Peramivir binding affinity with influenza A neuraminidase and research on its mutations using an induced-fit docking approach

References

• World Health Organization. Available at https://www.who.int/news-room/detail/14-12-2017-up-to-650-000-people-die-of-respiratory-diseases-linked-to-seasonal-flu-each-year (accessed 14 May 2019).
   Google Scholar
• X. Jing, C. Ma, Y. Ohigashi, F.A. Oliveira, T.S. Jardetzky, L.H. Pinto, and R.A. Lamb, Functional studies indicate amantadine binds to the pore of the influenza A virus M2 proton-selective ion channel, Proc. Natl. Acad. Sci. U.S.A. 105 (2008), pp. 10967–10972. doi:10.1073/pnas.0804958105.
   PubMed Web of Science ®Google Scholar
• T. Jefferson, V. Demicheli, C. Di Pietrantonj, and D. Rivetti, Amantadine and rimantadine for influenza A in adults, Cochrane Database Syst. Rev. 2 (2006), pp. CD001169. doi:10.1002/14651858.CD001169.pub3.
   PubMed Web of Science ®Google Scholar
• M.G. Alves Galvão, M.A. Rocha Crispino Santos, and A.J. Alves da Cunha, Amantadine and rimantadine for influenza A in children and the elderly, Cochrane Database Syst. Rev. 1 (2012), pp. CD002745. doi:10.1002/14651858.CD002745.pub3.
   PubMed Web of Science ®Google Scholar
• Y. Furuta, K. Takahashi, K. Shiraki, K. Sakamoto, D.F. Smee, D.L. Barnard, B.B. Gowen, J.G. Julander, and J.D. Morrey, T-705 (favipiravir) and related compounds: Novel broad-spectrum inhibitors of RNA viral infections, Antiviral Res. 82 (2009), pp. 95–102. doi:10.1016/j.antiviral.2009.02.198.
   PubMed Web of Science ®Google Scholar
• I.A. Leneva, R.J. Russell, Y.S. Boriskin, and A.J. Hay, Characteristics of arbidol-resistant mutants of influenza virus: Implications for the mechanism of anti-influenza action of arbidol, Antiviral Res. 81 (2009), pp. 132–140. doi:10.1016/j.antiviral.2008.10.009.
   PubMed Web of Science ®Google Scholar
• J.N. Varghese, J.L. McKimm-Breschkin, J.B. Caldwell, A.A. Kortt, and P.M. Colman, The structure of the complex between influenza virus neuraminidase and sialic acid, the viral receptor, Proteins Struct. Funct. Bioinf. 14 (1992), pp. 327–332. doi:10.1002/prot.340140302.
   PubMed Web of Science ®Google Scholar
• C. Oo, J. Barrett, G. Hill, J. Mann, A. Dorr, R. Dutkowski, and P. Ward, Pharmacokinetics and dosage recommendations for an oseltamivir oral suspension for the treatment of influenza in children, Paediatr. Drugs 3 (2001), pp. 229–236. doi:10.2165/00128072-200103030-00005.
   PubMedGoogle Scholar
• A.W. Peng, S. Milleri, and D.S. Stein, Direct measurement of the anti-influenza agent zanamivir in the respiratory tract following inhalation, Antimicrob. Agents Chemother. 44 (2000), pp. 1974–1976. doi:10.1128/aac.44.7.1974-1976.2000.
   PubMed Web of Science ®Google Scholar
• H. Ikematsu and N. Kawai, Laninamivir octanoate: A new long-acting neuraminidase inhibitor for the treatment of influenza, Expert Rev. Anti Infect. Ther. 9 (2011), pp. 851–857. doi:10.1586/eri.11.112.
   PubMed Web of Science ®Google Scholar
• A. Wester and A.K. Shetty, Peramivir injection in the treatment of acute influenza: A review of the literature, infect, Drug Resist. 9 (2016), pp. 201–214. doi:10.2147/IDR.S86460.
