Synthesis, NMR kinetics and dynamic structure of a 17-mer heptaloop RNA hairpin carrying a 3-N-methyluridine nucleotide residue in the loop region

References

• Altona, C., & Sundaralingam, M. (1972). Conformational analysis of the sugar ring in nucleosides and nucleotides. New description using the concept of pseudorotation. Journal of the American Chemical Society, 94(23), 8205–8212. https://doi.org/10.1021/ja00778a043
   PubMed Web of Science ®Google Scholar
• Andac, C. A., Miandji, A. M., Hornemann, U., & Noyanalpan, N. (2011). Use of the parmbsc0 force field and trajectory analysis to study the binding of netropsin to the DNA fragment (5’CCAATTGG)2 in the presence of excess NaCl salt in aqueous solution. International Journal of Biological Macromolecules, 48(4), 531–539. https://doi.org/10.1016/j.ijbiomac.2011.02.004
   PubMed Web of Science ®Google Scholar
• Anthis, N. J., & Clore, G. M. (2015). Visualizing transient dark states by NMR Spectroscopy. Quarterly Reviews of Biophysics, 48(1), 35–116. https://doi.org/10.1017/S0033583514000122
   PubMed Web of Science ®Google Scholar
• Auxilien, S., Crain, P. F., Trewyn, R. W., & Grosjean, H. (1996). Mechanism, specificity and general properties of the yeast enzyme catalysing the formation of inosine 34 in the anticodon of transfer RNA. Journal of Molecular Biology, 262(4), 437–458. https://doi.org/10.1006/jmbi.1996.0527
   PubMed Web of Science ®Google Scholar
• Bain, A. D. (2003). Chemical exchange in NMR. Progress in Nuclear Magnetic Resonance Spectroscopy, 43(3-4), 63–103. https://doi.org/10.1016/j.pnmrs.2003.08.001
   Web of Science ®Google Scholar
• Balasubramaian, R., & Seetharamulu, P. (1983). A conformational rationale for the wobble behaviour on the first base of the anticodon triplet in tRNA. Journal of Theoretical Biology, 101(1), 77–86. https://doi.org/10.1016/0022-5193(83)90273-4
   PubMed Web of Science ®Google Scholar
• Barraud, P., Gato, A., Heiss, M., Catala, M., Kellner, S., & Tisné, C. (2019). Time-resolved NMR monitoring of tRNA maturation. Nature Communications, 10(1), 3373. https://doi.org/10.1038/s41467-019-11356-w
   PubMedGoogle Scholar
• Basturea, G. N., & Deutscher, M. P. (2007). Substrate specificity and properties of the Escherichia coli 16S rRNA methyltransferase, RsmE. RNA (New York, N.Y.), 13(11), 1969–1976. https://doi.org/10.1261/rna.700507
   PubMed Web of Science ®Google Scholar
• Basturea, G. N., Rudd, K. E., & Deutscher, M. P. (2006). Identification and characterization of RsmE, the founding member of a new RNA base methyltransferase family. RNA (New York, N.Y.), 12(3), 426–434. https://doi.org/10.1261/rna.2283106
   PubMed Web of Science ®Google Scholar
• Bergonzo, C., & Cheatham, T. E. III, (2015). Improved force field parameters lead to a better description of RNA structure. Journal of Chemical Theory and Computation, 11(9), 3969–3972. https://doi.org/10.1021/acs.jctc.5b00444
   PubMed Web of Science ®Google Scholar
• Bergonzo, C., Henriksen, N. M., Roe, D. R., Swails, J. M., Roitberg, A. E., & Cheatham, T. E. III, (2014). Multidimensional replica exchange molecular dynamics yields a converged ensemble of an RNA Tetranucleotide. Journal of Chemical Theory and Computation, 10(1), 492–499. https://doi.org/10.1021/ct400862k
   PubMed Web of Science ®Google Scholar
