Home LiteratureArticle Details
PMID: 30275275 Published · epublish English Journal Article Research Support, U.S. Gov't, Non-P.H.S. Review

Technique Development for Probing RNA Structure In Vivo and Genome-Wide.

Cold Spring Harbor perspectives in biology ·Vol. 10 ·No. 10 ·2018-00-01

Bevilacqua PC, Assmann SM

Abstract

How organisms perceive and respond to their surroundings is one of the great questions in biology. It is clear that RNA plays key roles in sensing. Cellular and environmental cues that RNA responds to include temperature, ions, metabolites, and biopolymers. Recent advances in next-generation sequencing and in vivo chemical probing have provided unprecedented insights into RNA folding in vivo and genome-wide. Patterns of chemical reactivity have implicated control of gene expression by RNA and aided prediction of RNA structure. Central to these advances has been development of molecular biological and chemical techniques. Key advances are improvements in the quality, cost, and throughput of library preparation; availability of a wider array of chemicals for probing RNA structure in vivo; and robustness and user friendliness of data analysis. Insights from probing transcriptomes and future directions are provided.

MeSH Terms
Animals Base Sequence Genome-Wide Association Study/methods Humans Nucleic Acid Amplification Techniques Nucleic Acid Conformation RNA/chemistry,genetics
Chemicals
RNA
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Bevilacqua Philip C ORCID
Departments of Chemistry and Biochemistry & Molecular Biology, Pennsylvania State University, University Park, Pennsylvania 16802.
Assmann Sarah M ORCID
Department of Biology, Pennsylvania State University, University Park, Pennsylvania 16802.
References (96)
96 references, click to expand
  1. Light-activated chemical probing of nucleobase solvent accessibility inside cells.
    Nat Chem Biol. 2018 Mar;14(3):276-283 PMID: 29334380
  2. Accurate detection of chemical modifications in RNA by mutational profiling (MaP) with ShapeMapper 2.
    RNA. 2018 Feb;24(2):143-148 PMID: 29114018
  3. Sizing up long non-coding RNAs: do lncRNAs have secondary and tertiary structure?
    Bioarchitecture. 2012 Nov-Dec;2(6):189-99 PMID: 23267412
  4. FragSeq: transcriptome-wide RNA structure probing using high-throughput sequencing.
    Nat Methods. 2010 Dec;7(12):995-1001 PMID: 21057495
  5. Determination of in vivo RNA structure in low-abundance transcripts.
    Nat Commun. 2013;4:2971 PMID: 24336128
  6. Long noncoding RNAs: past, present, and future.
    Genetics. 2013 Mar;193(3):651-69 PMID: 23463798
  7. RNA thermometers.
    FEMS Microbiol Rev. 2006 Jan;30(1):3-16 PMID: 16438677
  8. Statistical modeling of RNA structure profiling experiments enables parsimonious reconstruction of structure landscapes.
    Nat Commun. 2018 Feb 9;9(1):606 PMID: 29426922
  9. Genome-wide measurement of RNA folding energies.
    Mol Cell. 2012 Oct 26;48(2):169-81 PMID: 22981864
  10. DMS-Seq for In Vivo Genome-wide Mapping of Protein-DNA Interactions and Nucleosome Centers.
    Cell Rep. 2017 Oct 3;21(1):289-300 PMID: 28978481
  11. Pervasive transcription of the human genome produces thousands of previously unidentified long intergenic noncoding RNAs.
    PLoS Genet. 2013 Jun;9(6):e1003569 PMID: 23818866
  12. Probing the structure of RNAs in solution.
    Nucleic Acids Res. 1987 Nov 25;15(22):9109-28 PMID: 2446263
  13. Mobile Bacterial Group II Introns at the Crux of Eukaryotic Evolution.
    Microbiol Spectr. 2015 Feb;3(1):MDNA3-0050-2014 PMID: 26104554
  14. Do nucleic acids moonlight as molecular chaperones?
    Nucleic Acids Res. 2016 Jun 2;44(10):4835-45 PMID: 27105849
  15. Structural architecture of the human long non-coding RNA, steroid receptor RNA activator.
    Nucleic Acids Res. 2012 Jun;40(11):5034-51 PMID: 22362738
  16. Pervasive transcription: detecting functional RNAs in bacteria.
    Transcription. 2014;5(4):e944039 PMID: 25483405
  17. Mod-seq: high-throughput sequencing for chemical probing of RNA structure.
    RNA. 2014 May;20(5):713-20 PMID: 24664469
  18. Selective 2'-hydroxyl acylation analyzed by primer extension and mutational profiling (SHAPE-MaP) for direct, versatile and accurate RNA structure analysis.
