Understanding the errors of SHAPE-directed RNA structure modeling

Biochemistry

Volumn 50, Issue 37, 2011, Pages 8049-8056

  Kladwang, Wipapat ^a   Vanlang, Christopher C ^b   Cordero, Pablo ^a   Das, Rhiju ^a  

^a STANFORD UNIVERSITY   (United States)

^b Stanford University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMICAL MAPPING; COMPUTATIONAL ALGORITHM; CRYSTALLOGRAPHIC DATA; DEOXYINOSINE; ERROR RATE; FALSE DISCOVERY RATE; FALSE NEGATIVE RATE; HELIX PREDICTION; INFORMATION CONTENTS; LOW LEVEL; MODELING ERRORS; MODELING PARAMETERS; NON-PARAMETRIC; PRIMER EXTENSION; RESIDUAL STRUCTURE; RIBOSWITCHES; RIBOZYMES; RNA GENOME; RNA SECONDARY STRUCTURES; RNA STRUCTURES; SHAPE DATA; TETRAHYMENA; TRIPHOSPHATE;

AMINO ACIDS; COMPUTATIONAL CHEMISTRY; DATA HANDLING; ERRORS; ESCHERICHIA COLI;

RNA;

CYCLIC GMP; DEOXYINOSINE; DEOXYINOSINE TRIPHOSPHATE; GLYCINE; RIBOZYME; RNA; TRANSFER RNA; UNCLASSIFIED DRUG;

ARTICLE; BOOTSTRAPPING; CRYSTALLOGRAPHY; ERROR; ESCHERICHIA COLI; FALSE NEGATIVE RESULT; GENOME; HUMAN IMMUNODEFICIENCY VIRUS 1; INFORMATION PROCESSING; LABORATORY DIAGNOSIS; LIGAND BINDING; MOLECULAR MODEL; MOLECULE; NONHUMAN; PREDICTION ERROR; PRIORITY JOURNAL; RNA STRUCTURE; SELECTIVE 2' HYDROXYL ACYLATION BY PRIMER EXTENSION; TETRAHYMENA;

BASE SEQUENCE; CHROMOSOME MAPPING; CRYSTALLOGRAPHY, X-RAY; MODELS, GENETIC; MOLECULAR SEQUENCE DATA; NUCLEIC ACID CONFORMATION; RNA, BACTERIAL; RNA, RIBOSOMAL, 5S; RNA, TRANSFER;

ESCHERICHIA COLI; HUMAN IMMUNODEFICIENCY VIRUS 1; TETRAHYMENA;

EID: 80052729501     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi200524n     Document Type: Article

References (51)