• Betz, R. M., & Walker, R. C. (2015). Paramfit: Automated optimization of force field parameters for molecular dynamics simulations. Journal of Computational Chemistry, 36(2), 79–87. https://doi.org/10.1002/jcc.23775
   PubMed Web of Science ®Google Scholar
• Boccaletto, P., Machnicka, M. A., Purta, E., Piatkowski, P., Baginski, B., Wirecki, T. K., de Crécy-Lagard, V., Ross, R., Limbach, P. A., Kotter, A., Helm, M., & Bujnicki, J. M. (2018). MODOMICS: A database of RNA modification pathways. 2017 Update. Nucleic Acids Research, 46(D1), D303–D307. https://doi.org/10.1093/nar/gkx1030
   PubMed Web of Science ®Google Scholar
• Boswell, Z. K., & Latham, M. P. (2019). Methyl-Based NMR spectroscopy methods for uncovering structural dynamics in large proteins and protein complexes. Biochemistry, 58(3), 144–155. https://doi.org/10.1021/acs.biochem.8b00953
   PubMed Web of Science ®Google Scholar
• Byrne, R. T., Konevega, A. L., Rodnina, M. V., & Antson, A. A. (2010). The crystal structure of unmodified tRNAPhe from Escherichia coli. Nucleic Acids Research, 38(12), 4154–4162. https://doi.org/10.1093/nar/gkq133
   PubMed Web of Science ®Google Scholar
• Case, D. A., Ben-Shalom, I. Y., Brozell, S. R., Cerutti, D. S., Cheatham, T. E., Cruzeiro, V. W. D., Darden, T. A., Duke, R. E., Ghoreishi, D., Gilson, M. K., Gohlke, H., Goetz, A. W., Greene, D., Harris, R., Homeyer, N., Huang, Y., Izadi, S., Kovalenko, A., Kurtzman, T., … Kollman, P. A. (2020). AMBER. University of California.
   Google Scholar
• Claesson, C., Lustig, F., Boren, T., Simonsson, C., Barciszewska, M., & Lagerkvist, U. (1995). Glycine codon discrimination and the nucleotide in position 32 of the anticodon loop. Journal of Molecular Biology, 247(2), 191–196. https://doi.org/10.1006/jmbi.1994.0132
   PubMed Web of Science ®Google Scholar
• Connolly, M. L. (1983). Analytical molecular surface calculation. Journal of Applied Crystallography, 16(5), 548–558. https://doi.org/10.1107/S0021889883010985
   Web of Science ®Google Scholar
• Conte, M. R., Conn, G. L., Brown, T., & Lane, A. N. (1997). Conformational properties and thermodynamics of the RNA duplex r(CGCAAAUUUGCG)2: Comparison with the DNA analogue d(CGCAAATTTGCG)2. Nucleic Acids Research, 25(13), 2627–2634. https://doi.org/10.1093/nar/25.13.2627
   PubMed Web of Science ®Google Scholar
• Crick, F. H. (1966). Codon-anticodon pairing: The wobble hypothesis. Journal of Molecular Biology, 19(2), 548–555. https://doi.org/10.1016/s0022-2836(66)80022-0
   PubMed Web of Science ®Google Scholar
• Curran, C. F. (1998). Chapter 27: Modified nucleosides in translation. In H. Grosjean & B. Benne (Eds.), Modification and editing of RNA (pp. 493–516). American Society for Microbiology Press. https://doi.org/10.1128/9781555818296.ch27
   Google Scholar
• Damha, M. J., & Ogilvie, K. K. (1993). Protocols for oligonucleotides and analogs: Synthesis and properties. In S. Agrawal (Ed.), Methods in molecular biology (Vol. 20, pp. 81–114). Humana Press. https://doi.org/10.1385/0-89603-281-7:81
   Google Scholar
• Darden, T., York, D., & Pedersen, L. (1993). Particle mesh Ewald: An N_log(N) method for Ewald sums in large systems. Journal of Chemical Physics, 98(12), 10089–10092. https://doi.org/10.1063/1.464397
   Web of Science ®Google Scholar
• Deb, I., Sarzynska, J., Nilsson, L., & Lahiri, A. (2019). Structural stability of the anticodon stem loop domains of the unmodified yeast and Escherichia coli tRNAPhe: Differing views from different force fields. ACS Omega, 4(2), 3029–3044. https://doi.org/10.1021/acsomega.8b02383
