Progress and challenges for chemical probing of RNA structure inside living cells

Nature Chemical Biology

Volumn 11, Issue 12, 2015, Pages 933-941

  Kubota, Miles ^a   Tran, Catherine ^a   Spitale, Robert C ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

RNA; MOLECULAR PROBE;

BIOLOGY; CHEMICAL PROBING; CHEMICAL REACTION; HUMAN; IN VITRO STUDY; IN VIVO STUDY; NONHUMAN; PRIORITY JOURNAL; REVIEW; RNA PROBE; RNA SEQUENCE; RNA STRUCTURE; CHEMICAL STRUCTURE; CHEMISTRY; CONFORMATION; MOLECULAR PROBE;

HUMANS; MODELS, MOLECULAR; MOLECULAR PROBES; NUCLEIC ACID CONFORMATION; RNA;

EID: 84947445864     PISSN: 15524450     EISSN: 15524469     Source Type: Journal    
DOI: 10.1038/nchembio.1958     Document Type: Review

References (93)

1. Xie, X. et al. Systematic discovery of regulatory motifs in human promoters and 3 UTRs by comparison of several mammals. Nature 434, 338-345 (2005).
2. Badis, G. et al. Diversity and complexity in DNA recognition by transcription factors. Science 324, 1720-1723 (2009).
3. Kruger, K. et al. Self-splicing RNA: autoexcision and autocyclization of the ribosomal RNA intervening sequence of Tetrahymena. Cell 31, 147-157 (1982).
4. Guerrier-Takada, C., Gardiner, K., Marsh, T., Pace, N. , Altman, S. The RNA moiety of ribonuclease P is the catalytic subunit of the enzyme. Cell 35, 849-857 (1983).
5. Noller, H.F., Hoffarth, V. , Zimniak, L. Unusual resistance of peptidyl transferase to protein extraction procedures. Science 256, 1416-1419 (1992).
6. Nissen, P., Hansen, J., Ban, N., Moore, P.B. , Steitz, T.A. The structural basis of ribosome activity in peptide bond synthesis. Science 289, 920-930 (2000).
7. Serganov, A. , Nudler, E. A decade of riboswitches. Cell 152, 17-24 (2013).
8. Rinn, J.L. et al. Functional demarcation of active and silent chromatin domains in human HOX loci by noncoding RNAs. Cell 129, 1311-1323 (2007).
9. McHugh, C.A. et al. The Xist lncRNA interacts directly with SHARP to silence transcription through HDAC3. Nature 521, 232-236 (2015).
10. Lunde, B.M., Moore, C. , Varani, G. RNA-binding proteins: modular design for efficient function. Nat. Rev. Mol. Cell Biol. 8, 479-490 (2007).
11. Stefl, R., Skrisovska, L. , Allain, F.H. RNA sequence-and shape-dependent recognition by proteins in the ribonucleoprotein particle. EMBO Rep. 6, 33-38 (2005).
12. Kedde, M. et al. A Pumilio-induced RNA structure switch in p27-3 UTR controls miR-221 and miR-222 accessibility. Nat. Cell Biol. 12, 1014-1020 (2010).
13. Chartrand, P., Meng, X.H., Singer, R.H. , Long, R.M. Structural elements required for the localization of ASH1 mRNA and of a green fluorescent protein reporter particle in vivo. Curr. Biol. 9, 333-336 (1999).
14. Goodarzi, H. et al. Metastasis-suppressor transcript destabilization through TARBP2 binding of mRNA hairpins. Nature 513, 256-260 (2014).
15. Sobczak, K., de Mezer, M., Michlewski, G., Krol, J. , Krzyzosiak, W.J. RNA structure of trinucleotide repeats associated with human neurological diseases. Nucleic Acids Res. 31, 5469-5482 (2003).
16. Duan, R., Sharma, S., Xia, Q., Garber, K. , Jin, P. Towards understanding RNA-mediated neurological disorders. J. Genet. Genomics 41, 473-484 (2014).
17. Houck-Loomis, B. et al. An equilibrium-dependent retroviral mRNA switch regulates translational recoding. Nature 480, 561-564 (2011).
18. Kang, M., Eichhorn, C.D. , Feigon, J. Structural determinants for ligand capture by a class II preQ1 riboswitch. Proc. Natl. Acad. Sci. USA 111, E663-E671 (2014).
19. Jiang, J. et al. The architecture of Tetrahymena telomerase holoenzyme. Nature 496, 187-192 (2013).
20. Weeks, K.M. Advances in RNA structure analysis by chemical probing. Curr. Opin. Struct. Biol. 20, 295-304 (2010).
21. Ziehler, W.A. , Engelke, D.R. Probing RNA structure with chemical reagents and enzymes. Curr. Protoc. Nucleic Acid Chem. Ch. 6, 6.1.1-6.1.21 (2001).
