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Research Articles

Assessment of tools for RNA secondary structure prediction and extraction: a final-user perspective

ORCID Icon, ORCID Icon, ORCID Icon, ORCID Icon & ORCID Icon
Pages 6917-6936 | Received 04 Mar 2022, Accepted 09 Aug 2022, Published online: 15 Sep 2022

References

  • Akiyama, B. M., Laurence, H. M., Massey, A. R., Costantino, D. A., Xie, X., Yang, Y., Shi, P.-Y., Nix, J. C., Beckham, J. D., & Kieft, J. S. (2016). Zika virus produces noncoding RNAs using a multi-pseudoknot structure that confounds a cellular exonuclease. Science, 354(6316), 1148–1152. https://doi.org/10.1126/science.aah3963
  • Antczak, M., Popenda, M., Zok, T., Sarzynska, J., Ratajczak, T., Tomczyk, K., Walenty Adamiak, R., & Szachniuk, M. (2016). New functionality of RNA composer: Application to shape the axis of miR160 precursor structure. Acta Biochimica Polonica, 63(4), 737–744.
  • Antczak, M., Zok, T., Popenda, M., Lukasiak, P., Adamiak, R. W., Blazewicz, J., & Szachniuk, M. (2014). RNApdbee – A webserver to derive secondary structures from pdb files of knotted and unknotted RNAs. Nucleic Acids Research, 42(Web Server issue), W368–W372. https://doi.org/10.1093/nar/gku330
  • Arun, G., Aggarwal, D., & Spector, D. L. (2020). MALAT1 long non-coding RNA: Functional implications. Non-Coding RNA, 6(2), 22. https://doi.org/10.3390/ncrna6020022
  • Berman, H. M., Westbrook, J., Feng, Z., Gilliland, G., Bhat, T. N., Weissig, H., Shindyalov, I. N., & Bourne, P. E. (2000). The Protein Data Bank. Nucleic Acids Research, 28(1), 235–242. https://doi.org/10.1093/nar/28.1.235
  • 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 & Molecular Biology, 21(7), 633–640. https://doi.org/10.1038/nsmb.2844
  • Butcher, S. E., & Pyle, A. M. (2011). The molecular interactions that stabilize RNA tertiary structure: RNA motifs, patterns, and networks. Accounts of Chemical Research, 44(12), 1302–1311. https://doi.org/10.1021/ar200098t
  • Cech, T. R., & Steitz, J. A. (2014). The noncoding RNA revolution–trashing old rules to forge new ones. Cell, 157(1), 77–94. https://doi.org/10.1016/j.cell.2014.03.008
  • Cerase, A., & Tartaglia, G. G. (2020). Long non-coding RNA-polycomb intimate rendezvous. Open Biology, 10(9), 200126. https://doi.org/10.1098/rsob.200126
  • Condon, A., Davy, B., Rastegari, B., Zhao, S., & Tarrant, F. (2004). Classifying RNA pseudoknotted structures. Theoretical Computer Science, 320(1), 35–50. https://doi.org/10.1016/j.tcs.2004.03.042
  • Costa, M., Walbott, H., Monachello, D., Westhof, E., & Michel, F. (2016). Crystal structures of a group II intron lariat primed for reverse splicing. Science, 354(6316), aaf9258-1, aaf9258-7. https://doi.org/10.1126/science.aaf9258
  • Cruz, J. A., Blanchet, M.-F., Boniecki, M., Bujnicki, J. M., Chen, S.-J., Cao, S., Das, R., Ding, F., Dokholyan, N. V., Flores, S. C., Huang, L., Lavender, C. A., Lisi, V., Major, F., Mikolajczak, K., Patel, D. J., Philips, A., Puton, T., Santalucia, J., … Westhof, E. (2012). RNA-puzzles: A CASP-like evaluation of RNA three-dimensional structure prediction. RNA, 18(4), 610–625. https://doi.org/10.1261/rna.031054.111
  • Dam, E. T., Pleij, K., & Draper, D. (1992). Structural and functional aspects of RNA pseudoknots. Biochemistry, 31(47), 11665–11676. https://doi.org/10.1021/bi00162a001
  • Danaee, P., Rouches, M., Wiley, M., Deng, D., Huang, L., & Hendrix, D. (2018). bpRNA: Large-scale automated annotation and analysis of RNA secondary structure. Nucleic Acids Research, 46(11), 5381–5394. https://doi.org/10.1093/nar/gky285