    Nat Protoc. 2015 Nov;10(11):1643-69 PMID: 26426499
  19. 2-D structure of the A region of Xist RNA and its implication for PRC2 association.
    PLoS Biol. 2010 Jan;8(1):e1000276 PMID: 20052282
  20. Where to begin? Mapping transcription start sites genome-wide in Escherichia coli.
    J Bacteriol. 2015 Jan 1;197(1):4-6 PMID: 25331438
  21. The mechanisms of RNA SHAPE chemistry.
    J Am Chem Soc. 2012 Apr 18;134(15):6617-24 PMID: 22475022
  22. RNA helical imperfections regulate activation of the protein kinase PKR: effects of bulge position, size, and geometry.
    RNA. 2011 May;17(5):957-66 PMID: 21460237
  23. Integration of omic networks in a developmental atlas of maize.
    Science. 2016 Aug 19;353(6301):814-8 PMID: 27540173
  24. RNA-Puzzles Round III: 3D RNA structure prediction of five riboswitches and one ribozyme.
    RNA. 2017 May;23(5):655-672 PMID: 28138060
  25. Sensing of RNA viruses: a review of innate immune receptors involved in recognizing RNA virus invasion.
    J Virol. 2012 Mar;86(6):2900-10 PMID: 22258243
  26. Mapping tRNA structure in solution using double-strand-specific ribonuclease V1 from cobra venom.
    Nucleic Acids Res. 1981 Oct 10;9(19):5125-40 PMID: 7031604
  27. CryoEM structures of two spliceosomal complexes: starter and dessert at the spliceosome feast.
    Curr Opin Struct Biol. 2016 Feb;36:48-57 PMID: 26803803
  28. Modeling RNA secondary structure folding ensembles using SHAPE mapping data.
    Nucleic Acids Res. 2018 Jan 9;46(1):314-323 PMID: 29177466
  29. Comparison of SHAPE reagents for mapping RNA structures inside living cells.
    RNA. 2017 Feb;23(2):169-174 PMID: 27879433
  30. In vivo genome-wide profiling of RNA secondary structure reveals novel regulatory features.
    Nature. 2014 Jan 30;505(7485):696-700 PMID: 24270811
  31. Regulation of innate immunity through RNA structure and the protein kinase PKR.
    Curr Opin Struct Biol. 2011 Feb;21(1):119-27 PMID: 21145228
  32. An overview of chemical processes that damage cellular DNA: spontaneous hydrolysis, alkylation, and reactions with radicals.
    Chem Res Toxicol. 2009 Nov;22(11):1747-60 PMID: 19757819
  33. Cotranscriptional folding of a riboswitch at nucleotide resolution.
    Nat Struct Mol Biol. 2016 Dec;23(12):1124-1131 PMID: 27798597
  34. Characterizing RNA structures in vitro and in vivo with selective 2'-hydroxyl acylation analyzed by primer extension sequencing (SHAPE-Seq).
    Methods. 2016 Jul 1;103:34-48 PMID: 27064082
  35. Global analysis of protein expression in yeast.
    Nature. 2003 Oct 16;425(6959):737-41 PMID: 14562106
  36. Quantifying E. coli proteome and transcriptome with single-molecule sensitivity in single cells.
    Science. 2010 Jul 30;329(5991):533-8 PMID: 20671182
  37. Genome-Wide Analysis of RNA Secondary Structure.
    Annu Rev Genet. 2016 Nov 23;50:235-266 PMID: 27648642
  38. RNA motif discovery by SHAPE and mutational profiling (SHAPE-MaP).
    Nat Methods. 2014 Sep;11(9):959-65 PMID: 25028896
  39. RNA structural analysis by evolving SHAPE chemistry.
    Wiley Interdiscip Rev RNA. 2014 Nov-Dec;5(6):867-81 PMID: 25132067
  40. Transcription attenuation: a highly conserved regulatory strategy used by bacteria.
    Trends Genet. 2005 May;21(5):260-4 PMID: 15851059
  41. Structural imprints in vivo decode RNA regulatory mechanisms.
    Nature. 2015 Mar 26;519(7544):486-90 PMID: 25799993
  42. The riboswitch control of bacterial metabolism.
    Trends Biochem Sci. 2004 Jan;29(1):11-7 PMID: 14729327
  43. DNA sequencing at 40: past, present and future.
    Nature. 2017 Oct 19;550(7676):345-353 PMID: 29019985
  44. Genome-wide probing of RNA structure reveals active unfolding of mRNA structures in vivo.
    Nature. 2014 Jan 30;505(7485):701-5 PMID: 24336214
  45. Regulation of cytoplasmic mRNA decay.
    Nat Rev Genet. 2012 Mar 06;13(4):246-59 PMID: 22392217
  46. Lethal and temperature-sensitive mutations and their suppressors identify an essential structural element in U2 small nuclear RNA.
