Using an RNA secondary structure partition function to determine confidence in base pairs predicted by free energy minimization

RNA

Volumn 10, Issue 8, 2004, Pages 1178-1190

  Mathews, David H ^a,b  

^a UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

^b SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

RNA partition function; RNA secondary structure; Statistical mechanics

Indexed keywords

ARTICLE; BASE PAIRING; CHEMICAL MODIFICATION; ENERGY CONSUMPTION; PARTITION COEFFICIENT; PREDICTION; PRIORITY JOURNAL; PROBABILITY; PROTEIN LOCALIZATION; PROTEIN SECONDARY STRUCTURE; RNA SPLICING; RNA STRUCTURE; STATISTICAL ANALYSIS; X RAY CRYSTALLOGRAPHY;

ALGORITHMS; ANIMALS; COMPUTATIONAL BIOLOGY; DATA INTERPRETATION, STATISTICAL; HUMANS; NUCLEIC ACID CONFORMATION; SEQUENCE ANALYSIS, RNA;

EID: 3342977915     PISSN: 13558382     EISSN: None     Source Type: Journal    
DOI: 10.1261/rna.7650904     Document Type: Article

References (83)

1. Adams, M.D., Celniker, S.E., Holt, R.A., Evans, C.A., Gocayne, J.D., Amanatides, P.G., Scherer, S.E., Li, P.W., Hoskins, R.A., Galle, R.F., et al. 2000. The genome sequence of Drosphila melanogaster. Science 287: 2185-2195.
2. Andreazzoli, M. and Gerbi, S.A. 1991. Changes in 7SL RNA conformation during the signal recognition particle cycle. EMBO J. 10: 767-777.
3. Arabidopsis Genome Initiative. 2000. Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408: 796-815.
4. 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.
5. Baumstark, T., Schröder, A.R.W., and Riesner, D. 1997. Viroid processing: Switch from cleavage to ligation is driven by a change from tetraloop to a loop A conformation. EMBO J. 16: 599-610.
6. Brennan, T. and Sundaralingam, M. 1976. Structure of transfer RNA molecules containing the long variable loop. Nucleic Acids Res. 3: 3235-3250.
7. Brown, J.W. 1999. The ribonuclease P database. Nucleic Acids Res. 27: 314.
8. Burgstaller, P. and Famulok, M. 1997. Flavin-dependent photocleavage of RNA at G·U base pairs. J. Am. Chem. Soc. 119: 1137-1138.
9. Burgstaller, P., Hermann, T., Huber, C., Westhof, E., and Famulok, M. 1997. Isoalloxazine derivatives promote photocleavage of natural RNAs at G·U base pairs embedded within helices. Nucleic Acids Res. 25: 4018-4027.
10. C. elegans Sequencing Consortium. 1998. Genome sequence of the nematode C. elegans: A platform for investigating biology. Science 282: 2012-2018.
11. Cannone, J.J., Subramanian, S., Schnare, M.N., Collett, J.R., D'Souza, L.M., Du, Y., Feng, B., Lin, N., Madabusi, L.V., Muller, K.M., et al. 2002. The comparative RNA web (CRW) site: An online database of comparative sequence and structure information for ribosomal, intron, and other RNAs. BMC Bioinformatics 3.
12. Chamberlin, S.I. and Weeks, K.M. 2003. Differential helix stabilities and sites pre-organized for tertiary interactions revealed by monitoring local nucleotide flexibility in the bI5 group I intron RNA. Biochemistry 42: 901-909.
13. Costa, M., Christian, E.L., and Michel, F. 1998. Differential chemical probing of a group II self-splicing intron identifies bases involved in tertiary interactions and supports an alternative secondary structure model of domain V. RNA 4: 1055-1068.
14. Diamond, J.M., Turner, D.H., and Mathews, D.H. 2001. Thermodynamics of three-way multibranch loops in RNA. Biochemistry 40: 6971-6981.
15. Ding, Y. and Lawrence, C. 2001. Statistical prediction of single-stranded regions in RNA secondary structure and application to predicting effective antisense target sites and beyond. Nucleic Acids Res. 29: 1034-1046.
