A set of nearest neighbor parameters for predicting the enthalpy change of RNA secondary structure formation

Nucleic Acids Research

Volumn 34, Issue 17, 2006, Pages 4912-4924

  Lu, Zhi John ^a   Turner, Douglas H ^b   Mathews, David H ^a  

^a UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

^b UNIVERSITY OF ROCHESTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

RNA;

ARTICLE; BASE PAIRING; CHEMICAL PARAMETERS; CONTROLLED STUDY; CORRELATION ANALYSIS; ENERGY TRANSFER; ENTHALPY; ESCHERICHIA COLI; GEOBACILLUS STEAROTHERMOPHILUS; GROWTH RATE; MELTING POINT; NONHUMAN; PARTITION COEFFICIENT; PREDICTION; PRIORITY JOURNAL; PROBABILITY; RNA SEQUENCE; RNA STRUCTURE; SACCHAROMYCES CEREVISIAE; SENSITIVITY ANALYSIS; TEMPERATURE DEPENDENCE; TETRAHYMENA THERMOPHILA;

ALGORITHMS; BASE PAIRING; BASE SEQUENCE; MODELS, CHEMICAL; MOLECULAR SEQUENCE DATA; NUCLEIC ACID CONFORMATION; NUCLEIC ACID DENATURATION; RNA; RNA, TRANSFER; SACCHAROMYCES CEREVISIAE; TEMPERATURE; THERMODYNAMICS;

EID: 33750214512     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkl472     Document Type: Article

References (80)