   Google Scholar
• J. Lee, J.H. Park, H. Jwa, and Y.H. Kim, Comparison of efficacy of intravenous peramivir and oral oseltamivir for the treatment of influenza: Systematic review and meta-analysis, Yonsei Med. J. 58 (2017), pp. 778–785. doi:10.3349/ymj.2017.58.4.778.
   PubMed Web of Science ®Google Scholar
• J.L. McKimm-Breschkin, Influenza neuraminidase inhibitors: Antiviral action and mechanisms of resistance, Influenza Other Respir. Viruses 7, Suppl. 1 (2013), pp. 25–36. doi:10.1111/irv.12047.
   PubMed Web of Science ®Google Scholar
• P. Palese, K. Tobita, and M. Ueda, Characterization of temperature sensitive influenza virus mutants defective in neuraminidase, Virology 61 (1974), pp. 397–410. doi:10.1016/0042-6822(74)90276-1.
   PubMed Web of Science ®Google Scholar
• D.Q. Wei, Q.S. Du, H. Sun, and K.C. Chou, Insights from modeling the 3D structure of H5N1 influenza virus neuraminidase and its binding interactions with ligands, Biochem. Biophys. Res. Commun. 344 (2006), pp. 1048–1055. doi:10.1016/j.bbrc.2006.03.210.
   PubMed Web of Science ®Google Scholar
• Q.S. Du, S.Q. Wang, and K.C. Chou, Analogue inhibitors by modifying oseltamivir based on the crystal neuraminidase structure for treating drug-resistant H5N1 virus, Biochem. Biophys. Res. Commun. 362 (2007), pp. 525–531. doi:10.1016/j.bbrc.2007.08.025.
   PubMed Web of Science ®Google Scholar
• K. Gong, L. Li, J.F. Wang, F. Cheng, D.Q. Wei, and K.C. Chou, Binding mechanism of H5N1 influenza virus neuraminidase with ligands and its implication for drug design, Med. Chem. 5 (2009), pp. 242–249. doi:10.2174/157340609788185936.
   PubMed Web of Science ®Google Scholar
• C.J. Woods, M. Malaisree, B. Long, S. McIntosh-Smith, and A.J. Mulholland, Computational assay of H7N9 influenza neuraminidase reveals R292K mutation reduces drug binding affinity, Sci. Rep. 3 (2013), pp. 3561. doi:10.1038/srep03561.
   PubMed Web of Science ®Google Scholar
• A.F. Eweas and A.S. Abdel-Moneim, In-silico structural analysis of the influenza A subtype H7N9 neuraminidase and molecular docking with different neuraminidase inhibitors, Virusdisease 26 (2015), pp. 27–32. doi:10.1007/s13337-014-0245-5.
   PubMedGoogle Scholar
• V. Karthick, V. Shanthi, R. Rajasekaran, and K. Ramanathan, In silico analysis of drug-resistant mutant of neuraminidase (N294S) against oseltamivir, Protoplasma 250 (2013), pp. 197–207. doi:10.1007/s00709-012-0394-6.
   PubMed Web of Science ®Google Scholar
• H. Tan, K. Wei, J. Bao, and X. Zhou, In silico study on multidrug resistance conferred by I223R/H275Y double mutant neuraminidase, Mol. Biosyst. 9 (2013), pp. 2764–2774. doi:10.1039/c3mb70253g.
   PubMedGoogle Scholar
• R.S. Mandal, S. Panda, and S. Das, In silico prediction of drug resistance due to S247R mutation of influenza H1N1 neuraminidase protein, J. Biomol. Struct. Dyn. 36 (2018), pp. 966–980. doi:10.1080/07391102.2017.1305295.
   PubMed Web of Science ®Google Scholar
• J. Zhang, Y. Shan, X. Pan, C. Wang, W. Xu, and L. He, Molecular docking, 3D-QSAR studies, and in silico ADME prediction of p-aminosalicylic acid derivatives as neuraminidase inhibitors, Chem. Biol. Drug Des. 78 (2011), pp. 709–717. doi:10.1111/j.1747-0285.2011.01179.x.
