Improvement of RNA secondary structure prediction using RNase H cleavage and randomized oligonucleotides

Nucleic Acids Research

Volumn 37, Issue 18, 2009, Pages

  Kauffmann, Andrew D ^a   Campagna, Ryan J ^a   Bartels, Chantal B ^a   Childs Disney, Jessica L ^a  

^a CANISIUS COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

OLIGONUCLEOTIDE; RIBONUCLEASE H; RIBOSOME RNA; PHENYLALANINE TRANSFER RNA; RNA; RNA 5S;

ACCURACY; ANALYTIC METHOD; ARTICLE; BASE PAIRING; BINDING SITE; CONTROLLED STUDY; DNA LIBRARY; ESCHERICHIA COLI; NONHUMAN; PHYLOGENY; PRIORITY JOURNAL; PROTEIN SECONDARY STRUCTURE; RNA ANALYSIS; RNA CLEAVAGE; RNA STRUCTURE; STRUCTURE ANALYSIS; CHEMISTRY; CONFORMATION; GENE LIBRARY; OLIGONUCLEOTIDE PROBE;

ESCHERICHIA COLI;

GENE LIBRARY; NUCLEIC ACID CONFORMATION; OLIGONUCLEOTIDE PROBES; RIBONUCLEASE H; RNA; RNA, RIBOSOMAL, 5S; RNA, TRANSFER, PHE;

EID: 70350664452     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkp587     Document Type: Article

References (77)