1. Nelson,P., Kiriakidou,M., Sharma,A., Maniataki,E. and Mourelatos,Z. (2003) The microRNA world: Small is mighty. Trends Biochem. Sci., 28, 534-540.
2. Doudna,J. and Cech,T. (2002) The chemical repertoire of natural ribozymes. Nature, 418, 222-228.
3. Walter,P. and Blobel,G. (1982) Signal recognition particle contains a 7S RNA essential for protein translocation across the endoplasmic reticulum. Nature, 299, 691-698.
4. Lau,N.C., Lim,L.P., Weinstein,E.G. and Bartel,D.P. (2001) An abundant class of tiny RNAs with probable regulatory roles in Caenorhabditis elegans. Science, 294, 858-862.
5. Lagos-Quintana,M., Rauhut,R., Lendeckel,W. and Tuschl,T. (2001) Identification of novel genes coding for small expressed RNAs. Science, 294, 853-858.
6. Onoa,B. and Tinoco,I.,Jr (2004) RNA folding and unfolding. Curr. Opin. Struct. Biol., 14, 374-379.
7. Crothers,D.M., Cole,P.E., Hilbers,C.W. and Schulman,R.G. (1974) The molecular mechanism of thermal unfolding of Escherichia coli formylmethionine transfer RNA. J. Mol. Biol., 87, 63-88.
8. Mathews,D.H., Banerjee,A.R., Luan,D.D., Eickbush,T.H. and Turner,D.H. (1997) Secondary structure model of the RNA recognized by the reverse transcriptase from the R2 retrotransposable element. RNA, 3, 1-16.
9. Banerjee,A.R., Jaeger,J.A. and Turner,D.H. (1993) Thermal unfolding of a group I ribozyme: The low temperature transition is primarily a disruption of tertiary structure. Biochemistry, 32, 153-163.
10. Woodson,S.A. (2000) Recent insights on RNA folding mechanisms from catalytic RNA. Cell Mol. Life Sci., 57, 796-808.
11. James,B.D., Olsen,G.J. and Pace,N.R. (1989) Phylogenetic comparative analysis of RNA secondary structure. Methods Enzymol., 180, 227-239.
12. Pace,N.R., Thomas,B.C. and Woese,C.R. (1999) Probing RNA structure, function, and history by comparative analysis. In Gesteland,R.F., Cech,T.R. and Atkins,J.F. (eds), The RNA World, 2nd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, pp. 113-141.
13. Woese,C.R., Gutell,R.R., Gupta,R. and Noller,H.F. (1983) Detailed analysis of the higher order structure of 16S-like ribosomal ribonucleic acids. Microbiol. Rev., 47, 621-669.
14. Andronescu,M., Aguirre-Hernandez,R., Condon,A. and Hoos,H.H. (2003) RNAsoft: A suite of RNA secondary structure prediction and design software tools. Nucleic Acids Res., 31, 3416-3422.
15. Hofacker,I.L. (2003) Vienna RNA secondary structure server. Nucleic Acids Res., 31, 3429-3431.
16. Zuker,M. (2003) Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res., 31, 3406-3415.
17. 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.
18. Mathews,D.H., Sabina,J., Zuker,M. and Turner,D.H. (1999) Expanded sequence dependence of thermodynamic parameters provides improved prediction of RNA Secondary Structure. J. Mol. Biol., 288, 911-940.
19. Turner,D.H. (2000) Conformational changes. In Bloomfield,V., Crothers,D. and Tinoco,I. (eds), Nucleic Acids. University Science Books, Sausalito, CA, pp. 259-334.
20. Xia,T., Mathews,D.H. and Turner,D.H. (1999) Thermodynamics of RNA secondary structure formation. In Soll,D.G., Nishimura,S. and Moore,P.B. (eds), Prebiotic Chemistry, Molecular Fossils, Nucleosides, and RNA. Elsevier, NY, pp. 21-47.
21. Xia,T., SantaLucia,J.,Jr, Burkard,M.E., Kierzek,R., Schroeder,S.J., Jiao,X., Cox,C. and Turner,D.H. (1998) Thermodynamic parameters for an expanded nearest-neighbor model for formation of RNA duplexes with Watson-Crick pairs. Biochemistry, 37, 14719-14735.
22. Mathews,D.H. (2004) Using an RNA secondary structure partition function to determine confidence in base pairs predicted by free energy minimization. RNA, 10, 1178-1190.
23. McCaskill,J.S. (1990) The equilibrium partition function and base pair probabilities for RNA secondary structure. Biopolymers, 29, 1105-1119.
24. Serra,M.J. and Turner,D.H. (1995) Predicting thermodynamic properties of RNA. Methods Enzymol., 259, 242-261.
25. Giese,M.R., Betschart,K., Dale,T., Riley,C.K., Rowan,C., Sprouse,K.J. and Serra,M.J. (1998) Stability of RNA hairpins closed by wobble base pairs. Biochemistry, 37, 1094-1100.
26. Serra,M.J., Lyttle,M.H., Axenson,T.J., Schadt,C.A. and Turner,D.H. (1993) RNA hairpin loop stability depends on closing pair. Nucleic Acids Res., 21, 3845-3849.
27. Serra,M.J., Axenson,T.J. and Turner,D.H. (1994) A model for the stabilities of RNA hairpins based on a study of the sequence dependence of stability for hairpins of six nucleotides. Biochemistry, 33, 14289-14296.