  • Darty, K., Denise, A., & Ponty, Y. (2009). VARNA: Interactive drawing and editing of the RNA secondary structure. Bioinformatics, 25(15), 1974–1975. https://doi.org/10.1093/bioinformatics/btp250
  • DasGupta, S., Suslov, N. B., & Piccirilli, J. A. (2017). Structural basis for substrate helix remodeling and cleavage loop activation in the varkud satellite ribozyme. Journal of the American Chemical Society, 139(28), 9591–9597. https://doi.org/10.1021/jacs.7b03655
  • Dawson, W. K., Fujiwara, K., & Kawai, G. (2007). Prediction of RNA pseudoknots using heuristic modeling with mapping and sequential folding. PLoS One. 2(9), e905. https://doi.org/10.1371/journal.pone.0000905
  • Ding, Y. E. (2006). Statistical and Bayesian approaches to RNA secondary structure prediction. RNA, 12(3), 323–331. https://doi.org/10.1261/rna.2274106
  • Do, C. B., Foo, C.-S., & Batzoglou, S. (2008). A max-margin model for efficient simultaneous alignment and folding of RNA sequences. Bioinformatics, 24(13), i68–i76. https://doi.org/10.1093/bioinformatics/btn177
  • Ganguly, A., Weissman, B. P., Giese, T. J., Li, N.-S., Hoshika, S., Rao, S., Benner, S. A., Piccirilli, J. A., & York, D. M. (2020). Confluence of theory and experiment reveals the catalytic mechanism of the Varkud satellite ribozyme. Nature Chemistry, 12(2), 193–201. https://doi.org/10.1038/s41557-019-0391-x
  • Gardner, P. P., & Giegerich, R. (2004). A comprehensive comparison of comparative RNA structure prediction approaches. BMC Bioinformatics, 5(1), 140–118. https://doi.org/10.1186/1471-2105-5-140
  • Gendron, P., Lemieux, S., & Major, F. (2001). Quantitative analysis of nucleic acid three-dimensional structures. Journal of Molecular Biology, 308(5), 919–936. https://doi.org/10.1006/jmbi.2001.4626
  • Geraets, J. A., Pothula, K. R., & Schröder, G. F. (2020). Integrating Cryo-EM and NMR data. Current Opinion in Structural Biology, 61, 173–181. https://doi.org/10.1016/j.sbi.2020.01.008
  • Goyal, B., Yadav, S. R. M., Awasthee, N., Gupta, S., Kunnumakkara, A. B., & Gupta, S. C. (2021). Diagnostic, prognostic, and therapeutic significance of long non-coding RNA MALAT1 in cancer. Biochimica et Biophysica Acta (BBA)-Reviews on Cancer, 1875(2), 188502. https://doi.org/10.1016/j.bbcan.2021.188502
  • Gruber, A. R., Lorenz, R., Bernhart, S. H., Neuböck, R., & Hofacker, I. L. (2008). The vienna RNA websuite. Nucleic Acids Research, 36(Web Server issue), W70–W74. https://doi.org/10.1093/nar/gkn188
  • Hamada, M., Kiryu, H., Sato, K., Mituyama, T., & Asai, K. (2009). Prediction of RNA secondary structure using generalized centroid estimators. Bioinformatics, 25(4), 465–473. https://doi.org/10.1093/bioinformatics/btn601
  • Hofacker, I. L. (2009). RNA secondary structure analysis using the Vienna RNA package. Current Protocols in Bioinformatics, 26(1), 12–12. https://doi.org/10.1002/0471250953.bi1202s26
  • Humphrey, W., Dalke, A., & Schulten, K. (1996). VMD – Visual molecular dynamics. Journal of Molecular Graphics, 14(1), 33–38. https://doi.org/10.1016/0263-7855(96)00018-5
  • Janssen, S., & Giegerich, R. (2015). The RNA shapes studio. Bioinformatics, 31(3), 423–425. https://doi.org/10.1093/bioinformatics/btu649
  • Jumper, J., Evans, R., Pritzel, A., Green, T., Figurnov, M., Ronneberger, O., Tunyasuvunakool, K., Bates, R., Žídek, A., Potapenko, A., Bridgland, A., Meyer, C., Kohl, S. A. A., Ballard, A. J., Cowie, A., Romera-Paredes, B., Nikolov, S., Jain, R., Adler, J., … Hassabis, D. (2021). Highly accurate protein structure prediction with AlphaFold. Nature, 596(7873), 583–589. https://doi.org/10.1038/s41586-021-03819-2
