Targeting RNA with small molecules using state-of-the-art methods provides highly predictive affinities of riboswitch inhibitors

  • Harries, L. W. RNA biology provides new therapeutic targets for human disease. Front. Genet. 10, 205 (2019).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Zhu, Y., Zhu, L., Wang, X. & Jin, H. RNA-based therapeutics: an overview and prospectus. Cell Death Dis. 13, 644 (2022).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Yu, A.-M., Choi, Y. H. & Tu, M.-J. RNA drugs and RNA targets for small molecules: principles, progress, and challenges. Pharmacol. Rev. 72, 862–898 (2020).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Lightfoot, H. L. & Smith, G. F. Targeting RNA with small molecules-a safety perspective. Br. J. Pharmacol. 182, 4201–4220 (2023).

  • Bennett, C. F. Therapeutic antisense oligonucleotides are coming of age. Annu. Rev. Med. 70, 307–321 (2019).

    CAS 
    PubMed 

    Google Scholar 

  • Luther, D., Lee, Y., Nagaraj, H., Scaletti, F. & Rotello, V. Delivery approaches for crispr/cas9 therapeutics in vivo: advances and challenges. Expert Opin. Drug Deliv. 15, 905–913 (2018).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Wu, P. Inhibition of RNA-binding proteins with small molecules. Nat. Rev. Chem. 4, 441–458 (2020).

    CAS 
    PubMed 

    Google Scholar 

  • Childs-Disney, J. L. et al. Targeting RNA structures with small molecules. Nat. Rev. Drug Discov. 21, 736–762 (2022).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Howe, J. A. et al. Selective small-molecule inhibition of an RNA structural element. Nature 526, 672–677 (2015).

    CAS 
    PubMed 

    Google Scholar 

  • Dibrov, S. M. et al. Hepatitis C virus translation inhibitors targeting the internal ribosomal entry site: miniperspective. J. Med. Chem. 57, 1694–1707 (2014).

    CAS 
    PubMed 

    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).

    CAS 
    PubMed 

    Google Scholar 

  • Ratni, H. et al. Discovery of risdiplam, a selective survival of motor neuron-2 (smn2) gene splicing modifier for the treatment of spinal muscular atrophy (SMA). J Med Chem. 61, 6501–6517 (2018).

  • Gresh, N. et al. Addressing the issues of non-isotropy and non-additivity in the development of quantum chemistry-grounded polarizable molecular mechanics. in Quantum Modeling of Complex Molecular Systems, 1–49 (Springer, 2015).

  • Jing, Z. et al. Polarizable force fields for biomolecular simulations: recent advances and applications. Annu. Rev. Biophys. 48, 371–394 (2019).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Shi, Y., Ren, P., Schnieders, M. & Piquemal, J.-P. Polarizable force fields for biomolecular modeling. Rev. Comput. Chem. 28, 51–86 (2015).

  • Melcr, J. & Piquemal, J.-P. Accurate biomolecular simulations account for electronic polarization. Front. Mol. Biosci. 6, 143 (2019).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • El Khoury, L. et al. Computationally driven discovery of SARS-CoV-2 M pro inhibitors: from design to experimental validation. Chem. Sci. 13, 3674–3687 (2022).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Ponder, J. W. et al. Current status of the amoeba polarizable force field. J. Phys. Chem. B 114, 2549–2564 (2010).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Zhang, C. et al. Amoeba polarizable atomic multipole force field for nucleic acids. J. Chem. Theory Comput. 14, 2084–2108 (2018).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Gresh, N., Cisneros, G. A., Darden, T. A. & Piquemal, J.-P. Anisotropic, polarizable molecular mechanics studies of inter-and intramolecular interactions and ligand- macromolecule complexes. a bottom-up strategy. J. Chem. Theory Comput. 3, 1960–1986 (2007).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • El Hage, K., Piquemal, J.-P., Hobaika, Z., Maroun, R. G. & Gresh, N. Substituent-modulated affinities of halobenzene derivatives to the HIV-1 integrase recognition site. Analyses of the interaction energies by parallel quantum chemical and polarizable molecular mechanics. J. Phys. Chem. A 118, 9772–9782 (2014).

    CAS 
    PubMed 

    Google Scholar 

  • Adjoua, O. et al. Tinker-hp: Accelerating molecular dynamics simulations of large complex systems with advanced point dipole polarizable force fields using GPUs and multi-GPU systems. J. Chem. Theory Comput. 17, 2034–2053 (2021).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Lagardère, L., Aviat, F. & Piquemal, J.-P. Pushing the limits of multiple-time-step strategies for polarizable point dipole molecular dynamics. J. Phys. Chem. Lett. 10, 2593–2599 (2019).

