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Unraveling the structure and biological functions of RNA triple helices

Advanced Review

Jessica A. Brown

Published Online: May 22 2020

DOI: 10.1002/wrna.1598

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Abstract It has been nearly 63 years since the first characterization of an RNA triple helix in vitro by Gary Felsenfeld, David Davies, and Alexander Rich. An RNA triple helix consists of three strands: A Watson–Crick RNA double helix whose major‐groove establishes hydrogen bonds with the so‐called “third strand”. In the past 15 years, it has been recognized that these major‐groove RNA triple helices, like single‐stranded and double‐stranded RNA, also mediate prominent biological roles inside cells. Thus far, these triple helices are known to mediate catalysis during telomere synthesis and RNA splicing, bind to ligands and ions so that metabolite‐sensing riboswitches can regulate gene expression, and provide a clever strategy to protect the 3′ end of RNA from degradation. Because RNA triple helices play important roles in biology, there is a renewed interest in better understanding the fundamental properties of RNA triple helices and developing methods for their high‐throughput discovery. This review provides an overview of the fundamental biochemical and structural properties of major‐groove RNA triple helices, summarizes the structure and function of naturally occurring RNA triple helices, and describes prospective strategies to isolate RNA triple helices as a means to establish the “triplexome”. This article is categorized under: RNA Structure and Dynamics > RNA Structure and Dynamics RNA Structure and Dynamics > RNA Structure, Dynamics and Chemistry RNA Structure and Dynamics > Influence of RNA Structure in Biological Systems

Composition and structural arrangement of major‐groove RNA triple helices. Hydrogen‐bonding interactions (gray dashed lines) are shown for the two canonical major‐groove base triples: (a) U•A‐U and C⁺•G‐C (ball‐and‐stick representation of base triples from PDB 6SVS; Ruszkowska, Ruszkowski, Hulewicz, Dauter, & Brown, 2020). Interactions are shown along with the Hoogsteen and Watson–Crick faces. (b) Schematics are shown for strand polarity and nucleotide composition in parallel and anti‐parallel motifs. Interbase interactions are represented as a circle (•) for Hoogsteen base pair, a single dash (−) for Watson–Crick base pair, and a square (■) for reverse Hoogsteen base pair. (c) Major‐groove RNA triple helices are commonly found in H‐type or I‐type pseudoknot structures. The three strands of triple helix are identified by the following tricolor scheme: Hoogsteen strand is blue, Watson strand is purple, and Crick strand is green

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Chemical structures of triplex‐binding small molecules. Chemical structures are shown for small molecules that (a) broadly recognize RNA triple helices and (b) bind to the MALAT1 RNA triple helix

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Structures of triple helices that function as RNA stability elements. (a) A generalized schematic diagram is shown for a single‐domain stability element alongside the X‐ray crystal structure of the KSHV PAN RNA triple helix (cartoon representation). Important structural regions are labeled. (b) A generalized schematic diagram is shown for the predicted structure of a double‐domain stability element: TWIFB1_Osa. Gray circles (•) and dashed lines (−) indicate putative nucleotide interactions. (c) A generalized schematic diagram and X‐ray crystal structure is shown for a blunt‐ended RNA triple helix: Human MALAT1 (cartoon representation). The tricolor scheme of strands and symbols for their interactions are described in Figure 1. The PDB IDs are listed below each RNA label

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Structural basis of ligand recognition by an RNA triple helix. The 3D structures are shown for six ligand‐bound riboswitches: (a) SAM‐II, SAM‐V, (b) PreQ₁‐II, PreQ₁‐III, (c) c‐di‐GMP‐II, and (d) guanidine‐III. For each riboswitch, there is a panel that displays the entire experimentally determined structure with PDB in parenthesis (left panel, cartoon representation), the triple helix interacting with ligand (middle panel, cartoon representation), and noncovalent interactions of ligand and nucleotides (right panel, ball‐and‐stick representation). The ligand is shown in orange and triple helix components are shown in tricolor scheme

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Catalytic triplexes involved in splicing. (a) The catalytic triplex of both the group II self‐splicing intron (tricolor stick representation) and the spliceosome (not shown) coordinate two catalytic metal ions (orange spheres) via electrostatic interactions with phosphate backbone. Two views are shown. (b) His5 of CWC2P (orange stick representation) may form hydrogen bonds (gray dashed lines) with two of the three base triples (tricolor sticks) in the catalytic triplex observed for the S. cerevisiae spliceosome

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Triple helix in telomerase RNA. Telomerase RNA forms a nearly continuous triple helix (tricolor cartoon representation) in which a U•A‐U major‐groove triple helix is adjacent to a minor‐groove triple helix

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Structural views of triple and double helices. The top and side views are shown for X‐ray crystal structures (cartoon representation) solved for an RNA triple helix, A‐RNA double helix, A′‐RNA double helix, and B‐DNA double helix. Hoogsteen strand is blue, Watson (or purine‐rich) strand is purple, and Crick (or pyrimidine‐rich) strand is green. Select structural parameters are defined by red text and pictures. The PDB IDs for displayed structures are listed below each name