  • Kalvari, I., Nawrocki, E. P., Argasinska, J., Quinones-Olvera, N., Finn, R. D., Bateman, A., & Petrov, A. I. (2018). Non-coding RNA analysis using the Rfam database. Current Protocols in Bioinformatics, 62(1), e51. https://doi.org/10.1002/cpbi.51
  • Keane, S. C., Heng, X., Lu, K., Kharytonchyk, S., Ramakrishnan, V., Carter, G., Barton, S., Hosic, A., Florwick, A., Santos, J., Bolden, N. C., McCowin, S., Case, D. A., Johnson, B. A., Salemi, M., Telesnitsky, A., & Summers, M. F. (2015). Structure of the HIV-1 RNA packaging signal. Science, 348(6237), 917–921. https://doi.org/10.1126/science.aaa9266
  • Kings Oluoch, I., Akalin, A., Vural, Y., & Canbay, Y. (2018). A review on RNA secondary structure prediction algorithms [Paper presentation]. 2018 InteRNAtional Congress on Big Data, Deep Learning and Fighting Cyber Terrorism (IBIGDELFT), 18–23. IEEE, https://doi.org/10.1109/IBIGDELFT.2018.8625347
  • Kotar, A., Foley, H. N., Baughman, K. M., & Keane, S. C. (2020). Advanced approaches for elucidating structures of large RNAs using NMR spectroscopy and complementary methods. Methods, 183, 93–107. https://doi.org/10.1016/j.ymeth.2020.01.009
  • Laing, C., & Schlick, T. (2011). Computational approaches to RNA structure prediction, analysis, and design. Current Opinion in Structural Biology, 21(3), 306–318. https://doi.org/10.1016/j.sbi.2011.03.015
  • Leontis, N. B., & Westhof, E. (2001). Geometric nomenclature and classification of RNA base pairs. RNA, 7(4), 499–512. https://doi.org/10.1017/s1355838201002515
  • Leontis, N. B., & Westhof, E. (2003). Analysis of RNA motifs. Current Opinion in Structural Biology, 13(3), 300–308. https://doi.org/10.1016/s0959-440x(03)00076-9
  • Li, B., Cao, Y., Westhof, E., & Miao, Z. (2020). Advances in RNA 3D structure modeling using experimental data. Frontiers in Genetics, 11, 574485–1, 574485–19.
  • 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
  • Lu, X.-J., Bussemaker, H. J., & Olson, W. K. (2015). DSSR: an integrated software tool for dissecting the spatial structure of RNA. Nucleic Acids Research, 43(21), e142–e142. https://doi.org/10.1093/nar/gkv716
  • Martinez-Zapien, D., Legrand, P., McEwen, A. G., Proux, F., Cragnolini, T., Pasquali, S., & Dock-Bregeon, A.-C. (2017). The crystal structure of the 5′ functional domain of the transcription riboregulator 7SK. Nucleic Acids Research, 45(6), 3568–3579. https://doi.org/10.1093/nar/gkw1351
  • Miao, Z., & Westhof, E. (2017). RNA structure: Advances and assessment of 3D structure prediction. Annual Review of Biophysics, 46, 483–503. https://doi.org/10.1146/annurev-biophys-070816-034125
  • Miao, Z., Adamiak, R. W., Antczak, M., Batey, R. T., Becka, A. J., Biesiada, M., Boniecki, M. J., Bujnicki, J. M., Chen, S.-J., Cheng, C. Y., Chou, F.-C., Ferré-D'Amaré, A. R., Das, R., Dawson, W. K., Ding, F., Dokholyan, N. V., Dunin-Horkawicz, S., Geniesse, C., Kappel, K., … Westhof, E. (2017). RNA-puzzles round III: 3D RNA structure prediction of five riboswitches and one ribozyme. RNA, 23(5), 655–672. https://doi.org/10.1261/rna.060368.116
  • Miao, Z., Adamiak, R. W., Antczak, M., Boniecki, M. J., Bujnicki, J., Chen, S.-J., Cheng, C. Y., Cheng, Y., Chou, F.-C., Das, R., Dokholyan, N. V., Ding, F., Geniesse, C., Jiang, Y., Joshi, A., Krokhotin, A., Magnus, M., Mailhot, O., Major, F., … Westhof, E. (2020). RNA-Puzzles round IV: 3D structure predictions of four ribozymes and two aptamers. RNA, 26(8), 982–995. https://doi.org/10.1261/rna.075341.120