    PubMed 

    Google Scholar 

  • Jaffrelot-Inizan, T. et al. High-resolution mining of SARS-CoV-2 main protease conformational space: Supercomputer-driven unsupervised adaptive sampling. Chem. Sci. 12, 4889–4907 (2021).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Célerse, F. et al. An efficient Gaussian-accelerated molecular dynamics (GAMD) multilevel enhanced sampling strategy: application to polarizable force fields simulations of large biological systems. J. Chem. Theory Comput. 18, 968–977 (2022).

    PubMed 

    Google Scholar 

  • Célerse, F., Lagardère, L., Derat, E. & Piquemal, J.-P. Massively parallel implementation of steered molecular dynamics in tinker-hp: Comparisons of polarizable and non-polarizable simulations of realistic systems. J. Chem. Theory Comput. 15, 3694–3709 (2019).

    PubMed 

    Google Scholar 

  • Lagardère, L. et al. Lambda-abf: Simplified, portable, accurate, and cost-effective alchemical free-energy computation. J. Chem. Theory Comput. 20, 4481–4498 (2024).

    PubMed 

    Google Scholar 

  • Blazhynska, M. et al. Water–glycan interactions drive the SARS-CoV-2 spike dynamics: insights into glycan-gate control and camouflage mechanisms. Chem. Sci. 15, 14177–14187 (2024).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Wang, L. et al. Accurate and reliable prediction of relative ligand binding potency in prospective drug discovery by way of a modern free-energy calculation protocol and force field. J. Am. Chem. Soc. 137, 2695–2703 (2015).

    CAS 
    PubMed 

    Google Scholar 

  • Zhang, C.-H. et al. Potent noncovalent inhibitors of the main protease of sars-cov-2 from molecular sculpting of the drug perampanel guided by free energy perturbation calculations. ACS Cent. Sci. 7, 467–475 (2021).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Chodera, J. D. et al. Alchemical free energy methods for drug discovery: progress and challenges. Curr. Opin. Struct. Biol. 21, 150–160 (2011).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • El Hage, K. et al. Targeting the major groove of the palindromic d (ggcgcc) 2 sequence by oligopeptide derivatives of anthraquinone intercalators. J. Chem. Inf. Model. 62, 6649–6666 (2022).

    CAS 
    PubMed 

    Google Scholar 

  • Gresh, N. et al. Enforcing local DNA kinks by sequence-selective trisintercalating oligopeptides of a tricationic porphyrin: a polarizable molecular dynamics study. ChemPhysChem 25, e202300776 (2024).

    CAS 
    PubMed 

    Google Scholar 

  • El Hage, K., Mondal, P. & Meuwly, M. Free energy simulations for protein ligand binding and stability. Mol. Sim. 44, 1044–1061 (2018).

    CAS 

    Google Scholar 

  • Rasouli, A., Pickard IV, F. C., Sur, S., Grossfield, A. & Işık Bennett, M. Essential considerations for free energy calculations of RNA-small molecule complexes: lessons from the theophylline-binding RNA aptamer. J. Chem. Inf. Model. 65, 223–239 (2025).

  • Abramyan, A. M. et al. Accurate physics-based prediction of binding affinities of RNA- and DNA-targeting ligands. J. Chem. Inf. Model. 65, 1392–1403 (2025).

  • Clark, F., Robb, G., Cole, D. J. & Michel, J. Comparison of receptor–ligand restraint schemes for alchemical absolute binding free energy calculations. J. Chem. Theory Comput. 19, 3686–3704 (2023).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Salari, R., Joseph, T., Lohia, R., Hénin, J. & Brannigan, G. A streamlined, general approach for computing ligand binding free energies and its application to GPCR-bound cholesterol. J. Chem. Theory Comput. 14, 6560–6573 (2018).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Zhang, H. et al. Accurate estimation of the standard binding free energy of netropsin with DNA. Molecules 23, 228 (2018).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Gapsys, V. et al. Accurate absolute free energies for ligand–protein binding based on non-equilibrium approaches. Commun. Chem. 4, 61 (2021).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Dibrov, S. M. et al. Structure of a hepatitis C virus RNA domain in complex with a translation inhibitor reveals a binding mode reminiscent of riboswitches. Proc. Natl Acad. Sci. 109, 5223–5228 (2012).

    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).

    CAS 
    PubMed 

    Google Scholar 

  • Wu, J. C., Chattree, G. & Ren, P. Automation of amoeba polarizable force field parameterization for small molecules. Theor. Chem. Acc. 131, 1–11 (2012).

