A novel N-heterocycles substituted oseltamivir derivatives as potent inhibitors of influenza virus neuraminidase: discovery, synthesis and biological evaluation

References

• Tang L, Yan H, Wu W, Chen D, Gao Z, Hou J, Zhang C, Jiang Y. Synthesis and anti-influenza virus effects of novel substituted polycyclic pyridone derivatives modified from baloxavir. J Med Chem. 2021;64(19):14465–14476.
   PubMed Web of Science ®Google Scholar
• Wang Z, Zalloum WA, Wang W, Jiang X, De Clercq E, Pannecouque C, Kang D, Zhan P, Liu X. Discovery of novel dihydrothiopyrano[4,3-d]pyrimidine derivatives as potent HIV-1 NNRTIs with significantly reduced hERG inhibitory activity and improved resistance profiles. J Med Chem. 2021;64(18):13658–13675.
   PubMed Web of Science ®Google Scholar
• Fineberg HV. Pandemic preparedness and response–lessons from the H1N1 influenza of 2009. N Engl J Med. 2014;370(14):1335–1342.
   PubMed Web of Science ®Google Scholar
• Swets MC, Russell CD, Harrison EM, Docherty AB, Lone N, Girvan M, Hardwick HE, Visser LG, Openshaw PJM, Groeneveld GH, et al. SARS-CoV-2 co-infection with influenza viruses, respiratory syncytial virus, or adenoviruses. Lancet. 2022;399(10334):1463–1464.
   PubMed Web of Science ®Google Scholar
• Chen JR, Liu YM, Tseng YC, Ma C. Better influenza vaccines: an industry perspective. J Biomed Sci. 2020;27(1):33.
   PubMed Web of Science ®Google Scholar
• Shirley M. Baloxavir marboxil: a review in acute uncomplicated influenza. Drugs. 2020;80(11):1109–1118.
   PubMed Web of Science ®Google Scholar
• Dunn CJ, Goa KL. Zanamivir: a review of its use in influenza. Drugs. 1999;58(4):761–784.
   PubMed Web of Science ®Google Scholar
• McClellan K, Perry CM. Oseltamivir: a review of its use in influenza. Drugs. 2001;61(2):263–283.
   PubMed Web of Science ®Google Scholar
• Scott LJ. Peramivir: a review in uncomplicated influenza. Drugs. 2018;78(14):1525.
   PubMed Web of Science ®Google Scholar
• Kubo S, Tomozawa T, Kakuta M, Tokumitsu A, Yamashita M. Laninamivir prodrug CS-8958, a long-acting neuraminidase inhibitor, shows superior anti-influenza virus activity after a single administration. Antimicrob Agents Chemother. 2010;54(3):1256–1264.
   PubMed Web of Science ®Google Scholar
• Loregian A, Mercorelli B, Nannetti G, Compagnin C, Palù G. Antiviral strategies against influenza virus: towards new therapeutic approaches. Cell Mol Life Sci. 2014;71(19):3659–3683.
   PubMed Web of Science ®Google Scholar
• Baz M, Abed Y, Simon P, Hamelin ME, Boivin G. Effect of the neuraminidase mutation H274Y conferring resistance to oseltamivir on the replicative capacity and virulence of old and recent human influenza A(H1N1) viruses. J Infect Dis. 2010;201(5):740–745.
   PubMed Web of Science ®Google Scholar
• Kode SS, Pawar SD, Tare DS, Keng SS, Hurt AC, Mullick J. A novel I117T substitution in neuraminidase of highly pathogenic avian influenza H5N1 virus conferring reduced susceptibility to oseltamivir and zanamivir. Vet Microbiol. 2019;235:21–24.
   PubMed Web of Science ®Google Scholar
• Wu Y, Wu Y, Tefsen B, Shi Y, Gao GF. Bat-derived influenza-like viruses H17N10 and H18N11. Trends Microbiol. 2014;22(4):183–191.
   PubMed Web of Science ®Google Scholar
• Russell RJ, Haire LF, Stevens DJ, Collins PJ, Lin YP, Blackburn GM, Hay AJ, Gamblin SJ, Skehel JJ. The structure of H5N1 avian influenza neuraminidase suggests new opportunities for drug design. Nature. 2006;443(7107):45–49.
   PubMed Web of Science ®Google Scholar
• Han N, Mu Y. Plasticity of 150-loop in influenza neuraminidase explored by Hamiltonian replica exchange molecular dynamics simulations. PLoS One. 2013;8(4):e60995.
   PubMed Web of Science ®Google Scholar
• Wu Y, Qin G, Gao F, Liu Y, Vavricka CJ, Qi J, Jiang H, Yu K, Gao GF. Induced opening of influenza virus neuraminidase N2 150-loop suggests an important role in inhibitor binding. Sci Rep. 2013;3(1):1551.
   PubMedGoogle Scholar
• Ju H, Zhang J, Sun Z, Huang Z, Qi W, Huang B, Zhan P, Liu X. Discovery of C-1 modified oseltamivir derivatives as potent influenza neuraminidase inhibitors. Eur J Med Chem. 2018;146:220–231.
   PubMed Web of Science ®Google Scholar
• Zhang J, Poongavanam V, Kang D, Bertagnin C, Lu H, Kong X, Ju H, Lu X, Gao P, Tian Y, et al. Optimization of N-substituted oseltamivir derivatives as potent inhibitors of group-1 and -2 influenza a neuraminidases, including a drug-resistant variant. J Med Chem. 2018;61(14):6379–6397.
   PubMed Web of Science ®Google Scholar
• Jia R, Zhang J, Shi F, Bonomini A, Lucca C, Bertagnin C, Zhang J, Liu C, Jia H, Jiang Y, et al. Discovery of N-substituted oseltamivir derivatives as novel neuraminidase inhibitors with improved drug resistance profiles and favorable drug-like properties. Eur J Med Chem. 2023;252:115275.