22. Low, J.T. , Weeks, K.M. SHAPE-directed RNA secondary structure prediction. Methods 52, 150-158 (2010).
23. Mathews, D.H. et al. Incorporating chemical modification constraints into a dynamic programming algorithm for prediction of RNA secondary structure. Proc. Natl. Acad. Sci. USA 101, 7287-7292 (2004).
24. Lempereur, L. et al. Conformation of yeast 18S rRNA. Direct chemical probing of the 5 domain in ribosomal subunits and in deproteinized RNA by reverse transcriptase mapping of dimethyl sulfate-accessible. Nucleic Acids Res. 13, 8339-8357 (1985).
25. Mortimer, S.A., Johnson, J.S. , Weeks, K.M. Quantitative analysis of RNA solvent accessibility by N-silylation of guanosine. Biochemistry 48, 2109-2114 (2009).
26. Burgstaller, P., Kochoyan, M. , Famulok, M. Structural probing and damage selection of citrulline-and arginine-specific RNA aptamers identify base positions required for binding. Nucleic Acids Res. 23, 4769-4776 (1995).
27. Wilkinson, K.A., Merino, E.J. , Weeks, K.M. RNA SHAPE chemistry reveals nonhierarchical interactions dominate equilibrium structural transitions in tRNAAsp transcripts. J. Am. Chem. Soc. 127, 4659-4667 (2005).
28. Merino, E.J., Wilkinson, K.A., Coughlan, J.L. , Weeks, K.M. RNA structure analysis at single nucleotide resolution by selective 2-hydroxyl acylation and primer extension (SHAPE). J. Am. Chem. Soc. 127, 4223-4231 (2005).
29. Watts, J.M. et al. Architecture and secondary structure of an entire HIV-1 RNA genome. Nature 460, 711-716 (2009).
30. McGinnis, J.L., Duncan, C.D. , Weeks, K.M. High-throughput SHAPE and hydroxyl radical analysis of RNA structure and ribonucleoprotein assembly. Methods Enzymol. 468, 67-89 (2009).
31. Wan, Y., Qu, K., Ouyang, Z. , Chang, H.Y. Genome-wide mapping of RNA structure using nuclease digestion and high-throughput sequencing. Nat. Protoc. 8, 849-869 (2013).
32. Peng, Y., Soper, T.J. Ouyang, Z. , Woodson, S.A. RNase footprinting of protein binding sites on an mRNA target of small RNAs. Methods Mol. Biol. 905, 213-224 (2012).
33. Ingle, S., Azad, R.N., Jain, S.S. , Tullius, T.D. Chemical probing of RNA with the hydroxyl radical at single-atom resolution. Nucleic Acids Res. 42, 12758-12767 (2014).
34. Costa, M. , Monachello, D. Probing RNA folding by hydroxyl radical footprinting. Methods Mol. Biol. 1086, 119-142 (2014).
35. Ding, F., Lavender, C.A., Weeks, K.M. , Dokholyan, N.V. Three-dimensional RNA structure refinement by hydroxyl radical probing. Nat. Methods 9, 603-608 (2012).
36. Regulski, E.E. , Breaker, R.R. In-line probing analysis of riboswitches. Methods Mol. Biol. 419, 53-67 (2008).
37. Heilman-Miller, S.L. , Woodson, S.A. Effect of transcription on folding of the Tetrahymena ribozyme. RNA 9, 722-733 (2003).
38. Perdrizet, G.A. II, Artsimovitch, I., Furman, R., Sosnick, T.R. , Pan, T. Transcriptional pausing coordinates folding of the aptamer domain and the expression platform of a riboswitch. Proc. Natl. Acad. Sci. USA 109, 3323-3328 (2012).
39. Mahen, E.M., Watson, P.Y., Cottrell, J.W. , Fedor, M.J. mRNA secondary structures fold sequentially but exchange rapidly in vivo. PLoS Biol. 8, e1000307 (2010).
40. Pan, T., Artsimovitch, I., Fang, X.W., Landick, R. , Sosnick, T.R. Folding of a large ribozyme during transcription and the effect of the elongation factor NusA. Proc. Natl. Acad. Sci. USA 96, 9545-9550 (1999).
41. Tyrrell, J., McGinnis, J.L., Weeks, K.M. , Pielak, G.J. The cellular environment stabilizes adenine riboswitch RNA structure. Biochemistry 52, 8777-8785 (2013).
42. Frieda, K.L. , Block, S.M. Direct observation of cotranscriptional folding in an adenine riboswitch. Science 338, 397-400 (2012).
43. Tijerina, P., Mohr, S. , Russell, R. DMS footprinting of structured RNAs and RNA-protein complexes. Nat. Protoc. 2, 2608-2623 (2007).
