Selective 2'-hydroxyl acylation analyzed by primer extension and mutational profiling (SHAPE-MaP) for direct, versatile and accurate RNA structure analysis

Nature Protocols

Volumn 10, Issue 11, 2015, Pages 1643-1669

  Smola, Matthew J ^a   Rice, Greggory M ^a   Busan, Steven ^a   Siegfried, Nathan A ^a   Weeks, Kevin M ^a  

^a University of North Carolina at Chapel Hill   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

RNA DIRECTED DNA POLYMERASE; RNA;

ALGORITHM; ARTICLE; DATA PROCESSING; MASSIVELY PARALLEL SEQUENCING; MUTATIONAL PROFILING; PRIORITY JOURNAL; RNA SECONDARY STRUCTURE; RNA STRUCTURE; SELECTIVE 2' HYDROXYL ACYLATION ANALYZED BY PRIMER EXTENSION; SEQUENCE ANALYSIS; STRUCTURE ANALYSIS; TRANSCRIPTOMICS; ACYLATION; BIOLOGY; CHEMISTRY; CONFORMATION; MOLECULAR BIOLOGY; MOLECULAR MODEL; MUTATION; PROCEDURES; RNA PROCESSING;

ACYLATION; COMPUTATIONAL BIOLOGY; MODELS, MOLECULAR; MOLECULAR BIOLOGY; MUTATION; NUCLEIC ACID CONFORMATION; RNA; RNA PROCESSING, POST-TRANSCRIPTIONAL;

EID: 84944398591     PISSN: 17542189     EISSN: 17502799     Source Type: Journal    
DOI: 10.1038/nprot.2015.103     Document Type: Article

References (60)