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References

Abu Almakarem,, A. S., Petrov,, A. I., Stombaugh,, J., Zirbel,, C. L., & Leontis,, N. B. (2012). Comprehensive survey and geometric classification of base triples in RNA structures. Nucleic Acids Research, 40(4), 1407–1423. https://doi.org/10.1093/nar/gkr810
Abulwerdi,, F. A., Xu,, W., Ageeli,, A. A., Yonkunas,, M. J., Arun,, G., Nam,, H., … Le Grice,, S. F. J. (2019). Selective small‐molecule targeting of a triple helix encoded by the long noncoding RNA, MALAT1. ACS Chemical Biology, 14(2), 223–235. https://doi.org/10.1021/acschembio.8b00807
Adams,, P. L., Stahley,, M. R., Kosek,, A. B., Wang,, J., & Strobel,, S. A. (2004). Crystal structure of a self‐splicing group I intron with both exons. Nature, 430(6995), 45–50. https://doi.org/10.1038/nature02642
Ageeli,, A. A., McGovern‐Gooch,, K. R., Kaminska,, M. M., & Baird,, N. J. (2019). Finely tuned conformational dynamics regulate the protective function of the lncRNA MALAT1 triple helix. Nucleic Acids Research, 47(3), 1468–1481. https://doi.org/10.1093/nar/gky1171
Arnott,, S., & Bond,, P. J. (1973). Structures for poly(U)•poly(A)‐poly(U) triple‐stranded polynucleotides. Nature: New Biology, 244(134), 99–101. https://doi.org/10.1038/newbio244099a0
Arnott,, S., Bond,, P. J., Selsing,, E., & Smith,, P. J. (1976). Models of triple‐stranded polynucleotides with optimised stereochemistry. Nucleic Acids Research, 3(10), 2459–2470.
Arnott,, S., Hukins,, D. W., Dover,, S. D., Fuller,, W., & Hodgson,, A. R. (1973). Structures of synthetic polynucleotides in the A‐RNA and A`‐RNA conformations: X‐ray diffraction analyses of the molecular conformations of polyadenylic acid‐polyuridylic acid and polyinosinic acid‐polycytidylic acid. Journal of Molecular Biology, 81(2), 107–122. https://doi.org/10.1016/0022-2836(73)90183-6
Arya,, D. P., Coffee,, R. L., Jr., Willis,, B., & Abramovitch,, A. I. (2001). Aminoglycoside‐nucleic acid interactions: Remarkable stabilization of DNA and RNA triple helices by neomycin. Journal of the American Chemical Society, 123(23), 5385–5395.
Arya,, D. P., Xue,, L., & Tennant,, P. (2003). Combining the best in triplex recognition: Synthesis and nucleic acid binding of a BQQ‐neomycin conjugate. Journal of the American Chemical Society, 125(27), 8070–8071. https://doi.org/10.1021/ja034241t
Asensio,, J. L., Lane,, A. N., Dhesi,, J., Bergqvist,, S., & Brown,, T. (1998). The contribution of cytosine protonation to the stability of parallel DNA triple helices. Journal of Molecular Biology, 275(5), 811–822. https://doi.org/10.1006/jmbi.1997.1520
Aytenfisu,, A. H., Liberman,, J. A., Wedekind,, J. E., & Mathews,, D. H. (2015). Molecular mechanism for PreQ₁‐II riboswitch function revealed by molecular dynamics. RNA, 21(11), 1898–1907. https://doi.org/10.1261/rna.051367.115
Bahal,, R., Gupta,, A., & Glazer,, P. M. (2016). Precise genome modification using triplex forming oligonucleotides and peptide nucleic acids. In T. Cathomen,, M. Hirsch,, & M. Porteus, (Eds.), Genome Editing. Advances in Experimental Medicine and Biology (pp. 93–110). New York, NY: Springer.
Bao,, P., Boon,, K. L., Will,, C. L., Hartmuth,, K., & Luhrmann,, R. (2018). Multiple RNA‐RNA tertiary interactions are dispensable for formation of a functional U2/U6 RNA catalytic core in the spliceosome. Nucleic Acids Research, 46(22), 12126–12138. https://doi.org/10.1093/nar/gky966
Belashov,, I. A., Crawford,, D. W., Cavender,, C. E., Dai,, P., Beardslee,, P. C., Mathews,, D. H., … Wedekind,, J. E. (2018). Structure of HIV TAR in complex with a lab‐evolved RRM provides insight into duplex RNA recognition and synthesis of a constrained peptide that impairs transcription. Nucleic Acids Research, 46(13), 6401–6415. https://doi.org/10.1093/nar/gky529
Bellaousov,, S., & Mathews,, D. H. (2010). ProbKnot: Fast prediction of RNA secondary structure including pseudoknots. RNA, 16(10), 1870–1880. https://doi.org/10.1261/rna.2125310
Bertram,, K., Agafonov,, D. E., Liu,, W. T., Dybkov,, O., Will,, C. L., Hartmuth,, K., … Luhrmann,, R. (2017). Cryo‐EM structure of a human spliceosome activated for step 2 of splicing. Nature, 542(7641), 318–323. https://doi.org/10.1038/nature21079
Best,, G. C., & Dervan,, P. B. (1995). Energetics of formation of sixteen triple helical complexes which vary at a single position within a pyrimidine motif. Journal of the American Chemical Society, 117, 1187–1193.
Bhowmik,, D., Das,, S., Hossain,, M., Haq,, L., & Suresh Kumar,, G. (2012). Biophysical characterization of the strong stabilization of the RNA triplex poly(U)•poly(A)‐poly(U) by 9‐O‐(omega‐amino) alkyl ether berberine analogs. PLoS One, 7(5), e37939. https://doi.org/10.1371/journal.pone.0037939
Bhuiya,, S., Haque,, L., Goswami,, R., & Das,, S. (2017). Multispectroscopic and theoretical exploration of the comparative binding aspects of bioflavonoid fisetin with triple‐ and double‐helical forms of RNA. Journal of Physical Chemistry B, 121(49), 11037–11052. https://doi.org/10.1021/acs.jpcb.7b07972
Boulanger,, S. C., Belcher,, S. M., Schmidt,, U., Dib‐Hajj,, S. D., Schmidt,, T., & Perlman,, P. S. (1995). Studies of point mutants define three essential paired nucleotides in the domain 5 substructure of a group II intron. Molecular and Cellular Biology, 15(8), 4479–4488. https://doi.org/10.1128/mcb.15.8.4479
Breaker,, R. R. (2012). Riboswitches and the RNA world. Cold Spring Harbor Perspectives in Biology, 4(2), a003566. https://doi.org/10.1101/cshperspect.a003566
Breaker,, R. R. (2018). Riboswitches and translation control. Cold Spring Harbor Perspectives in Biology, 10(11), a032797. https://doi.org/10.1101/cshperspect.a032797
Brown,, J. A., Bulkley,, D., Wang,, J., Valenstein,, M. L., Yario,, T. A., Steitz,, T. A., & Steitz,, J. A. (2014). Structural insights into the stabilization of MALAT1 noncoding RNA by a bipartite triple helix. Nature Structural %26 Molecular Biology, 21(7), 633–640. https://doi.org/10.1038/nsmb.2844
Brown,, J. A., Kinzig,, C. G., DeGregorio,, S. J., & Steitz,, J. A. (2016a). Hoogsteen‐position pyrimidines promote the stability and function of the MALAT1 RNA triple helix. RNA, 22(5), 743–749. https://doi.org/10.1261/rna.055707.115
Brown,, J. A., Kinzig,, C. G., DeGregorio,, S. J., & Steitz,, J. A. (2016b). Methyltransferase‐like protein 16 binds the 3′‐terminal triple helix of MALAT1 long noncoding RNA. Proceedings of the National Academy of Sciences of the United States of America, 113(49), 14013–14018. https://doi.org/10.1073/pnas.1614759113
Brown,, J. A., Valenstein,, M. L., Yario,, T. A., Tycowski,, K. T., & Steitz,, J. A. (2012). Formation of triple‐helical structures by the 3′‐end sequences of MALAT1 and MENβ noncoding RNAs. Proceedings of the National Academy of Sciences of the United States of America, 109(47), 19202–19207. https://doi.org/10.1073/pnas.12173381091217338109
