Specificity and nonspecificity in RNA-protein interactions

Nature Reviews Molecular Cell Biology

Volumn 16, Issue 9, 2015, Pages 533-544

  Jankowsky, Eckhard ^a,b   Harris, Michael E ^b  

^a CASE WESTERN RESERVE UNIVERSITY   (United States)

^b CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALTERNATIVE RNA SPLICING; ASSOCIATION RATE CONSTANT; BINDING AFFINITY; BINDING SITE; CONSENSUS SEQUENCE; DISSOCIATION CONSTANT; DISSOCIATION RATE CONSTANT; ENZYME SPECIFICITY; HIDDEN MARKOV MODEL; HIGH THROUGHPUT SEQUENCING; HUMAN; HYDROLYSIS; MICHAELIS CONSTANT; NEXT GENERATION SEQUENCING; NONHUMAN; POSITION WEIGHT MATRIX; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DOMAIN; PROTEIN LOCALIZATION; PROTEIN RNA BINDING; REVIEW; RNA STRUCTURE; ANIMAL; CHEMICAL STRUCTURE; CHEMISTRY; CONFORMATION; KINETICS; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; PROTEIN CONFORMATION; THERMODYNAMICS;

PROTEIN BINDING; RNA; RNA BINDING PROTEIN;

ANIMALS; BASE SEQUENCE; HUMANS; KINETICS; MODELS, MOLECULAR; NUCLEIC ACID CONFORMATION; PROTEIN BINDING; PROTEIN CONFORMATION; RNA; RNA-BINDING PROTEINS; THERMODYNAMICS;

EID: 84940435596     PISSN: 14710072     EISSN: 14710080     Source Type: Journal    
DOI: 10.1038/nrm4032     Document Type: Review

References (134)

1. Gerstberger, S., Hafner, M. & Tuschl, T. A census of human RNA-binding proteins. Nat. Rev. Genet. 15, 829-845 (2014).
2. Moore, M. J. From birth to death: the complex lives of eukaryotic mRNAs. Science 309, 1514-1518 (2005).
3. Mitchell, S. F. & Parker, R. Principles and properties of eukaryotic mRNPs. Mol. Cell 54, 547-558 (2014).
4. Licatalosi, D. D. & Darnell, R. B. RNA processing and its regulation: global insights into biological networks. Nat. Rev. Genet. 1 1, 75-87 (2010).
5. Gerstberger, S., Hafner, M., Ascano, M. & Tuschl, T. in Systems Biology of RNA Binding Proteins (ed. Yeo, G. W.) 1-55 (Springer, 2014).
6. Castello, A., Fischer, B., Hentze, M. W. & Preiss, T. RNA-binding proteins in Mendelian disease. Trends Genet. 29, 318-327 (2013).
7. Scheper, G. C., van der Knaap, M. S. & Proud, C. G. Translation matters: protein synthesis defects in inherited disease. Nat. Rev. Genet. 8, 711-723 (2007).
8. McGettigan, P. A. Transcriptomics in the RNA-seq era. Curr. Opin. Chem. Biol. 17, 4-11 (2013).
9. Parker, R. & Song, H. The enzymes and control of eukaryotic mRNA turnover. Nat. Struct. Mol. Biol. 11, 121-127 (2004).
10. Aitken, C. E. & Lorsch, J. R. A mechanistic overview of translation initiation in eukaryotes. Nat. Struct. Mol. Biol. 19, 568-576 (2012).
11. Janga, S. C. & Mittal, N. Construction, structure and dynamics of post-transcriptional regulatory network directed by RNA-binding proteins. Adv. Exp. Med. Biol. 722, 103-107 (2011).
12. Gerstberger, S., Hafner, M. & Tuschl, T. Learning the language of post-transcriptional gene regulation. Genome Biol. 14, 130 (2013).
13. Campbell, Z. T., Valley, C. T. & Wickens, M. A protein-RNA specificity code enables targeted activation of an endogenous human transcript. Nat. Struct. Mol. Biol. 21, 732-738 (2014).
14. Wang, Y., Wang, Z. & Tanaka Hall, T. M. Engineered proteins with Pumilio/fem-3 mRNA binding factor scaffold to manipulate RNA metabolism. FEBS J. 280, 3755-3767 (2013).