  • Miao, Z., Adamiak, R. W., Blanchet, M.-F., Boniecki, M., Bujnicki, J. M., Chen, S.-J., Cheng, C., Chojnowski, G., Chou, F.-C., Cordero, P., Cruz, J. A., Ferré-D'Amaré, A. R., Das, R., Ding, F., Dokholyan, N. V., Dunin-Horkawicz, S., Kladwang, W., Krokhotin, A., Lach, G., … Westhof, E. (2015). RNA-puzzles round II: Assessment of RNA structure prediction programs applied to three large RNA structures. RNA, 21(6), 1066–1084. https://doi.org/10.1261/rna.049502.114
  • Pérard, J., Leyrat, C., Baudin, F., Drouet, E., & Jamin, M. (2013). Structure of the full-length HCV IRES in solution. Nature Communications, 4(1), 1–11. https://doi.org/10.1038/ncomms2611
  • Pleij, C. W. (1994). RNA pseudoknots. Current Opinion in Structural Biology, 4(3), 337–344. https://doi.org/10.1016/S0959-440X(94)90101-5
  • Pleij, C. W. A., & Bosch, L. (1989). RNA pseudoknot: Structure, detection, and prediction. In Dahlberg, J. E., & Abelson, J. N. (Eds.), RNA Processing Part A: General Methods. In Methods in enzymology (Vol. 180, pp. 289–303). Elsevier. https://doi.org/10.1016/0076-6879(89)80107-7
  • Popenda, M., Szachniuk, M., Antczak, M., Purzycka, K. J., Lukasiak, P., Bartol, N., Blazewicz, J., & Adamiak, R. W. (2012). Automated 3D structure composition for large RNAs. Nucleic Acids Research, 40(14), e112. https://doi.org/10.1093/nar/gks339
  • Puton, T., Kozlowski, L. P., Rother, K. M., & Bujnicki, J. M. (2013). CompaRNA: A server for continuous benchmarking of automated methods for RNA secondary structure prediction. Nucleic Acids Research, 41(7), 4307–4323. https://doi.org/10.1093/nar/gkt101
  • Quade, N., Boehringer, D., Leibundgut, M., van den Heuvel, J., & Ban, N. (2015). Joop Van Den Heuvel, and Nenad Ban. Cryo-EM structure of hepatitis C virus IRES bound to the human ribosome at 3.9-å resolution. Nature Communications, 6(1), 1–9. https://doi.org/10.1038/ncomms8646
  • Reidys, C. M., Huang, F. W., Andersen, J. E., Penner, R. C., Stadler, P. F., & Nebel, M. E. (2011). Topology and prediction of RNA pseudoknots. Bioinformatics, 27(8), 1076–1085. https://doi.org/10.1093/bioinformatics/btr090
  • Reinharz, V., Soulé, A., Westhof, E., Waldispühl, J., & Denise, A. (2018). Mining for recurrent long-range interactions in RNA structures reveals embedded hierarchies in network families. Nucleic Acids Research, 46(8), 3841–3851. https://doi.org/10.1093/nar/gky197
  • Renumber residue numbers in pdb file. http://www.canoz.com/sdh/renumberpdbchain.pl
  • Reuter, J. S., & Mathews, D. H. (2010). RNAstructure: Software for RNA secondary structure prediction and analysis. BMC Bioinformatics, 11(1), 1–9. https://doi.org/10.1186/1471-2105-11-129
  • Rivas, M., & Fox, G. E. (2022). Nonstandard RNA/RNA interactions likely enhance folding and stability of segmented ribosomes. RNA, 28(3), 340–352. https://doi.org/10.1261/rna.079006.121
  • 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
  • Rother, M., Rother, K., Puton, T., & Bujnicki, J. M. (2011). ModeRNA: A tool for comparative modeling of RNA 3D structure. Nucleic Acids Research, 39(10), 4007–4022. https://doi.org/10.1093/nar/gkq1320
  • Saibil, H. R. (2022). Cryo-EM in molecular and cellular biology. Molecular Cell, 82(2), 274–284. https://doi.org/10.1016/j.molcel.2021.12.016
  • Salerno, D., Chiodo, L., Alfano, V., Floriot, O., Cottone, G., Paturel, A., Pallocca, M., Plissonnier, M.-L., Jeddari, S., Belloni, L., Zeisel, M., Levrero, M., & Guerrieri, F. (2020). Hepatitis B protein HBx binds the DLEU2 lncRNA to sustain cccDNA and host cancer-related gene transcription. Gut, 69(11), 2016–2024. https://doi.org/10.1136/gutjnl-2019-319637
  • Sarver, M., Zirbel, C. L., Stombaugh, J., Mokdad, A., & Leontis, N. B. (2008). FR3D: finding local and composite recurrent structural motifs in RNA 3D structures. Journal of Mathematical Biology, 56(1-2), 215–252.