Buske,, F. A., Bauer,, D. C., Mattick,, J. S., & Bailey,, T. L. (2012). Triplexator: Detecting nucleic acid triple helices in genomic and transcriptomic data. Genome Research, 22(7), 1372–1381. https://doi.org/10.1101/gr.130237.111
Buske,, F. A., Mattick,, J. S., & Bailey,, T. L. (2011). Potential in vivo roles of nucleic acid triple helices. RNA Biology, 8(3), 427–439.
Callahan,, D. E., Trapane,, T. L., Miller,, P. S., Ts`o,, P. O., & Kan,, L. S. (1991). Comparative circular dichroism and fluorescence studies of oligodeoxyribonucleotide and oligodeoxyribonucleoside methylphosphonate pyrimidine strands in duplex and triplex formation. Biochemistry, 30(6), 1650–1655. https://doi.org/10.1021/bi00220a030
Cash,, D. D., Cohen‐Zontag,, O., Kim,, N. K., Shefer,, K., Brown,, Y., Ulyanov,, N. B., … Feigon,, J. (2013). Pyrimidine motif triple helix in the Kluyveromyces lactis telomerase RNA pseudoknot is essential for function in vivo. Proceedings of the National Academy of Sciences of the United States of America, 110(27), 10970–10975. https://doi.org/10.1073/pnas.13095901101309590110
Cash,, D. D., & Feigon,, J. (2017). Structure and folding of the Tetrahymena telomerase RNA pseudoknot. Nucleic Acids Research, 45(1), 482–495. https://doi.org/10.1093/nar/gkw1153
Chan,, R. T., Peters,, J. K., Robart,, A. R., Wiryaman,, T., Rajashankar,, K. R., & Toor,, N. (2018). Structural basis for the second step of group II intron splicing. Nature Communications, 9(1), 4676. https://doi.org/10.1038/s41467-018-06678-0
Chandrasekaran,, R., Giacometti,, A., & Arnott,, S. (2000). Structure of poly(U)•poly(A)‐poly(U). Journal of Biomolecular Structure %26 Dynamics, 17(6), 1023–1034. https://doi.org/10.1080/07391102.2000.10506590
Chen,, B., Zuo,, X., Wang,, Y. X., & Dayie,, T. K. (2012). Multiple conformations of SAM‐II riboswitch detected with SAXS and NMR spectroscopy. Nucleic Acids Research, 40(7), 3117–3130. https://doi.org/10.1093/nar/gkr1154
Chen,, G., Chang,, K. Y., Chou,, M. Y., Bustamante,, C., & Tinoco,, I., Jr. (2009). Triplex structures in an RNA pseudoknot enhance mechanical stability and increase efficiency of −1 ribosomal frameshifting. Proceedings of the National Academy of Sciences of the United States of America, 106(31), 12706–12711. https://doi.org/10.1073/pnas.0905046106
Chen,, J. L., Blasco,, M. A., & Greider,, C. W. (2000). Secondary structure of vertebrate telomerase RNA. Cell, 100(5), 503–514. https://doi.org/10.1016/s0092-8674(00)80687-x
Conrad,, N. K. (2014). The emerging role of triple helices in RNA biology. WIREs RNA, 5(1), 15–29. https://doi.org/10.1002/wrna.1194
Conrad,, N. K. (2016). New insights into the expression and functions of the Kaposi`s sarcoma‐associated herpesvirus long noncoding PAN RNA. Virus Research, 212, 53–63. https://doi.org/10.1016/j.virusres.2015.06.012
Conrad,, N. K., Mili,, S., Marshall,, E. L., Shu,, M. D., & Steitz,, J. A. (2006). Identification of a rapid mammalian deadenylation‐dependent decay pathway and its inhibition by a viral RNA element. Molecular Cell, 24(6), 943–953. https://doi.org/10.1016/j.molcel.2006.10.029
Conrad,, N. K., Shu,, M. D., Uyhazi,, K. E., & Steitz,, J. A. (2007). Mutational analysis of a viral RNA element that counteracts rapid RNA decay by interaction with the polyadenylate tail. Proceedings of the National Academy of Sciences of the United States of America, 104(25), 10412–10417. https://doi.org/10.1073/pnas.0704187104
Conrad,, N. K., & Steitz,, J. A. (2005). A Kaposi`s sarcoma virus RNA element that increases the nuclear abundance of intronless transcripts. EMBO Journal, 24(10), 1831–1841. https://doi.org/10.1038/sj.emboj.7600662
Das,, S., Kumar,, G. S., Ray,, A., & Maiti,, M. (2003). Spectroscopic and thermodynamic studies on the binding of sanguinarine and berberine to triple and double helical DNA and RNA structures. Journal of Biomolecular Structure %26 Dynamics, 20(5), 703–714. https://doi.org/10.1080/07391102.2003.10506887
Devi,, G., Zhou,, Y., Zhong,, Z., Toh,, D. F., & Chen,, G. (2015). RNA triplexes: From structural principles to biological and biotech applications. WIREs RNA, 6(1), 111–128. https://doi.org/10.1002/wrna.1261
Donlic,, A., Morgan,, B. S., Xu,, J. L., Liu,, A., Roble,, C., Jr., & Hargrove,, A. E. (2018). Discovery of small molecule ligands for MALAT1 by tuning an RNA‐binding scaffold. Angewandte Chemie (International Edition in English), 57(40), 13242–13247. https://doi.org/10.1002/anie.201808823
Doucet,, A. J., Wilusz,, J. E., Miyoshi,, T., Liu,, Y., & Moran,, J. V. (2015). A 3′‐ poly(A) tract is required for LINE‐1 retrotransposition. Molecular Cell, 60(5), 728–741. https://doi.org/10.1016/j.molcel.2015.10.012
Drew,, H. R., Wing,, R. M., Takano,, T., Broka,, C., Tanaka,, S., Itakura,, K., & Dickerson,, R. E. (1981). Structure of a B‐DNA dodecamer: Conformation and dynamics. Proceedings of the National Academy of Sciences of the United States of America, 78(4), 2179–2183. https://doi.org/10.1073/pnas.78.4.2179
Duconge,, F., & Toulme,, J. J. (1999). In vitro selection identifies key determinants for loop‐loop interactions: RNA aptamers selective for the TAR RNA element of HIV‐1. RNA, 5(12), 1605–1614. https://doi.org/10.1017/s1355838299991318
Dutta,, D., Belashov,, I. A., & Wedekind,, J. E. (2018). Coupling green fluorescent protein expression with chemical modification to probe functionally relevant riboswitch conformations in live bacteria. Biochemistry, 57(31), 4620–4628. https://doi.org/10.1021/acs.biochem.8b00316
Dutta,, D., & Wedekind,, J. E. (2019). Nucleobase mutants of a bacterial PreQ₁‐II riboswitch that uncouple metabolite sensing from gene regulation. Journal of Biological Chemistry, 295, 2555–2567. https://doi.org/10.1074/jbc.RA119.010755
Escude,, C., Francois,, J. C., Sun,, J. S., Ott,, G., Sprinzl,, M., Garestier,, T., & Helene,, C. (1993). Stability of triple helices containing RNA and DNA strands: Experimental and molecular modeling studies. Nucleic Acids Research, 21(24), 5547–5553. https://doi.org/10.1093/nar/21.24.5547
Eysmont,, K., Matylla‐Kulinska,, K., Jaskulska,, A., Magnus,, M., & Konarska,, M. M. (2019). Rearrangements within the U6 snRNA core during the transition between the two catalytic steps of splicing. Molecular Cell, 75(3), 538–548.e533. https://doi.org/10.1016/j.molcel.2019.05.018
Felsenfeld,, G., Davies,, D. R., & Rich,, A. (1957). Formation of a 3‐stranded polynucleotide molecule. Journal of the American Chemical Society, 79(8), 2023–2024.
Fica,, S. M., Mefford,, M. A., Piccirilli,, J. A., & Staley,, J. P. (2014). Evidence for a group II intron‐like catalytic triplex in the spliceosome. Nature Structural %26 Molecular Biology, 21(5), 464–471. https://doi.org/10.1038/nsmb.2815
Fica,, S. M., Tuttle,, N., Novak,, T., Li,, N. S., Lu,, J., Koodathingal,, P., … Piccirilli,, J. A. (2013). RNA catalyses nuclear pre‐mRNA splicing. Nature, 503(7475), 229–234. https://doi.org/10.1038/nature12734
Firdaus‐Raih,, M., Harrison,, A. M., Willett,, P., & Artymiuk,, P. J. (2011). Novel base triples in RNA structures revealed by graph theoretical searching methods. BMC Bioinformatics, 12(Suppl 13), S2. https://doi.org/10.1186/1471-2105-12-S13-S2