    Google Scholar 

  • Shi, Y. et al. Polarizable atomic multipole-based amoeba force field for proteins. J. Chem. Theory Comput. 9, 4046–4063 (2013).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Yang, X., Liu, C., Kuo, Y.-A., Yeh, H.-C. & Ren, P. Computational study on the binding of mango-II RNA aptamer and fluorogen using the polarizable force field amoeba. Front. Mol. Biosci. 9, 946708 (2022).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Lagardère, L. et al. Tinker-hp: a massively parallel molecular dynamics package for multiscale simulations of large complex systems with advanced point dipole polarizable force fields. Chem. Sci. 9, 956–972 (2018).

    PubMed 

    Google Scholar 

  • Jolly, L.-H. et al. Raising the performance of the tinker-hp molecular modeling package [article v1.0]. Living J. Comput. Mol. Sci. 1, 10409 (2019).

    Google Scholar 

  • Fiorin, G., Klein, M. L. & Hénin, J. Using collective variables to drive molecular dynamics simulations. Mol. Phys. 111, 3345–3362 (2013).

    CAS 

    Google Scholar 

  • Bonati, L., Rizzi, V. & Parrinello, M. Data-driven collective variables for enhanced sampling. J. Phys. Chem. Lett. 11, 2998–3004 (2020).

    CAS 
    PubMed 

    Google Scholar 

  • Padroni, G., Patwardhan, N., Schapira, M. & Hargrove, A. Systematic analysis of the interactions driving small molecule–rna recognition. RSC Med. Chem. 11, 802–813 (2020).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Chen, W. et al. Enhancing hit discovery in virtual screening through absolute protein–ligand binding free-energy calculations. J. Chem. Inf. Model. 63, 3171–3185 (2023).

    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).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Santiago-McRae, E., Ebrahimi, M., Sandberg, J. W., Brannigan, G. & Hénin, J. Computing absolute binding affinities by streamlined alchemical free energy perturbation (safep)[article v1. 0]. Living J. Comput. Mol. Sci. 5, 2067–2067 (2023).

    Google Scholar 

  • Invernizzi, M. & Parrinello, M. Rethinking metadynamics: from bias potentials to probability distributions. J. Phys. Chem. Lett. 11, 2731–2736 (2020).

    CAS 
    PubMed 

    Google Scholar 

  • Invernizzi, M. & Parrinello, M. Exploration vs convergence speed in adaptive-bias enhanced sampling. J. Chem. Theory Comput. 18, 3988–3996 (2022).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Walker, B., Liu, C., Wait, E. & Ren, P. Automation of amoeba polarizable force field for small molecules: Poltype 2. J. Comput. Chem. 43, 1530–1542 (2022).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Turney, J. M. et al. Psi4: an open-source ab initio electronic structure program. Wiley Interdiscip. Rev. Comput. Mol. Sci. 2, 556–565 (2012).

    CAS 

    Google Scholar 

  • Stone, A. J. & Alderton, M. Distributed multipole analysis: methods and applications. Mol. Phys. 56, 1047–1064 (1985).

    CAS 

    Google Scholar 

  • Rackers, J. A. et al. Tinker 8: software tools for molecular design. J. Chem. theory Comput. 14, 5273–5289 (2018).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Ren, P., Wu, C. & Ponder, J. W. Polarizable atomic multipole-based molecular mechanics for organic molecules. J. Chem. Theory Comput. 7, 3143–3161 (2011).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Zhang, C., Bell, D., Harger, M. & Ren, P. Polarizable multipole-based force field for aromatic molecules and nucleobases. J. Chem. Theory Comput. 13, 666–678 (2017).

    CAS 
    PubMed 

    Google Scholar 

  • Bannwarth, C. et al. Extended tight-binding quantum chemistry methods. Wiley Interdiscip. Rev. Comput. Mol. Sci. 11, e1493 (2021).

    CAS 

    Google Scholar 

  • Bannwarth, C., Ehlert, S. & Grimme, S. Gfn2-xtb-an accurate and broadly parametrized self-consistent tight-binding quantum chemical method with multipole electrostatics and density-dependent dispersion contributions. J. Chem. Theory Comput. 15, 1652–1671 (2019).

    CAS 
    PubMed 

    Google Scholar 

  • Chai, J.-D. & Head-Gordon, M. Long-range corrected hybrid density functionals with damped atom–atom dispersion corrections. Phys. Chem. Chem. Phys. 10, 6615–6620 (2008).

    CAS 
    PubMed 

    Google Scholar 

  • Tuckerman, M., Berne, B. J. & Martyna, G. J. Reversible multiple time scale molecular dynamics. J. Chem. Phys. 97, 1990–2001 (1992).

    CAS 

    Google Scholar 

  • Bussi, G., Donadio, D. & Parrinello, M. Canonical sampling through velocity rescaling. J. Chem. Phys. 126, 014101 (2007).