1. Sharp, P.A. The centrality of RNA. Cell 136, 577-580 (2009).
2. Dethoff, E.A., Chugh, J., Mustoe, A.M. & Al-Hashimi, H.M. Functional complexity and regulation through RNA dynamics. Nature 482, 322-330 (2012).
3. Mauger, D.M., Siegfried, N.A. & Weeks, K.M. The genetic code as expressed through relationships between mRNA structure and protein function. FEBS Lett. 587, 1180-1188 (2013).
4. Weeks, K.M. Advances in RNA structure analysis by chemical probing. Curr. Opin. Struct. Biol. 20, 295-304 (2010).
5. 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).
6. 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).
7. 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).
8. Gherghe, C.M., Shajani, Z., Wilkinson, K.A., Varani, G. & Weeks, K.M. Strong correlation between SHAPE chemistry and the generalized NMR order parameter (S2) in RNA. J. Am. Chem. Soc. 130, 12244-12245 (2008).
9. Wilkinson, K.A. et al. Influence of nucleotide identity on ribose 2'-hydroxyl reactivity in RNA. RNA 15, 1314-1321 (2009).
10. McGinnis, J.L., Dunkle, J.A., Cate, J.H.D. & Weeks, K.M. The mechanisms of RNA SHAPE chemistry. J. Am. Chem. Soc. 134, 6617-6624 (2012).
11. Wilkinson, K.A. et al. High-throughput SHAPE analysis reveals structures in HIV-1 genomic RNA strongly conserved across distinct biological states. PLoS Biol. 6, e96 (2008).
12. Gherghe, C. et al. Definition of a high-affinity Gag recognition structure mediating packaging of a retroviral RNA genome. Proc. Natl. Acad. Sci. 107, 19248-19253 (2010).
13. Archer, E.J. et al. Long-range architecture in a viral RNA genome. Biochemistry 52, 3182-3190 (2013).
14. Spitale, R.C. et al. RNA SHAPE analysis in living cells. Nat. Chem. Biol. 9, 18-20 (2013).
15. Tyrrell, J., McGinnis, J.L., Weeks, K.M. & Pielak, G.J. The cellular environment stabilizes adenine riboswitch RNA structure. Biochemistry 52, 8777-8785 (2013).
16. McGinnis, J.L. & Weeks, K.M. Ribosome RNA assembly intermediates visualized in living cells. Biochemistry 53, 3237-3247 (2014).
17. McGinnis, J.L. et al. In-cell SHAPE reveals that free 30S ribosome subunits are in the inactive state. Proc. Natl. Acad. Sci. 112, 2425-2430 (2015).
18. Mortimer, S.A. & Weeks, K.M. A fast-acting reagent for accurate analysis of RNA secondary and tertiary structure by SHAPE chemistry. J. Am. Chem. Soc. 129, 4144-4145 (2007).
19. Deigan, K.E., Li, T.W., Mathews, D.H. & Weeks, K.M. Accurate SHAPE-directed RNA structure determination. Proc. Natl. Acad. Sci. 106, 97-102 (2009).
20. Hajdin, C.E. et al. Accurate SHAPE-directed RNA secondary structure modeling, including pseudoknots. Proc. Natl. Acad. Sci. 110, 5498-5503 (2013).
21. Rice, G.M., Leonard, C.W. & Weeks, K.M. RNA secondary structure modeling at consistent high accuracy using differential SHAPE. RNA 20, 846-854 (2014).
22. Underwood, J.G. et al. FragSeq: transcriptome-wide RNA structure probing using high-throughput sequencing. Nat. Methods 7, 995-1001 (2010).
23. Kertesz, M. et al. Genome-wide measurement of RNA secondary structure in yeast. Nature 467, 103-107 (2010).
24. 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. 108, 11063-11068 (2011).
25. Incarnato, D., Neri, F., Anselmi, F. & Oliviero, S. Genome-wide profiling of mouse RNA secondary structures reveals key features of the mammalian transcriptome. Genome Biol. 15, 491 (2014).
26. 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).
27. Ding, Y. et al. In vivo genome-wide profiling of RNA secondary structure reveals novel regulatory features. Nature 505, 696-700 (2014).
28. Siegfried, N.A., Busan, S., Rice, G.M., Nelson, J.A.E. & Weeks, K.M. RNA motif discovery by SHAPE and mutational profiling (SHAPE-MaP). Nat. Methods 11, 959-965 (2014).
29. Vogel, J., Hess, W.R. & Börner, T. Precise branch point mapping and quantification of splicing intermediates. Nucleic Acids Res. 25, 2030-2031 (1997).
30. Ule, J., Jensen, K., Mele, A. & Darnell, R.B. CLIP: a method for identifying protein-RNA interaction sites in living cells. Methods 37, 376-386 (2005).
31. Mauger, D.M. et al. Functionally conserved architecture of hepatitis C virus RNA genomes. Proc. Natl. Acad. Sci. 112, 3692-3697 (2015).