Flavell,, R. A., & van den Berg,, F. M. (1975). The isolation of duplex DNA containing (dA‐dT) clusters by affinity chromatography on poly(U) sephadex. FEBS Letters, 58(1), 90–93. https://doi.org/10.1016/0014-5793(75)80232-8
Galej,, W. P., Toor,, N., Newman,, A. J., & Nagai,, K. (2018). Molecular mechanism and evolution of nuclear pre‐mRNA and group II intron splicing: Insights from cryo‐electron microscopy structures. Chemical Reviews, 118(8), 4156–4176. https://doi.org/10.1021/acs.chemrev.7b00499
Gilbert,, S. D., Rambo,, R. P., Van Tyne,, D., & Batey,, R. T. (2008). Structure of the SAM‐II riboswitch bound to S‐adenosylmethionine. Nature Structural %26 Molecular Biology, 15(2), 177–182. https://doi.org/10.1038/nsmb.1371
Gordon,, P. M., Fong,, R., & Piccirilli,, J. A. (2007). A second divalent metal ion in the group II intron reaction center. Chemistry %26 Biology, 14(6), 607–612. https://doi.org/10.1016/j.chembiol.2007.05.008
Gordon,, P. M., & Piccirilli,, J. A. (2001). Metal ion coordination by the AGC triad in domain 5 contributes to group II intron catalysis. Nature Structural Biology, 8(10), 893–898. https://doi.org/10.1038/nsb1001-893
Gordon,, P. M., Sontheimer,, E. J., & Piccirilli,, J. A. (2000). Metal ion catalysis during the exon‐ligation step of nuclear pre‐mRNA splicing: Extending the parallels between the spliceosome and group II introns. RNA, 6(2), 199–205. https://doi.org/10.1017/s1355838200992069
Greider,, C. W., & Blackburn,, E. H. (1989). A telomeric sequence in the RNA of Tetrahymena telomerase required for telomere repeat synthesis. Nature, 337(6205), 331–337. https://doi.org/10.1038/337331a0
Gutschner,, T., Hammerle,, M., & Diederichs,, S. (2013). MALAT1—A paradigm for long noncoding RNA function in cancer. Journal of Molecular Medicine (Berlin, Germany), 91(7), 791–801. https://doi.org/10.1007/s00109-013-1028-y
Haack,, D. B., Yan,, X., Zhang,, C., Hingey,, J., Lyumkis,, D., Baker,, T. S., & Toor,, N. (2019). Cryo‐EM structures of a group II intron reverse splicing into DNA. Cell, 178(3), 612–623.e612. https://doi.org/10.1016/j.cell.2019.06.035
Haller,, A., Rieder,, U., Aigner,, M., Blanchard,, S. C., & Micura,, R. (2011). Conformational capture of the SAM‐II riboswitch. Nature Chemical Biology, 7(6), 393–400. https://doi.org/10.1038/nchembio.562
Hang,, J., Wan,, R., Yan,, C., & Shi,, Y. (2015). Structural basis of pre‐mRNA splicing. Science, 349(6253), 1191–1198. https://doi.org/10.1126/science.aac8159
Haq,, I., & Ladbury,, J. (2000). Drug‐DNA recognition: Energetics and implications for design. Journal of Molecular Recognition, 13(4), 188–197. https://doi.org/10.1002/1099-1352(200007/08)13:4%3C188::AID-JMR503%3E3.0.CO;2-1
He,, S., Zhang,, H., Liu,, H., & Zhu,, H. (2015). LongTarget: A tool to predict lncRNA DNA‐binding motifs and binding sites via Hoogsteen base‐pairing analysis. Bioinformatics, 31(2), 178–186. https://doi.org/10.1093/bioinformatics/btu643
He,, X. J., & Tan,, L. F. (2014). Interactions of octahedral ruthenium(II) polypyridyl complexes with the RNA triplex poly(U)•poly(A)‐poly(U) effect on the third‐strand stabilization. Inorganic Chemistry, 53(20), 11152–11159. https://doi.org/10.1021/ic5017565
Hoogsteen,, K. (1959). The crystal and molecular structure of a hydrogen‐bonded complex between 1‐methylthymine and 9‐methyladenine. Acta Crystallographica, 12, 822–823.
Holbrook,, S. R., Sussman,, J. L., Warrant,, R. W., & Kim,, S. H. (1978). Crystal structure of yeast phenylalanine transfer RNA. II. Structural features and functional implications. Journal of Molecular Biology, 123(4), 631–660. https://doi.org/10.1016/0022-2836(78)90210-3
Hoshika,, S., Leal,, N. A., Kim,, M. J., Kim,, M. S., Karalkar,, N. B., Kim,, H. J., … Benner,, S. A. (2019). Hachimoji DNA and RNA: A genetic system with eight building blocks. Science, 363(6429), 884–887. https://doi.org/10.1126/science.aat0971
Huang,, J., Brown,, A. F., Wu,, J., Xue,, J., Bley,, C. J., Rand,, D. P., … Lei,, M. (2014). Structural basis for protein‐RNA recognition in telomerase. Nature Structural %26 Molecular Biology, 21(6), 507–512. https://doi.org/10.1038/nsmb.2819
Huang,, L., & Lilley,, D. M. J. (2018). Structure and ligand binding of the SAM‐V riboswitch. Nucleic Acids Research, 46(13), 6869–6879. https://doi.org/10.1093/nar/gky520
Huang,, L., Wang,, J., Wilson,, T. J., & Lilley,, D. M. J. (2017). Structure of the guanidine III riboswitch. Cell Chemical Biology, 24(11), 1407–1415.e1402. https://doi.org/10.1016/j.chembiol.2017.08.021
Isogawa,, A., Fuchs,, R. P., & Fujii,, S. (2018). Versatile and efficient chromatin pull‐down methodology based on DNA triple helix formation. Scientific Reports, 8(1), 5925. https://doi.org/10.1038/s41598-018-24417-9
Jain,, A., Bacolla,, A., Chakraborty,, P., Grosse,, F., & Vasquez,, K. M. (2010). Human DHX9 helicase unwinds triple‐helical DNA structures. Biochemistry, 49(33), 6992–6999. https://doi.org/10.1021/bi100795m
James,, P. L., Brown,, T., & Fox,, K. R. (2003). Thermodynamic and kinetic stability of intermolecular triple helices containing different proportions of C⁺•G‐C and T•A‐T triplets. Nucleic Acids Research, 31(19), 5598–5606.
Jenkins,, J. L., Krucinska,, J., McCarty,, R. M., Bandarian,, V., & Wedekind,, J. E. (2011). Comparison of a PreQ₁ riboswitch aptamer in metabolite‐bound and free states with implications for gene regulation. Journal of Biological Chemistry, 286(28), 24626–24637. https://doi.org/10.1074/jbc.M111.230375
Jiang,, J., Chan,, H., Cash,, D. D., Miracco,, E. J., Ogorzalek Loo,, R. R., Upton,, H. E., … Feigon,, J. (2015). Structure of Tetrahymena telomerase reveals previously unknown subunits, functions, and interactions. Science, 350(6260), aab4070. https://doi.org/10.1126/science.aab4070
Johnson,, A. F., Wang,, R., Ji,, H., Chen,, D., Guilfoyle,, R. A., & Smith,, L. M. (1996). Purification of single‐stranded M13 DNA by cooperative triple‐helix‐mediated affinity capture. Analytical Biochemistry, 234(1), 83–95. https://doi.org/10.1006/abio.1996.0053
Jones,, C. P., & Ferre‐D`Amare,, A. R. (2017). Long‐range interactions in riboswitch control of gene expression. Annual Review of Biophysics, 46, 455–481. https://doi.org/10.1146/annurev-biophys-070816-034042
Kalwa,, M., Hanzelmann,, S., Otto,, S., Kuo,, C. C., Franzen,, J., Joussen,, S., … Wagner,, W. (2016). The lncRNA HOTAIR impacts on mesenchymal stem cells via triple helix formation. Nucleic Acids Research, 44(22), 10631–10643. https://doi.org/10.1093/nar/gkw802
Kang,, M., Eichhorn,, C. D., & Feigon,, J. (2014). Structural determinants for ligand capture by a class II PreQ₁ riboswitch. Proceedings of the National Academy of Sciences of the United States of America, 111(6), E663–E671. https://doi.org/10.1073/pnas.1400126111
Kim,, N. K., Zhang,, Q., Zhou,, J., Theimer,, C. A., Peterson,, R. D., & Feigon,, J. (2008). Solution structure and dynamics of the wild‐type pseudoknot of human telomerase RNA. Journal of Molecular Biology, 384(5), 1249–1261. https://doi.org/10.1016/j.jmb.2008.10.005