1. Fire,A., Xu,S., Montgomery,M.K., Kostas,S.A., Driver,S.E. and Mello,C.C. (1998) Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature, 391, 806-811.
2. Winkler,W., Nahvi,A. and Breaker,R.R. (2002) Thiamine derivatives bind messenger RNAs directly to regulate bacterial gene expression. Nature 419, 952-956.
3. Winkler,W.C., Cohen-Chalamish,S. and Breaker,R.R. (2002) An mRNA structure that controls gene expression by binding FMN. Proc. Natl Acad. Sci. USA, 99, 15908-15913.
4. Keenan,R.J., Freymann,D.M., Stroud,R.M. and Walter,P. (2001) The signal recognition particle. Annu. Rev. Biochem., 70, 755-775.
5. Zaug,A.J. and Cech,T.R. (1986) The intervening sequence RNA of Tetrahymena is an enzyme. Sciencei, 231, 470-475.
6. Stark,B.C., Kole,R., Bowman,E.J., Altman,S. and Altman,S. (1978) Ribonuclease P: An enzyme with an essential RNA component. Proc. Natl Acad. Sci. USA, 75, 3717-3721.
7. James,B.D., Olsen,G.J., Liu,J.S. and Pace,N.R. (1988) The secondary structure of ribonuclease P RNA, the catalytic element of a ribonucleoprotein enzyme. Cell, 52, 19-26.
8. Qiao,F. and Cech,T.R. (2008) Triple-helix structure in telomerase RNA contributes to catalysis. Nat. Struct. Mol. Biol., 15, 634-640.
9. DeRose,V.J. (2002) Two decades of RNA catalysis. Chem. Biol., 9 961-969.
10. Fedor,M.J. and Williamson,J.R. (2005) The catalytic diversity of RNAs. Nat. Rev. Mol. Cell Biol., 6, 399-412.
11. Staley,J.P. and Guthrie,C. (1998) Mechanical devices of the spliceosome: motors, clocks, springs, and things. Cell, 92, 315-326.
12. Nissen,P., Hansen,J., Ban,N., Moore,P.B. and Steitz,T.A. (2000) The structural basis of ribosome activity in peptide bond synthesis. Science, 289, 920-930.
13. Woodson,S.A. and Cech,T.R. (1991) Alternative secondary structures in the 50 exon affect both forward and reverse self-splicing of the Tetrahymena intervening sequence RNA. Biochemistry, 30, 2042-2050.
14. Nikolcheva,T. and Woodson,S.A. (1999) Facilitation of group I splicing in vivo: Misfolding of the Tetrahymena IVS and the role of ribosomal RNA exons. J. Mol. Biol., 292, 557-567.
15. Pan,J. and Woodson,S.A. (1998) Folding intermediates of a self-splicing RNA: Mispairing of the catalytic core. J. Mol. Biol., 280, 597-609.
16. Emerick,V.L. and Woodson,S.A. (1993) Self-splicing of the Tetrahymena pre-rRNA is decreased by misfolding during transcription. Biochemistry, 32, 14062-14067.
17. Duncan,C.D. and Weeks,K.M. (2008) SHAPE analysis of long-range interactions reveals extensive and thermodynamically preferred misfolding in a fragile group I intron RNA. Biochemistry, 47 8504-8513.
18. Altman,S. and Guerrier-Takada,C. (1986) M1 RNA, the RNA subunit of Escherichia coli ribonuclease P, can undergo a pH-sensitive conformational change. Biochemistry, 25, 1205-1208.
19. Pan,T. and Sosnick,T.R. (1997) Intermediates and kinetic traps in the folding of a large ribozyme revealed by circular dichroism and UV absorbance spectroscopies and catalytic activity. Nat. Struct. Biol. 4, 931-938.
20. Zarrinkar,P.P., Wang,J. and Williamson,J.R. (1996) Slow folding kinetics of RNase P RNA. RNA, 2, 564-573.
21. Hogan,J.J., Gutell,R.R. and Noller,H.F. (1984) Probing the conformation of 26S rRNA in yeast 60S ribosomal subunits with kethoxal. Biochemistry, 23, 3330-3335.
22. Hogan,J.J., Gutell,R.R. and Noller,H.F. (1984) Probing the conformation of 18S rRNA in yeast 40S ribosomal subunits with kethoxal. Biochemistry, 23, 3322-3330.
23. Hogan,J.J. and Noller,H.F. (1978) Altered topography of 16S RNA in the inactive form of Escherichia coli 30S ribosomal subunits. Biochemistry, 17, 587-593.
24. Woese,C.R., Magrum,L.J., Gupta,R., Siegel,R.B., Stahl,D.A., Kop,J., Crawford,N., Brosius,J., Gutell,R., Hogan,J.J. et al. (1980) Secondary structure model for bacterial 16S ribosomal RNA: Phylogenetic, enzymatic and chemical evidence. Nucleic Acids Res., 8, 2275-2293.
25. Gutell,R.R., Weiser,B., Woese,C.R. and Noller,H.F. (1985) Comparative anatomy of 16-S-like ribosomal RNA. Prog. Nucleic Acid Res. Mol. Biol., 32, 155-216.
26. Torres-Larios,A., Swinger,K.K., Krasilnikov,A.S., Pan,T. and Mondragon,A. (2005) Crystal structure of the RNA component of bacterial ribonuclease P. Nature, 437, 584-587.
27. Kazantsev,A.V., Krivenko,A.A., Harrington,D.J., Holbrook,S.R., Adams,P.D. and Pace,N.R. (2005) Crystal structure of a bacterial ribonuclease P RNA. Proc. Natl Acad. Sci. USA, 102, 13392-13397.
28. Cate,J.H., Gooding,A.R., Podell,E., Zhou,K., Golden,B.L., Kundrot,C.E., Cech,T.R. and Doudna,J.A. (1996) Crystal structure of a group I ribozyme domain: Principles of RNA packing. Science, 273, 1678-1685.
