Virtual screening and molecular growth guide the design of inhibitors for the influenza virus drug-resistant mutant M2-V27A/S31N

References

• Abed, Y., Goyette, N., & Boivin, G. (2005). Generation and characterization of recombinant influenza A (H1N1) viruses harboring amantadine resistance mutations. Antimicrobial Agents and Chemotherapy, 49(2), 556–559. https://doi.org/10.1128/AAC.49.2.556-559.2005
   PubMed Web of Science ®Google Scholar
• Abraham, M. J., Murtola, T., Schulz, R., Páll, S., Smith, J. C., Hess, B., & Lindahl, E. (2015). GROMACS: High performance molecular simulations through multi-level parallelism from laptops to supercomputers. SoftwareX, 1–2, 19–25. https://doi.org/10.1016/j.softx.2015.06.001
   Google Scholar
• Anton, A., Marcos, M. A., Martinez, M. J., Ramon, S., Isanta, R., de Molina, P., de Anta, M. T., & Pumarola, T. (2010). Double (V27A/S31N) mutant 2009 pandemic influenza A (H1N1) virus isolated from adamantane non-treated inmunocompetent child. Diagnostic Microbiology and Infectious Disease, 67(1), 114–115. https://doi.org/10.1016/j.diagmicrobio.2009.12.019
   PubMed Web of Science ®Google Scholar
• Balannik, V., Wang, J., Ohigashi, Y., Jing, X., Magavern, E., Lamb, R. A., Degrado, W. F., & Pinto, L. H. (2009). Design and pharmacological characterization of inhibitors of amantadine-resistant mutants of the M2 ion channel of influenza A virus. Biochemistry, 48(50), 11872–11882. https://doi.org/10.1021/bi9014488
   PubMed Web of Science ®Google Scholar
• Berendsen, H. J. C., van der Spoel, D., & van Drunen, R. (1995). GROMACS: A message-passing parallel molecular dynamics implementation. ComputerPhysics Communication, 91(1–3), 43–56. https://doi.org/10.1016/0010-4655(95)00042-e
   Web of Science ®Google Scholar
• Brooks, B. R., Brooks, C. L., Mackerell, A. D., Nilsson, L., Petrella, R. J., Roux, B., Won, Y., Archontis, G., Bartels, C., Boresch, S., Caflisch, A., Caves, L., Cui, Q., Dinner, A. R., Feig, M., Fischer, S., Gao, J., Hodoscek, M., Im, W., … Karplus, M. (2009). CHARMM: The biomolecular simulation program. Journal of Computational Chemistry, 30(10), 1545–1614. https://doi.org/10.1002/jcc.21287
   PubMed Web of Science ®Google Scholar
• Brown, A. N., McSharry, J. J., Weng, Q., Driebe, E. M., Engelthaler, D. M., Sheff, K., Keim, P. S., Nguyen, J., & Drusano, G. L. (2010). In vitro system for modeling influenza A virus resistance under drug pressure. Antimicrobial Agents and Chemotherapy, 54(8), 3442–3450. https://doi.org/10.1128/aac.01385-09
   PubMed Web of Science ®Google Scholar
• Cady, S. D., Schmidt-Rohr, K., Wang, J., Soto, C. S., Degrado, W. F., & Hong, M. (2010). Structure of the amantadine binding site of influenza M2 proton channels in lipid bilayers. Nature, 463(7281), 689–692. https://doi.org/10.1038/nature08722
   PubMed Web of Science ®Google Scholar
• Ceron-Carrasco, J. P. (2022). When virtual screening yields inactive drugs: Dealing with false theoretical friends. ChemMedChem, 17(16), e202200278. https://doi.org/10.1002/cmdc.202200278
   PubMed Web of Science ®Google Scholar