   PubMed Web of Science ®Google Scholar
• N. Jusoh, H. Zainal, A.A. Abdul Hamid, N.M. Bunnori, K.B. Abd Halim, and S. Abd Hamid, In silico study of carvone derivatives as potential neuraminidase inhibitors, J. Mol. Model. 24 (2018), pp. 93. doi:10.1007/s00894-018-3619-6.
   PubMed Web of Science ®Google Scholar
• S.M. Sadati, N. Gheibi, S. Ranjbar, and M.S. Hashemzadeh, Docking study of flavonoid derivatives as potent inhibitors of influenza H1N1 virus neuraminidase, Biomed. Rep. 10 (2019), pp. 33–38. doi:10.3892/br.2018.1173.
   PubMed Web of Science ®Google Scholar
• Q. Zhu, H.B. Tran, K. Ohnuki, T. Sawai, K. Sawai, and K. Shimizu, Inhibition of neuraminidase by Ganoderma triterpenoids and implications for neuraminidase inhibitor design, Sci. Rep. 5 (2015), pp. 13194. doi:10.1038/srep13194.
   PubMed Web of Science ®Google Scholar
• Y. Ali, N. Muhamad Bunnori, D. Susanti, A. Muhammad Alhassan, and S. Abd Hamid, Synthesis, in-vitro and in silico studies of azo-based calix[4]arenes as antibacterial agent and neuraminidase inhibitor: A new look into an old scaffold, Front. Chem. 6 (2018), pp. 210. doi:10.3389/fchem.2018.00210.
   PubMed Web of Science ®Google Scholar
• LeadIT. 2012. Version 2.0.2, BioSolveIT – GmbH, Germany.
   Google Scholar
• Sybyl-X Molecular Modeling Software Packages. 2011. Version 2.0, TRIPOS Associates, Inc. Louis, USA.
   Google Scholar
• Molecular Operating Environment (MOE). 2015. Version 2008.10, Chemical Computing Group Inc., Montreal, QC, Canada.
   Google Scholar
• V.R. Atigadda, W.J. Brouillette, F. Duarte, S.M. Ali, Y.S. Babu, S. Bantia, P. Chand, N. Chu, J.A. Montgomery, D.A. Walsh, E.A. Sudbeck, J. Finley, M. Luo, G.M. Air, and G.W. Laver, Potent inhibition of influenza sialidase by a benzoic acid containing a 2-pyrrolidinone substituent, J. Med. Chem. 42 (1999), pp. 2332–2343. doi:10.1021/jm980707k.
   PubMed Web of Science ®Google Scholar
• X. Yi, Z. Guo, and F.M. Chu, Study on molecular mechanism and 3D-QSAR of influenza neuraminidase inhibitors, Bioorg. Med. Chem. 11 (2003), pp. 1465–1474. doi:10.1016/S0968-0896(02)00602-8.
   PubMed Web of Science ®Google Scholar
• E. Feng, D. Ye, J. Li, D. Zhang, J. Wang, F. Zhao, R. Hilgenfeld, M. Zheng, H. Jiang, and H. Liu, Recent advances in neuraminidase inhibitor development as anti-influenza drugs, Chem. Med. Chem. 7 (2012), pp. 1527–1536. doi:10.1002/cmdc.201200155.
   Google Scholar
• A.V. Ivachtchenko, Y.A. Ivanenkov, O.D. Mitkin, P.M. Yamanushkin, V.V. Bichko, I.A. Leneva, and O.V. Borisova, A novel influenza virus neuraminidase inhibitor AV5027, Antiviral Res. 100 (2013), pp. 698–708. doi:10.1016/j.antiviral.2013.10.008.
   PubMed Web of Science ®Google Scholar
• C.U. Kim, W. Lew, M.A. Williams, H. Wu, L. Zhang, X. Chen, P.A. Escarpe, D.B. Mendel, W.G. Laver, and R.C. Stevens, Structure-activity relationship studies of novel carbocyclic influenza neuraminidase inhibitors, J. Med. Chem. 41 (1998), pp. 2451–2460. doi:10.1021/jm980162u.
