Li Hua
Department of Biomedical Engineering and Genome Center, University of California at Davis, Davis, CA, 95616, USA.
Aviran Sharon ORCID
Department of Biomedical Engineering and Genome Center, University of California at Davis, Davis, CA, 95616, USA. saviran@ucdavis.edu.
References (69)
69 references, click to expand
  1. RNA secondary structure prediction by centroids in a Boltzmann weighted ensemble.
    RNA. 2005 Aug;11(8):1157-66 PMID: 16043502
  2. Non-coding RNAs: regulators of disease.
    J Pathol. 2010 Jan;220(2):126-39 PMID: 19882673
  3. Transcending the prediction paradigm: novel applications of SHAPE to RNA function and evolution.
    Wiley Interdiscip Rev RNA. 2017 Jan;8(1): PMID: 27396578
  4. Genome-wide probing of RNA structure reveals active unfolding of mRNA structures in vivo.
    Nature. 2014 Jan 30;505(7485):701-5 PMID: 24336214
  5. RNA motif discovery by SHAPE and mutational profiling (SHAPE-MaP).
    Nat Methods. 2014 Sep;11(9):959-65 PMID: 25028896
  6. Assessing the reliability of RNA folding using statistical mechanics.
    J Mol Biol. 1997 Apr 18;267(5):1104-12 PMID: 9150399
  7. Regulation of bacterial gene expression by riboswitches.
    Annu Rev Microbiol. 2005;59:487-517 PMID: 16153177
  8. Fast gapped-read alignment with Bowtie 2.
    Nat Methods. 2012 Mar 04;9(4):357-9 PMID: 22388286
  9. GTfold: enabling parallel RNA secondary structure prediction on multi-core desktops.
    BMC Res Notes. 2012 Jul 02;5:341 PMID: 22747589
  10. ViennaRNA Package 2.0.
    Algorithms Mol Biol. 2011 Nov 24;6:26 PMID: 22115189
  11. Comparative Visualization of the RNA Suboptimal Conformational Ensemble In Vivo.
    Biophys J. 2017 Jul 25;113(2):290-301 PMID: 28625696
  12. RNAstructure: software for RNA secondary structure prediction and analysis.
    BMC Bioinformatics. 2010 Mar 15;11:129 PMID: 20230624
  13. Rich RNA Structure Landscapes Revealed by Mutate-and-Map Analysis.
    PLoS Comput Biol. 2015 Nov 13;11(11):e1004473 PMID: 26566145
  14. Improving RNA secondary structure prediction with structure mapping data.
    Methods Enzymol. 2015;553:91-114 PMID: 25726462
  15. Sensitive measurement of single-nucleotide polymorphism-induced changes of RNA conformation: application to disease studies.