Kunkler,, C. N., Hulewicz,, J. P., Hickman,, S. C., Wang,, M. C., McCown,, P. J., & Brown,, J. A. (2019). Stability of an RNA•DNA‐DNA triple helix depends on base triplet composition and length of the RNA third strand. Nucleic Acids Research, 47(14), 7213–7222. https://doi.org/10.1093/nar/gkz573
Kuo,, C. C., Hanzelmann,, S., Senturk Cetin,, N., Frank,, S., Zajzon,, B., Derks,, J. P., … Costa,, I. G. (2019). Detection of RNA‐DNA binding sites in long noncoding RNAs. Nucleic Acids Research, 47(6), e32. https://doi.org/10.1093/nar/gkz037
Lee,, E. R., Baker,, J. L., Weinberg,, Z., Sudarsan,, N., & Breaker,, R. R. (2010). An allosteric self‐splicing ribozyme triggered by a bacterial second messenger. Science, 329(5993), 845–848. https://doi.org/10.1126/science.1190713
Leitner,, D., Schroder,, W., & Weisz,, K. (2000). Influence of sequence‐dependent cytosine protonation and methylation on DNA triplex stability. Biochemistry, 39(19), 5886–5892.
Lescoute,, A., & Westhof,, E. (2006). The A‐minor motifs in the decoding recognition process. Biochimie, 88(8), 993–999. https://doi.org/10.1016/j.biochi.2006.05.018
Letai,, A. G., Palladino,, M. A., Fromm,, E., Rizzo,, V., & Fresco,, J. R. (1988). Specificity in formation of triple‐stranded nucleic acid helical complexes: Studies with agarose‐linked polyribonucleotide affinity columns. Biochemistry, 27(26), 9108–9112. https://doi.org/10.1021/bi00426a007
Levene,, P. A., Bass,, L. W., & Simms,, H. S. (1926). The ionization of pyrimidines in relation to the structure of pyrimidine nucleosides. Journal of Biological Chemistry, 70, 229–241.
Li,, Y., Syed,, J., & Sugiyama,, H. (2016). RNA‐DNA triplex formation by long noncoding RNAs. Cell Chemical Biology, 23(11), 1325–1333. https://doi.org/10.1016/j.chembiol.2016.09.011
Liberman,, J. A., Salim,, M., Krucinska,, J., & Wedekind,, J. E. (2013). Structure of a class II PreQ₁ riboswitch reveals ligand recognition by a new fold. Nature Chemical Biology, 9(6), 353–355. https://doi.org/10.1038/nchembio.1231
Liberman,, J. A., Suddala,, K. C., Aytenfisu,, A., Chan,, D., Belashov,, I. A., Salim,, M., … Wedekind,, J. E. (2015). Structural analysis of a class III PreQ₁ riboswitch reveals an aptamer distant from a ribosome‐binding site regulated by fast dynamics. Proceedings of the National Academy of Sciences of the United States of America, 112(27), E3485–E3494. https://doi.org/10.1073/pnas.1503955112
Lin,, J., Wen,, Y., He,, S., Yang,, X., Zhang,, H., & Zhu,, H. (2019). Pipelines for cross‐species and genome‐wide prediction of long noncoding RNA binding. Nature Protocols, 14(3), 795–818. https://doi.org/10.1038/s41596-018-0115-5
Linder,, B., Grozhik,, A. V., Olarerin‐George,, A. O., Meydan,, C., Mason,, C. E., & Jaffrey,, S. R. (2015). Single‐nucleotide‐resolution mapping of m⁶A and m⁶Am throughout the transcriptome. Nature Methods, 12(8), 767–772. https://doi.org/10.1038/nmeth.3453
Lingner,, J., Hughes,, T. R., Shevchenko,, A., Mann,, M., Lundblad,, V., & Cech,, T. R. (1997). Reverse transcriptase motifs in the catalytic subunit of telomerase. Science, 276(5312), 561–567. https://doi.org/10.1126/science.276.5312.561
Liu,, F., & Theimer,, C. A. (2012). Telomerase activity is sensitive to subtle perturbations of the TLC1 pseudoknot 3′ stem and tertiary structure. Journal of Molecular Biology, 423(5), 719–735. https://doi.org/10.1016/j.jmb.2012.08.025
Lu,, Z., Zhang,, Q. C., Lee,, B., Flynn,, R. A., Smith,, M. A., Robinson,, J. T., … Chang,, H. Y. (2016). RNA duplex map in living cells reveals higher‐order transcriptome structure. Cell, 165(5), 1267–1279. https://doi.org/10.1016/j.cell.2016.04.028
Lund,, P. E., Chatterjee,, S., Daher,, M., & Walter,, N. G. (2019). Protein unties the pseudoknot: S1‐mediated unfolding of RNA higher order structure. Nucleic Acids Research, 48, 2107–2125. https://doi.org/10.1093/nar/gkz1166
Marcia,, M., & Pyle,, A. M. (2012). Visualizing group II intron catalysis through the stages of splicing. Cell, 151(3), 497–507. https://doi.org/10.1016/j.cell.2012.09.033
Marcia,, M., & Pyle,, A. M. (2014). Principles of ion recognition in RNA: Insights from the group II intron structures. RNA, 20(4), 516–527. https://doi.org/10.1261/rna.043414.113
McCown,, P. J., Corbino,, K. A., Stav,, S., Sherlock,, M. E., & Breaker,, R. R. (2017). Riboswitch diversity and distribution. RNA, 23(7), 995–1011. https://doi.org/10.1261/rna.061234.117
McCown,, P. J., Liang,, J. J., Weinberg,, Z., & Breaker,, R. R. (2014). Structural, functional, and taxonomic diversity of three PreQ₁ riboswitch classes. Chemistry %26 Biology, 21(7), 880–889. https://doi.org/10.1016/j.chembiol.2014.05.015
McCown,, P. J., Ruszkowska,, A., Kunkler,, C. N., Breger,, K., Hulewicz,, J. P., Wang,, M. C., … Brown,, J. A. (2020). Modified ribonucleosides in biology. WIREs RNA, e1595. https://doi.org/10.1002/wrna.1595
Mefford,, M. A., & Staley,, J. P. (2009). Evidence that U2/U6 helix I promotes both catalytic steps of pre‐mRNA splicing and rearranges in between these steps. RNA, 15(7), 1386–1397. https://doi.org/10.1261/rna.1582609
Mergny,, J. L., Sun,, J. S., Rougee,, M., Montenay‐Garestier,, T., Barcelo,, F., Chomilier,, J., & Helene,, C. (1991). Sequence specificity in triple‐helix formation: Experimental and theoretical studies of the effect of mismatches on triplex stability. Biochemistry, 30(40), 9791–9798. https://doi.org/10.1021/bi00104a031
Meyer,, M. M., Roth,, A., Chervin,, S. M., Garcia,, G. A., & Breaker,, R. R. (2008). Confirmation of a second natural PreQ₁ aptamer class in Streptococcaceae bacteria. RNA, 14(4), 685–695. https://doi.org/10.1261/rna.937308
Mihalusova,, M., Wu,, J. Y., & Zhuang,, X. (2011). Functional importance of telomerase pseudoknot revealed by single‐molecule analysis. Proceedings of the National Academy of Sciences of the United States of America, 108(51), 20339–20344. https://doi.org/10.1073/pnas.1017686108
Mitton‐Fry,, R. M., DeGregorio,, S. J., Wang,, J., Steitz,, T. A., & Steitz,, J. A. (2010). Poly(A) tail recognition by a viral RNA element through assembly of a triple helix. Science, 330(6008), 1244–1247. doi: https://doi.org/10.1126/science.1195858
Mondal,, T., Subhash,, S., Vaid,, R., Enroth,, S., Uday,, S., Reinius,, B., … Kanduri,, C. (2015). MEG3 long noncoding RNA regulates the TGFβ‐ pathway genes through formation of RNA‐DNA triplex structures. Nature Communications, 6, 7743. https://doi.org/10.1038/ncomms8743
Morgan,, A. R., & Wells,, R. D. (1968). Specificity of the three‐stranded complex formation between double‐stranded DNA and single‐stranded RNA containing repeating nucleotide sequences. Journal of Molecular Biology, 37(1), 63–80.
Nakamura,, T. M., Morin,, G. B., Chapman,, K. B., Weinrich,, S. L., Andrews,, W. H., Lingner,, J., … Cech,, T. R. (1997). Telomerase catalytic subunit homologs from fission yeast and human. Science, 277(5328), 955–959. https://doi.org/10.1126/science.277.5328.955