44. Waldsich, C., Masquida, B., Westhof, E. , Schroeder, R. Monitoring intermediate folding states of the td group I intron in vivo. EMBO J. 21, 5281-5291 (2002).
45. Waldsich, C., Grossberger, R. , Schroeder, R. RNA chaperone StpA loosens interactions of the tertiary structure in the td group I intron in vivo. Genes Dev. 16, 2300-2312 (2002).
46. Swiatkowska, A. et al. Kinetic analysis of pre-ribosome structure in vivo. RNA 18, 2187-2200 (2012).
47. McGinnis, J.L. , Weeks, K.M. Ribosome RNA assembly intermediates visualized in living cells. Biochemistry 53, 3237-3247 (2014).
48. McGinnis, J.L. et al. In-cell SHAPE reveals that free 30S ribosome subunits are in the inactive state. Proc. Natl. Acad. Sci. USA 112, 2425-2430 (2015).
49. Spitale, R.C. et al. RNA SHAPE analysis in living cells. Nat. Chem. Biol. 9, 18-20 (2013).
50. Kwok, C.K., Ding, Y., Tang, Y., Assmann, S.M. , Bevilacqua, P.C. Determination of in vivo RNA structure in low-abundance transcripts. Nat. Commun. 4, 2971 (2013).
51. Hector, R.D. et al. Snapshots of pre-rRNA structural flexibility reveal eukaryotic 40S assembly dynamics at nucleotide resolution. Nucleic Acids Res. 42, 12138-12154 (2014).
52. Latham, J.A. , Cech, T.R. Defining the inside and outside of a catalytic RNA molecule. Science 245, 276-282 (1989).
53. Sclavi, B., Woodson, S., Sullivan, M., Chance, M.R. , Brenowitz, M. Time-resolved synchrotron X-ray "footprinting", a new approach to the study of nucleic acid structure and function: application to protein-DNA interactions and RNA folding. J. Mol. Biol. 266, 144-159 (1997).
54. Sclavi, B., Sullivan, M., Chance, M.R., Brenowitz, M. , Woodson, S.A. RNA folding at millisecond intervals by synchrotron hydroxyl radical footprinting. Science 279, 1940-1943 (1998).
55. Adilakshmi, T., Soper, S.F. , Woodson, S.A. Structural analysis of RNA in living cells by in vivo synchrotron X-ray footprinting. Methods Enzymol. 468, 239-258 (2009).
56. Kim, H. et al. Protein-guided RNA dynamics during early ribosome assembly. Nature 506, 334-338 (2014).
57. Clatterbuck Soper, S.F., Dator, R.P., Limbach, P.A. , Woodson, S.A. In vivo X-ray footprinting of pre-30S ribosomes reveals chaperone-dependent remodeling of late assembly intermediates. Mol. Cell 52, 506-516 (2013).
58. Blower, M.D. Molecular insights into intracellular RNA localization. Int. Rev. Cell. Mol. Biol. 302, 1-39 (2013).
59. Hogan, D.J., Riordan, D.P., Gerber, A.P., Herschlag, D. , Brown, P.O. Diverse RNA-binding proteins interact with functionally related sets of RNAs, suggesting an extensive regulatory system. PLoS Biol. 6, e255 (2008).
60. Mortimer, S.A., Kidwell, M.A. , Doudna, J.A. Insights into RNA structure and function from genome-wide studies. Nat. Rev. Genet. 15, 469-479 (2014).
61. Kwok, C.K., Tang, Y., Assmann, S.M. , Bevilacqua, P.C. The RNA structurome: transcriptome-wide structure probing with next-generation sequencing. Trends Biochem. Sci. 40, 221-232 (2015).
62. Lucks, J.B. et al. Multiplexed RNA structure characterization with selective 2-hydroxyl acylation analyzed by primer extension sequencing (SHAPE-Seq). Proc. Natl. Acad. Sci. USA 108, 11063-11068 (2011).
63. Ding, Y. et al. In vivo genome-wide profiling of RNA secondary structure reveals novel regulatory features. Nature 505, 696-700 (2014).
64. Rouskin, S., Zubradt, M., Washietl, S., Kellis, M. , Weissman, J.S. Genome-wide probing of RNA structure reveals active unfolding of mRNA structures in vivo. Nature 505, 701-705 (2014).
65. Spitale, R.C. et al. Structural imprints in vivo decode RNA regulatory mechanisms. Nature 519, 486-490 (2015).
66. Schwartz, S. et al. High-resolution mapping reveals a conserved, widespread, dynamic mRNA methylation program in yeast meiosis. Cell 155, 1409-1421 (2013).
67. Liu, N. et al. N(6)-methyladenosine-dependent RNA structural switches regulate RNA-protein interactions. Nature 518, 560-564 (2015).
