Principles for targeting RNA with drug-like small molecules (original) (raw)

• Clamp, M. et al. Distinguishing protein-coding and noncoding genes in the human genome. Proc. Natl Acad. Sci. USA 104, 19428–19433 (2007).
  Article CAS PubMed PubMed Central Google Scholar
• Ezkurdia, I. et al. Multiple evidence strands suggest that there may be as few as 19,000 human protein-coding genes. Hum. Mol. Genet. 23, 5866–5878 (2014).
  Article CAS PubMed PubMed Central Google Scholar
• Hopkins, A. L. & Groom, C. R. The druggable genome. Nat. Rev. Drug Discov. 1, 727–730 (2002).
  Article CAS PubMed Google Scholar
• Overington, J. P., Al-Lazikani, B. & Hopkins, A. L. How many drug targets are there? Nat. Rev. Drug Discov. 5, 993–996 (2006).
  Article CAS PubMed Google Scholar
• Dixon, S. J. & Stockwell, B. R. Identifying druggable disease-modifying gene products. Curr. Opin. Chem. Biol. 13, 549–555 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Santos, R. et al. A comprehensive map of molecular drug targets. Nat. Rev. Drug Discov. 16, 19–34 (2017).
  Article CAS PubMed Google Scholar
• Sharp, P. A. The centrality of RNA. Cell 136, 577–580 (2009).
  Article CAS PubMed Google Scholar
• Cech, T. R. & Steitz, J. A. The noncoding RNA revolution-trashing old rules to forge new ones. Cell 157, 77–94 (2014).
  Article CAS PubMed Google Scholar
• Djebali, S. et al. Landscape of transcription in human cells. Nature 489, 101–108 (2012).
  Article CAS PubMed PubMed Central Google Scholar
• Matsui, M. & Corey, D. R. Non-coding RNAs as drug targets. Nat. Rev. Drug Discov. 16, 167–179 (2017).
  Article CAS PubMed Google Scholar
• Adams, B. D., Parsons, C., Walker, L., Zhang, W. C. & Slack, F. J. Targeting noncoding RNAs in disease. J. Clin. Invest. 127, 761–771 (2017).
  Article PubMed PubMed Central Google Scholar
• Harrow, J. et al. GENCODE: the reference human genome annotation for The ENCODE Project. Genome Res. 22, 1760–1774 (2012).
  Article CAS PubMed PubMed Central Google Scholar
• Liang, X.-H. et al. Translation efficiency of mRNAs is increased by antisense oligonucleotides targeting upstream open reading frames. Nat. Biotechnol. 34, 875–880 (2016).
  Article CAS PubMed Google Scholar
• Liang, X.-H. et al. Antisense oligonucleotides targeting translation inhibitory elements in 5′ UTRs can selectively increase protein levels. Nucleic Acids Res. 45, 9528–9546 (2017).
  Article CAS PubMed PubMed Central Google Scholar
• Crooke, S. T., Witztum, J. L., Bennett, C. F. & Baker, B. F. RNA-targeted therapeutics. Cell Metab. 27, 714–739 (2018).
  Article CAS PubMed Google Scholar
• Fellmann, C., Gowen, B. G., Lin, P.-C., Doudna, J. A. & Corn, J. E. Cornerstones of CRISPR-Cas in drug discovery and therapy. Nat. Rev. Drug Discov. 16, 89–100 (2017).
  Article CAS PubMed Google Scholar
• McCown, P. J., Corbino, K. A., Stav, S., Sherlock, M. E. & Breaker, R. R. Riboswitch diversity and distribution. RNA 23, 995–1011 (2017).
  Article CAS PubMed PubMed Central Google Scholar
• Wilson, D. N. Ribosome-targeting antibiotics and mechanisms of bacterial resistance. Nat. Rev. Microbiol. 12, 35–48 (2014).
  Article CAS PubMed Google Scholar
• Childs-Disney, J. L. & Disney, M. D. Approaches to validate and manipulate RNA targets with small molecules in cells. Annu. Rev. Pharmacol. Toxicol. 56, 123–140 (2016).
  Article CAS PubMed Google Scholar
• Thomas, J. R. & Hergenrother, P. J. Targeting RNA with small molecules. Chem. Rev. 108, 1171–1224 (2008).