29. Vila-Sanjurjo,A., Ridgeway,W.K., Seymaner,V., Zhang,W., Santoso,S., Yu,K. and Cate,J.H. (2003) X-ray crystal structures of the WT and a hyper-accurate ribosome from Escherichia coli. Proc. Natl Acad. Sci. USA, 100, 8682-8687.
30. Ban,N., Nissen,P., Hansen,J., Moore,P.B. and Steitz,T.A. (2000) The complete atomic structure of the large ribosomal subunit at 2.4 Å resolution. Science, 289, 905-920.
31. Blount,K.F. and Breaker,R.R. (2006) Riboswitches as antibacterial drug targets. Nat. Biotechnol., 24, 1558-1564.
32. Blount,K.F., Wang,J.X., Lim,J., Sudarsan,N. and Breaker,R.R. (2007) Antibacterial lysine analogs that target lysine riboswitches. Nat. Chem. Biol., 3, 44-49.
33. Berman,H.M., Westbrook,J., Feng,Z., Gilliland,G., Bhat,T.N., Weissig,H., Shindyalov,I.N. and Bourne,P.E. (2000) The Protein Data Bank. Nucleic Acids Res., 28, 235-242.
34. Mathews,D.H., Sabina,J., Zuker,M. and Turner,D.H. (1999) Expanded sequence dependence of thermodynamic parameters improves prediction of RNA secondary structure. J. Mol. Biol., 288, 911-940.
35. Mathews,D.H., Disney,M.D., Childs,J.L., Schroeder,S.J., Zuker,M. and Turner,D.H. (2004) Incorporating chemical modification constraints into a dynamic programming algorithm for prediction of RNA secondary structure. Proc. Natl Acad. Sci. USA, 101, 7287-7292.
36. Das,R. and Baker,D. (2007) Automated de novo prediction of native-like RNA tertiary structures. Proc. Natl Acad. Sci. USA, 104, 14664-14669.
37. Berkower,I., Leis,J. and Hurwitz,J. (1973) Isolation and characterization of an endonuclease from Escherichia coli specific for ribonucleic acid in ribonucleic acid-deoxyribonucleic acid hybrid structures. J. Biol. Chem., 248, 5914-5921.
38. Matveeva,O., Felden,B., Audlin,S., Gesteland,R.F. and Atkins,J.F. (1997) A rapid in vitro method for obtaining RNA accessibility patterns for complementary DNA probes: Correlation with an intracellular pattern and known RNA structures. Nucleic Acids Res., 25, 5010-5016.
39. Wrzesinski,J., Legiewicz,M. and Ciesiolka,J. (2000) Mapping of accessible sites for oligonucleotide hybridization on hepatitis delta virus ribozymes. Nucleic Acids Res., 28, 1785-1793.
40. Lima,W.F., Brown-Driver,V., Fox,M., Hanecak,R. and Bruice,T.W. (1997) Combinatorial screening and rational optimization for hybridization to folded hepatitis C virus RNA of oligonucleotides with biological antisense activity. J. Biol. Chem., 272, 626-638.
41. Birikh,K.R., Berlin,Y.A., Soreq,H. and Eckstein,F. (1997) Probing accessible sites for ribozymes on human acetylcholinesterase RNA. RNA 3, 429-437.
42. Ho,S.P., Bao,Y., Lesher,T., Malhotra,R., Ma,L.Y., Fluharty,S.J. and Sakai,R.R. (1998) Mapping of RNA accessible sites for antisense experiments with oligonucleotide libraries. Nat. Biotechnol., 16, 59-63.
43. Ho,S.P., Britton,D.H., Stone,B.A., Behrens,D.L., Leffet,L.M., Hobbs,F.W., Miller,J.A. and Trainor,G.L. (1996) Potent antisense oligonucleotides to the human multidrug resistance-1 mRNA are rationally selected by mapping RNA-accessible sites with oligonucleotide libraries. Nucleic Acids Res., 24, 1901-1907.
44. Cload,S.T. and Schepartz,A. (1994) Selection of structure-specific inhibitors of the HIV Rev-Rev response element complex. J. Am. Chem. Soc., 116, 437-442.
45. Scherr,M. and Rossi,J.J. (1998) Rapid determination and quantitation of the accessibility to native RNAs by antisense oligodeoxynucleotides in murine cell extracts. Nucleic Acids Res., 26, 5079-5085.
46. Zarrinkar,P.P. and Williamson,J.R. (1994) Kinetic intermediates in RNA folding. Science, 265, 918-924.
47. Mathews,D.H., Burkard,M.E., Freier,S.M., Wyatt,J.R. and Turner,D.H. (1999) Predicting oligonucleotide affinity to nucleic acid targets. RNA, 5, 1458-1469.
48. Lu,Z.J. and Mathews,D.H. (2008) OligoWalk: An online siRNA design tool utilizing hybridization thermodynamics. Nucleic Acids Res., 36 W104-W108.
49. Moore,P.B., Abo,S., Freeborn,B., Gewirth,D.T., Leontis,N.B. and Sun,G. (1988) Preparation of 5S RNA-related materials for nuclear magnetic resonance and crystallography studies. Methods Enzymol., 164 158-174.
50. Peyret,N., Seneviratne,P.A., Allawi,H.T. and SantaLucia,J. Jr. (1999) Nearest-neighbor thermodynamics and NMR of DNA sequences with internal A•A, C•C, G•G, and T•T mismatches. Biochemistry, 38, 3468-3477.
51. Puglisi,J.D. and Tinoco,I. Jr. (1989) Absorbance melting curves of RNA. Methods Enzymol., 180, 304-325.