  • Berendsen, H. J., Postma, J. V., Van Gunsteren, W. F., DiNola, A. & Haak, J. R. Molecular dynamics with coupling to an external bath. J. Chem. Phys. 81, 3684–3690 (1984).

    CAS 

    Google Scholar 

  • Essmann, U. et al. A smooth particle mesh ewald method. J. Chem. Phys. 103, 8577–8593 (1995).

    CAS 

    Google Scholar 

  • Lagardère, L. et al. Scalable evaluation of polarization energy and associated forces in polarizable molecular dynamics: Ii. toward massively parallel computations using smooth particle mesh ewald. J. Chem. Theory Comput. 11, 2589–2599 (2015).

    PubMed 

    Google Scholar 

  • Laury, M. L., Wang, Z., Gordon, A. S. & Ponder, J. W. Absolute binding free energies for the sampl6 cucurbit [8] uril host–guest challenge via the amoeba polarizable force field. J. Comput. Aided Mol. Des. 32, 1087–1095 (2018).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Boresch, S., Tettinger, F., Leitgeb, M. & Karplus, M. Absolute binding free energies: a quantitative approach for their calculation. J. Phys. Chem. B 107, 9535–9551 (2003).

    CAS 

    Google Scholar 

  • Hénin, J., Lopes, L. J. & Fiorin, G. Human learning for molecular simulations: the collective variables dashboard in VMD. J. Chem. Theory Comput. 18, 1945–1956 (2022).

    PubMed 

    Google Scholar 

  • Humphrey, W., Dalke, A. & Schulten, K. Vmd: visual molecular dynamics. J. Mol. Graph. 14, 33–38 (1996).

    CAS 
    PubMed 

    Google Scholar 

  • Straatsma, T. P. & McCammon, J. A. Multiconfiguration thermodynamic integration. J. Chem. Phys. 95, 1175–1188 (1991).

    CAS 

    Google Scholar 

  • Zwanzig, R. W. High-temperature equation of state by a perturbation method. i. nonpolar gases. J. Chem. Phys. 22, 1420–1426 (1954).

    CAS 

    Google Scholar 

  • Jiang, W. & Roux, B. Free energy perturbation hamiltonian replica-exchange molecular dynamics (fep/h-remd) for absolute ligand binding free energy calculations. J. Chem. Theory Comput. 6, 2559–2565 (2010).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Lyubartsev, A., Martsinovski, A., Shevkunov, S. & Vorontsov-Velyaminov, P. New approach to Monte Carlo calculation of the free energy: method of expanded ensembles. J. Chem. Phys. 96, 1776–1783 (1992).

    CAS 

    Google Scholar 

  • Thomas, J. R. & Hergenrother, P. J. Targeting RNA with small molecules. Chem. Rev. 108, 1171–1224 (2008).

    CAS 
    PubMed 

    Google Scholar 

  • Far, S. et al. Bis-and tris-DNA intercalating porphyrins designed to target the major groove: Synthesis of acridylbis-arginyl-porphyrins, molecular modelling of their DNA complexes, and experimental tests. Eur. J. Org. Chem. 2004, 1781–1797 (2004).

    Google Scholar 

  • Petrov, D., Perthold, J. W., Oostenbrink, C., de Groot, B. L. & Gapsys, V. Guidelines for free-energy calculations involving charge changes. J. Chem. Theory Comput. 20, 914–925 (2024).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Barducci, A., Bonomi, M. & Parrinello, M. Metadynamics. WIREs Comput. Mol. Sci. 1, 826–843 (2011).

    CAS 

    Google Scholar 

  • Welling, M. Fisher Linear Discriminant Analysis. Tech. Rep., Dep. Comput. Sci. Univ. Toronto (2005).

  • Rizzi, V., Bonati, L., Ansari, N. & Parrinello, M. The role of water in host-guest interaction. Nat. Commun. 12, 93 (2021).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Ansari, N., Rizzi, V., Carloni, P. & Parrinello, M. Water-triggered, irreversible conformational change of SARS-CoV-2 main protease on passing from the solid state to aqueous solution. J. Am. Chem. Soc. 143, 12930–12934 (2021).

    CAS 
    PubMed 

    Google Scholar 

  • Ansari, N., Rizzi, V. & Parrinello, M. Water regulates the residence time of benzamidine in trypsin. Nat. Commun. 13, 5438 (2022).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Bjelobrk, Z. et al. Naphthalene crystal shape prediction from molecular dynamics simulations. Cryst. Eng. Comm. 21, 3280–3288 (2019).

    CAS 

    Google Scholar 

  • Leontis, N. B., Stombaugh, J. & Westhof, E. The non–Watson–Crick base pairs and their associated isostericity matrices. Nucleic Acids Res. 30, 3497–3531 (2002).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

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