  Article CAS PubMed Google Scholar
• Aboul-ela, F. Strategies for the design of RNA-binding small molecules. Future Med. Chem. 2, 93–119 (2010).
  Article CAS PubMed Google Scholar
• Guan, L. & Disney, M. D. Recent advances in developing small molecules targeting RNA. ACS Chem. Biol. 7, 73–86 (2012).
  Article CAS PubMed Google Scholar
• Connelly, C. M., Moon, M. H. & Schneekloth, J. S. The emerging role of RNA as a therapeutic target for small molecules. Cell Chem. Biol. 23, 1077–1090 (2016).
  Article CAS PubMed PubMed Central Google Scholar
• Morgan, B. S., Forte, J. E., Culver, R. N., Zhang, Y. & Hargrove, A. E. Discovery of key physicochemical, structural, and spatial properties of RNA-targeted bioactive ligands. Angew. Chem. Int. Ed. Engl. 56, 13498–13502 (2017).
  Article CAS PubMed PubMed Central Google Scholar
• Hermann, T. Small molecules targeting viral RNA. Wiley Interdiscip. Rev. RNA 7, 726–743 (2016).
  Article CAS PubMed PubMed Central Google Scholar
• Rizvi, N. F. & Smith, G. F. RNA as a small molecule druggable target. Bioorg. Med. Chem. Lett. 27, 5083–5088 (2017).
  Article CAS PubMed Google Scholar
• Bickerton, G. R., Paolini, G. V., Besnard, J., Muresan, S. & Hopkins, A. L. Quantifying the chemical beauty of drugs. Nat. Chem. 4, 90–98 (2012).
  Article CAS PubMed PubMed Central Google Scholar
• Moellering, R. C. Linezolid: the first oxazolidinone antimicrobial. Ann. Intern. Med. 138, 135–142 (2003).
  Article CAS PubMed Google Scholar
• Wilson, D. N. et al. The oxazolidinone antibiotics perturb the ribosomal peptidyl-transferase center and effect tRNA positioning. Proc. Natl Acad. Sci. USA 105, 13339–13344 (2008).
  Article PubMed PubMed Central Google Scholar
• Howe, J. A. et al. Selective small-molecule inhibition of an RNA structural element. Nature 526, 672–677 (2015).
  Article CAS PubMed Google Scholar
• Howe, J. A. et al. Atomic resolution mechanistic studies of ribocil: a highly selective unnatural ligand mimic of the E. coli FMN riboswitch. RNA Biol. 13, 946–954 (2016).
  Article PubMed PubMed Central Google Scholar
• Palacino, J. et al. SMN2 splice modulators enhance U1-pre-mRNA association and rescue SMA mice. Nat. Chem. Biol. 11, 511–517 (2015).
  Article CAS PubMed Google Scholar
• Sivaramakrishnan, M. et al. Binding to SMN2 pre-mRNA-protein complex elicits specificity for small molecule splicing modifiers. Nat. Commun. 8, 1476 (2017).
  Article CAS PubMed PubMed Central Google Scholar
• Kondo, Y., Oubridge, C., van Roon, A.-M. M. & Nagai, K. Crystal structure of human U1 snRNP, a small nuclear ribonucleoprotein particle, reveals the mechanism of 5′ splice site recognition. eLife 4, 360 (2015).
  Article Google Scholar
• Calder, A. N., Androphy, E. J. & Hodgetts, K. J. Small molecules in development for the treatment of spinal muscular atrophy. J. Med. Chem. 59, 10067–10083 (2016).
  Article CAS PubMed PubMed Central Google Scholar
• Seth, P. P. et al. SAR by MS: discovery of a new class of RNA-binding small molecules for the hepatitis C virus: internal ribosome entry site IIA subdomain. J. Med. Chem. 48, 7099–7102 (2005).
  Article CAS PubMed Google Scholar
• Mei, H. Y. et al. Discovery of selective, small-molecule inhibitors of RNA complexes—I. The Tat protein/TAR RNA complexes required for HIV-1 transcription. Bioorg. Med. Chem. 5, 1173–1184 (1997).
  Article CAS PubMed Google Scholar
• Prado, S. et al. Bioavailable inhibitors of HIV-1 RNA biogenesis identified through a Rev-based screen. Biochem. Pharmacol. 107, 14–28 (2016).