  • Sato, K., Hamada, M., Asai, K., & Mituyama, T. (2009). CENTROIDFOLD: A web server for RNA secondary structure prediction. Nucleic Acids Research, 37(Web Server issue), W277–W280.
  • Sato, K., Kato, Y., Hamada, M., Akutsu, T., & Asai, K. (2011). IPknot: Fast and accurate prediction of RNA secondary structures with pseudoknots using integer programming. Bioinformatics, 27(13), i85–i93.
  • Schrödinger, LLC. (2021, November). The PyMOL Molecular Graphics System, version 2.5.2.
  • Seetin, M. G., & Mathews, D. H. (2012). RNA structure prediction: An overview of methods. In Keiler, K. (Ed.), Bacterial regulatory RNA. In Methods in Molecular Biology (Vol. 905, pp. 99–122). Totowa, NJ: Humana Press. https://doi.org/10.1007/978-1-61779-949-5_8
  • Shapiro, B. A., Yingling, Y. G., Kasprzak, W., & Bindewald, E. (2007). Bridging the gap in RNA structure prediction. Current Opinion in Structural Biology, 17(2), 157–165. https://doi.org/10.1016/j.sbi.2007.03.001
  • Singh, J., Hanson, J., Paliwal, K., & Zhou, Y. (2019). RNA secondary structure prediction using an ensemble of two-dimensional deep neural networks and transfer learning. Nature Communications, 10(1), 1–13. https://doi.org/10.1038/s41467-019-13395-9
  • Somarowthu, S., Legiewicz, M., Chillón, I., Marcia, M., Liu, F., & Pyle, A. M. (2015). HOTAIR forms an intricate and modular secondary structure. Molecular Cell, 58(2), 353–361. https://doi.org/10.1016/j.molcel.2015.03.006
  • Sperschneider, J., & Datta, A. (2010). Dotknot: Pseudoknot prediction using the probability dot plot under a refined energy model. Nucleic Acids Research, 38(7), e103–e103. https://doi.org/10.1093/nar/gkq021
  • Sperschneider, J., Datta, A., & Wise, M. J. (2011). Heuristic RNA pseudoknot prediction including intramolecular kissing hairpins. RNA, 17(1), 27–38. https://doi.org/10.1261/rna.2394511
  • Spokoini-Stern, R., Stamov, D., Jessel, H., Aharoni, L., Haschke, H., Giron, J., Unger, R., Segal, E., Abu-Horowitz, A., & Bachelet, I. (2020). Visualizing the structure and motion of the long noncoding RNA HOTAIR. RNA, 26(5), 629–636. https://doi.org/10.1261/rna.074633.120
  • Staple, D. W., & Butcher, S. E. (2005). Pseudoknots: RNA structures with diverse functions. PLoS Biology, 3(6), e213. https://doi.org/10.1371/journal.pbio.0030213
  • The RNA Central Consortium. (2019). RNAcentral: A hub of information for non-coding RNA sequences. Nucleic Acids Research, 47(D1), D221–D229.
