Probing viral genomic structure: Alternative viewpoints and alternative structures for satellite tobacco mosaic virus RNA

Biochemistry

Volumn 53, Issue 43, 2014, Pages 6728-6737

  Schroeder, Susan J ^a  

^a UNIVERSITY OF OKLAHOMA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COMPUTATIONAL METHODS; DISEASES; FORECASTING; TOBACCO; VIRUSES;

ALTERNATIVE STRUCTURE; CHEMICAL REAGENTS; COMPUTATIONAL TOOLS; FUTURE PREDICTIONS; GENOMIC STRUCTURE; PRIMARY STRUCTURES; RNA SECONDARY STRUCTURE PREDICTION; TOBACCO MOSAIC VIRUS;

RNA;

VIRUS RNA;

5' UNTRANSLATED REGION; AMINO ACID SEQUENCE; ARTICLE; COMPARATIVE STUDY; CONTROLLED STUDY; CRYSTALLOGRAPHY; GENE STRUCTURE; HUMAN IMMUNODEFICIENCY VIRUS; NONHUMAN; PHILOSOPHY; PHYSICAL CHEMISTRY; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN SECONDARY STRUCTURE; RIBOSOME; RNA STRUCTURE; SATELLITE TOBACCO MOSAIC VIRUS; THERMODYNAMICS; TOBACCO MOSAIC VIRUS; VIRUS ASSEMBLY; VIRUS MORPHOLOGY; VIRUS PARTICLE; CHEMICAL STRUCTURE; CHEMISTRY; COMPUTER SIMULATION; CONFORMATION; DEFECTIVE VIRUS; X RAY CRYSTALLOGRAPHY;

SATELLITE TOBACCO MOSAIC VIRUS;

COMPUTER SIMULATION; CRYSTALLOGRAPHY, X-RAY; MODELS, MOLECULAR; NUCLEIC ACID CONFORMATION; RNA, VIRAL; TOBACCO MOSAIC SATELLITE VIRUS;

EID: 84920819299     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi501051k     Document Type: Article

References (77)