   PubMed Web of Science ®Google Scholar
• W. Lew, H. Wu, D.B. Mendel, P.A. Escarpe, X. Chen, W.G. Laver, B.J. Graves, and C.U. Kim, A new series of C3-aza carbocyclic influenza neuraminidase inhibitors: Synthesis and inhibitory activity, Bioorg. Med. Chem. Lett. 8 (1998), pp. 3321–3324. doi:10.1016/S0960-894X(98)00587-3.
   PubMed Web of Science ®Google Scholar
• M.A. Williams, W. Lew, D.B. Mendel, C.Y. Tai, P.A. Escarpe, W.G. Laver, R.C. Stevens, and C.U. Kim, Structure-activity relationships of carbocyclic influenza neuraminidase inhibitors, Bioorg. Med. Chem. Lett. 7 (1997), pp. 1837–1842. doi:10.1016/S0960-894X(97)00333-8.
   Web of Science ®Google Scholar
• P. Chand, Y.S. Babu, S. Bantia, S. Rowland, A. Dehghani, P.L. Kotian, T.L. Hutchison, S. Ali, W. Brouillette, Y. El-Kattan, and T.H. Lin, Syntheses and neuraminidase inhibitory activity of multisubstituted cyclopentane amide derivatives, J. Med. Chem. 47 (2004), pp. 1919–1929. doi:10.1021/jm0303406.
   PubMed Web of Science ®Google Scholar
• P.W. Smith, S.L. Sollis, P.D. Howes, P.C. Cherry, I.D. Starkey, K.N. Cobley, H. Weston, J. Scicinski, A. Merritt, A. Whittington, P. Wyatt, N. Taylor, D. Green, R. Bethell, S. Madar, R.J. Fenton, P.J. Morley, T. Pateman, and A. Beresford, Dihydropyrancarboxamides related to zanamivir: A new series of inhibitors of influenza virus sialidases. 1. Discovery, synthesis, biological activity, and structure-activity relationships of 4-guanidino- and 4-amino-4h-pyran-6-carboxamides, J. Med. Chem. 41 (1998), pp. 787–797. doi:10.1021/jm970374b.
   PubMed Web of Science ®Google Scholar
• G.T. Wang, Y. Chen, S. Wang, R. Gentles, T. Sowin, W. Kati, S. Muchmore, V. Giranda, K. Stewart, H. Sham, D. Kempf, and W.G. Laver, Design, synthesis, and structural analysis of influenza neuraminidase inhibitors containing pyrrolidine cores, J. Med. Chem. 44 (2001), pp. 1192–1201. doi:10.1021/jm000468c.
   PubMed Web of Science ®Google Scholar
• G.T. Wang, S. Wang, R. Gentles, T. Sowin, C.J. Maring, D.J. Kempf, W.M. Kati, V. Stoll, K.D. Stewart, and G. Laver, Design, synthesis, and structural analysis of inhibitors of influenza neuraminidase containing a 2,3-disubstituted tetrahydrofuran-5-carboxylic acid core, Bioorg. Med. Chem. Lett. 15 (2005), pp. 125–128. doi:10.1016/j.bmcl.2004.10.022.
   PubMed Web of Science ®Google Scholar
• K.M. Thai, D.P. Le, N.V. Tran, T.T. Nguyen, T.D. Tran, and M.T. Le, Computational assay of Zanamivir binding affinity with original and mutant influenza neuraminidase 9 using molecular docking, J. Theor. Biol. 385 (2015), pp. 31–39. doi:10.1016/j.jtbi.2015.08.019.
   PubMed Web of Science ®Google Scholar
• H.M. Berman, J. Westbrook, Z. Feng, G. Gilliland, T.N. Bhat, H. Weissig, I.N. Shindyalov, and P.E. Bourne, The protein data bank, Nuc. Acids Res. 28 (2000), pp. 235–242. doi:10.1093/nar/28.1.235.