28. Serra,M.J., Barnes,T.W., Betschart,K., Gutierrez,M.J., Sprouse,K.J., Riley,C.K., Stewart,L. and Temel,R.E. (1997) Improved parameters for the prediction of RNA hairpin stability. Biochemistry, 36, 4844-4851.
29. Groebe,D.R. and Uhlenbeck,O.C. (1988) Characterization of RNA hairpin loop stability. Nucleic Acids Res., 16, 11725-11735.
30. Dale,T., Smith,R. and Serra,M.J. (2000) A test of the model to predict unusually stable RNA hairpin loop stability. RNA, 6, 608-615.
31. Antao,V.P. and Tinoco,I.,Jr (1992) Thermodynamic parameters for loop formation in RNA and DNA hairpin tetraloops. Nucleic Acids Res., 20, 819-824.
32. Longfellow,C.E., Kierzek,R. and Turner,D.H. (1990) Thermodynamic and spectroscopic study of bulge loops in oligoribonucleotides. Biochemistry, 29, 278-285.
33. Znosko,B.M., Silvestri,S.B., Volkman,H., Boswell,B. and Serra,M.J. (2002) Thermodynamic parameters for an expanded nearest-neighbor model for the formation of RNA duplexes with single nucleotide bulges. Biochemistry, 41, 10406-10417.
34. Shu,Z. and Bevilacqua,P.C. (1999) Isolation and characterization of thermodynamically stable and unstable RNA hairpins from a triloop combinatorial library. Biochemistry, 38, 15369-15379.
35. Proctor,D.J., Schaak,J.E., Bevilacqua,J.M., Falzone,C.J. and Bevilacqua,P.C. (2002) Isolation and characterization of stable tetraloops with the motif YNMG that participates in tertiary interactions. Biochemistry, 41, 12062-12075.
36. Laing,L.G. and Hall,K.B. (1996) A model of the iron responsive element RNA hairpin loop structure determined from NMR and thermodynamic data. Biochemistry, 35, 13586-13596.
37. Groebe,D.R. and Uhlenbeck,O.C. (1989) Thermal stability of RNA hairpins containing a four-membered loop and a bulge nucleotide. Biochemistry, 28, 742-747.
38. Fink,T.R. and Crothers,D.M. (1972) Free energy of imperfect nucleic acid helices,I. The bulge defect. J. Mol. Biol., 66, 1-12.
39. Jaeger,J.A., Turner,D.H. and Zuker,M. (1989) Improved predictions of secondary structures for RNA. Proc. Natl Acad. Sci. USA, 86, 7706-7710.
40. Weeks,K.M. and Crothers,D.M. (1993) Major groove accessibility of RNA. Science, 261, 1574-1577.
41. Chen,G., Znosko,B.M., Jiao,X. and Turner,D.H. (2004) Factors affecting thermodynamic stabilities of RNA 3 × 3 internal loops. Biochemistry, 43, 12865-12876.
42. Gutell,R.R. (1994) Collection of small subunit (16S- and 16S-like) ribosomal RNA structures. Nucleic Acids Res., 22, 3502-3507.
43. Gutell,R.R., Gray,M.W. and Schnare,M.N. (1993) A compilation of large subunit (23S- and 23S-like) ribosomal RNA structures. Nucleic Acids Res., 21, 3055-3074.
44. Schnare,M.N., Damberger,S.H., Gray,M.W. and Gutell,R.R. (1996) Comprehensive comparison of structural characteristics in eukaryotic cytoplasmic large subunit (23S-like) ribosomal RNA. J. Mol. Biol., 256, 701-719.
45. Szymanski,M., Specht,T., Barciszewska,M.Z., Barciszewski,J. and Erdmann,V.A. (1998) 5S rRNA data bank. Nucleic Acids Res., 26, 156-159.
46. Sprinzl,M., Horn,C., Brown,M., Ioudovitch,A. and Steinberg,S. (1998) Compilation of tRNA sequences and sequences of tRNA genes. Nucleic Acids Res., 26, 148-153.
47. Larsen,N., Samuelsson,T. and Zwieb,C. (1998) The signal recognition particle database (SRPDB). Nucleic Acids Res., 26, 177-178.
48. Brown,J.W. (1998) The ribonuclease P database. Nucleic Acids Res., 26, 351-352.
49. Damberger,S.H. and Gutell,R.R. (1994) A comparative database of group I intron structures. Nucleic Acids Res., 22, 3508-3510.
50. Mathews,D.H. and Turner,D.H. (2002) Experimentally derived nearest neighbor parameters for the stability of RNA three- and four-way multibranch loops. Biochemistry, 41, 869-880.
51. Diamond,J.M., Turner,D.H. and Mathews,D.H. (2001) Thermodynamics of three-way multibranch loops in RNA. Biochemistry, 40, 6971-6981.
52. Walter,A.E., Wu,M. and Turner,D.H. (1994) The stability and structure of tandem GA mismatches in RNA depend on closing base pairs. Biochemistry, 33, 11349-11354.
53. Walter,A.E., Turner,D.H., Kim,J., Lyttle,M.H., Miller,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.
54. Kim,J., Walter,A.E. and Turner,D.H. (1996) Thermodynamics of coaxially stacked helices with GA and CC mismatches. Biochemistry, 35, 13753-13761.
55. SantaLucia,J.,Jr, Kierzek,R. and Turner,D.H. (1991) Functional group substitutions as probes of hydrogen bonding between GA mismatches in RNA internal loops. J. Am. Chem. Soc., 113, 4313-4322.