15. Chen, Y. & Varani, G. Engineering RNA-binding proteins for biology. FEBS J. 280, 3734-3754 (2013).
16. Choudhury, R., Tsai, Y. S., Dominguez, D., Wang, Y. & Wang, Z. Engineering RNA endonucleases with customized sequence specificities. Nat. Commun. 3, 1147 (2012).
17. Anantharaman, V., Koonin, E. V. & Aravind, L. Comparative genomics and evolution of proteins involved in RNA metabolism. Nucleic Acids Res. 30, 1427-1464 (2002).
18. Baltz, A. G. et al. The mRNA-bound proteome and its global occupancy profile on protein-coding transcripts. Mol. Cell 46, 674-690 (2012).
19. Castello, A. et al. Insights into RNA biology from an atlas of mammalian mRNA-binding proteins. Cell 149, 1393-1406 (2012).
20. Thomson, T. & Lin, H. The biogenesis and function of PIWI proteins and piRNAs: progress and prospect. Annu. Rev. Cell Dev. Biol. 25, 355-376 (2009).
21. Brook, M., Smith, J. W. & Gray, N. K. The DAZL & PABP families: RNA-binding proteins with interrelated roles in translational control in oocytes. Reproduction 137, 595-617 (2009).
22. Singh, R. & Valcárcel, J. Building specificity with nonspecific RNA-binding proteins. Nat. Struct. Mol. Biol. 12, 645-653 (2005).
23. Lunde, B. M., Moore, C. & Varani, G. RNA-binding proteins: modular design for efficient function. Nat. Rev. Mol. Cell Biol. 8, 479-490 (2007).
24. Cléry, A., Blatter, M. & Allain, F. H. RNA recognition motifs: boring? Not quite. Curr. Opin. Struct. Biol. 18, 290-298 (2008).
25. Fairman-Williams, M. E., Guenther, U.-P. & Jankowsky, E. SF1 and SF2 helicases: family matters. Curr. Opin. Struct. Biol. 20, 313-324 (2010).
26. Ghosh, A. & Lima, C. D. Enzymology of RNA cap synthesis. Wiley Interdiscip. Rev. RNA 1, 152-172 (2010).
27. Firczuk, H. et al. An in vivo control map for the eukaryotic mRNA translation machinery. Mol. Syst. Biol. 9, 635 (2013).
28. Hentze, M. W. & Preiss, T. The REM phase of gene regulation. Trends Biochem. Sci. 35, 423-426 (2010).
29. Mitchell, S. F., Jain, S., She, M. & Parker, R. Global analysis of yeast mRNPs. Nat. Struct. Mol. Biol. 20, 127-133 (2013).
30. Ng, S. Y., Bogu, G. K., Soh, B. S. & Stanton, L. W. The long noncoding RNA RMST interacts with SOX2 to regulate neurogenesis. Mol. Cell 51, 349-359 (2013).
31. Di Ruscio, A. et al. DNMT1-interacting RNAs block gene-specific DNA methylation. Nature 503, 371-376 (2013).
32. Hudson, W. H. & Ortlund, E. A. The structure, function and evolution of proteins that bind DNA and RNA. Nat. Rev. Mol. Cell Biol. 15, 749-760 (2014).
33. Ramsköld, D., Wang, E. T., Burge, C. B. & Sandberg, R. An abundance of ubiquitously expressed genes revealed by tissue transcriptome sequence data. PLoS Comput. Biol. 5, e1000598 (2009).
34. Nilsen, T. W. & Graveley, B. R. Expansion of the eukaryotic proteome by alternative splicing. Nature 463, 457-463 (2010).
35. 6-methyladenosine RNA modification status at single nucleotide resolution in mRNA and long noncoding RNA. RNA 19, 1848-1856 (2013).
36. 6A-seq. Nature 485, 201-206 (2012).
37. 6-methyl-adenosine modification in messenger and long non-coding RNA. Trends Biochem. Sci. 38, 204-209 (2013).
38. Carlile, T. M. et al. Pseudouridine profiling reveals regulated mRNA pseudouridylation in yeast and human cells. Nature 515, 143-146 (2014).