1. Cruz, J. A. and Westhof, E. (2009) The dynamic landscapes of RNA architecture Cell 136, 604-609
2. Gesteland, R. F., Cech, T. R., and Atkins, J. F. (2006) The RNA world: The nature of modern RNA suggests a prebiotic RNA world, Cold Spring Harbor Laboratory Press, Plainview, NY.
3. Noller, H. F. (2005) RNA structure: Reading the ribosome Science 309, 1508-1514 (Pubitemid 41266466)
4. Pedersen, J. S., Bejerano, G., Siepel, A., Rosenbloom, K., Lindblad-Toh, K., Lander, E. S., Kent, J., Miller, W., and Haussler, D. (2006) Identification and classification of conserved RNA secondary structures in the human genome PLoS Comput. Biol. 2, e33
5. Collins, K. (2006) The biogenesis and regulation of telomerase holoenzymes Nat. Rev. Mol. Cell Biol. 7, 484-494 (Pubitemid 44036454)
6. Staley, J. P. and Guthrie, C. (1998) Mechanical devices of the spliceosome: Motors, clocks, springs, and things Cell 92, 315-326 (Pubitemid 28093010)
7. Panning, B., Dausman, J., and Jaenisch, R. (1997) X chromosome inactivation is mediated by Xist RNA stabilization Cell 90, 907-916 (Pubitemid 27381629)
8. Winkler, W. C. and Breaker, R. R. (2003) Genetic control by metabolite-binding riboswitches ChemBioChem 4, 1024-1032 (Pubitemid 37267591)
9. Regulski, E. E. and Breaker, R. R. (2008) In-line probing analysis of riboswitches Methods Mol. Biol. 419, 53-67
10. Wilkinson, K. A., Gorelick, R. J., Vasa, S. M., Guex, N., Rein, A., Mathews, D. H., Giddings, M. C., and Weeks, K. M. (2008) High-throughput SHAPE analysis reveals structures in HIV-1 genomic RNA strongly conserved across distinct biological states PLoS Biol. 6, e96
11. Mitra, S., Shcherbakova, I. V., Altman, R. B., Brenowitz, M., and Laederach, A. (2008) High-throughput single-nucleotide structural mapping by capillary automated footprinting analysis Nucleic Acids Res. 36, e63
12. Das, R., Karanicolas, J., and Baker, D. (2010) Atomic accuracy in predicting and designing noncanonical RNA structure Nat. Methods 7, 291-294
13. Kladwang, W. and Das, R. (2010) A mutate-and-map strategy for inferring base pairs in structured nucleic acids: Proof of concept on a DNA/RNA helix Biochemistry 49, 7414-7416
14. Kladwang, W., Cordero, P., and Das, R. (2011) A mutate-and-map strategy accurately infers the base pairs of a 35-nucleotide model RNA RNA 17, 522-534
15. 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 (Pubitemid 29248642)
16. 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. U.S.A. 101, 7287-7292 (Pubitemid 38638025)
17. Deigan, K. E., Li, T. W., Mathews, D. H., and Weeks, K. M. (2009) Accurate SHAPE-directed RNA structure determination Proc. Natl. Acad. Sci. U.S.A. 106, 97-102
18. Levitt, M. (1969) Detailed molecular model for transfer ribonucleic acid Nature 224, 759-763
19. Sussman, J. L. and Kim, S. (1976) Three-dimensional structure of a transfer RNA in two crystal forms Science 192, 853-858
20. Brunel, C., Romby, P., Westhof, E., Ehresmann, C., and Ehresmann, B. (1991) Three-dimensional model of Escherichia coli ribosomal 5 S RNA as deduced from structure probing in solution and computer modeling J. Mol. Biol. 221, 293-308 (Pubitemid 121003573)
21. Leontis, N. B. and Westhof, E. (1998) The 5S rRNA loop E: Chemical probing and phylogenetic data versus crystal structure RNA 4, 1134-1153 (Pubitemid 28413459)
22. Mills, D. R. and Kramer, F. R. (1979) Structure-independent nucleotide sequence analysis Proc. Natl. Acad. Sci. U.S.A. 76, 2232-2235
23. Das, R., Laederach, A., Pearlman, S. M., Herschlag, D., and Altman, R. B. (2005) SAFA: Semi-automated footprinting analysis software for high-throughput quantification of nucleic acid footprinting experiments RNA 11, 344-354 (Pubitemid 40270826)
24. Yoon, S., Kim, J., Hum, J., Kim, H., Park, S., Kladwang, W., and Das, R. (2011) HiTRACE: High-Throughput Robust Analysis for Capillary Electropherograms Bioinformatics 27, 1798-1805
25. Vasa, S. M., Guex, N., Wilkinson, K. A., Weeks, K. M., and Giddings, M. C. (2008) ShapeFinder: A software system for high-throughput quantitative analysis of nucleic acid reactivity information resolved by capillary electrophoresis RNA 14, 1979-1990
26. Aviran, S., Trapnell, C., Lucks, J. B., Mortimer, S. A., Luo, S., Schroth, G. P., Doudna, J. A., Arkin, A. P., and Pachter, L. (2011) Modeling and automation of sequencing-based characterization of RNA structure Proc. Natl. Acad. Sci. U.S.A. 108, 11069-11074
27. Efron, B. and Tibshirani, R. J. (1998) An Introduction to the Bootstrap, Chapman & Hall, Boca Raton, FL.