32. Lavender, C.A., Gorelick, R.J. & Weeks, K.M. Structure-based alignment and consensus secondary structures for three HIV-related RNA genomes. PLoS Comput. Biol. 11, e1004230 (2015).
33. Reuter, J.S. & Mathews, D.H. RNAstructure: software for RNA secondary structure prediction and analysis. BMC Bioinformatics 11, 129 (2010).
34. McCaskill, J.S. The equilibrium partition function and base pair binding probabilities for RNA secondary structure. Biopolymers 29, 1105-1119 (1990).
35. Mathews, D.H. Using an RNA secondary structure partition function to determine confidence in base pairs predicted by free energy minimization. RNA 10, 1178-1190 (2004).
36. Shannon, E. A mathematical theory of communication. Bell Syst. Tech. J. 27, 379-423 (1948).
37. Talkish, J., May, G., Lin, Y., Woolford, J.L. & McManus, C.J. Mod-seq: high-throughput sequencing for chemical probing of RNA structure. RNA 20, 713-720 (2014).
38. Staple, D.W. et al. Fast gapped-read alignment with Bowtie 2. Nat. Methods 9, 357-359 (2012).
39. Taylor, A.I. et al. Catalysts from synthetic genetic polymers. Nature 518, 427-430 (2015).
40. Wang, B., Wilkinson, K.A. & Weeks, K.M. Complex ligand-induced conformational changes in tRNA(Asp) revealed by single-nucleotide resolution SHAPE chemistry. Biochemistry 47, 3454-3461 (2008).
41. Warner, K.D. et al. Structural basis for activity of highly efficient RNA mimics of green fluorescent protein. Nat. Struct. Mol. Biol. 21, 658-663 (2014).
42. Mortimer, S.A. & Weeks, K.M. C2'-endo nucleotides as molecular timers suggested by the folding of an RNA domain. Proc. Natl. Acad. Sci. 106, 15622-15627 (2009).
43. Duncan, C.D.S. & Weeks, K.M. Nonhierarchical ribonucleoprotein assembly suggests a strain-propagation model for protein-facilitated RNA folding. Biochemistry 49, 5418-5425 (2010).
44. Grohman, J.K. et al. A guanosine-centric mechanism for RNA chaperone function. Science 340, 190-195 (2013).
45. Raabe, C.A., Tang, T.-H., Brosius, J. & Rozhdestvensky, T.S. Biases in small RNA deep sequencing data. Nucleic Acids Res. 42, 1414-1426 (2014).
46. Weeks, K.M. Review toward all RNA structures, concisely. Biopolymers 103, 438-448 (2015).
47. Loughrey, D., Watters, K.E., Settle, A.H. & Lucks, J.B. SHAPE-Seq 2.0: systematic optimization and extension of high-throughput chemical probing of RNA secondary structure with next generation sequencing. Nucleic Acids Res. 42, e165 (2014).
48. Homan, P.J. et al. Single-molecule correlated chemical probing of RNA. Proc. Natl. Acad. Sci. 111, 13858-13863 (2014).
49. Nicholson, B.L. & White, K.A. Functional long-range RNA-RNA interactions in positive-strand RNA viruses. Nat. Rev. Microbiol. 12, 493-504 (2014).
50. Duncan, C.D.S. & Weeks, K.M. SHAPE analysis of long-range interactions reveals extensive and thermodynamically preferred misfolding in a fragile group I intron RNA. Biochemistry 47, 8504-8513 (2008).
51. 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).
52. Watts, J.M. et al. Architecture and secondary structure of an entire HIV-1 RNA genome. Nature 460, 711-716 (2009).
53. Steen, K.-A., Rice, G.M. & Weeks, K.M. Fingerprinting noncanonical and tertiary RNA structures by differential SHAPE reactivity. J. Am. Chem. Soc. 134, 13160-13163 (2012).
54. Mortimer, S.A. & Weeks, K.M. Time-resolved RNA SHAPE chemistry. J. Am. Chem. Soc. 130, 16178-16180 (2008).
55. Bai, Y., Tambe, A., Zhou, K. & Doudna, J.A. RNA-guided assembly of Rev-RRE nuclear export complexes. Elife 3, e03656 (2014).
56. Steen, K.-A., Siegfried, N.A. & Weeks, K.M. Synthesis of 1-methyl-7-nitroisatoic anhydride (1M7). Protoc. Exch. doi:10.1038/protex.2011.255 (2011).
57. Turner, R., Shefer, K. & Ares, M. Safer one-pot synthesis of the 'SHAPE' reagent 1-methyl-7-nitroisatoic anhydride (1m7). RNA 19, 1857-1863 (2013).
58. Ye, J. et al. Primer-BLAST: a tool to design target-specific primers for polymerase chain reaction. BMC Bioinformatics 13, 134 (2012).
59. Byun, Y. & Han, K. PseudoViewer: web application and web service for visualizing RNA pseudoknots and secondary structures. Nucleic Acids Res. 34, W416-W422 (2006).
60. Serganov, A., Polonskaia, A., Phan, A.T., Breaker, R.R. & Patel, D.J. Structural basis for gene regulation by a thiamine pyrophosphate-sensing riboswitch. Nature 441, 1167-1171 (2006).