39. Weick, E. M. & Miska, E. A. piRNAs: from biogenesis to function. Development. 141, 3458-3471 (2014).
40. Thompson, D. M., Lu, C., Green, P. J. & Parker, R. tRNA cleavage is a conserved response to oxidative stress in eukaryotes. RNA 14, 2095-2103 (2008).
41. Ivanov, P., Emara, M. M., Villen, J., Gygi, S. P. & Anderson, P. Angiogenin-induced tRNA fragments inhibit translation initiation. Mol. Cell 43, 613-623 (2011).
42. Saikia, M. et al. Angiogenin-cleaved tRNA halves interact with cytochrome c, protecting cells from apoptosis during osmotic stress. Mol. Cell. Biol. 34, 2450-2463 (2014).
43. Milek, M., Wyler, E. & Landthaler, M. Transcriptome-wide analysis of protein-RNA interactions using high-throughput sequencing. Semin. Cell Dev. Biol. 23, 206-212 (2012).
44. Müller-McNicoll, M. & Neugebauer, K. M. How cells get the message: dynamic assembly and function of mRNA-protein complexes. Nat. Rev. Genet. 14, 275-287 (2013).
45. Agirrezabala, X. & Frank, J. Elongation in translation as a dynamic interaction among the ribosome, tRNA, and elongation factors EF-G and EF-Tu. Q. Rev. Biophys. 42, 159-200 (2009).
46. Jangi, M. & Sharp, P. A. Building robust transcriptomes with master splicing factors. Cell 159, 487-498 (2014).
47. Zhou, Z. & Fu, X. D. Regulation of splicing by SR proteins and SR protein-specific kinases. Chromosoma 122, 191-207 (2013).
48. Bartel, D. P. MicroRNAs: target recognition and regulatory functions. Cell 136, 215-233 (2009).
49. Tay, Y., Rinn, J. & Pandolfi, P. P. The multilayered complexity of ceRNA crosstalk and competition. Nature 505, 344-352 (2014).
50. König, J., Zarnack, K., Luscombe, N. M. & Ule, J. Protein-RNA interactions: new genomic technologies and perspectives. Nat. Rev. Genet. 13, 77-83 (2012).
51. McHugh, C. A., Russell, P. & Guttman, M. Methods for comprehensive experimental identification of RNA-protein interactions. Genome Biol. 15, 203 (2014).
52. Ule, J. et al. CLIP identifies Nova-regulated RNA networks in the brain. Science 14, 1212-1215 (2003).
53. Licatalosi, D. D. et al. HITS-CLIP yields genome-wide insights into brain alternative RNA processing. Nature 456, 464-469 (2008).
54. Hafner, M. et al. Transcriptome-wide identification of RNA-binding protein and microRNA target sites by PAR-CLIP. Cell 141, 129-141 (2010).
55. König, J. et al. iCLIP reveals the function of hnRNP particles in splicing at individual nucleotide resolution. Nat. Struct. Mol. Biol. 17, 909-915 (2010).
56. Singh, G., Ricci, E. P. & Moore, M. J. RIPiT-Seq: a high-throughput approach for footprinting RNA:protein complexes. Methods 65, 320-332 (2014).
57. Singh, G. et al. The cellular EJC interactome reveals higher-order mRNP structure and an EJC-SR protein nexus. Cell 151, 750-764 (2012).
58. Campbell, Z. T. et al. Cooperativity in RNA-protein interactions: global analysis of RNA binding specificity. Cell Rep. 1, 570-581 (2012).
59. Ozer, A., Pagano, J. M. & Lis, J. T. New technologies provide quantum changes in the scale, speed, and success of SELEX methods and aptamer characterization. Mol. Ther. Nucleic Acids 5, e183 (2014).
60. Lorenz, C. et al. Genomic SELEX for Hfq-binding RNAs identifies genomic aptamers predominantly in antisense transcripts. Nucleic Acids Res. 38, 3794-3808 (2010).
61. Stormo, G. & Zhao, Y. Determining the specificity of protein-DNA interactions. Nat. Rev. Genet. 11, 751-760 (2010).
62. Sanford, J. R. et al. Splicing factor SFRS1 recognizes a functionally diverse landscape of RNA transcripts. Genome Res. 19, 381-394 (2009).
63. Badis, G. et al. Diversity and complexity in DNA recognition by transcription factors. Science 324, 1720-1723 (2009).
