Home LiteratureArticle Details
PMID: 8990394 Published · ppublish English Comparative Study Journal Article Research Support, U.S. Gov't, P.H.S.

Secondary structure model of the RNA recognized by the reverse transcriptase from the R2 retrotransposable element.

RNA (New York, N.Y.) ·Vol. 3 ·No. 1 ·1997-01-00 ·Pages 1-16

Mathews DH, Banerjee AR, Luan DD, Eickbush TH, Turner DH

Abstract

RNA transcripts corresponding to the 250-nt 3' untranslated region of the R2 non-LTR retrotransposable element are recognized by the R2 reverse transcriptase and are sufficient to serve as templates in the target DNA-primed reverse transcription (TPRT) reaction. The R2 protein encoded by the Bombyx mori R2 can recognize this region from both the B. mori and Drosophila melanogaster R2 elements even though these regions show little nucleotide sequence identity. A model for the RNA secondary structure of the 3' untranslated region of the D. melanogaster R2 retrotransposon was developed by sequence comparison of 10 species aided by free energy minimization. Chemical modification experiments are consistent with this prediction. A secondary structure model for the 3' untranslated region of R2 RNA from the R2 element from B. mori was obtained by a combination of chemical modification data and free energy minimization. These two secondary structure models, found independently, share several common sites. This study shows the utility of combining free energy minimization, sequence comparison, and chemical modification to model an RNA secondary structure.