1. Kurath, G., Rey, M. E., and Dodds, J. A. (1992) Analysis of Genetic Heterogeneity Within the Type Strain of Satellite Tobacco Mosaic Virus Reveals Variants and a Strong Bias for G to A Substitution Mutants Virology 189, 233-244
2. Kurath, G., Heick, J., and Dodds, J. A. (1993) RNAse Protection Analyses Show High Genetic Diversity among Field Isolates of Satellite Tobacco Mosaic Virus Virology 194, 414-418
3. Mirkov, T. E., Mathews, D. M., Du Plessis, D. H., and Dodds, J. A. (1989) Nucleotide Sequence and Translation of Satellite Tobacco Mosaic Virus RNA Virology 170, 139-146
4. Archer, E. J., Simpson, M. A., Watts, N. J., O'Kane, R., Wang, B., Erie, D. A., McPherson, A., and Weeks, K. M. (2013) Long-range architecture in a viral RNA genome Biochemistry 52, 3182-3190
5. Athavale, S. S., Gossett, J. J., Bowman, J. C., Hud, N. V., Williams, L. D., and Harvey, S. C. (2013) In vitro secondary structure of the genomic RNA of satellite tobacco mosaic virus PLoS One 8, e54384
6. Schroeder, S. J., Stone, J. W., Bleckley, S., Gibbons, T., and Mathews, D. M. (2011) Ensemble of Secondary Structures for Encapsidated Satellite Tobacco Mosaic Virus RNA Consistent with Chemical Probing and Crystallography Constraints Biophys. J. 101, 167-175
7. Larson, N. B., Day, J., Greenwood, A., and McPherson, A. (1998) Refined Structure of Satellite Tobacco Mosaic Virus at 1.8 Å Resolution J. Mol. Biol. 277, 37-59
8. Larson, S. B., Koszelak, S., Day, J., Greenwood, A., Dodds, J. A., and McPherson, A. (1993) Double Helical RNA in Stallite Tobacco Mosaic Virus Nature 361, 179-182
9. Larson, S. B. and McPherson, A. (2001) Satellite Tobacco Mosaic Virus RNA: Structure and Implications for Assembly Curr. Opin. Struct. Biol. 11, 59-65
10. Zeng, Y., Larson, S. B., Heitsch, C. E., McPherson, A., and Harvey, S. C. (2012) A model for the structure of satellite tobacco mosaic virus J. Struct. Biol. 180, 110-116
11. Rodrigues-Alvarado, G. and Roossinck, M. J. (1997) Structural Analysis of a Necrogenic Strain of Cucumber Mosaic Cucumovirus satellite RNA in planta Virology 236, 155-166
12. Burrill, C. P., Westesson, O., Schulte, M. B., Strings, V. R., Segal, M., and Andino, R. (2013) Global RNA structure analysis of poliovirus identifies a conserved RNA structure involved in viral replication and infectivity J. Virol. 87, 11670-11683
13. Ding, Y., Tang, Y., Kwok, C. K., Zhang, Y., Bevilacqua, P. C., and Assmann, S. M. (2014) In vivo genome-wide profiling of RNA secondary structure reveals novel regulatory features Nature 505, 696-700
14. Reuter, J. S. and Mathews, D. H. (2010) RNAstructure: Software for RNA secondary structure prediction and analysis BMC Bioinf. 11, 129
15. Lorenz, R., Bernhart, S. H., Honer Zu Siederdissen, C., Tafer, H., Flamm, C., Stadler, P. F., and Hofacker, I. L. (2011) ViennaRNA Package 2.0 Algorithms Mol. Biol. AMB 6, 26
16. Markham, N. R. and Zuker, M. (2008) UNAFold: Software for nucleic acid folding and hybridization Methods Mol. Biol. 453, 3-31
17. Greenleaf, W., Frieda, K., Foster, D., Woodside, M., and Block, S. (2008) Direct observation of hierarchical folding in single riboswitch aptamers Science 319, 630-633
18. Mahen, E. M., Harger, J. W., Calderon, E. M., and Fedor, M. J. (2005) Kinetics and thermodynamics make different contributions to RNA folding in vitro and in yeast Mol. Cell 19, 27-37
19. Mahen, E. M., Watson, P. Y., Cottrell, J. W., and Fedor, M. J. (2010) mRNA Secondary Structures Fold Sequentially but Exchange Rapdily In Vivo PLoS Biol. 8, e1000307
20. Lai, D., Proctor, J. R., and Meyer, I. M. (2013) On the importance of cotranscriptional RNA structure formation RNA 19, 1461-1473
21. Frieda, K. L. and Block, S. M. (2012) Direct observation of cotranscriptional folding in an adenine riboswitch Science 338, 397-400
22. Grohman, J. K., Gorelick, R. J., Kottegoda, S., Allbritton, N. L., Rein, A., and Weeks, K. M. (2014) An immature retroviral RNA genome resembles a kinetically trapped intermediate state J. Virol. 88, 6061-6068
23. 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
24. Do, C., Woods, D., and Batzglou, S. (2006) CONTRAfold: RNA secondary structure prediction without physics-based models Bioinformatics 22, e90-e98
