The enterovirus protease inhibitor rupintrivir exerts cross-genotypic anti-norovirus activity and clears cells from the norovirus replicon

Antimicrobial Agents and Chemotherapy

Volumn 58, Issue 8, 2014, Pages 4675-4681

  Rocha Pereira, J ^a,b   Nascimento, M S J ^a   Ma, Q ^c   Hilgenfeld, R ^c   Neyts, J ^b   Jochmansb, D ^b  

^a UNIVERSITY OF PORTO   (Portugal)

^b REGA INSTITUTE FOR MEDICAL RESEARCH   (Belgium)

^c UNIVERSITY OF LÜBECK   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

2 PYRROLIDONE DERIVATIVE; 2'-C-METHYLCYTIDINE; AMIDE; ANTIVIRUS AGENT; CYSTEINE PROTEINASE; CYTIDINE; DRUG COMBINATION; FAVIPIRAVIR; ISOXAZOLE DERIVATIVE; PAPAIN; PYRAZINE DERIVATIVE; RNA DIRECTED RNA POLYMERASE; RUPINTRIVIR; VIRUS PROTEIN;

ANALOGS AND DERIVATIVES; ANTAGONISTS AND INHIBITORS; CELL LINE; CHEMISTRY; DRUG COMBINATION; DRUG EFFECTS; DRUG POTENTIATION; ENZYMOLOGY; GENETICS; HUMAN; LIVER CELL; METABOLISM; MOLECULAR DOCKING; NORWALK VIRUS; REPLICON; VIROLOGY; VIRUS REPLICATION;

AMIDES; ANTIVIRAL AGENTS; CELL LINE; CYSTEINE ENDOPEPTIDASES; CYTIDINE; DRUG COMBINATIONS; DRUG SYNERGISM; HEPATOCYTES; HUMANS; ISOXAZOLES; MOLECULAR DOCKING SIMULATION; NORWALK VIRUS; PAPAIN; PYRAZINES; PYRROLIDINONES; REPLICON; RNA REPLICASE; VIRAL PROTEINS; VIRUS REPLICATION;

EID: 84905371055     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.02546-13     Document Type: Article

References (35)