    Nucleic Acids Res. 2013 Jan 7;41(1):44-53 PMID: 23125360
  16. New insights from cluster analysis methods for RNA secondary structure prediction.
    Wiley Interdiscip Rev RNA. 2016 May;7(3):278-94 PMID: 26971529
  17. RNA-guided assembly of Rev-RRE nuclear export complexes.
    Elife. 2014 Aug 27;3:e03656 PMID: 25163983
  18. Folding of a transcriptionally acting preQ1 riboswitch.
    Proc Natl Acad Sci U S A. 2010 Jun 15;107(24):10804-9 PMID: 20534493
  19. Comparative and integrative analysis of RNA structural profiling data: current practices and emerging questions.
    Quant Biol. 2017 Mar;5(1):3-24 PMID: 28717530
  20. Disease-associated mutations that alter the RNA structural ensemble.
    PLoS Genet. 2010 Aug 19;6(8):e1001074 PMID: 20808897
  21. SHAPE directed RNA folding.
    Bioinformatics. 2016 Jan 1;32(1):145-7 PMID: 26353838
  22. RNA Thermodynamic Structural Entropy.
    PLoS One. 2015 Nov 10;10(11):e0137859 PMID: 26555444
  23. Insights into RNA structure and function from genome-wide studies.
    Nat Rev Genet. 2014 Jul;15(7):469-79 PMID: 24821474
  24. Statistical and Bayesian approaches to RNA secondary structure prediction.
    RNA. 2006 Mar;12(3):323-31 PMID: 16495231
  25. Structural Analysis using SHALiPE to Reveal RNA G-Quadruplex Formation in Human Precursor MicroRNA.
    Angew Chem Int Ed Engl. 2016 Jul 25;55(31):8958-61 PMID: 27355429
  26. Widespread genetic switches and toxicity resistance proteins for fluoride.
    Science. 2012 Jan 13;335(6065):233-235 PMID: 22194412
  27. SEQualyzer: interactive tool for quality control and exploratory analysis of high-throughput RNA structural profiling data.
    Bioinformatics. 2017 Feb 1;33(3):441-443 PMID: 28172632
  28. Multiple conformations are a conserved and regulatory feature of the RB1 5' UTR.
    RNA. 2015 Jul;21(7):1274-85 PMID: 25999316
  29. A decade of riboswitches.
    Cell. 2013 Jan 17;152(1-2):17-24 PMID: 23332744
  30. Cotranscriptional folding of a riboswitch at nucleotide resolution.
    Nat Struct Mol Biol. 2016 Dec;23 (12 ):1124-1131 PMID: 27798597
  31. Computational analysis of conserved RNA secondary structure in transcriptomes and genomes.
    Annu Rev Biophys. 2014;43:433-56 PMID: 24895857
  32. An excited state underlies gene regulation of a transcriptional riboswitch.
    Nat Chem Biol. 2017 Sep;13(9):968-974 PMID: 28719589
  33. Evaluating the accuracy of SHAPE-directed RNA secondary structure predictions.
    Nucleic Acids Res. 2013 Mar 1;41(5):2807-16 PMID: 23325843
  34. An RNA hairpin to G-quadruplex conformational transition.
    J Am Chem Soc. 2012 Dec 12;134(49):19953-6 PMID: 23190255
  35. Prediction of RNA secondary structure by free energy minimization.
    Curr Opin Struct Biol. 2006 Jun;16(3):270-8 PMID: 16713706
  36. Three-state mechanism couples ligand and temperature sensing in riboswitches.
    Nature. 2013 Jul 18;499(7458):355-9 PMID: 23842498
  37. Quantitative dimethyl sulfate mapping for automated RNA secondary structure inference.
    Biochemistry. 2012 Sep 11;51(36):7037-9 PMID: 22913637
  38. Modeling RNA secondary structure folding ensembles using SHAPE mapping data.
    Nucleic Acids Res. 2018 Jan 9;46(1):314-323 PMID: 29177466
  39. Accurate SHAPE-directed RNA secondary structure modeling, including pseudoknots.
    Proc Natl Acad Sci U S A. 2013 Apr 2;110(14):5498-503 PMID: 23503844
  40. The noncoding RNA revolution-trashing old rules to forge new ones.
    Cell. 2014 Mar 27;157(1):77-94 PMID: 24679528
  41. UNAFold: software for nucleic acid folding and hybridization.
    Methods Mol Biol. 2008;453:3-31 PMID: 18712296
  42. SHAPE-directed RNA secondary structure prediction.
    Methods. 2010 Oct;52(2):150-8 PMID: 20554050
  43. Progress and challenges for chemical probing of RNA structure inside living cells.
    Nat Chem Biol. 2015 Dec;11(12):933-41 PMID: 26575240
  44. Systematic probing of the bacterial RNA structurome to reveal new functions.
    Curr Opin Microbiol. 2017 Apr;36:14-19 PMID: 28160611
  45. Rational experiment design for sequencing-based RNA structure mapping.
    RNA. 2014 Dec;20(12):1864-77 PMID: 25332375
  46. DMS-MaPseq for genome-wide or targeted RNA structure probing in vivo.
    Nat Methods. 2017 Jan;14 (1):75-82 PMID: 27819661
  47. Bacterial RNA thermometers: molecular zippers and switches.
    Nat Rev Microbiol. 2012 Mar 16;10(4):255-65 PMID: 22421878
  48. Improving RNA-Seq expression estimates by correcting for fragment bias.
    Genome Biol. 2011;12(3):R22 PMID: 21410973
  49. The mechanisms of RNA SHAPE chemistry.
    J Am Chem Soc. 2012 Apr 18;134(15):6617-24 PMID: 22475022
  50. Engineering and In Vivo Applications of Riboswitches.
    Annu Rev Biochem. 2017 Jun 20;86:515-539 PMID: 28375743
  51. Comparison of solution and crystal structures of preQ1 riboswitch reveals calcium-induced changes in conformation and dynamics.