56. 2 and determinants of stability for single guanosine-guanosine base pairs. Biochemistry, 39, 11748-11762.
57. Jacobson,H. and Stockmayer,W.H. (1950) Intramolecular reaction in polycondensations. I. The theory of linear systems. J. Chem. Phys., 18, 1600-1606.
58. Michel,F., Umesono,K. and Ozeki,H. (1989) Comparative and functional anatomy of group II catalytic introns - a review. Gene, 82, 5-30.
59. Waring,R.B. and Davies,R.W. (1984) Assessment of a model for intron RNA secondary structure relevant to RNA self-splicing - a review. Gene, 28, 277-291.
60. Kowalak,J.A., Dalluge,J.J., McCloskey,J.A. and Stetter,K.O. (1994) The role of posttranscriptional modification in stabilization of transfer RNA from hyperthermophiles. Biochemistry, 33, 7869-7876.
61. Dubins,D.N., Lee,A., Macgregor,R.B.,Jr and Chalikian,T.V. (2001) On the stability of double stranded nucleic acids. J. Am. Chem. Soc., 123, 9254-9259.
62. Petersheim,M. and Turner,D.H. (1983) Base-stacking and base-pairing contributions to helix stability: Thermodynamics of double-helix formation with CCGG, CCGGp, CCGGAp, ACCGGp, CCGGUp, and ACCGGUp. Biochemistry, 22, 256-268.
63. Holbrook,J.A., Capp,M.W., Saecker,R.M. and Record,M.T.,Jr (1999) Enthalpy and heat capacity changes for formation of an oligomeric DNA duplex: Interpretation in terms of coupled processes of formation and association of single-stranded helices. Biochemistry, 38, 8409-8422.
64. Suurkuusk,J., Alvarez,J., Freire,E. and Biltonen,R. (1977) Calorimetric determination of the heat capacity changes associated with the conformational transitions of polyriboadenylic acid and polyribouridylic acid. Biopolymers, 16, 2641-2652.
65. Pörschke,D., Uhlenbeck,O.C. and Martin,F.H. (1973) Thermodynamics and kinetics of the helix-coil transition of oligomers containing GC base pairs. Biopolymers, 12, 1313-1335.
66. Appleby,D.W. and Kallenbach,N.R. (1973) Theory of oligonucleotide stabilization. I. The effect of single-strand stacking. Biopolymers, 12, 2093-2120.
67. Freier,S.M., Hill,K.D., Dewey,T.G., Marky,L.A., Breslauer,K.J. and Turner,D.H. (1981) Solvent effects on the kinetics and thermodynamics of stacking in poly(cytidylic acid). Biochemistry, 20, 1419-1426.
68. Takach,J.C., Mikulecky,P.J. and Feig,A.L. (2004) Salt-dependent heat capacity changes for RNA duplex formation. J. Am. Chem. Soc., 126, 6530-6531.
69. Mikulecky,P.J., Takach,J.C. and Feig,A.L. (2004) Entropy-driven folding of an RNA helical junction: An isothermal titration calorimetric analysis of the hammerhead ribozyme. Biochemistry, 43, 5870-5881.
70. Mathews,D.H. (2005) Predicting a set of minimal free energy RNA secondary structures common to two sequences. Bioinformatics, 21, 2246-2253.
71. Lyngsø,R., Zuker,M. and Pederson,C. (1999) Fast evaluation of internal loops in RNA secondary structure prediction. Bioinformatics, 15, 440-445.
72. Layton,D.M. and Bundschuh,R. (2005) A statistical analysis of RNA folding algorithms through thermodynamic parameter perturbation. Nucleic Acids Res., 33, 519-524.
73. Borer,P.N., Dengler,B., Tinoco,I.,Jr and Uhlenbeck,O.C. (1974) Stability of ribonucleic acid double-stranded helices. J. Mol. Biol., 86, 843-853.
74. Khachane,A.N., Timmis,K.N. and dos Santos,V.A. (2005) Uracil content of 16S rRNA of thermophilic and psychrophilic prokaryotes correlates inversely with their optimal growth temperatures. Nucleic Acids Res., 33, 4016-4022.
75. Adilakshmi,T., Ramaswamy,P. and Woodson,S.A. (2005) Protein-independent folding pathway of the 16S rRNA 50 domain. J. Mol. Biol., 351, 508-519.
76. Wu,M., McDowell,J.A. and Turner,D.H. (1995) A periodic table of symmetric tandem mismatches in RNA. Biochemistry, 34, 3204-3211.
77. + pairs. Biochemistry, 30, 8242-8251.
78. Znosko,B.M., Burkard,M.E., Krugh,T.R. and Turner,D.H. (2002) Molecular recognition in purine-rich internal loops: Thermodynamic, structural, and dynamic consequences of purine for adenine substitutions in 5′ (rGGCAAGCCU)2. Biochemistry, 41, 14978-14987.
79. Schroeder,S.J. and Turner,D.H. (2001) Thermodynamic stabilities of internal loops with GU closing pairs in RNA. Biochemistry, 40, 11509-11517.
80. Xia,T., McDowell,J.A. and Turner,D.H. (1997) Thermodynamics of nonsymmetric tandem mismatches adjacent to G·C base pairs in RNA. Biochemistry, 36, 12486-12487.