16. -. 2003. A statistical sampling algorithm for RNA secondary structure prediction. Nucleic Acids Res. 31: 7280-7301.
17. Dirks, R. and Pierce, N. 2003. A partition function algorithm for nucleic acid secondary structure including pseudoknots. J. Comput. Chem. 24: 1664-1677.
18. Doudna, J. and Cech, T. 2002. The chemical repertoire of natural ribozymes. Nature 418: 222-228.
19. Eddy, S.R. 2001. Non-coding RNA genes and the modern RNA world. Nat. Rev. 2: 919-929.
20. Egebjerg, J., Leffers, H., Christensen, A., Andersen, H., and Garrett, R.A. 1987. Structure and accessibility of domain I of Escherichia coli 23 S RNA in free RNA, in the L24-RNA complex and in 50 S subunits. J. Mol. Biol. 196: 125-136.
21. Ehresmann, C., Baudin, F., Mougel, M., Romby, P., Ebel, J., and Ehresmann, B. 1987. Probing the structure of RNAs in solution. Nucleic Acids Res. 15: 9109-9128.
22. Fekete, M., Hofacker, I.L., and Stadler, P.F. 2000. Prediction of RNA base pairing probabilities on massively parallel computers. J. Comput. Biol. 7: 171-182.
23. Flamm, C., Hofacker, I.L., Maurer-Stroh, S., Stadler, P.F., and Zehl, M. 2001. Design of multistable RNA molecules. RNA 7: 254-265.
24. Fraser, C., Eisen, J., and Salzberg, S. 2000. Microbial genome sequencing. Nature 406: 799-803.
25. Gaspin, C. and Westhof, E. 1995. An interactive framework for RNA secondary structure prediction with a dynamical treatment of constraints. J. Mol. Biol. 254: 163-174.
26. Goffeau, A., Barrell, B.G., Bussey, H., Davis, R.W., Dujon, B., Feldmann, H., Galibert, F., Hoheisel, J.D., Jacq, C., Johnston, M., et al. 1996. Life with 6000 genes. Science 274: 546, 563-567.
27. Gorodkin, J., Knudsen, B., Zwieb, C., and Samuelsson, T. 2001. SRPDB (signal recognition particle database). Nucleic Acids Res. 29: 169-170.
28. Gutell, R.R., Lee, J.C., and Cannone, J.J. 2002. The accuracy of ribosomal RNA comparative structure models. Curr. Opin. Struct. Biol. 12: 301-310.
29. Hansen, J.L., Schmeing, T.M., Moore, P.B., and Steitz, T.A. 2002. Structural insights into peptide bond formation. Proc. Natl. Acad. Sci. 99: 11670-11675.
30. Hofacker, I.L. 2003. Vienna RNA secondary structure server. Nucleic Acids Res. 31: 3429-3431.
31. Hofacker, I.L., Fontana, W., Stadler, P.F., Bonhoeffer, L.S., Tacker, M., and Schuster, P. 1994. Fast folding and comparison of RNA secondary structures. Monatsh Chem. 125: 167-168.
32. Hoffman, B., Mitchell, G.T., Gendron, P., Major, F., Anderson, A.A., Collins, R.A., and Legault, P. 2003. NMR structure of the active conformation of the Varkud satellite ribozyme cleavage site. Proc. Natl. Acad. Sci. 100: 7003-7008.
33. Huynen, M., Gutell, R., and Konings, D. 1997. Assessing the reliability of RNA folding using statistical mechanics. J. Mol. Biol. 267: 1104-1112.
34. International Human Genome Sequencing Consortium. 2001. Initial sequencing and analysis of the human genome. Nature 409: 860-921.
35. Kean, J.M. and Draper, D.E. 1985. Secondary structure of a 345-base RNA fragment covering the S8/S15 protein binding domain of Escherichia coli 16S ribosomal RNA. Biochemistry 24: 5052-5061.
36. Kim, J., Walter, A.E., and Turner, D.H. 1996. Thermodynamics of coaxially stacked helices with GA and CC mismatches. Biochemistry 35: 13753-13761.
37. Knapp, G. 1989. Enzymatic approaches to probing RNA secondary and tertiary structure. Methods Enzymol. 180: 192-212.
38. Kwakman, J.H.J.M., Konings, D.A.M., Hogweg, P., Patel, H.J., and Grivell, L.A. 1990. Structural analysis of a group II intron by chemical modifications and minimal energy calculations. J. Biomol. Struct. Dyn. 8: 413-430.