   Web of Science ®Google Scholar
• Dupradeau, F.-Y., Pigache, A., Zaffran, T., Savineau, C., Lelong, R., Grivel, N., Lelong, D., Rosanski, W., & Cieplak, P. (2010). The R.E.D. tools: Advances in RESP and ESP charge derivation and force field library building. Physical Chemistry Chemical Physics : PCCP, 12(28), 7821–7839. https://doi.org/10.1039/c0cp00111b
   PubMed Web of Science ®Google Scholar
• Elias, Y., & Huang, R. H. (2005). Biochemical and structural studies of A-to-I editing by tRNA: A34 deaminases at the wobble position of transfer RNA. Biochemistry, 44(36), 12057–12065. https://doi.org/10.1021/bi050499f
   PubMed Web of Science ®Google Scholar
• Ester, M., Kriegel, H., Sander, J., & Xu, X. (1996). A density-based algorithm for discovering clusters in large spatial databases with noise. In Proceedings of the 2nd International Conference Knowledge Discovery and Data Mining (KDD-96), pp. 226–231. https://doi.org/10.5555/3001460.3001507
   Google Scholar
• Fuller, W., & Hodgson, A. (1967). Conformation of the anticodon loop in tRNA. Nature, 215(5103), 817–821. https://doi.org/10.1038/215817a0
   PubMed Web of Science ®Google Scholar
• Gerber, A. P., & Keller, W. (1999). An adenosine deaminase that generates inosine at the wobble position of tRNAs. Science (New York, N.Y.), 286(5442), 1146–1149. https://doi.org/10.1126/science.286.5442.1146
   PubMed Web of Science ®Google Scholar
• Gilbert, W. (1986). Origin of life—the RNA world. Nature, 319(6055), 618–618. https://doi.org/10.1038/319618a0
   PubMed Web of Science ®Google Scholar
• Gutell, R. R., Cannone, J. J., Konings, D., & Gautheret, D. (2000). Predicting U-turns in ribosomal RNA with comparative sequence analysis. Journal of Molecular Biology, 300(4), 791–803. https://doi.org/10.1006/jmbi.2000.3900
   PubMed Web of Science ®Google Scholar
• Haines, J. A., Reese, C. B., & Todd, L. (1964). The methylation of nucleosides and mononucleotides with diazomethane. Journal of the Chemical Society (Resumed), Part II, 1406–1412. https://doi.org/10.1039/jr9640001406
   Google Scholar
• Hakimelahi, G. H., Proba, Z. A., & Ogilvie, K. K. (1982). New catalysts and procedures for the dimethoxytritylation and selective silylation of ribonucleosides. Canadian Journal of Chemistry, 60(9), 1106–1113. https://doi.org/10.1139/v82-165
   Web of Science ®Google Scholar
• Izadi, S., Anandakrishnan, R., & Onufriev, A. V. (2014). Building water models: A different approach. The Journal of Physical Chemistry Letters, 5(21), 3863–3871. https://doi.org/10.1021/jz501780a
   PubMed Web of Science ®Google Scholar
• Joyce, G. F. (2002). The antiquity of RNA-based evolution. Nature, 418(6894), 214–221. https://doi.org/10.1038/418214a
   PubMed Web of Science ®Google Scholar
• Joyce, G. F., & Szostak, J. W. (2018). Protocells and RNA self-replication. Cold Spring Harbor Perspectives in Biology, 10(9), a034801. https://doi.org/10.1101/cshperspect.a034801
   PubMed Web of Science ®Google Scholar
• Jukes, T. H. (1973). Possibilities for the evolution of the genetic code from a preceding form. Nature, 246(5427), 22–26. https://doi.org/10.1038/246022a0
   PubMed Web of Science ®Google Scholar