64. Rowe, W. et al. Analysis of a complete DNA-protein affinity landscape. J. R. Soc. Interface 7, 397-408 (2009).
65. Nutiu, R. et al. Direct measurement of DNA affinity landscapes on a high-throughput sequencing instrument. Nat. Biotechnol. 29, 659-664 (2011).
66. Maerkl, S. J. & Quake, S. R. A systems approach to measuring the binding energy landscapes of transcription factors. Science 315, 233-237 (2007).
67. Guenther, U. P. et al. Hidden specificity in an apparently nonspecific RNA-binding protein. Nature 502, 385-388 (2013).
68. Stormo, G. D. Modeling the specificity of protein-DNA interactions. Quant. Biol. 1, 115-130 (2013).
69. Ray, D. et al. A compendium of RNA-binding motifs for decoding gene regulation. Nature 499, 172-177 (2013).
70. Duss, O., Michel, E., Diarra dit Konté, N., Schubert, M. & Allain, F. H. Molecular basis for the wide range of affinity found in Csr/Rsm protein-RNA recognition. Nucleic Acids Res. 42, 5332-5346 (2014).
71. Maticzka, D., Lange, S. J., Costa, F. & Backofen, R. GraphProt: modeling binding preferences of RNA-binding proteins. Genome Biol. 15, R17 (2014).
72. Pancaldi, V. & Bähler, J. In silico characterization and prediction of global protein-mRNA interactions in yeast. Nucleic Acids Res. 39, 5826-5836 (2011).
73. Livi, C. M. & Blanzieri, E. Protein-specific prediction of mRNA binding using RNA sequences, binding motifs and predicted secondary structures. BMC Bioinformatics 15, 123 (2014).
74. Puton, T., Kozlowski, L., Tuszynska, I., Rother, K. & Bujnicki, J. M. Computational methods for prediction of protein-RNA interactions. J. Struct. Biol. 179, 261-268 (2012).
75. Bailey, T. L., Williams, N., Misleh, C. & Li, W. W. MEME: discovering and analyzing DNA and protein sequence motifs. Nucleic Acids Res. 34, W369-W373 (2006).
76. Tran, N. T. & Huang, C. H. A survey of motif finding Web tools for detecting binding site motifs in ChIP-Seq data. Biol. Direct 9, 4 (2014).
77. Crooks, G. E., Hon, G., Chandonia, J. M. & Brenner, S. E. WebLogo: a sequence logo generator. Genome Res. 14, 1188-1190 (2004).
78. Reyes-Herrera, P. H. & Ficarra, E. Computational methods for CLIP-seq data processing. Bioinform. Biol. Insights 8, 199-207 (2014).
79. Slattery, M. et al. Absence of a simple code: how transcription factors read the genome. Trends Biochem. Sci. 39, 381-399 (2014).
80. Zhao, Y. & Stormo, G. Jury remains out on simple model of transcription factors. Nat. Biotechnol. 6, 480-483 (2011).
81. Zhao, Y., Ruan, S., Pandey, M. & Stormo, G. D. Improved models for transcription factor binding site identification using nonindependent interactions. Genetics 191, 781-790 (2012).
82. Siddharthan, R. Dinucleotide weight matrices for predicting transcription factor binding sites: generalizing the position weight matrix. PLoS ONE 5, e9722 (2010).
83. Bulyk, M. L., Johnson, P. L. & Church, G. M. Nucleotides of transcription factor binding sites exert interdependent effects on the binding affinities of transcription factors. Nucleic Acids Res. 30, 1255-1261 (2002).
84. Mathelier, A. & Wasserman, W. W. The next generation of transcription factor binding site prediction. PLoS Comput. Biol. 9, e1003214 (2013).
85. Grau, J., Posch, S., Grosse, I. & Keilwagen, J. A general approach for discriminative de novo motif discovery from high-throughput data. Nucleic Acids Res. 41, e197 (2013).
86. Zhou, Q. & Liu, J. S. Extracting sequence features to predict protein-DNA interactions: a comparative study. Nucleic Acids Res. 36, 4137-4148 (2008).
87. Hooghe, B., Broos, S., van Roy, F. & De Bleser, P. A flexible integrative approach based on random forest improves prediction of transcription factor binding sites. Nucleic Acids Res. 40, e106 (2012).