Nawrocki,, E. P., & Eddy,, S. R. (2013). Infernal 1.1: 100‐fold faster RNA homology searches. Bioinformatics, 29(22), 2933–2935. https://doi.org/10.1093/bioinformatics/btt509
Neuner,, E., Frener,, M., Lusser,, A., & Micura,, R. (2018). Superior cellular activities of azido‐ over amino‐functionalized ligands for engineered PreQ₁ riboswitches in E. coli. RNA Biology, 15(10), 1376–1383. https://doi.org/10.1080/15476286.2018.1534526
Nguyen,, T. H. D., Tam,, J., Wu,, R. A., Greber,, B. J., Toso,, D., Nogales,, E., & Collins,, K. (2018). Cryo‐EM structure of substrate‐bound human telomerase holoenzyme. Nature, 557(7704), 190–195. https://doi.org/10.1038/s41586-018-0062-x
Nissen,, P., Ippolito,, J. A., Ban,, N., Moore,, P. B., & Steitz,, T. A. (2001). RNA tertiary interactions in the large ribosomal subunit: The A‐minor motif. Proceedings of the National Academy of Sciences of the United States of America, 98(9), 4899–4903. https://doi.org/10.1073/pnas.081082398081082398
Nissim,, L., Perli,, S. D., Fridkin,, A., Perez‐Pinera,, P., & Lu,, T. K. (2014). Multiplexed and programmable regulation of gene networks with an integrated RNA and CRISPR/Cas toolkit in human cells. Molecular Cell, 54(4), 698–710. https://doi.org/10.1016/j.molcel.2014.04.022
O`Leary,, V. B., Ovsepian,, S. V., Carrascosa,, L. G., Buske,, F. A., Radulovic,, V., Niyazi,, M., … Anastasov,, N. (2015). PARTICLE, a triplex‐forming long ncRNA, regulates locus‐specific methylation in response to low‐dose irradiation. Cell Reports, 11(3), 474–485. https://doi.org/10.1016/j.celrep.2015.03.043
Pendleton,, K. E., Chen,, B., Liu,, K., Hunter,, O. V., Xie,, Y., Tu,, B. P., & Conrad,, N. K. (2017). The U6 snRNA m⁶A methyltransferase METTL16 regulates SAM synthetase intron retention. Cell, 169(5), 824–835.e814. https://doi.org/10.1016/j.cell.2017.05.003
Peselis,, A., & Serganov,, A. (2014). Structure and function of pseudoknots involved in gene expression control. WIREs RNA, 5(6), 803–822. https://doi.org/10.1002/wrna.1247
Pham,, V. V., Salguero,, C., Khan,, S. N., Meagher,, J. L., Brown,, W. C., Humbert,, N., … D`Souza,, V. M. (2018). HIV‐1 Tat interactions with cellular 7SK and viral TAR RNAs identifies dual structural mimicry. Nature Communications, 9(1), 4266. https://doi.org/10.1038/s41467-018-06591-6
Pilch,, D. S., Kirolos,, M. A., & Breslauer,, K. J. (1995). Berenil binding to higher ordered nucleic acid structures: Complexation with a DNA and RNA triple helix. Biochemistry, 34(49), 16107–16124. https://doi.org/10.1021/bi00049a026
Plum,, G. E., & Breslauer,, K. J. (1995). Thermodynamics of an intramolecular DNA triple helix: A calorimetric and spectroscopic study of the pH and salt dependence of thermally induced structural transitions. Journal of Molecular Biology, 248(3), 679–695.
Poiata,, E., Meyer,, M. M., Ames,, T. D., & Breaker,, R. R. (2009). A variant riboswitch aptamer class for S‐adenosylmethionine common in marine bacteria. RNA, 15(11), 2046–2056. https://doi.org/10.1261/rna.1824209
Pradhan,, A. B., Bhuiya,, S., Haque,, L., & Das,, S. (2018). Role of hydroxyl groups in the B‐ring of flavonoids in stabilization of the Hoogsteen paired third strand of poly(U)•poly(A)‐poly(U) triplex. Archives of Biochemistry and Biophysics, 637, 9–20. https://doi.org/10.1016/j.abb.2017.11.008
Qiao,, F., & Cech,, T. R. (2008). Triple‐helix structure in telomerase RNA contributes to catalysis. Nature Structural %26 Molecular Biology, 15(6), 634–640. https://doi.org/10.1038/nsmb.1420
Qu,, G., Kaushal,, P. S., Wang,, J., Shigematsu,, H., Piazza,, C. L., Agrawal,, R. K., … Wang,, H. W. (2016). Structure of a group II intron in complex with its reverse transcriptase. Nature Structural %26 Molecular Biology, 23(6), 549–557. https://doi.org/10.1038/nsmb.3220
Raghunathan,, G., Miles,, H. T., & Sasisekharan,, V. (1995). Symmetry and structure of RNA and DNA triple helices. Biopolymers, 36(3), 333–343. https://doi.org/10.1002/bip.360360308
Rainen,, L. C., & Stollar,, B. D. (1977). Antisera to poly(A)‐poly(U)‐poly(I) contain antibody subpopulations specific for different aspects of the triple helix. Biochemistry, 16(9), 2003–2007. https://doi.org/10.1021/bi00628a038
Ren,, J., & Chaires,, J. B. (1999). Sequence and structural selectivity of nucleic acid binding ligands. Biochemistry, 38(49), 16067–16075. https://doi.org/10.1021/bi992070s
Ren,, J., Rastegari,, B., Condon,, A., & Hoos,, H. H. (2005). HotKnots: Heuristic prediction of RNA secondary structures including pseudoknots. RNA, 11(10), 1494–1504. https://doi.org/10.1261/rna.7284905
Rich,, A., & Watson,, J. D. (1954). Physical studies on ribonucleic acid. Nature, 173(4412), 995–996. https://doi.org/10.1038/173995a0
Rich,, A., & Davies,, D. R. (1956). A new two‐stranded helical structure: Polyadenylic acid and polyuridylic acid. Journal of the American Chemical Society, 78, 3548–3549.
Rivas,, E., & Eddy,, S. R. (1999). A dynamic programming algorithm for RNA structure prediction including pseudoknots. Journal of Molecular Biology, 285(5), 2053–2068. https://doi.org/10.1006/jmbi.1998.2436
Robart,, A. R., Chan,, R. T., Peters,, J. K., Rajashankar,, K. R., & Toor,, N. (2014). Crystal structure of a eukaryotic group II intron lariat. Nature, 514(7521), 193–197. https://doi.org/10.1038/nature13790
Roberts,, R. W., & Crothers,, D. M. (1996). Prediction of the stability of DNA triplexes. Proceedings of the National Academy of Sciences of the United States of America, 93(9), 4320–4325.
Roy,, S., Lammert,, H., Hayes,, R. L., Chen,, B., LeBlanc,, R., Dayie,, T. K., … Sanbonmatsu,, K. Y. (2017). A magnesium‐induced triplex pre‐organizes the SAM‐II riboswitch. PLoS Computational Biology, 13(3), e1005406. https://doi.org/10.1371/journal.pcbi.1005406
Rusling,, D. A., Powers,, V. E., Ranasinghe,, R. T., Wang,, Y., Osborne,, S. D., Brown,, T., & Fox,, K. R. (2005). Four base recognition by triplex‐forming oligonucleotides at physiological pH. Nucleic Acids Research, 33(9), 3025–3032. https://doi.org/10.1093/nar/gki625
Russo,, M., De Lucca,, B., Flati,, T., Gioiosa,, S., Chillemi,, G., & Capranico,, G. (2019). DROPA: DRIP‐seq optimized peak annotator. BMC Bioinformatics, 20(1), 414. https://doi.org/10.1186/s12859-019-3009-9
Ruszkowska,, A., Ruszkowski,, M., Hulewicz,, J. P., Dauter,, Z., & Brown,, J. A. (2020). Molecular structure of a U•A‐U‐rich RNA triple helix with 11 consecutive base triples. Nucleic Acids Research, 48(6), 3304–3314. https://doi.org/10.1093/nar/gkz1222
Schindelin,, H., Zhang,, M., Bald,, R., Furste,, J. P., Erdmann,, V. A., & Heinemann,, U. (1995). Crystal structure of an RNA dodecamer containing the Escherichia coli Shine‐Dalgarno sequence. Journal of Molecular Biology, 249(3), 595–603. https://doi.org/10.1006/jmbi.1995.0321
Semerad,, C. L., & Maher,, L. J., 3rd. (1994). Exclusion of RNA strands from a purine motif triple helix. Nucleic Acids Research, 22(24), 5321–5325. https://doi.org/10.1093/nar/22.24.5321
