Home LiteratureArticle Details
PMID: 20554050 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Review

SHAPE-directed RNA secondary structure prediction.

Methods (San Diego, Calif.) ·Vol. 52 ·No. 2 ·2010-10-00 ·Pages 150-8

Low JT, Weeks KM

Abstract

The diverse functional roles of RNA are determined by its underlying structure. Accurate and comprehensive knowledge of RNA structure would inform a broader understanding of RNA biology and facilitate exploiting RNA as a biotechnological tool and therapeutic target. Determining the pattern of base pairing, or secondary structure, of RNA is a first step in these endeavors. Advances in experimental, computational, and comparative analysis approaches for analyzing secondary structure have yielded accurate structures for many small RNAs, but only a few large (>500 nts) RNAs. In addition, most current methods for determining a secondary structure require considerable effort, analytical expertise, and technical ingenuity. In this review, we outline an efficient strategy for developing accurate secondary structure models for RNAs of arbitrary length. This approach melds structural information obtained using SHAPE chemistry with structure prediction using nearest-neighbor rules and the dynamic programming algorithm implemented in the RNAstructure program. Prediction accuracies reach >or=95% for RNAs on the kilobase scale. This approach facilitates both development of new models and refinement of existing RNA structure models, which we illustrate using the Gag-Pol frameshift element in an HIV-1 M-group genome. Most promisingly, integrated experimental and computational refinement brings closer the ultimate goal of efficiently and accurately establishing the secondary structure for any RNA sequence.

MeSH Terms
Algorithms Biochemistry/methods Computational Biology Electrophoresis, Capillary HIV-1/genetics Models, Molecular Nucleic Acid Conformation RNA/chemistry RNA, Viral/chemistry
Chemicals
RNA, Viral RNA
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Low Justin T
Department of Biochemistry and Biophysics, University of North Carolina, Chapel Hill, NC 27599-3290, USA.
Weeks Kevin M
References (74)
74 references, click to expand
  1. Direct observation of hierarchical folding in single riboswitch aptamers.
    Science. 2008 Feb 1;319(5863):630-3 PMID: 18174398
  2. Selection of peptides interfering with a ribosomal frameshift in the human immunodeficiency virus type 1.
    RNA. 2008 May;14(5):981-91 PMID: 18367719
  3. HIV expression strategies: ribosomal frameshifting is directed by a short sequence in both mammalian and yeast systems.
    Cell. 1988 Dec 23;55(6):1159-69 PMID: 3060262
  4. 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
  5. Ribosomal pausing during translation of an RNA pseudoknot.
    Mol Cell Biol. 1993 Nov;13(11):6931-40 PMID: 8413285
  6. Local RNA structural changes induced by crystallization are revealed by SHAPE.
    RNA. 2007 Apr;13(4):536-48 PMID: 17299128
  7. How RNA folds.
    J Mol Biol. 1999 Oct 22;293(2):271-81 PMID: 10550208
  8. Prediction of RNA secondary structure by free energy minimization.
    Curr Opin Struct Biol. 2006 Jun;16(3):270-8 PMID: 16713706
  9. Structure of the autoregulatory pseudoknot within the gene 32 messenger RNA of bacteriophages T2 and T6: a model for a possible family of structurally related RNA pseudoknots.
    Biochemistry. 1996 Apr 2;35(13):4187-98 PMID: 8672455
  10. Time-resolved RNA SHAPE chemistry: quantitative RNA structure analysis in one-second snapshots and at single-nucleotide resolution.