88. Ben-Gal, I. et al. Identification of transcription factor binding sites with variable-order Bayesian networks. Bioinformatics 21, 2657-2666 (2005).
89. Liu, L. A. & Bradley, P. Atomistic modeling of protein-DNA interaction specificity: progress and applications. Curr. Opin. Struct. Biol. 22, 397-405 (2012).
90. Han, A. et al. De novo prediction of PTBP1 binding and splicing targets reveals unexpected features of its RNA recognition and function. PLoS Comput. Biol. 10, e1003442 (2014).
91. Buenrostro, J. D. et al. Quantitative analysis of RNA-protein interactions on a massively parallel array reveals biophysical and evolutionary landscapes. Nat. Biotechnol. 32, 562-568 (2014).
92. SantaLucia, J. J. & Turner, D. H. Measuring the thermodynamics of RNA secondary structure formation. Biopolymers 44, 309-319 (1997).
93. Forsdyke, D. R. Calculation of folding energies of single-stranded nucleic acid sequences: conceptual issues. J. Theor. Biol. 248, 745-753 (2007).
94. Zhuang, F., Fuchs, R. T., Sun, Z., Zheng, Y. & Robb, G. B. Structural bias in T4 RNA ligase-mediated 3?-adapter ligation. Nucleic Acids Res. 40, e54 (2012).
95. Maenner, S., Müller, M., Fröhlich, J., Langer, D. & Becker, P. B. ATP-dependent roX RNA remodeling by the helicase maleless enables specific association of MSL proteins. Mol. Cell 51, 174-184 (2013).
96. Smith, J. K., Hsieh, J. & Fierke, C. A. Importance of RNA-protein interactions in bacterial ribonuclease P structure and catalysis. Biopolymers 87, 329-338 (2007).
97. Rueda, D., Hsieh, J., Day-Storms, J. J., Fierke, C. A. & Walter, N. G. The 5′ leader of precursor tRNAAsp bound to the Bacillus subtilis RNase P holoenzyme has an extended conformation. Biochemistry 44, 16130-16139 (2005).
98. Snoussi, K. & Leroy, J. L. Imino proton exchange and base-pair kinetics in RNA duplexes. Biochemistry 40, 8898-8904 (2001).
99. Faustino, I., Pérez, A. & Orozco, M. Toward a consensus view of duplex RNA flexibility. Biophys. J. 99, 1876-1885 (2010).
100. Bothe, J. R. et al. Characterizing RNA dynamics at atomic resolution using solution-state NMR spectroscopy. Nat. Methods 8, 919-931 (2011).
101. Masliah, G., Barraud, P. & Allain, F. H. RNA recognition by double-stranded RNA binding domains: a matter of shape and sequence. Cell. Mol. Life Sci. 70, 1875-1895 (2013).
102. Cornish-Bowden, A. Enzyme specificity: its meaning in the general case. J. Theor. Biol. 108, 451-457 (1984).
103. Li, J. et al. Identifying mRNA sequence elements for target recognition by human Argonaute proteins. Genome Res. 24, 775-785 (2014).
104. Lambert, N. et al. RNA Bind-n-Seq: quantitative assessment of the sequence and structural binding specificity of RNA binding proteins. Mol Cell. 54, 887-900 (2014).
105. Zearfoss, N. R. et al. A conserved three-nucleotide core motif defines Musashi RNA-binding specificity. J. Biol. Chem. 289, 35530-35541 (2014).
106. Herschlag, D. Implications of ribozyme kinetics for targeting the cleavage of specific RNA molecules in vivo: more isn't always better. Proc. Natl Acad. Sci. USA 88, 6921-9625 (1991).
107. Auweter, S. D., Oberstrass, F. C. & Allain, F. H. Sequence-specific binding of single-stranded RNA: is there a code for recognition? Nucleic Acids Res. 34, 4943-4959 (2006).
108. Lamichhane, R. et al. RNA looping by PTB: evidence using FRET and NMR spectroscopy for a role in splicing repression. Proc. Natl Acad. Sci. USA 107, 4105-4110 (2010).
109. Mickleburgh, I. et al. The organization of RNA contacts by PTB for regulation of FAS splicing. Nucleic Acids Res. 42, 8605-8620 (2014).