• Chen, Z., Li, H. L., Zhang, Q. J., Bao, X. G., Yu, K. Q., Luo, X. M., Zhu, W. L., & Jiang, H. L. (2009). Pharmacophore-based virtual screening versus docking-based virtual screening: A benchmark comparison against eight targets. Acta Pharmacologica Sinica, 30(12), 1694–1708. https://doi.org/10.1038/aps.2009.159
   PubMed Web of Science ®Google Scholar
• De Clercq, E. (2006). Antiviral agents active against influenza A viruses. Nature Reviews. Drug Discovery, 5(12), 1015–1025. https://doi.org/10.1038/nrd2175
   PubMed Web of Science ®Google Scholar
• Dong, J., Cao, D. S., Miao, H. Y., Liu, S., Deng, B. C., Yun, Y. H., Wang, N. N., Lu, A. P., Zeng, W. B., & Chen, A. F. (2015). ChemDes: An integrated web-based platform for molecular descriptor and fingerprint computation. Journal of Cheminformatics, 7(1), 60. https://doi.org/10.1186/s13321-015-0109-z
   PubMed Web of Science ®Google Scholar
• Duncan, M. C., Onguene, P. A., Kihara, I., Nebangwa, D. N., Naidu, M. E., Williams, D. E., Balgi, A. D., Andrae-Marobela, K., Roberge, M., Andersen, R. J., Niikura, M., Ntie-Kang, F., & Tietjen, I. (2020). Virtual screening identifies chebulagic acid as an inhibitor of the M2(S31N) viral ion channel and Influenza A virus. Molecules, 25(12), 2903. https://doi.org/10.3390/molecules25122903
   PubMed Web of Science ®Google Scholar
• Frances-Monerris, A., Garcia-Iriepa, C., Iriepa, I., Hognon, C., Miclot, T., Barone, G., Monari, A., & Marazzi, M. (2021). Microscopic interactions between ivermectin and key human and viral proteins involved in SARS-CoV-2 infection. Physical Chemistry Chemical Physics: PCCP, 23(40), 22957–22971. https://doi.org/10.1039/d1cp02967c
   PubMed Web of Science ®Google Scholar
• Furuse, Y., Suzuki, A., Kamigaki, T., & Oshitani, H. (2009). Evolution of the M gene of the influenza A virus in different host species: Large-scale sequence analysis. Virology Journal, 6(1), 67. https://doi.org/10.1186/1743-422X-6-67
   PubMedGoogle Scholar
• Gapsys, V., & de Groot, B. L. (2017). Alchemical free energy calculations for nucleotide mutations in protein-DNA complexes. Journal of Chemical Theory and Computation, 13(12), 6275–6289. https://doi.org/10.1021/acs.jctc.7b00849
   PubMed Web of Science ®Google Scholar
• Gerdil, C. (2003). The annual production cycle for influenza vaccine. Vaccine, 21(16), 1776–1779. https://doi.org/10.1016/s0264-410x(03)00071-9
   PubMed Web of Science ®Google Scholar
• Giordano, D., Biancaniello, C., Argenio, M. A., & Facchiano, A. (2022). Drug design by pharmacophore and virtual screening approach. Pharmaceuticals, 15(5), 646. https://doi.org/10.3390/ph15050646
   Web of Science ®Google Scholar
• Gordon, N. A., McGuire, K. L., Wallentine, S. K., Mohl, G. A., Lynch, J. D., Harrison, R. G., & Busath, D. D. (2017). Divalent copper complexes as influenza A M2 inhibitors. Antiviral Research, 147, 100–106. https://doi.org/10.1016/j.antiviral.2017.10.009
   PubMed Web of Science ®Google Scholar
• Han, J., Perez, J., Schafer, A., Cheng, H., Peet, N., Rong, L., & Manicassamy, B. (2018). Influenza virus: Small molecule therapeutics and mechanisms of antiviral resistance. Current Medicinal Chemistry, 25(38), 5115–5127. https://doi.org/10.2174/0929867324666170920165926
   PubMed Web of Science ®Google Scholar
• Hayden, F. G., & de Jong, M. D. (2011). Emerging influenza antiviral resistance threats. The Journal of Infectious Diseases, 203(1), 6–10. https://doi.org/10.1093/infdis/jiq012