  Article CAS PubMed Google Scholar
• Sztuba-Solinska, J. et al. Identification of biologically active, HIV TAR RNA-binding small molecules using small molecule microarrays. J. Am. Chem. Soc. 136, 8402–8410 (2014).
  Article CAS PubMed PubMed Central Google Scholar
• Joly, J.-P. et al. Artificial nucleobase-amino acid conjugates: a new class of TAR RNA binding agents. Chemistry 20, 2071–2079 (2014).
  Article CAS PubMed Google Scholar
• Carnevali, M., Parsons, J., Wyles, D. L. & Hermann, T. A modular approach to synthetic RNA binders of the hepatitis C virus internal ribosome entry site. Chembiochem 11, 1364–1367 (2010).
  Article CAS PubMed PubMed Central Google Scholar
• Hilimire, T. A. et al. HIV-1 frameshift RNA-targeted triazoles inhibit propagation of replication-competent and multi-drug-resistant HIV in human cells. ACS Chem. Biol. 12, 1674–1682 (2017).
  Article CAS PubMed PubMed Central Google Scholar
• Barros, S. A., Yoon, I. & Chenoweth, D. M. Modulation of the E. coli rpoH Temperature sensor with triptycene-based small molecules. Angew. Chem. Int. Ed. Engl. 55, 8258–8261 (2016).
  Article CAS PubMed PubMed Central Google Scholar
• Nguyen, L. et al. Rationally designed small molecules that target both the DNA and RNA causing myotonic dystrophy type 1. J. Am. Chem. Soc. 137, 14180–14189 (2015).
  Article CAS PubMed Google Scholar
• Luu, L. M. et al. A potent inhibitor of protein sequestration by expanded triplet (CUG) repeats that shows phenotypic improvements in a Drosophila model of myotonic dystrophy. ChemMedChem 11, 1428–1435 (2016).
  Article CAS PubMed PubMed Central Google Scholar
• Lee, M.-K. et al. A novel small-molecule binds to the influenza A virus RNA promoter and inhibits viral replication. Chem. Commun. (Camb.) 50, 368–370 (2014).
  Article CAS Google Scholar
• Park, S.-J., Kim, Y.-G. & Park, H.-J. Identification of RNA pseudoknot-binding ligand that inhibits the -1 ribosomal frameshifting of SARS-coronavirus by structure-based virtual screening. J. Am. Chem. Soc. 133, 10094–10100 (2011).
  Article CAS PubMed Google Scholar
• Stelzer, A. C. et al. Discovery of selective bioactive small molecules by targeting an RNA dynamic ensemble. Nat. Chem. Biol. 7, 553–559 (2011).
  Article CAS PubMed PubMed Central Google Scholar
• Bottini, A. et al. Targeting influenza A virus RNA promoter. Chem. Biol. Drug Des. 86, 663–673 (2015).
  Article CAS PubMed PubMed Central Google Scholar
• Jin, L., Wang, W. & Fang, G. Targeting protein-protein interaction by small molecules. Annu. Rev. Pharmacol. Toxicol. 54, 435–456 (2014).
  Article CAS PubMed Google Scholar
• Doak, B. C., Over, B., Giordanetto, F. & Kihlberg, J. Oral druggable space beyond the rule of 5: insights from drugs and clinical candidates. Chem. Biol. 21, 1115–1142 (2014).
  Article CAS PubMed Google Scholar
• Matsson, P., Doak, B. C., Over, B. & Kihlberg, J. Cell permeability beyond the rule of 5. Adv. Drug Deliv. Rev. 101, 42–61 (2016).
  Article CAS PubMed Google Scholar
• Zimmerman, S. C. A journey in bioinspired supramolecular chemistry: from molecular tweezers to small molecules that target myotonic dystrophy. Beilstein J. Org. Chem. 12, 125–138 (2016).
  Article CAS PubMed PubMed Central Google Scholar
• Mustoe, A. M. et al. Pervasive regulatory functions of mRNA structure revealed by high-resolution SHAPE probing. Cell 173, 181–195.e18 (2018).
  Article CAS PubMed PubMed Central Google Scholar
• Siegfried, N. A., Busan, S., Rice, G. M., Nelson, J. A. E. & Weeks, K. M. RNA motif discovery by SHAPE and mutational profiling (SHAPE-MaP). Nat. Methods 11, 959–965 (2014).