    Nat Protoc. 2009;4(10):1413-21 PMID: 19745823
  11. On the significance of an RNA tertiary structure prediction.
    RNA. 2010 Jul;16(7):1340-9 PMID: 20498460
  12. Probing the structure of RNAs in solution.
    Nucleic Acids Res. 1987 Nov 25;15(22):9109-28 PMID: 2446263
  13. Secondary structure model of the RNA recognized by the reverse transcriptase from the R2 retrotransposable element.
    RNA. 1997 Jan;3(1):1-16 PMID: 8990394
  14. A high-throughput screen for synthetic riboswitches reveals mechanistic insights into their function.
    Chem Biol. 2007 Feb;14(2):173-84 PMID: 17317571
  15. Enzymatic approaches to probing of RNA secondary and tertiary structure.
    Methods Enzymol. 1989;180:192-212 PMID: 2482414
  16. Beyond Mfold: recent advances in RNA bioinformatics.
    J Biotechnol. 2006 Jun 25;124(1):41-55 PMID: 16530285
  17. Structure of the RNA signal essential for translational frameshifting in HIV-1.
    J Mol Biol. 2005 Jun 24;349(5):1024-35 PMID: 15907937
  18. Modelling of the three-dimensional architecture of group I catalytic introns based on comparative sequence analysis.
    J Mol Biol. 1990 Dec 5;216(3):585-610 PMID: 2258934
  19. Influence of nucleotide identity on ribose 2'-hydroxyl reactivity in RNA.
    RNA. 2009 Jul;15(7):1314-21 PMID: 19458034
  20. Structure of a viral cap-independent translation element that functions via high affinity binding to the eIF4E subunit of eIF4F.
    J Biol Chem. 2009 May 22;284(21):14189-202 PMID: 19276085
  21. The frameshift stimulatory signal of human immunodeficiency virus type 1 group O is a pseudoknot.
    J Mol Biol. 2003 Aug 15;331(3):571-83 PMID: 12899829
  22. Selective 2'-hydroxyl acylation analyzed by primer extension (SHAPE): quantitative RNA structure analysis at single nucleotide resolution.
    Nat Protoc. 2006;1(3):1610-6 PMID: 17406453
  23. Strong correlation between SHAPE chemistry and the generalized NMR order parameter (S2) in RNA.
    J Am Chem Soc. 2008 Sep 17;130(37):12244-5 PMID: 18710236
  24. High-throughput SHAPE and hydroxyl radical analysis of RNA structure and ribonucleoprotein assembly.
    Methods Enzymol. 2009;468:67-89 PMID: 20946765
  25. A fast-acting reagent for accurate analysis of RNA secondary and tertiary structure by SHAPE chemistry.
    J Am Chem Soc. 2007 Apr 11;129(14):4144-5 PMID: 17367143
  26. Mechanistic role of structurally dynamic regions in Dicistroviridae IGR IRESs.
    J Mol Biol. 2010 Jan 8;395(1):205-17 PMID: 19878683
  27. Structural principles from large RNAs.
    Annu Rev Biophys. 2008;37:445-64 PMID: 18573090
  28. Incorporating chemical modification constraints into a dynamic programming algorithm for prediction of RNA secondary structure.
    Proc Natl Acad Sci U S A. 2004 May 11;101(19):7287-92 PMID: 15123812
  29. Maintenance of the Gag/Gag-Pol ratio is important for human immunodeficiency virus type 1 RNA dimerization and viral infectivity.
    J Virol. 2001 Feb;75(4):1834-41 PMID: 11160682
  30. Characterization of ribosomal frameshifting in HIV-1 gag-pol expression.
    Nature. 1988 Jan 21;331(6153):280-3 PMID: 2447506
  31. How do RNA folding algorithms work?
    Nat Biotechnol. 2004 Nov;22(11):1457-8 PMID: 15529172
  32. The accuracy of ribosomal RNA comparative structure models.
    Curr Opin Struct Biol. 2002 Jun;12(3):301-10 PMID: 12127448
  33. The SL1-SL2 (stem-loop) domain is the primary determinant for stability of the gamma retroviral genomic RNA dimer.
    J Biol Chem. 2006 Dec 8;281(49):37952-61 PMID: 16984912
  34. Bridging the gap in RNA structure prediction.
    Curr Opin Struct Biol. 2007 Apr;17(2):157-65 PMID: 17383172
  35. The molecular mechanism of thermal unfolding of Escherichia coli formylmethionine transfer RNA.
    J Mol Biol. 1974 Jul 25;87(1):63-88 PMID: 4610153
  36. Thermal unfolding of a group I ribozyme: the low-temperature transition is primarily disruption of tertiary structure.