• Knapp, B., Ospina, L., & Deane, C. M. (2018). Avoiding false positive conclusions in molecular simulation: The importance of replicas. Journal of Chemical Theory and Computation, 14(12), 6127–6138. https://doi.org/10.1021/acs.jctc.8b00391
   PubMed Web of Science ®Google Scholar
• Lavery, R., Moakher, M., Maddocks, J. H., Petkeviciute, D., & Zakrzewska, K. (2009). Conformational analysis of nucleic acids revisited: Curves+. Nucleic Acids Research, 37(17), 5917–5929. https://doi.org/10.1093/nar/gkp608
   PubMed Web of Science ®Google Scholar
• Ledoux, S., Olejniczak, M., & Uhlenbeck, O. C. (2009). A sequence element that tunes Escherichia coli tRNAAlaGGC to ensure accurate decoding. Nature Structural & Molecular Biology, 16(4), 359–364. https://doi.org/10.1038/nsmb.1581
   PubMed Web of Science ®Google Scholar
• Lu, X.-J., & Olson, W. K. (2003). 3DNA: A software package for the analysis, rebuilding and visualization of three-dimensional nucleic acid structures. Nucleic Acids Research, 31(17), 5108–5121. https://doi.org/10.1093/nar/gkg680
   PubMed Web of Science ®Google Scholar
• Mikkelsen, N. E., Johansson, K., Virtanen, A., & Kirsebom, L. A. (2001). Aminoglycoside binding displaces a divalent metal ion in a tRNA-neomycin B complex. Nature Structural Biology, 8(6), 510–514. https://doi.org/10.1038/88569
   PubMedGoogle Scholar
• Morgado, C. A., Jurečka, P., Svozil, D., Hobza, P., & Šponer, J. (2009). Balance of attraction and repulsion in nucleic-acid base stacking: CCSD(T)/complete-basis-set-limit calculations on uracil dimer and a comparison with the force-field description. Journal of Chemical Theory and Computation, 5(6), 1524–1544. https://doi.org/10.1021/ct9000125
   PubMed Web of Science ®Google Scholar
• Morgado, C. A., Jurečka, P., Svozil, D., Hobza, P., & Šponer, J. (2010). Reference MP2/CBS and CCSD(T) quantum-chemical calculations on stacked adenine dimers. Comparison with DFT-D, MP2.5, SCS(MI)-MP2, M06-2X, CBS(SCS-D) and force field descriptions. Physical Chemistry Chemical Physics : PCCP, 12(14), 3522–3534. https://doi.org/10.1039/B924461A
   PubMed Web of Science ®Google Scholar
• Murakami, H., Ohta, A., & Suga, H. (2009). Bases in the anticodon loop of tRNA(Ala)(GGC) prevent misreading. Nature Structural & Molecular Biology, 16(4), 353–358. https://doi.org/10.1038/nsmb.1580
   PubMed Web of Science ®Google Scholar
• Neidle, S. (Ed.). (2008). Principles of nucleic acid structure. Academic Press. https://doi.org/10.1016/B978-0-12-369507-9.X5001-8
   Google Scholar
• Ogg, R. J., Kingsley, P. B., & Taylor, J. S. (1994). WET, a T1- and B1-insensitive water-suppression method for in vivo localized 1H NMR spectroscopy. Journal of Magnetic Resonance. Series B, 104(1), 1–10. https://doi.org/10.1006/jmrb.1994.1048
   PubMedGoogle Scholar
• Olejniczak, M., & Uhlenbeck, O. C. (2006). tRNA residues that have coevolved with their anticodon to ensure uniform and accurate codon recognition. Biochimie, 88(8), 943–950. https://doi.org/10.1016/j.biochi.2006.06.005
   PubMed Web of Science ®Google Scholar
• Olson, W. K., & Sussman, J. L. (1982). How flexible is the furanose ring? A comparison of experimental and theoretical studies. Journal of the American Chemical Society, 104(1), 270–278. https://doi.org/10.1021/ja00365a049
   Web of Science ®Google Scholar
• Orgel, L. E. (1989). Was RNA the first genetic polymer? Evolutionary Tinkering in Gene Expression, 169, 215–224. https://doi.org/10.1007/978-1-4684-5664-6_20