   PubMed Web of Science ®Google Scholar
• Hou, T., Wang, J., Li, Y., & Wang, W. (2011). Assessing the performance of the MM/PBSA and MM/GBSA methods. 1. The accuracy of binding free energy calculations based on molecular dynamics simulations. Journal of Chemical Information and Modeling, 51(1), 69–82. https://doi.org/10.1021/ci100275a
   PubMed Web of Science ®Google Scholar
• Hu, J., Fu, R., & Cross, T. A. (2007). The chemical and dynamical influence of the anti-viral drug amantadine on the M2 proton channel transmembrane domain. Biophysical Journal, 93(1), 276–283. https://doi.org/10.1529/biophysj.106.102103
   PubMed Web of Science ®Google Scholar
• Hu, Y., Wang, Y., Li, F., Ma, C., & Wang, J. (2017). Design and expeditious synthesis of organosilanes as potent antivirals targeting multidrug-resistant influenza A viruses. European Journal of Medicinal Chemistry, 135, 70–76. https://doi.org/10.1016/j.ejmech.2017.04.038
   PubMed Web of Science ®Google Scholar
• Jalily, P. H., Duncan, M. C., Fedida, D., Wang, J., & Tietjen, I. (2020). Put a cork in it: Plugging the M2 viral ion channel to sink influenza. Antiviral Research, 178, 104780. https://doi.org/10.1016/j.antiviral.2020.104780
   PubMed Web of Science ®Google Scholar
• Jing, R., Jian, L., Feng, S., Xin, W., Jian-Hua, H., Ye-Chun, X., Nai-Xia, Z., Bing, X., & Jing-Kang, S. (2013). Acta Pharmaceutica Sinica, 48(1), 14–24. https://doi.org/10.16438/j.0513-4870.2013.01.019
   PubMedGoogle Scholar
• Jurrus, E., Engel, D., Star, K., Monson, K., Brandi, J., Felberg, L. E., Brookes, D. H., Wilson, L., Chen, J., Liles, K., Chun, M., Li, P., Gohara, D. W., Dolinsky, T., Konecny, R., Koes, D. R., Nielsen, J. E., Head-Gordon, T., Geng, W., … Baker, N. A. (2018). Improvements to the APBS biomolecular solvation software suite. Protein Science: A Publication of the Protein Society, 27(1), 112–128. https://doi.org/10.1002/pro.3280
   PubMed Web of Science ®Google Scholar
• Kent, W. J. (2002). BLAT-the BLAST-like alignment tool. Genome Research, 12(4), 656–664. https://doi.org/10.1101/gr.229202
   PubMed Web of Science ®Google Scholar
• Kumari, R., Kumar, R., & Lynn, A., Open Source Drug Discovery, C. (2014). g_mmpbsa-a GROMACS tool for high-throughput MM-PBSA calculations. Journal of Chemical Information and Modeling, 54(7), 1951–1962. https://doi.org/10.1021/ci500020m
   PubMed Web of Science ®Google Scholar
• Lindorff-Larsen, K., Piana, S., Palmo, K., Maragakis, P., Klepeis, J. L., Dror, R. O., & Shaw, D. E. (2010). Improved side-chain torsion potentials for the Amber ff99SB protein force field. Proteins, 78(8), 1950–1958. https://doi.org/10.1002/prot.22711
   PubMed Web of Science ®Google Scholar
• Lu, J., Qiu, Y., Baron, R., & Molinero, V. (2014). Coarse-Graining of TIP4P/2005, TIP4P-Ew, SPC/E, and TIP3P to monatomic anisotropic water models using relative entropy minimization. Journal of Chemical Theory and Computation, 10(9), 4104–4120. https://doi.org/10.1021/ct500487h
   PubMed Web of Science ®Google Scholar