68. Zarrinkar, P.P., Wang, J. , Williamson, J.R. Slow folding kinetics of RNase P RNA. RNA 2, 564-573 (1996).
69. Zemora, G. , Waldsich, C. RNA folding in living cells. RNA Biol. 7, 634-641 (2010).
70. Wong, T.N. , Pan, T. RNA folding during transcription: protocols and studies. Methods Enzymol. 468, 167-193 (2009).
71. Pan, T. , Sosnick, T. RNA folding during transcription. Annu. Rev. Biophys. Biomol. Struct. 35, 161-175 (2006).
72. Mahen, E.M., Harger, J.W., Calderon, E.M. , Fedor, M.J. Kinetics and thermodynamics make different contributions to RNA folding in vitro and in yeast. Mol. Cell 19, 27-37 (2005).
73. Danko, C.G. et al. Identification of active transcriptional regulatory elements from GRO-seq data. Nat. Methods 12, 433-438 (2015).
74. Beach, D.L. , Bloom, K. ASH1 mRNA localization in three acts. Mol. Biol. Cell 12, 2567-2577 (2001).
75. Lécuyer, E. et al. Global analysis of mRNA localization reveals a prominent role in organizing cellular architecture and function. Cell 131, 174-187 (2007).
76. Riley, K.J., Yario, T.A. , Steitz, J.A. Association of Argonaute proteins and microRNAs can occur after cell lysis. RNA 18, 1581-1585 (2012).
77. Mili, S. , Steitz, J.A. Evidence for reassociation of RNA-binding proteins after cell lysis: implications for the interpretation of immunoprecipitation analyses. RNA 10, 1692-1694 (2004).
78. Mayerle, M. , Woodson, S.A. Specific contacts between protein S4 and ribosomal RNA are required at multiple stages of ribosome assembly. RNA 19, 574-585 (2013).
79. Panja, S., Schu, D.J. , Woodson, S.A. Conserved arginines on the rim of Hfq catalyze base pair formation and exchange. Nucleic Acids Res. 41, 7536-7546 (2013).
80. Lucas, C.H., Calvez, M., Babu, R. , Brown, A. Altered subcellular localization of the NeuN/Rbfox3 RNA splicing factor in HIV-associated neurocognitive disorders (HAND). Neurosci. Lett. 558, 97-102 (2014).
81. Kudla, G., Granneman, S., Hahn, D., Beggs, J.D. , Tollervey, D. Cross-linking, ligation, and sequencing of hybrids reveals RNA-RNA interactions in yeast. Proc. Natl. Acad. Sci. USA 108, 10010-10015 (2011).
82. Belton, J.M. et al. Hi-C: a comprehensive technique to capture the conformation of genomes. Methods 58, 268-276 (2012).
83. Yaffe, E. , Tanay, A. Probabilistic modeling of Hi-C contact maps eliminates systematic biases to characterize global chromosomal architecture. Nat. Genet. 43, 1059-1065 (2011).
84. Sugimoto, Y. et al. hiCLIP reveals the in vivo atlas of mRNA secondary structures recognized by Staufen 1. Nature 519, 491-494 (2015).
85. Mathews, D.H. RNA secondary structure analysis using RNAstructure. Curr. Protoc. Bioinformatics 46, 12.6.1-12.6.25 (2014).
86. Markham, N.R. , Zuker, M. UNAFold: software for nucleic acid folding and hybridization. Methods Mol. Biol. 453, 3-31 (2008).
87. Gruber, A.R., Lorenz, R., Bernhart, S.H., Neubock, R. , Hofacker, I.L. The Vienna RNA websuite. Nucleic Acids Res. 36, W70-W74 (2008).
88. Deigan, K.E., Li, T.W., Mathews, D.H. , Weeks, K.M. Accurate SHAPE-directed RNA structure determination. Proc. Natl. Acad. Sci. USA 106, 97-102 (2009).
89. Washietl, S. et al. Computational analysis of noncoding RNAs. Wiley Interdiscip Rev. RNA 3, 759-778 (2012).
90. Andronescu, M., Condon, A., Hoos, H.H., Mathews, D.H. , Murphy, K.P. Computational approaches for RNA energy parameter estimation. RNA 16, 2304-2318 (2010).
91. Ouyang, Z., Snyder, M.P. , Chang, H.Y. SeqFold: genome-scale reconstruction of RNA secondary structure integrating high-throughput sequencing data. Genome Res. 23, 377-387 (2013).
92. Tang, Y. et al. StructureFold: genome-wide RNA secondary structure mapping and reconstruction in vivo. Bioinformatics 31, 2668-2675 (2015).
93. Corley, M., Solem, A., Qu, K., Chang, H.Y. , Laederach, A. Detecting riboSNitches with RNA folding algorithms: a genome-wide benchmark. Nucleic Acids Res. 43, 1859-1868 (2015).