    Genes Dev. 1990 Dec;4(12A):2132-45 PMID: 2269428
  47. A compendium of RNA-binding motifs for decoding gene regulation.
    Nature. 2013 Jul 11;499(7457):172-7 PMID: 23846655
  48. Regulation of translation initiation in eukaryotes: mechanisms and biological targets.
    Cell. 2009 Feb 20;136(4):731-45 PMID: 19239892
  49. In vivo analysis of plant RNA structure: soybean 18S ribosomal and ribulose-1,5-bisphosphate carboxylase small subunit RNAs.
    Plant Mol Biol. 1992 Jan;18(2):219-34 PMID: 1731985
  50. Riboswitch diversity and distribution.
    RNA. 2017 Jul;23(7):995-1011 PMID: 28396576
  51. RNAs as chaperones.
    RNA Biol. 2016 Dec;13(12):1228-1231 PMID: 27791471
  52. Advances in RNA structure analysis by chemical probing.
    Curr Opin Struct Biol. 2010 Jun;20(3):295-304 PMID: 20447823
  53. Probing Xist RNA Structure in Cells Using Targeted Structure-Seq.
    PLoS Genet. 2015 Dec 08;11(12):e1005668 PMID: 26646615
  54. SHAPE-directed RNA secondary structure prediction.
    Methods. 2010 Oct;52(2):150-8 PMID: 20554050
  55. An independently folding domain of RNA tertiary structure within the Tetrahymena ribozyme.
    Biochemistry. 1993 May 25;32(20):5291-300 PMID: 7684607
  56. Riboswitches as versatile gene control elements.
    Curr Opin Struct Biol. 2005 Jun;15(3):342-8 PMID: 15919195
  57. Operon mRNAs are organized into ORF-centric structures that predict translation efficiency.
    Elife. 2017 Jan 31;6: PMID: 28139975
  58. Riboswitch RNAs: regulation of gene expression by direct monitoring of a physiological signal.
    RNA Biol. 2010 Jan-Feb;7(1):104-10 PMID: 20061810
  59. HOTAIR forms an intricate and modular secondary structure.
    Mol Cell. 2015 Apr 16;58(2):353-61 PMID: 25866246
  60. RNase-mediated protein footprint sequencing reveals protein-binding sites throughout the human transcriptome.
    Genome Biol. 2014 Jan 07;15(1):R3 PMID: 24393486
  61. Classification and comparison of small RNAs from plants.
    Annu Rev Plant Biol. 2013;64:137-59 PMID: 23330790
  62. Secondary structure of the circular form of the Tetrahymena rRNA intervening sequence: a technique for RNA structure analysis using chemical probes and reverse transcriptase.
    Proc Natl Acad Sci U S A. 1985 Feb;82(3):648-52 PMID: 2579378
  63. Bridging the gap between in vitro and in vivo RNA folding.
    Q Rev Biophys. 2016 Jan;49:e10 PMID: 27658939
  64. In vivo and in vitro structural analysis of the rplJ mRNA leader of Escherichia coli. Protection by bound L10-L7/L12.