   Google Scholar
• Palmer, A. G., Kroenke, C. D., & Loria, J.P. (2001). Nuclear magnetic resonance methods for quantifying microsecond-to-millisecond motions in biological macromolecules. Methods in Enzymology, 339, 204–238. https://doi.org/10.1016/S0076-6879(01)39315-1
   PubMed Web of Science ®Google Scholar
• Pastor, R. W., Brooks, B. R., & Szabo, A. (1988). An analysis of the accuracy of Langevin and molecular dynamics algorithms. Molecular Physics, 65(6), 1409–1419. https://doi.org/10.1080/00268978800101881
   Web of Science ®Google Scholar
• Pernod, K., Schaeffer, L., Chicher, J., Hok, E., Rick, C., Geslain, R., Eriani, G., Westhof, E., Ryckelynck, M., & Martin, F. (2020). The nature of the purine at position 34 in tRNAs of 4-codon boxes is correlated with nucleotides at positions 32 and 38 to maintain decoding fidelity. Nucleic Acids Research, 48(11), 6170–6183. https://doi.org/10.1093/nar/gkaa221
   PubMed Web of Science ®Google Scholar
• Pettersen, E. F., Goddard, T. D., Huang, C. C., Couch, G. S., Greenblatt, D. M., Meng, E. C., & Ferrin, T. E. (2004). UCSF Chimera–a visualization system for exploratory research and analysis. Journal of Computational Chemistry, 25(13), 1605–1612. https://doi.org/10.1002/jcc.20084
   PubMed Web of Science ®Google Scholar
• Preparation of Diazomethane. Aldrichimica Acta 1983; 16: NO.1.41. https://www.sigmaaldrich.com/deepweb/assets/sigmaaldrich/marketing/global/documents/187/633/acta-vol16.pdf
   Google Scholar
• Quigley, G. J., & Rich, A. (1976). Structural domains of transfer RNA molecules. Science (New York, N.Y.), 194(4267), 796–806. https://doi.org/10.1126/science.790568
   PubMed Web of Science ®Google Scholar
• Robertson, M. P., & Joyce, G. F. (2012). The origins of the RNA world. Cold Spring Harbor Perspectives in Biology, 4(5), a003608–a003608. https://doi.org/10.1101/cshperspect.a003608
   PubMed Web of Science ®Google Scholar
• Roe, D. R., & Cheatham, T. E. III, (2018). Parallelization of CPPTRAJ enables large scale analysis of molecular dynamics trajectory data. Journal of Computational Chemistry, 39(25), 2110–2117. https://doi.org/10.1002/jcc.25382
   PubMed Web of Science ®Google Scholar
• Roe, D. R., Bergonzo, C., & Cheatham, T. E. III, (2014). Evaluation of enhanced sampling provided by accelerated molecular dynamics with Hamiltonian replica exchange methods. The Journal of Physical Chemistry B, 118(13), 3543–3552. https://doi.org/10.1021/jp4125099
   PubMed Web of Science ®Google Scholar
• Ruschak, A. M., & Kay, L. E. (2010). Methyl groups as probes of supra-molecular structure, dynamics and function. Journal of Biomolecular NMR, 46(1), 75–87. https://doi.org/10.1007/s10858-009-9376-1
   PubMed Web of Science ®Google Scholar
• Ryckaert, J. P., Ciccotti, G., & Berendsen, H. J. C. (1977). Numerical integration of the cartesian equations of motion of a system with constraints: Molecular dynamics of n-alkanes. Journal of Computational Physics. 23(3), 327–341. https://doi.org/10.1016/0021-9991(77)90098-5
   Web of Science ®Google Scholar
• Saint-Léger, A., Bello, C., Dans, P. D., Torres, A. G., Novoa, E. M., Camacho, N., Orozco, M., Kondrashov, F. A., & De Pouplana, L. R. (2016). Saturation of recognition elements blocks evolution of new tRNA identities. Science Advances, 2(4), e1501860. https://doi.org/10.1126/sciadv.1501860