110. Zhang, W. et al. Crystal structures and RNA-binding properties of the RNA recognition motifs of heterogeneous nuclear ribonucleoprotein L: insights into its roles in alternative splicing regulation. J. Biol. Chem. 288, 22636-22649 (2013).
111. Romanelli, M. G., Diani, E. & Lievens, P. M. New insights into functional roles of the polypyrimidine tract-binding protein. Int. J. Mol. Sci. 14, 22906-22932 (2013).
112. LaRiviere, F. J., Wolfson, A. D. & Uhlenbeck, O. C. Uniform binding of aminoacyl-tRNAs to elongation factor Tu by thermodynamic compensation. Science 294, 165-168 (2001).
113. Nilsson, J. & Nissen, P. Elongation factors on the ribosome. Curr. Opin. Struct. Biol. 15, 349-354 (2005).
114. Hennig, J. et al. Structural basis for the assembly of the Sxl-Unr translation regulatory complex. Nature 515, 287-290 (2014).
115. Wasmuth, E. V., Januszyk, K. & Lima, C. D. Structure of an Rrp6-RNA exosome complex bound to poly(A) RNA. Nature 511, 435-439 (2014).
116. Andersen, C. B. et al. Structure of the exon junction core complex with a trapped DEAD-box ATPase bound to RNA. Science 313, 1968-1972 (2006).
117. Wahl, M. C., Will, C. L. & Lührmann, R. The spliceosome: design principles of a dynamic RNP machine. Cell. 136, 701-718 (2009).
118. Zhou, L. et al. Crystal structures of the Lsm complex bound to the 3′ end sequence of U6 small nuclear RNA. Nature 506, 116-120 (2014).
119. Weber, G., Trowitzsch, S., Kastner, B., Lührmann, R. & Wahl, M. C. Functional organization of the Sm core in the crystal structure of human U1 snRNP. EMBO J. 29, 4172-4184 (2010).
120. Kondo, Y., Oubridge, C., van Roon, A. M. & Nagai, K. Crystal structure of human U1 snRNP, a small nuclear ribonucleoprotein particle, reveals the mechanism of 5′ splice site recognition. eLife 4, e04986 (2015).
121. Montemayor, E. J. et al. Core structure of the U6 small nuclear ribonucleoprotein at 1.7-Å resolution. Nat. Struct. Mol. Biol. 21, 544-551 (2014).
122. Sonenberg, N. & Hinnebusch, A. G. Regulation of translation initiation in eukaryotes: mechanisms and biological targets. Cell 136, 731-745 (2009).
123. Erzberger, J. P. et al. Molecular architecture of the 40S·eIF1·eIF3 translation initiation complex. Cell 158, 1123-1135 (2014).
124. Marintchev, A. et al. Topology and regulation of the human eIF4A/4G/4H helicase complex in translation initiation. Cell 136, 447-460 (2009).
125. Antson, A. A. et al. Structure of the trp RNA-binding attenuation protein, TRAP, bound to RNA. Nature 401, 235-242 (1999).
126. Cieniková, Z., Damberger, F. F., Hall, J., Allain, F. H. & Maris, C. Structural and mechanistic insights into poly(uridine) tract recognition by the hnRNP C RNA recognition motif. J. Am. Chem. Soc. 136, 14536-14544 (2014).
127. 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).
128. Ding, Y. et al. In vivo genome-wide profiling of RNA secondary structure reveals novel regulatory features. Nature 505, 696-700 (2014).
129. Wan, Y. et al. Landscape and variation of RNA secondary structure across the human transcriptome. Nature 505, 706-709 (2014).
130. Ray, D. et al. Rapid and systematic analysis of the RNA recognition specificities of RNA-binding proteins. Nat. Biotechnol. 27, 667-670 (2009).
131. Tome, J. M. et al. Comprehensive analysis of RNA-protein interactions by high-thoughput sequencing-RNA affinity profiling. Nat. Methods 11, 683-688 (2014).
132. Roy, R., Hohng, S. & Ha, T. A practical guide to single-molecule FRET. Nat. Methods 5, 507-516 (2008).
133. Cech, T. R. & Steitz, J. A. The noncoding RNA revolution-trashing old rules to forge new ones. Cell 157, 77-94 (2014).
134. Motorin, Y. & Helm, M. RNA nucleotide methylation. Wiley Interdiscip. Rev. RNA 2, 611-631 (2011).