28. Efron, B., Halloran, E., and Holmes, S. (1996) Bootstrap confidence levels for phylogenetic trees Proc. Natl. Acad. Sci. U.S.A. 93, 13429-13434 (Pubitemid 126585356)
29. Hofacker, I. L. (2004) RNA secondary structure analysis using the Vienna RNA package. Current Protocols in Bioinformatics, Chapter 12, Unit 12, p 12, Wiley, New York.
30. Darty, K., Denise, A., and Ponty, Y. (2009) VARNA: Interactive drawing and editing of the RNA secondary structure Bioinformatics 25, 1974-1975
31. Byrne, R. T., Konevega, A. L., Rodnina, M. V., and Antson, A. A. (2010) The crystal structure of unmodified tRNAPhe from Escherichia coli Nucleic Acids Res. 38, 4154-4162
32. 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 (Pubitemid 26317777)
33. Mandal, M. and Breaker, R. R. (2004) Adenine riboswitches and gene activation by disruption of a transcription terminator Nat. Struct. Mol. Biol. 11, 29-35 (Pubitemid 38173438)
34. Serganov, A., Yuan, Y. R., Pikovskaya, O., Polonskaia, A., Malinina, L., Phan, A. T., Hobartner, C., Micura, R., Breaker, R. R., and Patel, D. J. (2004) Structural basis for discriminative regulation of gene expression by adenine- and guanine-sensing mRNAs Chem. Biol. 11, 1729-1741 (Pubitemid 39651306)
35. Sudarsan, N., Lee, E. R., Weinberg, Z., Moy, R. H., Kim, J. N., Link, K. H., and Breaker, R. R. (2008) Riboswitches in eubacteria sense the second messenger cyclic di-GMP Science 321, 411-413 (Pubitemid 352029978)
36. Kulshina, N., Baird, N. J., and Ferre-D'Amare, A. R. (2009) Recognition of the bacterial second messenger cyclic diguanylate by its cognate riboswitch Nat. Struct. Mol. Biol. 16, 1212-1217
37. Smith, K. D., Lipchock, S. V., Livingston, A. L., Shanahan, C. A., and Strobel, S. A. (2010) Structural and biochemical determinants of ligand binding by the c-di-GMP riboswitch Biochemistry 49, 7351-7359
38. Mandal, M., Lee, M., Barrick, J. E., Weinberg, Z., Emilsson, G. M., Ruzzo, W. L., and Breaker, R. R. (2004) A glycine-dependent riboswitch that uses cooperative binding to control gene expression Science 306, 275-279 (Pubitemid 39336872)
39. Butler, E. B., Xiong, Y., Wang, J., and Strobel, S. A. (2011) Structural basis of cooperative ligand binding by the glycine riboswitch Chem. Biol. 18, 293-298
40. Wilkinson, K. A., Merino, E. J., and Weeks, K. M. (2006) Selective 2′-hydroxyl acylation analyzed by primer extension (SHAPE): Quantitative RNA structure analysis at single nucleotide resolution Nat. Protoc. 1, 1610-1616
41. Mortimer, S. A. and Weeks, K. M. (2007) A fast-acting reagent for accurate analysis of RNA secondary and tertiary structure by SHAPE chemistry J. Am. Chem. Soc. 129, 4144-4145 (Pubitemid 46595421)
42. Russell, R. and Herschlag, D. (1999) New pathways in folding of the Tetrahymena group I RNA enzyme J. Mol. Biol. 291, 1155-1167 (Pubitemid 29423778)
43. Russell, R., Das, R., Suh, H., Travers, K. J., Laederach, A., Engelhardt, M. A., and Herschlag, D. (2006) The paradoxical behavior of a highly structured misfolded intermediate in RNA folding J. Mol. Biol. 363, 531-544 (Pubitemid 44436255)
44. Hickey, D. R. and Turner, D. H. (1985) Solvent effects on the stability of A7U7p Biochemistry 24, 2086-2094
45. Takamoto, K., Das, R., He, Q., Doniach, S., Brenowitz, M., Herschlag, D., and Chance, M. R. (2004) Principles of RNA compaction: Insights from the equilibrium folding pathway of the P4-P6 RNA domain in monovalent cations J. Mol. Biol. 343, 1195-1206 (Pubitemid 39387820)
46. Correll, C. C., Freeborn, B., Moore, P. B., and Steitz, T. A. (1997) Metals, motifs, and recognition in the crystal structure of a 5S rRNA domain Cell 91, 705-712 (Pubitemid 27513661)
47. Lemay, J. F., Penedo, J. C., Tremblay, R., Lilley, D. M., and Lafontaine, D. A. (2006) Folding of the adenine riboswitch Chem. Biol. 13, 857-868 (Pubitemid 44247776)
48. Kwon, M. and Strobel, S. A. (2008) Chemical basis of glycine riboswitch cooperativity RNA 14, 25-34
49. Kladwang, W., VanLang, C. C., Cordero, P., and Das, R. Two-dimensional chemical mapping for non-coding RNAs: The mutate-and-map strategy. Nat. Chem. 2011, in press.
50. Felsenstein, J. (1985) Confidence limits on phylogenies: An approach using the bootstrap Evolution 39, 783-791
51. Watts, J. M., Dang, K. K., Gorelick, R. J., Leonard, C. W., Bess, J. W., Jr., Swanstrom, R., Burch, C. L., and Weeks, K. M. (2009) Architecture and secondary structure of an entire HIV-1 RNA genome Nature 460, 711-716