   PubMed Web of Science ®Google Scholar
• Scaringe, S. A., Francklyn, C., & Usman, U. (1990). Chemical synthesis of biologically active oligonucleotides using beta-cyanoethyl protected ribonucleoside phosphoramidites. Nucleic Acids Research, 18(18), 5433–5441. https://doi.org/10.1093/nar/18.18.5433
   PubMed Web of Science ®Google Scholar
• Shao, J., Tanner, S. W., Thompson, N., & Cheatham, T. E. (2007). Clustering molecular dynamics trajectories: 1. Characterizing the performance of different clustering algorithms. Journal of Chemical Theory and Computation, 3(6), 2312–2334. https://doi.org/10.1021/ct700119m
   PubMed Web of Science ®Google Scholar
• Sharma, S., Yang, J., Düttmann, S., Watzinger, P., Kötter, P., & Entian, K.-D. (2014). Identification of novel methyltransferases, Bmt5 and Bmt6, responsible for the m3U methylations of 25S rRNA in Saccharomyces cerevisiae. Nucleic Acids Research, 42(5), 3246–3260. https://doi.org/10.1093/nar/gkt1281
   PubMed Web of Science ®Google Scholar
• Singh, U. C., & Kollman, P. A. (1984). An approach to computing electrostatic charges for molecules. Journal of Computational Chemistry, 5(2), 129–145. https://doi.org/10.1002/jcc.540050204
   Web of Science ®Google Scholar
• Szostak, J. W. (2017). The narrow road to the deep past: In search of the chemistry of the origin of life. Angewandte Chemie (International ed. in English), 56(37), 11037–11043. https://doi.org/10.1002/anie.201704048)
   PubMed Web of Science ®Google Scholar
• Tan, D., Piana, S., Dirks, R. M., & Shaw, D. E. (2018). RNA force field with accuracy comparable to state-of-the-art protein force fields. Proceedings of the National Academy of Sciences of the United States of America, 115(7), E1346–E1355. https://doi.org/10.1073/pnas.1713027115
   PubMed Web of Science ®Google Scholar
• Wang, J., Wolf, R. M., Caldwell, J. W., Kollman, P. A., & Case, D. A. (2004). Development and testing of a general amber force field. Journal of Computational Chemistry, 25(9), 1157–1174. https://doi.org/10.1002/jcc.20035
   PubMed Web of Science ®Google Scholar
• Werner, H. J., Manby, F. R., & Knowles, P. J. (2003). Fast linear scaling second-order Møller-Plesset perturbation theory (MP2) using local and density fitting approximations. Journal of Chemical Physics. 118(18), 8149–8160. https://doi.org/10.1063/1.1564816
   Web of Science ®Google Scholar
• Wolf, J., Gerber, A. P., & Keller, W. (2002). tadA, an essential tRNA-specific adenosine deaminase from Escherichia coli. The EMBO Journal, 21(14), 3841–3851. https://doi.org/10.1093/emboj/cdf362
   PubMed Web of Science ®Google Scholar
• Yildirim, I., Kennedy, S. D., Stern, H. A., Hart, J. M., Kierzek, R., & Turner, D. H. (2012). Revision of AMBER torsional parameters for RNA improves free energy predictions for tetramer duplexes with GC and iGiC base pairs. Journal of Chemical Theory and Computation, 8(1), 172–181. https://doi.org/10.1021/ct200557r
   PubMed Web of Science ®Google Scholar
• Zgarbová, M., Otyepka, M., Šponer, J., Mládek, A., Banáš, P., Cheatham, T. E., III, & Jurečka, P. (2011). Refinement of the Cornell et al. nucleic acids force field based on reference quantum chemical calculations of glycosidic torsion profiles. Journal of Chemical Theory and Computation, 7(9), 2886–2902. https://doi.org/10.1021/ct200162x
   PubMed Web of Science ®Google Scholar