25. Xia, T., Santa Lucia, 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 Base Pairs Biochemistry 37, 14719-14735
26. Jarmoskaite, I., Bhaskaran, H., Seifert, S., and Russell, R. (2014) DEAD-box protein CYT-19 is activated by exposed helices in a group I intron RNA Proc. Natl. Acad. Sci. U.S.A. 111, E2928-E2936
27. Jarmoskaite, I. and Russell, R. (2014) RNA helicase proteins as chaperones and remodelers Annu. Rev. Biochem. 83, 697-725
28. Mohr, H. and Schopfer, P. (1995) The Cell as an Open System, Dynamic Equilibrium. In Plant Physiology, p 41, Springer-Verlag, Berlin.
29. Shepotinovskaya, I. and Uhlenbeck, O. C. (2013) tRNA residues evolved to promote translational accuracy RNA 19, 510-516
30. Biebricher, C. K. and Eigen, M. (2006) What is a quasispecies? Curr. Top. Microbiol. Immunol. 299, 1-31
31. Acevedo, A., Brodsky, L., and Andino, R. (2014) Mutational and fitness landscapes of an RNA virus revealed through population sequencing Nature 505, 686-690
32. Rudinger-Thirion, J., Lescure, A., Paulus, C., and Frugier, M. (2011) Misfolded human tRNA isodecoder binds and neutralizes a 3′ UTR-embedded Alu element Proc. Natl. Acad. Sci. U.S.A. 108, E794-E802
33. Mak, J. and Kleiman, L. (1997) Primer tRNAs for reverse transcription J. Virol. 71, 8087-8095
34. Zaher, H. S. and Green, R. (2009) Fidelity at the molecular level: Lessons from protein synthesis Cell 136, 746-762
35. Shang, L., Gardner, D. P., Xu, W., Cannone, J. J., Miranker, D. P., Ozer, S., and Gutell, R. R. (2013) Two accurate sequence, structure, and phylogenetic template-based RNA alignment systems BMC Syst. Biol. 7 (Suppl. 4) S13
36. Felden, B., Florentz, C., McPherson, A., and Giege, R. (1994) A histidine accepting tRNA-like fold at the 3′end of satellite tobacco mosic virus RNA Nucleic Acids Res. 22, 2882-2886
37. Watts, J. M., Dang, K. K., Gorelick, R. J., Leonard, C. W., Bess, J. W., 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
38. Zuker, M. (1989) On finding all suboptimal foldings of an RNA molecule Science 244, 48-52
39. Zuker, M. and Stiegler, P. (1981) Optimal computer folding of large RNA sequences using thermodynamics and auxiliary information Nucleic Acids Res. 9, 133-148
40. McCaskill, J. (1990) The equilibrium partition function and base pair binding probabilities for RNA secondary structure Biopolymers 29, 1105-1119
41. Ding, Y., Chan, C., and Lawrence, C. (2004) A statistical sampling algorithm for RNA secondary structure prediction Nucleic Acids Res. 31, 7280-7301
42. Homan, P. J., Favorov, O. V., Lavender, C. A., Kursun, O., Ge, X., Busan, S., Dokholyan, N. V., and Weeks, K. M. (2014) Single-molecule correlated chemical probing of RNA Proc. Natl. Acad. Sci. U.S.A. 111, 13858-13863
43. 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
44. Pipas, J. and McMahon, J. (1975) Methods for Predicting RNA Secondary Structure Proc. Natl. Acad. Sci. U.S.A. 72, 2017-2021
45. Bleckley, S., Stone, J. W., and Schroeder, S. J. (2012) Crumple: A Method for Complete Enumeration of All Possible Pseudoknot-Free RNA Secondary Structures PLoS One 7, e52414
46. Reuter, J. S. and Mathews, D. H. (2010) RNAstructure: Software for RNA structure prediction and analysis BMC Bioinf. 11, 129
47. Schroeder, S. J. (2009) Advances in RNA structure prediction from sequence: New tools for generating hypotheses about viral RNA structure-function relationships J. Virol. 83, 6326-6334
48. Gruber, A., Lorenz, R., Bernhart, S., Neubock, R., and Hofacker, I. (2008) The Vienna RNA Websuite Nucleic Acids Res. 36, W70-W74
49. Zhao, P., Zhang, W., and Chen, S. J. (2011) Cotranscriptional folding kinetics of ribonucleic acid secondary structures J. Chem. Phys. 135, 245101
50. Geis, M., Flamm, C., Wolfinger, M. T., Tanzer, A., Hofacker, I. L., Middendorf, M., Mandl, C., Stadler, P. F., and Thurner, C. (2008) Folding Kinetics of Large RNAs J. Mol. Biol. 379, 160-173
51. Proctor, J. R. and Meyer, I. M. (2013) COFOLD: An RNA secondary structure prediction method that takes co-transcriptional folding into account Nucleic Acids Res. 41, e102
52. Andino, R., Rieckhof, G. E., and Baltimore, D. (1990) A Functional Ribonucleoprotein Complex Forms around the 5′ End of Poliovirus RNA Cell 63, 369-380