39. Lagos-Quintana, M., Rauhut, R., Lendeckel, W., and Tuschl, T. 2001. Identification of novel genes coding for small expressed RNAs. Science 294: 853-858.
40. LaGrandeur, T.E., Hüttenhofer, A., Noller, H.F., and Pace, N.R. 1994. Phylogenetic comparative chemical footprint analysis of the interaction between ribonuclease P RNA and tRNA. EMBO J. 17: 3945-3952.
41. Larsen, N., Samuelsson, T., and Zwieb, C. 1998. The signal recognition particle database (SRPDB). Nucleic Acids Res. 26: 177-178.
42. 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.
43. Lyngsø, R., Zuker, M., and Pederson, C. 1999. Fast evaluation of internal loops in RNA secondary structure prediction. Bioinformatics 15: 440-445.
44. Mathews, D.H. and Turner, D.H. 2002. Dynalign: An algorithm for finding the secondary structure common to two RNA sequences. J. Mol. Biol. 317: 191-203.
45. 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.
46. Mathews, D.H., Burkard, M.E., Freier, S.M., Wyatt, J.R., and Turner, D.H. 1999a. Predicting oligonucleotide affinity to nucleic acid targets. RNA 5: 1458-1469.
47. Mathews, D.H., Sabina, J., Zuker, M., and Turner, D.H. 1999b. Expanded sequence dependence of thermodynamic parameters provides improved prediction of RNA secondary structure. J. Mol. Biol. 288: 911-940.
48. 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. 101: 7287-7292.
49. Matveeva, O.V., Mathews, D.H., Tsodikov, A.D., Shabalina, S.A., Gesteland, R.F., Atkins, J.F., and Freier, S.M. 2003. Thermodynamic criteria for high hit rate antisense oligonucleotide design. Nucleic Acids Res. 31: 4989-4994.
50. McCaskill, J.S. 1990. The equilibrium partition function and base pair probabilities for RNA secondary structure. Biopolymers 29: 1105-1119.
51. Michel, F., Umesono, K., and Ozeki, H. 1989. Comparative and functional anatomy of group II catalytic introns-A review. Gene 82: 5-30.
52. Michiels, P.J.A., Schouten, C.H.J., Hilbers, C.W., and Heus, H.A. 2000. Structure of the ribozyme substrate hairpin of Neurospora VS RNA: A close look at the cleavage site. RNA 6: 1821-1832.
53. Miura, K., Tsuda, S., Ueda, T., Harada, F., and Kato, N. 1983. Chemical modification of guanine residues of mouse 5 S ribosomal RNA with kethoxal. Biochim. Biophys. Acta 739: 281-285.
54. Moazed, D., Stern, S., and Noller, H.F. 1986. Rapid chemical probing of conformation in 16S ribosomal RNA and 30S ribosomal subunits using primer extension. J. Mol. Biol. 187: 399-416.
55. Mouse Genome Sequencing Consortium. 2002. Initial sequencing and comparative analysis of the mouse genome. Nature 420: 520-562.
56. Nissen, P., Hansen, J., Ban, N., Moore, P.B., and Steitz, T.A. 2000. The structural basis of ribosomal activity in peptide bond synthesis. Science 289: 920-930.
57. Odell, L., Huang, V., Jakacka, M., and Pan, T. 1998. Interaction of structural modules in substrate binding by ribozyme from Bacillus subtilis RNase P. Nucleic Acids Res. 26: 3717-3723.
58. Pace, N.R., Thomas, B.C., and Woese, C.R. 1999. Probing RNA structure, function, and history by comparative analysis. In The RNA world, 2nd ed. (eds. R.F. Gesteland et al.), pp. 113-141. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
59. Pappalardo, L., Kerwood, D.J., Pelczer, I., and Borer, P.N. 1998. Three-dimensional folding of an RNA hairpin required for packaging HIV-1. J. Mol. Biol. 282: 801-818.
60. Rivas, E. and Eddy, S.R. 1999. A dynamic programming algorithm for RNA structure prediction including pseudoknots. J. Mol. Biol. 285: 2053-2068.
61. Romero, D.P. and Blackburn, E.H. 1991. A conserved secondary structure for telomerase RNA. Cell 67: 343-353.