   PubMed Web of Science ®Google Scholar
• H.J. Böhm, The development of a simple empirical scoring function to estimate the binding constant for a protein-ligand complex of known three-dimensional structure, J. Comput. Aided Mol. Des. 8 (1994), pp. 243–256. doi:10.1007/BF00126743.
   PubMed Web of Science ®Google Scholar
• J. Diharce, M. Cueto, M. Beltramo, V. Aucagne, and P. Bonnet, In silico peptide ligation: Iterative residue docking and linking as a new approach to predict protein-peptide interactions, Molecules 24 (2019), pp. 1351. doi:10.3390/molecules24071351.
   Web of Science ®Google Scholar
• K.C. Chou, Structural bioinformatics and its impact to biomedical science, Curr. Med. Chem. 11 (2004), pp. 2105–2134. doi:10.2174/0929867043364667.
   PubMed Web of Science ®Google Scholar
• X. Zhu, H. Yang, Z. Guo, W. Yu, P.J. Carney, Y. Li, L.M. Chen, J.C. Paulson, R.O. Donis, S. Tong, J. Stevens, and I.A. Wilson, Crystal structures of two subtype N10 neuraminidase-like proteins from bat influenza A viruses reveal a diverged putative active site, Proc. Natl. Acad. Sci. U.S.A. 109 (2012), pp. 18903–18908. doi:10.1073/pnas.1212579109.
   PubMed Web of Science ®Google Scholar
• Q. Li, X.M. Sun, Z.X. Li, Y. Liu, C.J. Vavricka, J.X. Qi, and G.F. Gao, Structural and functional characterization of neuraminidase-like molecule N10 derived from bat influenza A virus, Proc. Natl. Acad. Sci. U.S.A. 109 (2012), pp. 18897–18902. doi:10.1073/pnas.1211037109.
   PubMed Web of Science ®Google Scholar
• R.T. Lee, V. Gunalan, T.D. Van, L.T. Le, F. Eisenhaber, and S. Maurer-Stroh, A new piece in the puzzle of the novel avian-origin influenza A (H7N9) virus, Biol. Direct. 8 (2013), pp. 26. doi:10.1186/1745-6150-8-26.
   PubMed Web of Science ®Google Scholar
• N. Tran, T. Van, H. Nguyen, and L. Le, Identification of novel compounds against an R294K substitution of influenza A (H7N9) virus using ensemble based drug virtual screening, Int. J. Med. Sci. 12 (2015), pp. 163–176. doi:10.7150/ijms.10826.
   PubMed Web of Science ®Google Scholar
• W. Yan, B. Yuhai, J.V. Christopher, S. Xiaoman, Z. Yanfang, G. Feng, Z. Min, X. Haixia, Q. Chengfeng, H. Jianjua, L. Wenjun, Y. Jinghua, Q. Jianxun, and F.G. George, Characterization of two distinct neuraminidases from avian origin human infecting H7N9 influenza viruses, Cell Res. 23 (2013), pp. 1347–1355. doi:10.1038/cr.2013.144.
   PubMed Web of Science ®Google Scholar
• M. Samson, A. Pizzorno, Y. Abed, and G. Boivin, Influenza virus resistance to neuraminidase inhibitors, Antiviral Res. 98 (2013), pp. 174–185. doi:10.1016/j.antiviral.2013.03.014.
   PubMed Web of Science ®Google Scholar
• V.K. Tran-Nguyen, F. Da Silva, G. Bret, and D. Rognan, All in one: Cavity detection, druggability estimate, cavity-based pharmacophore perception, and virtual screening, J. Chem. Inf. Model. 59 (2019), pp. 573–585. doi:10.1021/acs.jcim.8b00684.
   PubMed Web of Science ®Google Scholar
• K.C. Chou and B. Mao, Collective motion in DNA and its role in drug intercalation, Biopolymers 27 (1988), pp. 1795–1815. doi:10.1002/bip.360271109.
   PubMed Web of Science ®Google Scholar