    J Biol Chem. 1988 Oct 15;263(29):15166-75 PMID: 3049601
  65. On the recognition of helical RNA by cobra venom V1 nuclease.
    J Biol Chem. 1986 Apr 25;261(12):5396-403 PMID: 2420800
  66. Regulation by small RNAs in bacteria: expanding frontiers.
    Mol Cell. 2011 Sep 16;43(6):880-91 PMID: 21925377
  67. A statistical test for conserved RNA structure shows lack of evidence for structure in lncRNAs.
    Nat Methods. 2017 Jan;14(1):45-48 PMID: 27819659
  68. Visualizing group II intron catalysis through the stages of splicing.
    Cell. 2012 Oct 26;151(3):497-507 PMID: 23101623
  69. Understanding the transcriptome through RNA structure.
    Nat Rev Genet. 2011 Aug 18;12(9):641-55 PMID: 21850044
  70. COOLAIR Antisense RNAs Form Evolutionarily Conserved Elaborate Secondary Structures.
    Cell Rep. 2016 Sep 20;16(12):3087-3096 PMID: 27653675
  71. Genomics. ENCODE project writes eulogy for junk DNA.
    Science. 2012 Sep 7;337(6099):1159, 1161 PMID: 22955811
  72. RNA SHAPE analysis in living cells.
    Nat Chem Biol. 2013 Jan;9(1):18-20 PMID: 23178934
  73. Secondary structure of 16S ribosomal RNA.
    Science. 1981 Apr 24;212(4493):403-11 PMID: 6163215
  74. Rice In Vivo RNA Structurome Reveals RNA Secondary Structure Conservation and Divergence in Plants.
    Mol Plant. 2018 Apr 2;11(4):607-622 PMID: 29409859
  75. Accurate SHAPE-directed RNA structure determination.
    Proc Natl Acad Sci U S A. 2009 Jan 6;106(1):97-102 PMID: 19109441
  76. Analysis of the structure of Tetrahymena nuclear RNAs in vivo: telomerase RNA, the self-splicing rRNA intron, and U2 snRNA.
    RNA. 1995 Jun;1(4):363-74 PMID: 7493315
  77. Chemical probes for higher-order structure in RNA.
    Proc Natl Acad Sci U S A. 1980 Aug;77(8):4679-82 PMID: 6159633
  78. Glyoxals as in vivo RNA structural probes of guanine base-pairing.
    RNA. 2018 Jan;24(1):114-124 PMID: 29030489
  79. Genome-wide measurement of RNA secondary structure in yeast.
    Nature. 2010 Sep 2;467(7311):103-7 PMID: 20811459
  80. Geometric nomenclature and classification of RNA base pairs.
    RNA. 2001 Apr;7(4):499-512 PMID: 11345429
  81. Three-dimensional structure of yeast phenylalanine transfer RNA: folding of the polynucleotide chain.
    Science. 1973 Jan 19;179(4070):285-8 PMID: 4566654
  82. RNA structure analysis at single nucleotide resolution by selective 2'-hydroxyl acylation and primer extension (SHAPE).
    J Am Chem Soc. 2005 Mar 30;127(12):4223-31 PMID: 15783204
  83. Protein Structure Is Related to RNA Structural Reactivity In Vivo.
    J Mol Biol. 2016 Feb 27;428(5 Pt A):758-766 PMID: 26598238
  84. Detection in vivo of protein-DNA interactions within the lac operon of Escherichia coli.
    Nature. 1985 Feb 28-Mar 6;313(6005):795-8 PMID: 3883194
  85. Detection of RNA-Protein Interactions in Living Cells with SHAPE.
    Biochemistry. 2015 Nov 24;54(46):6867-75 PMID: 26544910
  86. RNA Duplex Map in Living Cells Reveals Higher-Order Transcriptome Structure.
    Cell. 2016 May 19;165(5):1267-1279 PMID: 27180905
  87. The RNA structurome: transcriptome-wide structure probing with next-generation sequencing.
    Trends Biochem Sci. 2015 Apr;40(4):221-32 PMID: 25797096
  88. StructureFold: genome-wide RNA secondary structure mapping and reconstruction in vivo.
    Bioinformatics. 2015 Aug 15;31(16):2668-75 PMID: 25886980
  89. DMS-MaPseq for genome-wide or targeted RNA structure probing in vivo.
    Nat Methods. 2017 Jan;14(1):75-82 PMID: 27819661
  90. Architecture and secondary structure of an entire HIV-1 RNA genome.
    Nature. 2009 Aug 6;460(7256):711-6 PMID: 19661910
  91. StructureFold2: Bringing chemical probing data into the computational fold of RNA structural analysis.
    Methods. 2018 Jul 1;143:12-15 PMID: 29410279
  92. Genome-wide profiling of mouse RNA secondary structures reveals key features of the mammalian transcriptome.
    Genome Biol. 2014;15(10):491 PMID: 25323333
  93. FURTHER STUDIES ON THE ALKYLATION OF NUCLEIC ACIDS AND THEIR CONSTITUENT NUCLEOTIDES.
    Biochem J. 1963 Oct;89:127-38 PMID: 14097355
  94. Molecular biology: the expanding world of small RNAs.
    Nature. 2008 Jan 24;451(7177):414-6 PMID: 18216846
  95. Structure-seq2: sensitive and accurate genome-wide profiling of RNA structure in vivo.
    Nucleic Acids Res. 2017 Aug 21;45(14):e135 PMID: 28637286
  96. Regulation of translation initiation by RNA binding proteins.
    Annu Rev Microbiol. 2009;63:27-44 PMID: 19385727
Article Info
Journal
Cold Spring Harbor perspectives in biology
Abbr.
Cold Spring Harb Perspect Biol
ISSN
1943-0264
Published
2018-00-01
Epub
2018-00-01
Language
English
Region
United States
NLM ID
101513680
PMCID
PMC6169808
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com