  Article CAS PubMed PubMed Central Google Scholar
• Mauger, D. M. et al. Functionally conserved architecture of hepatitis C virus RNA genomes. Proc. Natl Acad. Sci. USA 112, 3692–3697 (2015).
  CAS PubMed PubMed Central Google Scholar
• Pirakitikulr, N., Kohlway, A., Lindenbach, B. D. & Pyle, A. M. The coding region of the HCV genome contains a network of regulatory RNA structures. Mol. Cell 62, 111–120 (2016).
  Article CAS PubMed PubMed Central Google Scholar
• Villordo, S. M., Carballeda, J. M., Filomatori, C. V. & Gamarnik, A. V. RNA structure duplications and flavivirus host adaptation. Trends Microbiol. 24, 270–283 (2016).
  Article CAS PubMed PubMed Central Google Scholar
• Kutchko, K. M. et al. Structural divergence creates new functional features in alphavirus genomes. Nucleic Acids Res. 46, 3657–3670 (2018).
  Article CAS PubMed PubMed Central Google Scholar
• Cencig, S. et al. Mapping and characterization of the minimal internal ribosome entry segment in the human c-myc mRNA 5′ untranslated region. Oncogene 23, 267–277 (2004).
  Article CAS PubMed Google Scholar
• Chakraborty, S., Mehtab, S., Patwardhan, A. & Krishnan, Y. Pri-miR-17-92a transcript folds into a tertiary structure and autoregulates its processing. RNA 18, 1014–1028 (2012).
  Article CAS PubMed PubMed Central Google Scholar
• Smola, M. J. et al. SHAPE reveals transcript-wide interactions, complex structural domains, and protein interactions across the Xist lncRNA in living cells. Proc. Natl Acad. Sci. USA 113, 10322–10327 (2016).
  Article CAS PubMed PubMed Central Google Scholar
• Ball, C. B., Solem, A. C., Meganck, R. M., Laederach, A. & Ramos, S. B. V. Impact of RNA structure on ZFP36L2 interaction with luteinizing hormone receptor mRNA. RNA 23, 1209–1223 (2017).
  Article CAS PubMed PubMed Central Google Scholar
• Corley, M. et al. An RNA structure-mediated, posttranscriptional model of human α-1-antitrypsin expression. Proc. Natl Acad. Sci. USA 114, E10244–E10253 (2017).
  Article CAS PubMed PubMed Central Google Scholar
• Lee, A. S. Y., Kranzusch, P. J. & Cate, J. H. D. eIF3 targets cell-proliferation messenger RNAs for translational activation or repression. Nature 522, 111–114 (2015).
  Article CAS PubMed PubMed Central Google Scholar
• Xue, Z. et al. A G-rich motif in the lncRNA Braveheart interacts with a zinc-finger transcription factor to specify the cardiovascular lineage. Mol. Cell 64, 37–50 (2016).
  Article CAS PubMed PubMed Central Google Scholar
• Long, K. S. & Vester, B. Resistance to linezolid caused by modifications at its binding site on the ribosome. Antimicrob. Agents Chemother. 56, 603–612 (2012).
  Article CAS PubMed PubMed Central Google Scholar
• World Health Organization. WHO Model Lists of Essential Medicines, March 2017 (WHO, 2017).
• Karthikeyan, S. et al. Crystal structure of human riboflavin kinase reveals a beta barrel fold and a novel active site arch. Structure 11, 265–273 (2003).
  Article CAS PubMed Google Scholar
• Serganov, A., Huang, L. & Patel, D. J. Coenzyme recognition and gene regulation by a flavin mononucleotide riboswitch. Nature 458, 233–237 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Schneider, T. D., Stormo, G. D., Gold, L. & Ehrenfeucht, A. Information content of binding sites on nucleotide sequences. J. Mol. Biol. 188, 415–431 (1986).
  Article CAS PubMed Google Scholar
• Witherell, G. W. & Uhlenbeck, O. C. Specific RNA binding by Q beta coat protein. Biochemistry 28, 71–76 (1989).
  Article CAS PubMed Google Scholar
• Carothers, J. M., Oestreich, S. C., Davis, J. H. & Szostak, J. W. Informational complexity and functional activity of RNA structures. J. Am. Chem. Soc. 126, 5130–5137 (2004).
  Article CAS PubMed PubMed Central Google Scholar
• Shang, L., Xu, W., Ozer, S. & Gutell, R. R. Structural constraints identified with covariation analysis in ribosomal RNA. PLoS ONE 7, e39383 (2012).