Senturk Cetin,, N., Kuo,, C. C., Ribarska,, T., Li,, R., Costa,, I. G., & Grummt,, I. (2019). Isolation and genome‐wide characterization of cellular DNA:RNA triplex structures. Nucleic Acids Research, 47(5), 2306–2321. https://doi.org/10.1093/nar/gky1305
Sharma,, E., Sterne‐Weiler,, T., O`Hanlon,, D., & Blencowe,, B. J. (2016). Global mapping of human RNA‐RNA interactions. Molecular Cell, 62(4), 618–626. https://doi.org/10.1016/j.molcel.2016.04.030
Shay,, J. W. (2016). Role of telomeres and telomerase in aging and cancer. Cancer Discovery, 6(6), 584–593. https://doi.org/10.1158/2159-8290.CD-16-0062
Shay,, J. W., & Bacchetti,, S. (1997). A survey of telomerase activity in human cancer. European Journal of Cancer, 33(5), 787–791. https://doi.org/10.1016/S0959-8049(97)00062-2
Shefer,, K., Brown,, Y., Gorkovoy,, V., Nussbaum,, T., Ulyanov,, N. B., & Tzfati,, Y. (2007). A triple helix within a pseudoknot is a conserved and essential element of telomerase RNA. Molecular and Cellular Biology, 27(6), 2130–2143. https://doi.org/10.1128/MCB.01826-06
Sherlock,, M. E., & Breaker,, R. R. (2017). Biochemical validation of a third guanidine riboswitch class in bacteria. Biochemistry, 56(2), 359–363. https://doi.org/10.1021/acs.biochem.6b01271
Singleton,, S. F., & Dervan,, P. B. (1992). Influence of pH on the equilibrium association constants for oligodeoxyribonucleotide‐directed triple helix formation at single DNA sites. Biochemistry, 31(45), 10995–11003. https://doi.org/10.1021/bi00160a008
Sinha,, R., & Kumar,, G. S. (2009). Interaction of isoquinoline alkaloids with an RNA triplex: Structural and thermodynamic studies of berberine, palmatine, and coralyne binding to poly(U)•poly(A)‐poly(U). Journal of Physical Chemistry. B, 113(40), 13410–13420. https://doi.org/10.1021/jp9069515
Smathers,, C. M., & Robart,, A. R. (2019). The mechanism of splicing as told by group II introns: Ancestors of the spliceosome. Biochimica et Biophysica Acta, Gene Regulatory Mechanisms, 1862(11–12), 194390. https://doi.org/10.1016/j.bbagrm.2019.06.001
Smith,, K. D., Shanahan,, C. A., Moore,, E. L., Simon,, A. C., & Strobel,, S. A. (2011). Structural basis of differential ligand recognition by two classes of bis‐(3′‐5′)‐cyclic dimeric guanosine monophosphate‐binding riboswitches. Proceedings of the National Academy of Sciences of the United States of America, 108(19), 7757–7762. https://doi.org/10.1073/pnas.1018857108
Sontheimer,, E. J., Gordon,, P. M., & Piccirilli,, J. A. (1999). Metal ion catalysis during group II intron self‐splicing: Parallels with the spliceosome. Genes %26 Development, 13(13), 1729–1741. https://doi.org/10.1101/gad.13.13.1729
Sontheimer,, E. J., Sun,, S., & Piccirilli,, J. A. (1997). Metal ion catalysis during splicing of premessenger RNA. Nature, 388(6644), 801–805. https://doi.org/10.1038/42068
Souliere,, M. F., Altman,, R. B., Schwarz,, V., Haller,, A., Blanchard,, S. C., & Micura,, R. (2013). Tuning a riboswitch response through structural extension of a pseudoknot. Proceedings of the National Academy of Sciences of the United States of America, 110(35), E3256–E3264. https://doi.org/10.1073/pnas.1304585110
Steitz,, T. A., & Steitz,, J. A. (1993). A general two‐metal‐ion mechanism for catalytic RNA. Proceedings of the National Academy of Sciences of the United States of America, 90(14), 6498–6502. https://doi.org/10.1073/pnas.90.14.6498
Stollar,, B. D., & Raso,, V. (1974). Antibodies recognise specific structures of triple‐helical polynucleotides built on poly(A) or poly(dA). Nature, 250(463), 231–234.
Su,, L., Chen,, L., Egli,, M., Berger,, J. M., & Rich,, A. (1999). Minor groove RNA triplex in the crystal structure of a ribosomal frameshifting viral pseudoknot. Nature Structural Biology, 6(3), 285–292. https://doi.org/10.1038/6722
Sun,, R., Lin,, S. F., Gradoville,, L., & Miller,, G. (1996). Polyadenylylated nuclear RNA encoded by Kaposi sarcoma‐associated herpesvirus. Proceedings of the National Academy of Sciences of the United States of America, 93(21), 11883–11888.
Sunwoo,, H., Dinger,, M. E., Wilusz,, J. E., Amaral,, P. P., Mattick,, J. S., & Spector,, D. L. (2009). MENε/β nuclear‐retained non‐coding RNAs are upregulated upon muscle differentiation and are essential components of paraspeckles. Genome Research, 19(3), 347–359. https://doi.org/10.1101/gr.087775.108
Sussman,, J. L., Holbrook,, S. R., Warrant,, R. W., Church,, G. M., & Kim,, S. H. (1978). Crystal structure of yeast phenylalanine transfer RNA. I. Crystallographic Refinement. Journal of Molecular Biology, 123(4), 607–630. https://doi.org/10.1016/0022-2836(78)90209-7
Szewczak,, A. A., Ortoleva‐Donnelly,, L., Ryder,, S. P., Moncoeur,, E., & Strobel,, S. A. (1998). A minor groove RNA triple helix within the catalytic core of a group I intron. Nature Structural Biology, 5(12), 1037–1042. https://doi.org/10.1038/4146
Tabaska,, J. E., Cary,, R. B., Gabow,, H. N., & Stormo,, G. D. (1998). An RNA folding method capable of identifying pseudoknots and base triples. Bioinformatics, 14(8), 691–699. https://doi.org/10.1093/bioinformatics/14.8.691
Tanaka,, Y., Fujii,, S., Hiroaki,, H., Sakata,, T., Tanaka,, T., Uesugi,, S., … Kyogoku,, Y. (1999). A`‐form RNA double helix in the single crystal structure of r(UGAGCUUCGGCUC). Nucleic Acids Research, 27(4), 949–955. https://doi.org/10.1093/nar/27.4.949
Theimer,, C. A., Blois,, C. A., & Feigon,, J. (2005). Structure of the human telomerase RNA pseudoknot reveals conserved tertiary interactions essential for function. Molecular Cell, 17(5), 671–682. https://doi.org/10.1016/j.molcel.2005.01.017
Thomas,, T. J., Seibold,, J. R., Adams,, L. E., & Hess,, E. V. (1995). Triplex‐DNA stabilization by hydralazine and the presence of anti‐(triplex DNA) antibodies in patients treated with hydralazine. Biochemical Journal, 311(Pt 1), 183–188. https://doi.org/10.1042/bj3110183
Tiwari,, R., Haque,, L., Bhuiya,, S., & Das,, S. (2017). Third strand stabilization of poly(U)•poly(A)‐poly(U) triplex by the naturally occurring flavone luteolin: A multi‐spectroscopic approach. International Journal of Biological Macromolecules, 103, 692–700. https://doi.org/10.1016/j.ijbiomac.2017.05.115
Toor,, N., Keating,, K. S., Taylor,, S. D., & Pyle,, A. M. (2008). Crystal structure of a self‐spliced group II intron. Science, 320(5872), 77–82. https://doi.org/10.1126/science.1153803
Tseng,, C. K., Wang,, H. F., Schroeder,, M. R., & Baumann,, P. (2018). The H/ACA complex disrupts triplex in hTR precursor to permit processing by RRP6 and PARN. Nature Communications, 9(1), 5430. https://doi.org/10.1038/s41467-018-07822-6
Tycowski,, K. T., Shu,, M. D., Borah,, S., Shi,, M., & Steitz,, J. A. (2012). Conservation of a triple‐helix‐forming RNA stability element in noncoding and genomic RNAs of diverse viruses. Cell Reports, 2(1), 26–32. https://doi.org/10.1016/j.celrep.2012.05.020
Tycowski,, K. T., Shu,, M. D., & Steitz,, J. A. (2016). Myriad triple‐helix‐forming structures in the transposable element RNAs of plants and fungi. Cell Reports, 15(6), 1266–1276. https://doi.org/10.1016/j.celrep.2016.04.010