52. Disney,M.D., Testa,S.M. and Turner,D.H. (2000) Targeting a Pneumocystis carinii group I intron with methylphosphonate oligonucleotides: Backbone charge is not required for binding or reactivity. Biochemistry, 39, 6991-7000.
53. Ciesiollka,J., Lorenz,S. and Erdmann,V.A. (1992) Different conformational forms of Escherichia coli and rat liver 5S rRNA revealed by Pb(II)-induced hydrolysis. Eur. J. Biochem., 204 583-589.
54. Kierzek,E., Kierzek,R., Turner,D.H. and Catrina,I.E. (2006) Facilitating RNA structure prediction with microarrays. Biochemistry, 45, 581-593.
55. Speek,M. and Lind,A. (1982) Structural analyses of E. coli 5S RNA fragments, their associates and complexes with proteins L18 and L25. Nucleic Acids Res., 10, 947-965.
56. Lu,M. and Steitz,T.A. (2000) Structure of Escherichia coli ribosomal protein L25 complexed with a 5S rRNA fragment at 1.8-A resolution. Proc. Natl Acad. Sci. USA, 97, 2023-2028.
57. Freier,S.M., Alkema,D., Sinclair,A., Neilson,T. and Turner,D.H. (1985) Contributions of dangling end stacking and terminal base-pair formation to the stabilities of XGGCCp, XCCGGp, XGGCCYp, and XCCGGYp helixes. Biochemistry, 24, 4533-4539.
58. Walter,A.E., Turner,D.H., Kim,J., Lyttle,M.H., Muller,P., Mathews,D.H. and Zuker,M. (1994) Coaxial stacking of helixes enhances binding of oligoribonucleotides and improves predictions of RNA folding. Proc. Natl Acad. Sci. USA, 91, 9218-9222.
59. Mir,K.U. and Southern,E.M. (1999) Determining the influence of structure on hybridization using oligonucleotide arrays. Nat. Biotechnol., 17, 788-792.
60. Ehresmann,C., Baudin,F., Mougel,M., Romby,P., Ebel,J.P. and Ehresmann,B. (1987) Probing the structure of RNAs in solution. Nucleic Acids Res. 15, 9109-9128.
61. Lewis,J.B. and Doty,P. (1977) Identification of the single-strand regions in Escherichia coli 5S RNA, native and A forms, by the binding of oligonucleotides. Biochemistry, 16, 5016-5025.
62. Uhlenbeck,O.C. (1972) Complementary oligonucleotide binding to transfer RNA. J. Mol. Biol., 65, 25-41.
63. Uhlenbeck,O.C., Baller,J. and Doty,P. (1970) Complementary oligonucleotide binding to the anticodon loop of fMet-transfer RNA. Nature, 225, 508-510.
64. Milner,N., Mir,K.U. and Southern,E.M. (1997) Selecting effective antisense reagents on combinatorial oligonucleotide arrays. Nat. Biotechnol., 15, 537-541.
65. Duan,S., Mathews,D.H. and Turner,D.H. (2006) Interpreting oligonucleotide microarray data to determine RNA secondary structure: application to the 3′ end of Bombyx mori R2 RNA. Biochemistry 45, 9819-9832.
66. Desai,N.A. and Shankar,V. (2003) Single-strand-specific nucleases. FEMS Microbiol. Rev., 26, 457-491.
67. Moody,E.M., Brown,T.S. and Bevilacqua,P.C. (2004) Simple method for determining nucleobase pK(a) values by indirect labeling and demonstration of a pK(a) of neutrality in dsDNA. J. Am. Chem. Soc. 126, 10200-10201.
68. Wadkins,T.S., Shih,I., Perrotta,A.T. and Been,M.D. (2001) A pH-sensitive RNA tertiary interaction affects self-cleavage activity of the HDV ribozymes in the absence of added divalent metal ion. J. Mol. Biol. 305, 1045-1055.
69. Ando,T. (1966) A nuclease specific for heat-denatured DNA in isolated from a product of Aspergillus oryzae. Biochim. Biophys. Acta, 114, 158-168.
70. Smith,R.M. and Wu,G.Y. (2004) Secondary structure and hybridization accessibility of the hepatitis C virus negative strand RNA 5′-terminus. J. Viral. Hepat., 11, 115-123.
71. Smith,R.M., Walton,C.M., Wu,C.H. and Wu,G.Y. (2002) Secondary structure and hybridization accessibility of hepatitis C virus 3′-terminal sequences. J. Virol., 76, 9563-9574.
72. Phe. Nucleic Acids Symp. Ser. (Oxf.), 219-220.
73. Ratmeyer,L., Vinayak,R., Zhong,Y.Y., Zon,G. and Wilson,W.D. (1994) Sequence specific thermodynamic and structural properties for DNA.RNA duplexes. Biochemistry, 33, 5298-5304.
74. Robertus,J.D., Ladner,J.E., Finch,J.T., Rhodes,D., Brown,R.S., Clark,B.F. and Klug,A. (1974) Structure of yeast phenylalanine tRNA at 3Å resolution. Nature, 250, 546-551.
75. Kim,S.H., Suddath,F.L., Quigley,G.J., McPherson,A., Sussman,J.L., Wang,A.H., Seeman,N.C. and Rich,A. (1974) Three-dimensional tertiary structure of yeast phenylalanine transfer RNA. Science, 185, 435-440.
76. Goringer,H.U. and Wagner,R. (1986) Does 5S RNA from Escherichia coli have a pseudoknotted structure? Nucleic Acids Res., 14, 7473-7485.
77. Schuwirth,B.S., Borovinskaya,M.A., Hau,C.W., Zhang,W., Vila-Sanjurjo,A., Holton,J.M. and Cate,J.H. (2005) Structures of the bacterial ribosome at 3.5Å resolution. Science, 310, 827-834.