   PubMed Web of Science ®Google Scholar
• Zhang J, Murugan NA, Tian Y, Bertagnin C, Fang Z, Kang D, Kong X, Jia H, Sun Z, Jia R, et al. Structure-based optimization of n-substituted oseltamivir derivatives as potent anti-influenza a virus agents with significantly improved potency against oseltamivir-resistant N1-H274Y variant, E. J Med Chem. 2018;61(22):9976–9999.
   PubMed Web of Science ®Google Scholar
• Jia R, Zhang J, Ju H, Kang D, Fang Z, Liu X, Zhan P. Discovery of novel anti-influenza agents via contemporary medicinal chemistry strategies (2014-2018 update. Future Med Chem. 2019;11(5):375–378.),
   PubMed Web of Science ®Google Scholar
• Jia R, Zhang J, Bertagnin C, Cherukupalli S, Ai W, Ding X, Li Z, Zhang J, Ju H, Ma X, et al. Discovery of highly potent and selective influenza virus neuraminidase inhibitors targeting 150-cavity. Eur J Med Chem. 2021;212:113097.
   PubMed Web of Science ®Google Scholar
• Jia R, Zhang J, Zhang J, Bertagnin C, Bonomini A, Guizzo L, Gao Z, Ji X, Li Z, Liu C, et al. Discovery of novel boron-containing N-substituted oseltamivir derivatives as anti-influenza A virus agents for overcoming N1-H274Y oseltamivir-resistant. Molecules. 2022;27(19):6426.
   PubMed Web of Science ®Google Scholar
• Xie Y, Xu D, Huang B, Ma X, Qi W, Shi F, Liu X, Zhang Y, Xu W. Discovery of N-substituted oseltamivir derivatives as potent and selective inhibitors of H5N1 influenza neuraminidase. J Med Chem. 2014;57(20):8445–8458.
   PubMed Web of Science ®Google Scholar
• Du J, Guo J, Kang D, Li Z, Wang G, Wu J, Zhang Z, Fang H, Hou X, Huang Z, et al. New techniques and strategies in drug discovery. Chin Chem Lett. 2020;31(7):1695–1708.
   Web of Science ®Google Scholar
• Muratore G, Mercorelli B, Goracci L, Cruciani G, Digard P, Palù G, Loregian A. Human cytomegalovirus inhibitor AL18 also possesses activity against influenza A and B viruses. Antimicrob Agents Chemother. 2012;56(11):6009–6013.
   PubMed Web of Science ®Google Scholar
• Nannetti G, Massari S, Mercorelli B, Bertagnin C, Desantis J, Palù G, Tabarrini O, Loregian A. Potent and broad-spectrum cycloheptathiophene-3-carboxamide compounds that target the PA-PB1 interaction of influenza virus RNA polymerase and possess a high barrier to drug resistance. Antiviral Res. 2019;165:55–64.
   PubMed Web of Science ®Google Scholar
• D’Agostino I, Giacchello I, Nannetti G, Fallacara AL, Deodato D, Musumeci F, Grossi G, Palù G, Cau Y, Trist IM, et al. Synthesis and biological evaluation of a library of hybrid derivatives as inhibitors of influenza virus PA-PB1 interaction. Eur J Med Chem. 2018;157:743–758.
   PubMed Web of Science ®Google Scholar
• Massari S, Bertagnin C, Pismataro MC, Donnadio A, Nannetti G, Felicetti T, Di Bona S, Nizi MG, Tensi L, Manfroni G, et al. Synthesis and characterization of 1,2,4-triazolo[1,5-a]pyrimidine-2-carboxamide-based compounds targeting the PA-PB1 interface of influenza A virus polymerase. Eur J Med Chem. 2021;209:112944.
   PubMed Web of Science ®Google Scholar
• Lu C, Wu C, Ghoreishi D, Chen W, Wang L, Damm W, Ross GA, Dahlgren MK, Russell E, Von Bargen CD, et al. OPLS4: improving force field accuracy on challenging regimes of chemical space. J Chem Theory Comput. 2021;17(7):4291–4300.
   PubMed Web of Science ®Google Scholar
• Sastry GM, Adzhigirey M, Day T, Annabhimoju R, Sherman W. Protein and ligand preparation: parameters, protocols, and influence on virtual screening enrichments. J Comput Aided Mol Des. 2013;27(3):221–234.
   PubMed Web of Science ®Google Scholar
• Sinha SK, Shakya A, Prasad SK, Singh S, Gurav NS, Prasad RS, Gurav SS. An in-silico evaluation of different Saikosaponins for their potency against SARS-CoV-2 using NSP15 and fusion spike glycoprotein as targets. J Biomol Struct Dyn. 2021;39(9):3244–3255.
   PubMed Web of Science ®Google Scholar
• Ju H, Murugan NA, Hou L, Li P, Guizzo L, Zhang Y, Bertagnin C, Kong X, Kang D, Jia R, et al. Identification of C5-NH(2) modified oseltamivir derivatives as novel influenza neuraminidase inhibitors with highly improved antiviral activities and favorable druggability. J Med Chem. 2021;64(24):17992–18009.
   PubMed Web of Science ®Google Scholar
• Bialy D, Shelton H. Functional neuraminidase inhibitor resistance motifs in avian influenza A(H5Nx) viruses. Antiviral Res. 2020;182:104886.
   PubMed Web of Science ®Google Scholar
• Samson M, Pizzorno A, Abed Y, Boivin G. Influenza virus resistance to neuraminidase inhibitors. Antiviral Res. 2013;98(2):174–185.
   PubMed Web of Science ®Google Scholar