53. Tian, S., Cordero, P., Kladwang, W., and Das, R. (2014) High-throughput mutate-map-rescue evaluates SHAPE-directed RNA structure and uncovers excited states RNA 20, 1815-1826
54. Clanton-Arrowood, K. (2010) Determining the Secondary Structure of Satellite Tobacco Mosaic Virus RNA: A Mutagenesis Approach, Univerrsity of Oklahoma, Norman, OK.
55. Clanton-Arrowood, K., McGurk, J., and Schroeder, S. J. (2008) 3′ Terminal Nucleotides Determine Thermodynamic Stabilities of Mismatches at the Ends of RNA Helices Biochemistry 47, 13418-13427
56. Nguyen, M.-T. and Schroeder, S. J. (2010) Consecutive Terminal GU Pairs Stabilize RNA Helices Biochemistry 49, 10574-10581
57. Hajdin, C. E., Bellaousov, S., Huggins, W., Leonard, C. W., Mathews, D. H., and Weeks, K. M. (2013) Accurate SHAPE-directed RNA secondary structure modeling, including pseudoknots Proc. Natl. Acad. Sci. U.S.A. 110, 5498-5503
58. Dirks, R. and Pierce, N. (2004) An algorithm for computing nucleic acid base-pairing probabilities including pseudoknots J. Comput. Biol. 25, 1295-1304
59. Rivas, E. and Eddy, S. (2000) The language of RNA: A formal grammar that includes pseudoknots Bioinformatics 16, 334-340
60. Mirkov, T. E., Kurath, G., Mathews, D. M., Elliott, K., Dodds, J. A., and Fitzmaurice, L. (1990) Factors Affecting Efficient Infection of Tobacco with in vitro RNA Transcripts from Cloned cDNAs of Satellite Tobacco Mosaic Virus Virology 179, 395-402
61. Nguyenle, T., Laurberg, M., Brenowitz, M., and Noller, H. F. (2006) Following the dynamics of changes in solvent accessibility of 16 and 23 S rRNA during ribosomal subunit association using synchrotron-generated hydroxyl radicals J. Mol. Biol. 359, 1235-1248
62. McGinnis, J. L., Dunkle, J. A., Cate, J. H., and Weeks, K. M. (2012) The mechanisms of RNA SHAPE chemistry J. Am. Chem. Soc. 134, 6617-6624
63. 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
64. Kladwang, W., Mann, T. H., Becka, A., Tian, S., Kim, H., Yoon, S., and Das, R. (2014) Standardization of RNA chemical mapping experiments Biochemistry 53, 3063-3065
65. Kladwang, W., VanLang, C. C., Cordero, P., and Das, R. (2011) Understanding the errors of SHAPE-directed RNA structure modeling Biochemistry 50, 8049-8056
66. Leonard, C. W., Hajdin, C. E., Karabiber, F., Mathews, D. H., Favorov, O. V., Dokholyan, N. V., and Weeks, K. M. (2013) Principles for understanding the accuracy of SHAPE-directed RNA structure modeling Biochemistry 52, 588-595
67. 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
68. 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
69. Paillart, J.-C., Dettenhofer, M., Yu, X., Ehresmann, C., Ehresmann, B., and Marquet, R. (2004) First Snapshots of the HIV-1 RNA Structure in Infected Cells and in Virions J. Biol. Chem. 279, 48397-48403
70. Moazed, D. and Noller, H. F. (1989) Interaction of tRNA with 23S rRNA in the ribosomal A, P, and E sites Cell 57, 585-597
71. Merryman, C., Moazed, D., Daubresse, G., and Noller, H. F. (1999) Nucleotides in 23S rRNA protected by the association of 30S and 50S ribosomal subunits J. Mol. Biol. 285, 107-113
72. Jiang, T., Kennedy, S. D., Moss, W. N., Kierzek, E., and Turner, D. H. (2014) Secondary Structure of a Conserved Domain in an Intron of Influenza A M1 mRNA Biochemistry 53, 5236-5248
73. Liang, R., Kierzek, E., Kierzek, R., and Turner, D. H. (2010) Comparisons between chemical mapping and binding to isoenergetic oligonucleotide microarrays reveal unexpected patterns of binding to the Bacillus subtilis RNase P RNA specificity domain Biochemistry 49, 8155-8168
74. Gherghe, C. M., Shajani, Z., Wilkinson, K. A., Varani, G., and Weeks, K. M. (2008) Strong correlation between SHAPE chemistry and the generalized NMR order parameter (S2) in RNA J. Am. Chem. Soc. 130, 12244-12245
75. Kwok, C. K., Ding, Y., Tang, Y., Assmann, S. M., and Bevilacqua, P. C. (2013) Determination of in vivo RNA structure in low-abundance transcripts Nat. Commun. 4, 2971
76. 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
77. Shepherd, C. M., Borelli, I. A., Lander, G., Natarajan, P., Siddavanahalli, V., Bajaj, C., Johnson, J. E., Brooks, C. L., and Reddy, V. S. (2006) VIPERdb: A Relational Database for Structural Virology Nucleic Acids Res. 34, D386-D389