    Biochemistry. 1993 Jan 12;32(1):153-63 PMID: 8418835
  37. Programmed ribosomal frameshifting in HIV-1 and the SARS-CoV.
    Virus Res. 2006 Jul;119(1):29-42 PMID: 16310880
  38. Architecture of a gamma retroviral genomic RNA dimer.
    Biochemistry. 2006 Oct 24;45(42):12664-72 PMID: 17042483
  39. Thermodynamics of base pairing.
    Curr Opin Struct Biol. 1996 Jun;6(3):299-304 PMID: 8804832
  40. tRNA-mRNA mimicry drives translation initiation from a viral IRES.
    Nat Struct Mol Biol. 2008 Jan;15(1):57-64 PMID: 18157151
  41. Optimal computer folding of large RNA sequences using thermodynamics and auxiliary information.
    Nucleic Acids Res. 1981 Jan 10;9(1):133-48 PMID: 6163133
  42. Mapping nucleic acid structure by hydroxyl radical cleavage.
    Curr Opin Chem Biol. 2005 Apr;9(2):127-34 PMID: 15811796
  43. A basis for new approaches to the chemotherapy of AIDS: novel genes in HIV-1 potentially encode selenoproteins expressed by ribosomal frameshifting and termination suppression.
    J Med Chem. 1994 Aug 19;37(17):2637-54 PMID: 8064794
  44. Expanded sequence dependence of thermodynamic parameters improves prediction of RNA secondary structure.
    J Mol Biol. 1999 May 21;288(5):911-40 PMID: 10329189
  45. Predicting thermodynamic properties of RNA.
    Methods Enzymol. 1995;259:242-61 PMID: 8538457
  46. SHAPE analysis of long-range interactions reveals extensive and thermodynamically preferred misfolding in a fragile group I intron RNA.
    Biochemistry. 2008 Aug 19;47(33):8504-13 PMID: 18642882
  47. Complex ligand-induced conformational changes in tRNA(Asp) revealed by single-nucleotide resolution SHAPE chemistry.
    Biochemistry. 2008 Mar 18;47(11):3454-61 PMID: 18290632
  48. Ribosomal pausing at a frameshifter RNA pseudoknot is sensitive to reading phase but shows little correlation with frameshift efficiency.
    Mol Cell Biol. 2001 Dec;21(24):8657-70 PMID: 11713298
  49. Thermodynamic parameters for an expanded nearest-neighbor model for formation of RNA duplexes with Watson-Crick base pairs.
    Biochemistry. 1998 Oct 20;37(42):14719-35 PMID: 9778347
  50. Solution structure and thermodynamic investigation of the HIV-1 frameshift inducing element.
    J Mol Biol. 2005 Jun 24;349(5):1011-23 PMID: 15927637
  51. NNDB: the nearest neighbor parameter database for predicting stability of nucleic acid secondary structure.
    Nucleic Acids Res. 2010 Jan;38(Database issue):D280-2 PMID: 19880381
  52. Structural characterization of the Rous sarcoma virus RNA stability element.
    J Virol. 2009 Mar;83(5):2119-29 PMID: 19091866
  53. Advances in RNA structure prediction from sequence: new tools for generating hypotheses about viral RNA structure-function relationships.
    J Virol. 2009 Jul;83(13):6326-34 PMID: 19369331
  54. A structural basis for the recognition of 2'-deoxyguanosine by the purine riboswitch.
    J Mol Biol. 2009 Jan 23;385(3):938-48 PMID: 19007790
  55. Ribosomal frameshifting: an emerging drug target for HIV.
    Curr Opin Investig Drugs. 2009 Feb;10(2):121-8 PMID: 19197789
  56. Characterization of the frameshift stimulatory signal controlling a programmed -1 ribosomal frameshift in the human immunodeficiency virus type 1.