MeSH Terms
Algorithms Animals Base Sequence Bombyx/genetics Computer Simulation Drosophila/classification,genetics Methylation Molecular Sequence Data Nucleic Acid Conformation Nucleic Acid Denaturation Protein Binding RNA/chemistry,drug effects,metabolism RNA-Directed DNA Polymerase/metabolism Retroelements/genetics Sequence Alignment Sequence Homology, Nucleic Acid Species Specificity Substrate Specificity Temperature Templates, Genetic Thermodynamics
Chemicals
Retroelements RNA RNA-Directed DNA Polymerase
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Mathews D H
Department of Chemistry, University of Rochester, New York 14627-0216, USA.
Banerjee A R
Luan D D
Eickbush T H
Turner D H
References (61)
61 references, click to expand
  1. A rapid method for the purification of deprotected oligodeoxynucleotides.
    Nucleic Acids Res. 1991 Feb 11;19(3):674 PMID: 2011537
  2. Three-dimensional tertiary structure of yeast phenylalanine transfer RNA.
    Science. 1974 Aug 2;185(4149):435-40 PMID: 4601792
  3. A comparison of optimal and suboptimal RNA secondary structures predicted by free energy minimization with structures determined by phylogenetic comparison.
    Nucleic Acids Res. 1991 May 25;19(10):2707-14 PMID: 1710343
  4. Structural features that give rise to the unusual stability of RNA hairpins containing GNRA loops.
    Science. 1991 Jul 12;253(5016):191-4 PMID: 1712983
  5. Crystal structure of an RNA double helix incorporating a track of non-Watson-Crick base pairs.
    Nature. 1991 Oct 10;353(6344):579-81 PMID: 1922368
  6. Nearest-neighbor parameters for G.U mismatches: [formula; see text] is destabilizing in the contexts [formula; see text] and [formula; see text] but stabilizing in [formula; see text].
    Biochemistry. 1991 Nov 19;30(46):11124-32 PMID: 1718426
  7. RNA structure and NMR spectroscopy.
    Q Rev Biophys. 1991 Nov;24(4):479-532 PMID: 1723809
  8. 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
  9. Structural studies on transfer ribonucleic acid. I. Labeling of exposed guanine sites in yeast phenylalanine transfer ribonucleic acid with kethoxal.
    Biochemistry. 1969 Aug;8(8):3249-53 PMID: 4897332
  10. The sarcin/ricin loop, a modular RNA.
    J Mol Biol. 1995 Mar 17;247(1):81-98 PMID: 7897662
  11. Structure of yeast phenylalanine tRNA at 3 A resolution.
    Nature. 1974 Aug 16;250(467):546-51 PMID: 4602655
  12. The molecular mechanism of thermal unfolding of Escherichia coli formylmethionine transfer RNA.
    J Mol Biol. 1974 Jul 25;87(1):63-88 PMID: 4610153
  13. Thermal unfolding of yeast glycine transfer RNA.
    Biochemistry. 1976 May 4;15(9):1874-82 PMID: 773427
  14. 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
  15. Rapid chemical probing of conformation in 16 S ribosomal RNA and 30 S ribosomal subunits using primer extension.
    J Mol Biol. 1986 Feb 5;187(3):399-416 PMID: 2422386
  16. Restrained refinement of the monoclinic form of yeast phenylalanine transfer RNA. Temperature factors and dynamics, coordinated waters, and base-pair propeller twist angles.
    Biochemistry. 1986 Aug 26;25(17):4868-78 PMID: 3533142
  17. Improved free-energy parameters for predictions of RNA duplex stability.
    Proc Natl Acad Sci U S A. 1986 Dec;83(24):9373-7 PMID: 2432595
  18. The site-specific ribosomal insertion element type II of Bombyx mori (R2Bm) contains the coding sequence for a reverse transcriptase-like enzyme.
    Mol Cell Biol. 1987 Jun;7(6):2221-30 PMID: 2439905
  19. Probing the structure of RNAs in solution.
    Nucleic Acids Res. 1987 Nov 25;15(22):9109-28 PMID: 2446263
  20. Changing the identity of a tRNA by introducing a G-U wobble pair near the 3' acceptor end.
    Science. 1988 May 6;240(4853):793-6 PMID: 2452483
  21. A simple structural feature is a major determinant of the identity of a transfer RNA.
    Nature. 1988 May 12;333(6169):140-5 PMID: 3285220
  22. Vertical transmission of the retrotransposable elements R1 and R2 during the evolution of the Drosophila melanogaster species subgroup.
    Genetics. 1995 Feb;139(2):671-84 PMID: 7713424
  23. R1 and R2 retrotransposable elements of Drosophila evolve at rates similar to those of nuclear genes.
    Genetics. 1995 Feb;139(2):685-95 PMID: 7713425
  24. Proton NMR and structural features of a 24-nucleotide RNA hairpin.
    Biochemistry. 1995 May 16;34(19):6488-503 PMID: 7756280
  25. RNA template requirements for target DNA-primed reverse transcription by the R2 retrotransposable element.
    Mol Cell Biol. 1995 Jul;15(7):3882-91 PMID: 7540721
  26. Determination of the folding topology of the SL1 RNA from Caenorhabditis elegans by multidimensional heteronuclear NMR.
    J Mol Biol. 1995 Sep 22;252(3):314-27 PMID: 7563053
  27. Solution structure of the CUUG hairpin loop: a novel RNA tetraloop motif.
    Biochemistry. 1995 Nov 7;34(44):14416-27 PMID: 7578046
  28. Solution structure of a bovine immunodeficiency virus Tat-TAR peptide-RNA complex.
    Science. 1995 Nov 17;270(5239):1200-3 PMID: 7502045
  29. 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
  30. A comparison of thermodynamic foldings with comparatively derived structures of 16S and 16S-like rRNAs.