62. Ruan, J., Stormo, G.D., and Zhang, W. 2004. An iterated loop matching approach to the prediction of RNA secondary structures with pseudoknots. Bioinformatics 20: 58-66.
63. Schluenzen, F., Tocilj, A., Zarivach, R., Harms, J., Gluehmann, M., Janell, D., Bashan, A., Bartels, H., Agmon, I., Franceschi, F., et al. 2000. Structure of functionally activated small ribosomal subunit at 3.3 Å resolution. Cell 102: 615-623.
64. Schultes, E.A. and Bartel, D.P. 2000. One sequence, two ribozymes: Implications for emergence of new ribozyme folds. Science 289: 448-452.
65. 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.
66. 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.
67. Szymanski, M., Barciszewska, M.Z., Barciszewski, J., and Erdmann, V.A. 2000. 5S ribosomal RNA database Y2K. Nucleic Acids Res. 28: 166-167.
68. ten Dam, E., van Belkum, A., and Pleij, K. 1991. A conserved pseudoknot in telomerase RNA. Nucleic Acids Res. 19: 6951.
69. Tranguch, A.J., Kinderberger, D.W., Rohlman, C.E., Lee, J., and Engelke, D.R. 1994. Structure-sensitive RNA footprinting of yeast nuclear ribonuclease P. Biochemistry 33: 1778-1787.
70. Turner, D.H. 2000. Conformational changes. In Nucleic Acids (eds. V. Bloomfield et al.), pp. 259-334. University Science Books, Sausalito, CA.
71. Venter, J.C., Adams, M.D., Myers, E.W., Li, P.W., Mural, R.J., Sutton, G.G., Smith, H.O., Yandell, M., Evans, C.A., Holt, R.A., et al. 2001. The sequence of the human genome. Science 291: 1304-1351.
72. 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.
73. Walter, A.E., Turner, D.H., Kim, J., Lyttle, M.H., Müller, P., Mathews, D.H., and Zuker, M. 1994a. Coaxial stacking of helixes enhances binding of oligoribonucleotides and improves predictions of RNA folding. Proc. Natl. Acad. Sci. 91: 9218-9222.
74. Walter, A.E., Wu, M., and Turner, D.H. 1994b. The stability and structure of tandem GA mismatches in RNA depend on closing base pairs. Biochemistry 33: 11349-11354.
75. Wimberly, B.T., Brodersen, D.E., Clemons, W.M., Morgan-Warren, R.J., Carter, A.P., Vonrhein, C., Hartsch, T., and Ramakrishnan, V. 2000. Structure of the 30S ribosomal subunit. Nature 407: 327-329.
76. Wuchty, S., Fontana, W., Hofacker, I.L., and Schuster, P. 1999. Complete suboptimal folding of RNA and the stability of secondary structures. Biopolymers 49: 145-165.
77. Xia, T., SantaLucia Jr., J., Burkard, M.E., Kierzek, R., Schroeder, S.J., Jiao, X., Cox, C., and Turner, D.H. 1998. Parameters for an expanded nearest-neighbor model for formation of RNA duplexes with Watson-Crick pairs. Biochemistry 37: 14719-14735.
78. Xia, T., Mathews, D.H., and Turner, D.H. 1999. Thermodynamics of RNA secondary structure formation. In Prebiotic chemistry, molecular fossils, nucleosides, and RNA (eds. D.G. Söll et al.), pp 21-47. Elsevier, New York.
79. Zaug, A.J. and Cech, T.R. 1995. Analysis of the structure of Tetrahymena nuclear RNAs in vivo: Telomerase RNA, the self-splicing rRNA intron, and U2 snRNA. RNA 1: 363-374.
80. Zavanelli, M.I. and Ares Jr., M. 1991. Efficient association of U2 snRNPs with pre-mRNA requires an essential U2 RNA structural element. Genes & Dev. 5: 2521-2533.
81. Zuker, M. 1989. On finding all suboptimal foldings of an RNA molecule. Science 244: 48-52.
82. Zuker, M. and Jacobson, A.B. 1995. "Well-determined" regions in RNA secondary structure predictions. Applications to small and large subunit rRNA. Nucleic Acids Res. 23: 2791-2798.
83. -. 1998. Using reliability information to annotate RNA secondary structures. RNA 4: 669-679.