  Article CAS PubMed PubMed Central Google Scholar
• Weeks, K. M. & Mauger, D. M. Exploring RNA structural codes with SHAPE chemistry. Acc. Chem. Res. 44, 1280–1291 (2011).
  Article CAS PubMed PubMed Central Google Scholar
• Smola, M. J., Rice, G. M., Busan, S., Siegfried, N. A. & Weeks, K. M. Selective 2′-hydroxyl acylation analyzed by primer extension and mutational profiling (SHAPE-MaP) for direct, versatile and accurate RNA structure analysis. Nat. Protoc. 10, 1643–1669 (2015).
  Article CAS PubMed PubMed Central Google Scholar
• Carothers, J. M., Davis, J. H., Chou, J. J. & Szostak, J. W. Solution structure of an informationally complex high-affinity RNA aptamer to GTP. RNA 12, 567–579 (2006).
  Article CAS PubMed PubMed Central Google Scholar
• Velagapudi, S. P. et al. Design of a small molecule against an oncogenic noncoding RNA. Proc. Natl Acad. Sci. USA 113, 5898–5903 (2016).
  Article CAS PubMed PubMed Central Google Scholar
• Pérot, S., Sperandio, O., Miteva, M. A., Camproux, A.-C. & Villoutreix, B. O. Druggable pockets and binding site centric chemical space: a paradigm shift in drug discovery. Drug Discov. Today 15, 656–667 (2010).
  Article CAS PubMed Google Scholar
• Fauman, E. B., Rai, B. K. & Huang, E. S. Structure-based druggability assessment — identifying suitable targets for small molecule therapeutics. Curr. Opin. Chem. Biol. 15, 463–468 (2011).
  Article CAS PubMed Google Scholar
• An, J., Totrov, M. & Abagyan, R. Pocketome via comprehensive identification and classification of ligand binding envelopes. Mol. Cell. Proteomics 4, 752–761 (2005).
  Article CAS PubMed Google Scholar
• Bonneau, E. & Legault, P. Nuclear magnetic resonance structure of the III-IV-V three-way junction from the Varkud satellite ribozyme and identification of magnesium-binding sites using paramagnetic relaxation enhancement. Biochemistry 53, 6264–6275 (2014).
  Article CAS PubMed Google Scholar
• Bonneau, E., Girard, N., Lemieux, S. & Legault, P. The NMR structure of the II-III-VI three-way junction from the Neurospora VS ribozyme reveals a critical tertiary interaction and provides new insights into the global ribozyme structure. RNA 21, 1621–1632 (2015).
  Article CAS PubMed PubMed Central Google Scholar
• Staple, D. W. & Butcher, S. E. Pseudoknots: RNA structures with diverse functions. PLoS Biol. 3, e213 (2005).
  Article CAS PubMed PubMed Central Google Scholar
• Michiels, P. J. et al. Solution structure of the pseudoknot of SRV-1 RNA, involved in ribosomal frameshifting. J. Mol. Biol. 310, 1109–1123 (2001).
  Article CAS PubMed Google Scholar
• Hajdin, C. E. et al. Accurate SHAPE-directed RNA secondary structure modeling, including pseudoknots. Proc. Natl Acad. Sci. USA 110, 5498–5503 (2013).
  Article PubMed PubMed Central Google Scholar
• Smola, M. J., Calabrese, J. M. & Weeks, K. M. Detection of RNA-protein interactions in living cells with SHAPE. Biochemistry 54, 6867–6875 (2015).
  Article CAS PubMed Google Scholar
• Gilbert, S. D., Reyes, F. E., Edwards, A. L. & Batey, R. T. Adaptive ligand binding by the purine riboswitch in the recognition of guanine and adenine analogs. Structure 17, 857–868 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Warner, K. D. et al. Validating fragment-based drug discovery for biological RNAs: lead fragments bind and remodel the TPP riboswitch specifically. Chem. Biol. 21, 591–595 (2014).
  Article CAS PubMed PubMed Central Google Scholar
• Miao, Z. & Westhof, E. RNA structure: advances and assessment of 3D structure prediction. Annu. Rev. Biophys. 46, 483–503 (2017).
  Article CAS PubMed Google Scholar
• Kozak, M. Regulation of translation via mRNA structure in prokaryotes and eukaryotes. Gene 361, 13–37 (2005).