• Mackoy, T., Kale, B., Papka, M. E., & Wheeler, R. A. (2021). viewSq, a Visual Molecular Dynamics (VMD) module for calculating, analyzing, and visualizing X-ray and neutron structure factors from atomistic simulations. Computer Physics Communications, 264, 107881. https://doi.org/10.1016/j.cpc.2021.107881
   Web of Science ®Google Scholar
• Maisuradze, G. G., Liwo, A., & Scheraga, H. A. (2009). Principal component analysis for protein folding dynamics. Journal of Molecular Biology, 385(1), 312–329. https://doi.org/10.1016/j.jmb.2008.10.018
   PubMed Web of Science ®Google Scholar
• McCown, M. F., & Pekosz, A. (2005). The influenza A virus M2 cytoplasmic tail is required for infectious virus production and efficient genome packaging. Journal of Virology, 79(6), 3595–3605. https://doi.org/10.1128/JVI.79.6.3595-3605.2005
   PubMed Web of Science ®Google Scholar
• Muñoz Robles, V., Ortega-Carrasco, E., Alonso-Cotchico, L., Rodriguez-Guerra, J., Lledós, A., & Maréchal, J.-D. (2015). Toward the computational design of artificial metalloenzymes: From protein–ligand docking to multiscale approaches. ACS Catalysis, 5(4), 2469–2480. https://doi.org/10.1021/acscatal.5b00010
   Web of Science ®Google Scholar
• Nisar, T., Sutherland-Foggio, H., & Husar, W. (2019). Antiviral amantadine. The Lancet Neurology, 18(12), 1080. https://doi.org/10.1016/s1474-4422(19)30361-8
   PubMed Web of Science ®Google Scholar
• Pinto, L. H., Dieckmann, G. R., Gandhi, C. S., Papworth, C. G., Braman, J., Shaughnessy, M. A., Lear, J. D., Lamb, R. A., & DeGrado, W. F. (1997). A functionally defined model for the M2 proton channel of influenza A virus suggests a mechanism for its ion selectivity. Proceedings of the National Academy of Sciences of the United States of America, 94(21), 11301–11306. https://doi.org/10.1073/pnas.94.21.11301
   PubMed Web of Science ®Google Scholar
• Ren, Y., Long, S., & Cao, S. (2021). Molecular docking and virtual screening of an influenza virus inhibitor that disrupts protein–protein interactions. Viruses, 13(11), 2229. https://doi.org/10.3390/v13112229
   PubMed Web of Science ®Google Scholar
• Roberts, N. J., & Krilov, L. R. (2022). The continued threat of Influenza A viruses. Viruses, 14(5), 883. https://doi.org/10.3390/v14050883
   PubMed Web of Science ®Google Scholar
• Sarker, A., Gu, Z., Mao, L., Ge, Y., Hou, D., Fang, J., Wei, Z., & Wang, Z. (2022). Influenza-existing drugs and treatment prospects. European Journal of Medicinal Chemistry, 232, 114189. https://doi.org/10.1016/j.ejmech.2022.114189
   PubMed Web of Science ®Google Scholar
• Sousa da Silva, A. W., & Vranken, W. F. (2012). ACPYPE - AnteChamber PYthon Parser interfacE. BMC Research Notes, 5(1), 367. https://doi.org/10.1186/1756-0500-5-367
   PubMedGoogle Scholar
• Stouffer, A. L., Acharya, R., Salom, D., Levine, A. S., Di Costanzo, L., Soto, C. S., Tereshko, V., Nanda, V., Stayrook, S., & DeGrado, W. F. (2008). Structural basis for the function and inhibition of an influenza virus proton channel. Nature, 451(7178), 596–599. https://doi.org/10.1038/nature06528
   PubMed Web of Science ®Google Scholar
• Suzuki, H., Saito, R., Masuda, H., Oshitani, H., Sato, M., & Sato, I. (2003). Emergence of amantadine-resistant influenza A viruses: Epidemiological study. Journal of Infection and Chemotherapy: Official Journal of the Japan Society of Chemotherapy, 9(3), 195–200. https://doi.org/10.1007/s10156-003-0262-6