    RNA. 1995 Aug;1(6):559-74 PMID: 7489516
  31. G.U base pairing motifs in ribosomal RNA.
    RNA. 1995 Oct;1(8):807-14 PMID: 7493326
  32. R4, a non-LTR retrotransposon specific to the large subunit rRNA genes of nematodes.
    Nucleic Acids Res. 1995 Nov 25;23(22):4628-34 PMID: 8524653
  33. Predicting thermodynamic properties of RNA.
    Methods Enzymol. 1995;259:242-61 PMID: 8538457
  34. Functional evidence for indirect recognition of G.U in tRNA(Ala) by alanyl-tRNA synthetase.
    Science. 1996 Jan 12;271(5246):195-7 PMID: 8539617
  35. Thermodynamic prediction of conserved secondary structure: application to the RRE element of HIV, the tRNA-like element of CMV and the mRNA of prion protein.
    J Mol Biol. 1996 May 24;258(5):813-26 PMID: 8637012
  36. Structural basis of ligand discrimination by two related RNA aptamers resolved by NMR spectroscopy.
    Science. 1996 May 31;272(5266):1343-7 PMID: 8650546
  37. Structural basis of RNA folding and recognition in an AMP-RNA aptamer complex.
    Nature. 1996 Jul 11;382(6587):183-6 PMID: 8700212
  38. Solution structure of an ATP-binding RNA aptamer reveals a novel fold.
    RNA. 1996 Jul;2(7):628-40 PMID: 8756406
  39. Crystal structure of a group I ribozyme domain: principles of RNA packing.
    Science. 1996 Sep 20;273(5282):1678-85 PMID: 8781224
  40. Molecular recognition in the bovine immunodeficiency virus Tat peptide-TAR RNA complex.
    Chem Biol. 1995 Dec;2(12):827-40 PMID: 8807816
  41. Deletion of nonconserved helices near the 3' end of the rRNA intron of Tetrahymena thermophila alters self-splicing but not core catalytic activity.
    Genes Dev. 1988 Jun;2(6):652-63 PMID: 3417146
  42. Functional expression of a sequence-specific endonuclease encoded by the retrotransposon R2Bm.
    Cell. 1988 Oct 21;55(2):235-46 PMID: 2844414
  43. On finding all suboptimal foldings of an RNA molecule.
    Science. 1989 Apr 7;244(4900):48-52 PMID: 2468181
  44. Pattern analysis of RNA secondary structure similarity and consensus of minimal-energy folding.
    J Mol Biol. 1989 Jun 5;207(3):597-614 PMID: 2474658
  45. Laser temperature-jump, spectroscopic, and thermodynamic study of salt effects on duplex formation by dGCATGC.
    Biochemistry. 1989 May 16;28(10):4283-91 PMID: 2765487
  46. Improved predictions of secondary structures for RNA.
    Proc Natl Acad Sci U S A. 1989 Oct;86(20):7706-10 PMID: 2479010
  47. Crystallographic structure of an RNA helix: [U(UA)6A]2.
    J Mol Biol. 1989 Oct 5;209(3):459-74 PMID: 2479753
  48. Phylogenetic comparative analysis of RNA secondary structure.
    Methods Enzymol. 1989;180:227-39 PMID: 2482415
  49. Predicting optimal and suboptimal secondary structure for RNA.
    Methods Enzymol. 1990;183:281-306 PMID: 1690335
  50. Type I (R1) and type II (R2) ribosomal DNA insertions of Drosophila melanogaster are retrotransposable elements closely related to those of Bombyx mori.
    J Mol Biol. 1990 Mar 5;212(1):37-52 PMID: 1690812
  51. 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
  52. Melting and chemical modification of a cyclized self-splicing group I intron: similarity of structures in 1 M Na+, in 10 mM Mg2+, and in the presence of substrate.
    Biochemistry. 1990 Nov 6;29(44):10147-58 PMID: 2271644
  53. Structure of an unusually stable RNA hairpin.
    Biochemistry. 1991 Apr 2;30(13):3280-9 PMID: 1706937
  54. Reverse transcription of R2Bm RNA is primed by a nick at the chromosomal target site: a mechanism for non-LTR retrotransposition.
    Cell. 1993 Feb 26;72(4):595-605 PMID: 7679954
  55. Determination of RNA structure and thermodynamics.
    Annu Rev Biochem. 1993;62:255-87 PMID: 7688943
  56. Monitoring of the cooperative unfolding of the sunY group I intron of bacteriophage T4. The active form of the sunY ribozyme is stabilized by multiple interactions with 3' terminal intron components.
    J Mol Biol. 1993 Nov 20;234(2):331-46 PMID: 8230218
  57. Structure of (rGGCGAGCC)2 in solution from NMR and restrained molecular dynamics.
    Biochemistry. 1993 Nov 30;32(47):12612-23 PMID: 8251479
  58. Thermodynamics of RNA folding in a conserved ribosomal RNA domain.
    J Mol Biol. 1994 Apr 15;237(5):560-76 PMID: 7512652
  59. Coaxial stacking of helixes enhances binding of oligoribonucleotides and improves predictions of RNA folding.
    Proc Natl Acad Sci U S A. 1994 Sep 27;91(20):9218-22 PMID: 7524072
  60. Minor groove recognition of the conserved G.U pair at the Tetrahymena ribozyme reaction site.
    Science. 1995 Feb 3;267(5198):675-9 PMID: 7839142
  61. Retrotransposable elements R1 and R2 interrupt the rRNA genes of most insects.
    Proc Natl Acad Sci U S A. 1991 Apr 15;88(8):3295-9 PMID: 1849649
Article Info
Journal
RNA (New York, N.Y.)
Abbr.
RNA
ISSN
1355-8382
Published
1997-01-00
Pages
1-16
Language
English
Region
United States
NLM ID
9509184
PMCID
PMC1369457
Subset
IM
Grants
NIGMS NIH HHS · GM07356 · United States
NIGMS NIH HHS · GM22939 · United States
NIGMS NIH HHS · GM42790 · United States
External Links
PubMed source PMC Full Text View journal details
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

Copyright © 2026.Genelibs Jinan Honghui Biotechnology Co., Ltd. 鲁ICP备20007159号-2