    Nucleic Acids Res. 2002 Dec 1;30(23):5094-102 PMID: 12466532
  57. High-throughput SHAPE analysis reveals structures in HIV-1 genomic RNA strongly conserved across distinct biological states.
    PLoS Biol. 2008 Apr 29;6(4):e96 PMID: 18447581
  58. Identifying kinetic barriers to mechanical unfolding of the T. thermophila ribozyme.
    Science. 2003 Mar 21;299(5614):1892-5 PMID: 12649482
  59. Evaluation of the suitability of free-energy minimization using nearest-neighbor energy parameters for RNA secondary structure prediction.
    BMC Bioinformatics. 2004 Aug 05;5:105 PMID: 15296519
  60. Accurate SHAPE-directed RNA structure determination.
    Proc Natl Acad Sci U S A. 2009 Jan 6;106(1):97-102 PMID: 19109441
  61. In-line probing analysis of riboswitches.
    Methods Mol Biol. 2008;419:53-67 PMID: 18369975
  62. Topology links RNA secondary structure with global conformation, dynamics, and adaptation.
    Science. 2010 Jan 8;327(5962):202-6 PMID: 20056889
  63. Secondary structure of the mature ex virio Moloney murine leukemia virus genomic RNA dimerization domain.
    J Virol. 2010 Jan;84(2):898-906 PMID: 19889760
  64. On finding all suboptimal foldings of an RNA molecule.
    Science. 1989 Apr 7;244(4900):48-52 PMID: 2468181
  65. Evaluation of several lightweight stochastic context-free grammars for RNA secondary structure prediction.
    BMC Bioinformatics. 2004 Jun 04;5:71 PMID: 15180907
  66. ShapeFinder: a software system for high-throughput quantitative analysis of nucleic acid reactivity information resolved by capillary electrophoresis.
    RNA. 2008 Oct;14(10):1979-90 PMID: 18772246
  67. CONTRAfold: RNA secondary structure prediction without physics-based models.
    Bioinformatics. 2006 Jul 15;22(14):e90-8 PMID: 16873527
  68. Structure of an RNA switch that enforces stringent retroviral genomic RNA dimerization.
    Proc Natl Acad Sci U S A. 2006 Sep 12;103(37):13640-5 PMID: 16945907
  69. Phylogenetic comparative analysis and the secondary structure of ribonuclease P RNA--a review.
    Gene. 1989 Oct 15;82(1):65-75 PMID: 2479592
  70. Architecture and secondary structure of an entire HIV-1 RNA genome.
    Nature. 2009 Aug 6;460(7256):711-6 PMID: 19661910
  71. Lack of secondary structure characterizes the 5' ends of mammalian mitochondrial mRNAs.
    RNA. 2008 May;14(5):862-71 PMID: 18367717
  72. Extracting stacking interaction parameters for RNA from the data set of native structures.
    J Mol Biol. 2005 Mar 18;347(1):53-69 PMID: 15733917
  73. Structure of stem-loop IV of Tetrahymena telomerase RNA.
    EMBO J. 2006 Jul 12;25(13):3156-66 PMID: 16778765
  74. RNA flexibility in the dimerization domain of a gamma retrovirus.
    Nat Chem Biol. 2005 Jul;1(2):104-11 PMID: 16408007
Article Info
Journal
Methods (San Diego, Calif.)
Abbr.
Methods
ISSN
1095-9130
Published
2010-10-00
Epub
2010-00-08
Pages
150-8
Language
English
Region
United States
NLM ID
9426302
PMCID
PMC2941709
Subset
IM
Grants
NIDA NIH HHS · F30DA027364 · United States
NIAID NIH HHS · AI068462 · United States
NIGMS NIH HHS · T32GM008719 · United States
NIGMS NIH HHS · T32 GM008719 · United States
NIAID NIH HHS · R01 AI068462 · United States
NIDA NIH HHS · F30 DA027364 · United States
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