  • Tolbert, M., Morgan, C. E., Pollum, M., Crespo-Hernández, C. E., Li, M.-L., Brewer, G., & Tolbert, B. S. (2017). HnRNP a1 alters the structure of a conserved enterovirus IRES domain to stimulate viral translation. Journal of Molecular Biology, 429(19), 2841–2858. https://doi.org/10.1016/j.jmb.2017.06.007
  • Toor, N., Keating, K. S., Fedorova, O., Rajashankar, K., Wang, J., & Pyle, A. M. (2010). Tertiary architecture of the Oceanobacillus iheyensis group II intron. RNA, 16(1), 57–69. https://doi.org/10.1261/rna.1844010
  • Wang, X., Alnabati, E., Aderinwale, T. W., Maddhuri Venkata Subramaniya, S. R., Terashi, G., & Kihara, D. (2021). Detecting protein and DNA/RNA structures in Cryo-EM maps of intermediate resolution using deep learning. Nature Communications, 12(1), 1–9. https://doi.org/10.1038/s41467-021-22577-3
  • Watkins, A. M., Rangan, R., & Das, R. (2019). Using Rosetta for RNA homology modeling. In Hargrove, A. E. (Ed.), RNA Recognition. In Methods in enzymology (Vol. 623, pp. 177–207). Elsevier. https://doi.org/10.1016/bs.mie.2019.05.026
  • Westhof, E., & Jaeger, L. (1992). RNA pseudoknots. Current Opinion in Structural Biology, 2(3), 327–333. https://doi.org/10.1016/0959-440X(92)90221-R
  • Wiese, K. C., & Hendriks, A. (2006). Comparison of P-RNAPredict and mfold – algorithms for RNA secondary structure prediction. Bioinformatics, 22(8), 934–942. https://doi.org/10.1093/bioinformatics/btl043
  • Yang, H., Jossinet, F., Leontis, N., Chen, L., Westbrook, J., Berman, H., & Westhof, E. (2003). Tools for the automatic identification and classification of RNA base pairs. Nucleic Acids Research, 31(13), 3450–3460. https://doi.org/10.1093/nar/gkg529
  • Yu, X., Zheng, H., Chan, M. T. V., & Wu, W. K. K. (2017). HULC: An oncogenic long non-coding RNA in human cancer. Journal of Cellular and Molecular Medicine, 21(2), 410–417.
  • Yuan, C., Ning, Y., & Pan, Y. (2020). Emerging roles of HOTAIR in human cancer. Journal of Cellular Biochemistry, 121(5-6), 3235–3247. https://doi.org/10.1002/jcb.29591
  • Zampetaki, A., Albrecht, A., & Steinhofel, K. (2018). Long non-coding RNA structure and function: is there a link? Frontiers in Physiology, 9, 1201. https://doi.org/10.3389/fphys.2018.01201
  • Zhang, Z., Xiong, P., Zhang, T., Wang, J., Zhan, J., & Zhou, Y. (2020). Accurate inference of the full base-pairing structure of RNA by deep mutational scanning and covariation-induced deviation of activity. Nucleic Acids Research, 48(3), 1451–1465. https://doi.org/10.1093/nar/gkz1192
  • Zhao, C., Rajashankar, K. R., Marcia, M., & Pyle, A. M. (2015). Crystal structure of group II intron domain 1 reveals a template for RNA assembly. Nature Chemical Biology, 11(12), 967–972. https://doi.org/10.1038/nchembio.1949
  • Zhao, Y., Huang, Y., Gong, Z., Wang, Y., Man, J., & Xiao, Y. (2012). Automated and fast building of three-dimensional RNA structures. Scientific Reports, 2(1), 734–736. https://doi.org/10.1038/srep00734
  • Zhuang, F., Qi, Z., Duan, K., Xi, D., Zhu, Y., Zhu, H., Xiong, H., & He, Q. (2021). A comprehensive survey on transfer learning. Proceedings of the IEEE, 109(1), 43–76. https://doi.org/10.1109/JPROC.2020.3004555
  • Zok, T., Antczak, M., Zurkowski, M., Popenda, M., Blazewicz, J., Adamiak, R. W., & Szachniuk, M. (2018). RNApdbee 2.0: Multifunctional tool for RNA structure annotation. Nucleic Acids Research, 46(W1), W30–W35. https://doi.org/10.1093/nar/gky314
  • Zuker, M. (2003). Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Research, 31(13), 3406–3415. https://doi.org/10.1093/nar/gkg595

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