  Article CAS PubMed Google Scholar
• Harvey, I., Garneau, P. & Pelletier, J. Inhibition of translation by RNA-small molecule interactions. RNA 8, 452–463 (2002).
  Article CAS PubMed PubMed Central Google Scholar
• Bandyopadhyay, S. et al. Novel 5′ untranslated region directed blockers of iron-regulatory protein-1 dependent amyloid precursor protein translation: implications for down syndrome and Alzheimer's disease. PLoS ONE 8, e65978 (2013).
  Article CAS PubMed PubMed Central Google Scholar
• Rzuczek, S. G. et al. Precise small-molecule recognition of a toxic CUG RNA repeat expansion. Nat. Chem. Biol. 13, 188–193 (2017).
  Article CAS PubMed Google Scholar
• Tinoco, I. & Bustamante, C. How RNA folds. J. Mol. Biol. 293, 271–281 (1999).
  Article CAS PubMed Google Scholar
• Lipinski, C. A. Lead- and drug-like compounds: the rule-of-five revolution. Drug Discov. Today Technol. 1, 337–341 (2004).
  Article CAS PubMed Google Scholar
• Ritchie, T. J. & Macdonald, S. J. F. How drug-like are 'ugly' drugs: do drug-likeness metrics predict ADME behaviour in humans? Drug Discov. Today 19, 489–495 (2014).
  Article CAS PubMed Google Scholar
• Gleitsman, K. R., Sengupta, R. N. & Herschlag, D. Slow molecular recognition by RNA. RNA 23, 1745–1753 (2017).
  Article CAS PubMed PubMed Central Google Scholar
• Weeks, K. M. & Crothers, D. M. RNA recognition by Tat-derived peptides: interaction in the major groove? Cell 66, 577–588 (1991).
  Article CAS PubMed Google Scholar
• Lin, A. H., Murray, R. W., Vidmar, T. J. & Marotti, K. R. The oxazolidinone eperezolid binds to the 50S ribosomal subunit and competes with binding of chloramphenicol and lincomycin. Antimicrob. Agents Chemother. 41, 2127–2131 (1997).
  Article CAS PubMed PubMed Central Google Scholar
• Ritchie, D. B., Soong, J., Sikkema, W. K. A. & Woodside, M. T. Anti-frameshifting ligand reduces the conformational plasticity of the SARS virus pseudoknot. J. Am. Chem. Soc. 136, 2196–2199 (2014).
  Article CAS PubMed Google Scholar
• Parsons, J. et al. Conformational inhibition of the hepatitis C virus internal ribosome entry site RNA. Nat. Chem. Biol. 5, 823–825 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Costales, M. G. et al. Small molecule inhibition of microRNA-210 reprograms an oncogenic hypoxic circuit. J. Am. Chem. Soc. 139, 3446–3455 (2017).
  Article CAS PubMed PubMed Central Google Scholar
• Yildirim, I., Park, H., Disney, M. D. & Schatz, G. C. A dynamic structural model of expanded RNA CAG repeats: a refined X-ray structure and computational investigations using molecular dynamics and umbrella sampling simulations. J. Am. Chem. Soc. 135, 3528–3538 (2013).
  Article CAS PubMed PubMed Central Google Scholar
• Leeper, T., Leulliot, N. & Varani, G. The solution structure of an essential stem-loop of human telomerase RNA. Nucleic Acids Res. 31, 2614–2621 (2003).
  Article CAS PubMed PubMed Central Google Scholar
• Chen, Y. et al. Rbfox proteins regulate microRNA biogenesis by sequence-specific binding to their precursors and target downstream Dicer. Nucleic Acids Res. 44, 4381–4395 (2016).
  Article CAS PubMed PubMed Central Google Scholar
• Faber, C., Sticht, H., Schweimer, K. & Rösch, P. Structural rearrangements of HIV-1 Tat-responsive RNA upon binding of neomycin B. J. Biol. Chem. 275, 20660–20666 (2000).
  Article CAS PubMed Google Scholar
• Zhang, Q., Harada, K., Cho, H. S., Frankel, A. D. & Wemmer, D. E. Structural characterization of the complex of the Rev response element RNA with a selected peptide. Chem. Biol. 8, 511–520 (2001).
  Article CAS PubMed Google Scholar