   PubMedGoogle Scholar
• Van Der Spoel, D., Lindahl, E., Hess, B., Groenhof, G., Mark, A. E., & Berendsen, H. J. (2005). GROMACS: Fast, flexible, and free. Journal of Computational Chemistry, 26(16), 1701–1718. https://doi.org/10.1002/jcc.20291
   PubMed Web of Science ®Google Scholar
• Waldmann, M., Jirmann, R., Hoelscher, K., Wienke, M., Niemeyer, F. C., Rehders, D., & Meyer, B. (2014). A nanomolar multivalent ligand as entry inhibitor of the hemagglutinin of avian influenza. Journal of the American Chemical Society, 136(2), 783–788. https://doi.org/10.1021/ja410918a
   PubMed Web of Science ®Google Scholar
• Wang, J., Cady, S. D., Balannik, V., Pinto, L. H., DeGrado, W. F., & Hong, M. (2009). Discovery of spiro-piperidine inhibitors and their modulation of the dynamics of the M2 proton channel from influenza A virus. Journal of the American Chemical Society, 131(23), 8066–8076. https://doi.org/10.1021/ja900063s
   PubMed Web of Science ®Google Scholar
• Wang, J., Ma, C., Fiorin, G., Carnevale, V., Wang, T., Hu, F., Lamb, R. A., Pinto, L. H., Hong, M., Klein, M. L., & DeGrado, W. F. (2011). Molecular dynamics simulation directed rational design of inhibitors targeting drug-resistant mutants of influenza A virus M2. Journal of the American Chemical Society, 133(32), 12834–12841. https://doi.org/10.1021/ja204969m
   PubMed Web of Science ®Google Scholar
• Wang, J., Ma, C., Wang, J., Jo, H., Canturk, B., Fiorin, G., Pinto, L. H., Lamb, R. A., Klein, M. L., & DeGrado, W. F. (2013). Discovery of novel dual inhibitors of the wild-type and the most prevalent drug-resistant mutant, S31N, of the M2 proton channel from influenza A virus. Journal of Medicinal Chemistry, 56(7), 2804–2812. https://doi.org/10.1021/jm301538e
   PubMed Web of Science ®Google Scholar
• Wang, Z., Sun, H., Yao, X., Li, D., Xu, L., Li, Y., Tian, S., & Hou, T. (2016). Comprehensive evaluation of ten docking programs on a diverse set of protein-ligand complexes: The prediction accuracy of sampling power and scoring power. Physical Chemistry Chemical Physics: PCCP, 18(18), 12964–12975. https://doi.org/10.1039/c6cp01555g
   PubMed Web of Science ®Google Scholar
• Xue, Q., Liu, X., Russell, P., Li, J., Pan, W., Fu, J., & Zhang, A. (2022). Evaluation of the binding performance of flavonoids to estrogen receptor alpha by Autodock, Autodock Vina and Surflex-Dock. Ecotoxicology and Environmental Safety, 233, 113323. https://doi.org/10.1016/j.ecoenv.2022.113323
   PubMed Web of Science ®Google Scholar
• Zaraket, H., Saito, R., Suzuki, Y., Baranovich, T., Dapat, C., Caperig-Dapat, I., & Suzuki, H. (2010). Genetic makeup of amantadine-resistant and oseltamivir-resistant human influenza A/H1N1 viruses. Journal of Clinical Microbiology, 48(4), 1085–1092. https://doi.org/10.1128/JCM.01532-09
   PubMed Web of Science ®Google Scholar
• Zhong, S., Huang, K., Luo, S., Dong, S., & Duan, L. (2020). Improving the performance of the MM/PBSA and MM/GBSA methods in recognizing the native structure of the Bcl-2 family using the interaction entropy method. Physical Chemistry Chemical Physics: PCCP, 22(7), 4240–4251. https://doi.org/10.1039/c9cp06459a
   PubMed Web of Science ®Google Scholar