    J Am Chem Soc. 2011 Apr 13;133(14):5190-3 PMID: 21410253
  52. A statistical sampling algorithm for RNA secondary structure prediction.
    Nucleic Acids Res. 2003 Dec 15;31(24):7280-301 PMID: 14654704
  53. Data-directed RNA secondary structure prediction using probabilistic modeling.
    RNA. 2016 Aug;22(8):1109-19 PMID: 27251549
  54. Single-molecule correlated chemical probing of RNA.
    Proc Natl Acad Sci U S A. 2014 Sep 23;111(38):13858-63 PMID: 25205807
  55. Fluoride ion encapsulation by Mg2+ ions and phosphates in a fluoride riboswitch.
    Nature. 2012 May 13;486(7401):85-9 PMID: 22678284
  56. Metrics for rapid quality control in RNA structure probing experiments.
    Bioinformatics. 2016 Dec 1;32(23 ):3575-3583 PMID: 27497441
  57. Accurate SHAPE-directed RNA structure determination.
    Proc Natl Acad Sci U S A. 2009 Jan 6;106(1):97-102 PMID: 19109441
  58. The dynamic landscapes of RNA architecture.
    Cell. 2009 Feb 20;136(4):604-9 PMID: 19239882
  59. Evaluation of the information content of RNA structure mapping data for secondary structure prediction.
    RNA. 2010 Jun;16(6):1108-17 PMID: 20413617
  60. Visualizing the global secondary structure of a viral RNA genome with cryo-electron microscopy.
    RNA. 2015 May;21(5):877-86 PMID: 25752599
  61. Design of RNAs: comparing programs for inverse RNA folding.
    Brief Bioinform. 2017 Jan 3;:null PMID: 28049135
  62. RNA Regulators: Formidable Modulators of Yersinia Virulence.
    Trends Microbiol. 2017 Jan;25(1):19-34 PMID: 27651123
  63. Profiling small RNA reveals multimodal substructural signals in a Boltzmann ensemble.
    Nucleic Acids Res. 2014 Dec 16;42(22):e171 PMID: 25392423
  64. Entropic stabilization of folded RNA in crowded solutions measured by SAXS.
    Nucleic Acids Res. 2016 Nov 2;44(19):9452-9461 PMID: 27378777
  65. PROBer Provides a General Toolkit for Analyzing Sequencing-Based Toeprinting Assays.
    Cell Syst. 2017 May 24;4(5):568-574.e7 PMID: 28501650
  66. Using an RNA secondary structure partition function to determine confidence in base pairs predicted by free energy minimization.
    RNA. 2004 Aug;10(8):1178-90 PMID: 15272118
  67. Probing the structure of RNAs in solution.
    Nucleic Acids Res. 1987 Nov 25;15(22):9109-28 PMID: 2446263
  68. Sparse linear modeling of next-generation mRNA sequencing (RNA-Seq) data for isoform discovery and abundance estimation.
    Proc Natl Acad Sci U S A. 2011 Dec 13;108(50):19867-72 PMID: 22135461
  69. Modeling and automation of sequencing-based characterization of RNA structure.
    Proc Natl Acad Sci U S A. 2011 Jul 5;108(27):11069-74 PMID: 21642536
Article Info
Journal
Nature communications
Abbr.
Nat Commun
ISSN
2041-1723
Published
2018-00-09
Epub
2018-00-09
Pages
606
Language
English
Region
England
NLM ID
101528555
PMCID
PMC5807309
Subset
IM
Grants
NHGRI NIH HHS · K99 HG006860 · United States
NHGRI NIH HHS · R00 HG006860 · United States
Corrections
ErratumIn
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