Tzfati,, Y., Knight,, Z., Roy,, J., & Blackburn,, E. H. (2003). A novel pseudoknot element is essential for the action of a yeast telomerase. Genes %26 Development, 17(14), 1779–1788. https://doi.org/10.1101/gad.1099403
Ulyanov,, N. B., Shefer,, K., James,, T. L., & Tzfati,, Y. (2007). Pseudoknot structures with conserved base triples in telomerase RNAs of ciliates. Nucleic Acids Research, 35(18), 6150–6160. https://doi.org/10.1093/nar/gkm660
van Vlack,, E. R., Topp,, S., & Seeliger,, J. C. (2017). Characterization of engineered PreQ₁ riboswitches for inducible gene regulation in mycobacteria. Journal of Bacteriology, 199(6), e00656‐16. https://doi.org/10.1128/JB.00656-16
Varani,, G., & McClain,, W. H. (2000). The G•U wobble base pair. A fundamental building block of RNA structure crucial to RNA function in diverse biological systems. EMBO Reports, 1(1), 18–23. https://doi.org/10.1093/embo-reports/kvd001
Vogan,, J. M., Zhang,, X., Youmans,, D. T., Regalado,, S. G., Johnson,, J. Z., Hockemeyer,, D., & Collins,, K. (2016). Minimized human telomerase maintains telomeres and resolves endogenous roles of H/ACA proteins, TCAB1, and Cajal bodies. Elife, 5, e18221. https://doi.org/10.7554/eLife.18221
Volker,, J., & Klump,, H. H. (1994). Electrostatic effects in DNA triple helices. Biochemistry, 33(45), 13502–13508.
Wan,, R., Yan,, C., Bai,, R., Huang,, G., & Shi,, Y. (2016). Structure of a yeast catalytic step I spliceosome at 3.4‐Å resolution. Science, 353(6302), 895–904. https://doi.org/10.1126/science.aag2235
Wang,, S., Friedman,, A. E., & Kool,, E. T. (1995). Origins of high sequence selectivity: A stopped‐flow kinetics study of DNA/RNA hybridization by duplex‐ and triplex‐forming oligonucleotides. Biochemistry, 34(30), 9774–9784. https://doi.org/10.1021/bi00030a015
Wang,, T., Chen,, C., Larcher,, L. M., Barrero,, R. A., & Veedu,, R. N. (2019). Three decades of nucleic acid aptamer technologies: Lessons learned, progress and opportunities on aptamer development. Biotechnology Advances, 37(1), 28–50. https://doi.org/10.1016/j.biotechadv.2018.11.001
Warda,, A. S., Kretschmer,, J., Hackert,, P., Lenz,, C., Urlaub,, H., Hobartner,, C., … Bohnsack,, M. T. (2017). Human METTL16 is a N⁶‐methyladenosine (m⁶A) methyltransferase that targets pre‐mRNAs and various non‐coding RNAs. EMBO Reports, 18(11), 2004–2014. https://doi.org/10.15252/embr.201744940
Warnasooriya,, C., Ling,, C., Belashov,, I. A., Salim,, M., Wedekind,, J. E., & Ermolenko,, D. N. (2019). Observation of PreQ₁‐II riboswitch dynamics using single‐molecule FRET. RNA Biology, 16(9), 1086–1092. https://doi.org/10.1080/15476286.2018.1536591
Watson,, J. D., & Crick,, F. H. (1953). The structure of DNA. Cold Spring Harbor Symposia on Quantitative Biology, 18, 123–131.
Wilkinson,, M. E., Charenton,, C., & Nagai,, K. (2019). RNA splicing by the spliceosome. Annual Review of Biochemistry, 89, 1.1–1.30. https://doi.org/10.1146/annurev-biochem-091719-064225
Wilusz,, J. E., Freier,, S. M., & Spector,, D. L. (2008). 3′‐end processing of a long nuclear‐retained noncoding RNA yields a tRNA‐like cytoplasmic RNA. Cell, 135(5), 919–932. https://doi.org/10.1016/j.cell.2008.10.012
Wilusz,, J. E., JnBaptiste,, C. K., Lu,, L. Y., Kuhn,, C. D., Joshua‐Tor,, L., & Sharp,, P. A. (2012). A triple helix stabilizes the 3′ ends of long noncoding RNAs that lack poly(A) tails. Genes %26 Development, 26(21), 2392–2407. https://doi.org/10.1101/gad.204438.112gad.204438.112
Wu,, R. A., Upton,, H. E., Vogan,, J. M., & Collins,, K. (2017). Telomerase mechanism of telomere synthesis. Annual Review of Biochemistry, 86, 439–460. https://doi.org/10.1146/annurev-biochem-061516-045019
Xodo,, L. E., Manzini,, G., Quadrifoglio,, F., van der Marel,, G. A., & van Boom,, J. H. (1991). Effect of 5‐methylcytosine on the stability of triple‐stranded DNA—A thermodynamic study. Nucleic Acids Research, 19(20), 5625–5631. https://doi.org/10.1093/nar/19.20.5625
Yamada,, M., Watanabe,, Y., Gootenberg,, J. S., Hirano,, H., Ran,, F. A., Nakane,, T., … Nureki,, O. (2017). Crystal structure of the minimal Cas9 from Campylobacter jejuni reveals the molecular diversity in the CRISPR‐Cas9 systems. Molecular Cell, 65(6), 1109–1121.e1103. https://doi.org/10.1016/j.molcel.2017.02.007
Yan,, C., Hang,, J., Wan,, R., Huang,, M., Wong,, C. C., & Shi,, Y. (2015). Structure of a yeast spliceosome at 3.6‐Å resolution. Science, 349(6253), 1182–1191. https://doi.org/10.1126/science.aac7629
Yan,, C., Wan,, R., Bai,, R., Huang,, G., & Shi,, Y. (2016). Structure of a yeast activated spliceosome at 3.5‐Å resolution. Science, 353(6302), 904–911. https://doi.org/10.1126/science.aag0291
Yang,, S. Y., Lejault,, P., Chevrier,, S., Boidot,, R., Robertson,, A. G., Wong,, J. M. Y., & Monchaud,, D. (2018). Transcriptome‐wide identification of transient RNA G‐quadruplexes in human cells. Nature Communications, 9(1), 4730. https://doi.org/10.1038/s41467-018-07224-8
Yean,, S. L., Wuenschell,, G., Termini,, J., & Lin,, R. J. (2000). Metal‐ion coordination by U6 small nuclear RNA contributes to catalysis in the spliceosome. Nature, 408(6814), 881–884. https://doi.org/10.1038/35048617
Yonkunas,, M. J., & Baird,, N. J. (2019). A highly ordered, nonprotective MALAT1 ENE structure is adopted prior to triplex formation. RNA, 25(8), 975–984. https://doi.org/10.1261/rna.069906.118
Zhan,, H., Xie,, H., Zhou,, Q., Liu,, Y., & Huang,, W. (2018). Synthesizing a genetic sensor based on CRISPR‐Cas9 for specifically killing p53‐deficient cancer cells. ACS Synthetic Biology, 7(7), 1798–1807. https://doi.org/10.1021/acssynbio.8b00202
Zhang,, B., Mao,, Y. S., Diermeier,, S. D., Novikova,, I. V., Nawrocki,, E. P., Jones,, T. A., … Spector,, D. L. (2017). Identification and characterization of a class of MALAT1‐like genomic loci. Cell Reports, 19(8), 1723–1738. https://doi.org/10.1016/j.celrep.2017.05.006
Zhang,, L., Vielle,, A., Espinosa,, S., & Zhao,, R. (2019). RNAs in the spliceosome: Insight from cryo‐EM structures. WIREs RNA, 10(3), e1523. https://doi.org/10.1002/wrna.1523
Zhao,, Z., Senturk,, N., Song,, C., & Grummt,, I. (2018). lncRNA PAPAS tethered to the rDNA enhancer recruits hypophosphorylated CHD4/NuRD to repress rRNA synthesis at elevated temperatures. Genes %26 Development, 32(11–12), 836–848. https://doi.org/10.1101/gad.311688.118
Zhong,, W., Wang,, H., Herndier,, B., & Ganem,, D. (1996). Restricted expression of Kaposi sarcoma‐associated herpesvirus (human herpesvirus 8) genes in Kaposi sarcoma. Proceedings of the National Academy of Sciences of the United States of America, 93(13), 6641–6646.
Zuidema,, D., Van den Berg,, F. M., & Flavell,, R. A. (1978). The isolation of duplex DNA fragments containing (dG‐dC) clusters by chromatography on poly(rC)‐Sephadex. Nucleic Acids Research, 5(7), 2471–2483. https://doi.org/10.1093/nar/5.7.2471

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