1. Glass RI, Parashar UD, Estes MK. 2009. Norovirus gastroenteritis. N. Engl. J. Med. 361:1776-1785. http://dx.doi.org/10.1056/NEJMra0804575.
2. Patel MM, Widdowson MA, Glass RI, Akazawa K, Vinje J, Parashar UD. 2008. Systematic literature review of role of noroviruses in sporadic gastroenteritis. Emerg. Infect. Dis. 14:1224-1231. http://dx.doi.org/10.3201/eid1408.071114.
3. Beersma MF, Schutten M, Vennema H, Hartwig NG, Mes TH, Osterhaus AD, van Doornum GJ, Koopmans M. 2009. Norovirus in a Dutch tertiary care hospital (2002-2007): frequent nosocomial transmission and dominance of GIIb strains in young children. J. Hosp. Infect. 71:199-205. http://dx.doi.org/10.1016/j.jhin. 2008.11.018.
4. Hansen S, Stamm-Balderjahn S, Zuschneid I, Behnke M, Ruden H, Vonberg RP, Gastmeier P. 2007. Closure of medical departments during nosocomial outbreaks: data from a systematic analysis of the literature. J. Hosp. Infect. 65:348-353. http://dx.doi.org/10.1016/j.jhin.2006.12.018.
5. Bok K, Green KY. 2012. Norovirus gastroenteritis in immunocompromised patients. N. Engl. J. Med. 367:2126-2132. http://dx.doi.org/10.1056/ NEJMra1207742.
6. Zanini B, Ricci C, Bandera F, Caselani F, Magni A, Laronga AM, Lanzini A. 2012. Incidence of post-infectious irritable bowel syndrome and functional intestinal disorders following a water-borne viral gastroenteritis outbreak. Am. J. Gastroenterol. 107:891-899. http://dx.doi.org/10.1038/ajg.2012.102.
7. Binford SL, Weady PT, Maldonado F, Brothers MA, Matthews DA, Patick AK. 2007. In vitro resistance study of rupintrivir, a novel inhibitor of human rhinovirus 3C protease. Antimicrob. Agents Chemother. 51:4366-4373. http://dx.doi.org/10.1128/AAC.00905-07.
8. Patick AK, Binford SL, Brothers MA, Jackson RL, Ford CE, Diem MD, Maldonado F, Dragovich PS, Zhou R, Prins TJ, Fuhrman SA, Meador JW, Zalman LS, Matthews DA, Worland ST. 1999. In vitro antiviral activity of AG7088, a potent inhibitor of human rhinovirus 3C protease. Antimicrob. Agents Chemother. 43:2444-2450.
9. De Palma AM, Purstinger G, Wimmer E, Patick AK, Andries K, Rombaut B, De Clercq E, Neyts J. 2008. Potential use of antiviral agents in polio eradication. Emerg. Infect. Dis. 14:545-551. http://dx.doi.org/10.3201/eid1404.070439.
10. Kim Y, Lovell S, Tiew KC, Mandadapu SR, Alliston KR, Battaile KP, Groutas WC, Chang KO. 2012. Broad-spectrum antivirals against 3C or 3C-like proteases of picornaviruses, noroviruses, and coronaviruses. J. Virol. 86:11754-11762. http://dx.doi.org/10.1128/JVI.01348-12.
11. Zeitler CE, Estes MK, Venkataram Prasad BV. 2006. X-ray crystallographic structure of the Norwalk virus protease at 1.5-A resolution. J. Virol. 80:5050-5058. http://dx.doi.org/10.1128/JVI.80.10.5050-5058.2006.
12. Paeshuyse J, Kaul A, De Clercq E, Rosenwirth B, Dumont JM, Scalfaro P, Bartenschlager R, Neyts J. 2006. The non-immunosuppressive cyclosporin DEBIO-025 is a potent inhibitor of hepatitis C virus replication in vitro. Hepatolog. 43:761-770. http://dx.doi.org/10.1002/hep.21102.
13. Spann KM, Tran KC, Chi B, Rabin RL, Collins PL. 2004. Suppression of the induction of alpha, beta, and lambda interferons by the NS1 and NS2 proteins of human respiratory syncytial virus in human epithelial cells and macrophages [corrected]. J. Virol. 78:4363-4369. http://dx.doi.org/10.1128/JVI.78.8.4363- 4369.2004.
14. Pfaffl MW. 2001. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29:e45. http://dx.doi.org/10.1093/nar/29.9. e45.
15. Rocha-Pereira J, Jochmans D, Dallmeier K, Leyssen P, Nascimento MS, Neyts J. 2012. Favipiravir (T-705) inhibits in vitro norovirus replication. Biochem. Biophys. Res. Commun. 424:777-780. http://dx.doi.org/10.1016/j.bbrc.2012.07.034.
16. Chang KO, Takahashi D, Prakash O, Kim Y. 2012. Characterization and inhibition of norovirus proteases of genogroups I and II using a fluorescence resonance energy transfer assay. Virolog. 423:125-133. http://dx.doi.org/10. 1016/j.virol.2011.12.002.
17. Wilkinson GN. 1961. Statistical estimations in enzyme kinetics. Biochem. J. 80:324-332.
18. Meara JP, Rich DH. 1995. Measurement of individual rate constants of irreversible inhibition of a cysteine proteinase by an epoxysuccinyl inhibitor. Bioorg. Med. Chem. Lett. 5:2277-2282. http://dx.doi.org/10.1016/0960-894X(95) 00396-B.
19. Wang J, Fan T, Yao X, Wu Z, Guo L, Lei X, Wang M, Jin Q, Cui S. 2011. Crystal structures of enterovirus 71 3C protease complexed with rupintrivir reveal the roles of catalytically important residues. J. Virol. 85:10021-10030. http://dx.doi.org/10.1128/JVI.05107-11.
20. Muhaxhiri Z, Deng L, Shanker S, Sankaran B, Estes MK, Palzkill T, Song Y, Prasad BV. 2013. Structural basis of substrate specificity and protease inhibition in Norwalk virus. J. Virol. 87:4281-4292. http://dx.doi.org/10.1128/ JVI.02869-12.
21. Arnold K, Bordoli L, Kopp J, Schwede T. 2006. The SWISS-MODEL workspace: a Web-based environment for protein structure homology modelling. Bioinformatic. 22:195-201. http://dx.doi.org/10.1093/bioinformatics/bti770.
22. Emsley P, Cowtan K. 2004. Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60:2126-2132. http://dx.doi.org/10.1107/S0907444904019158.
23. Wallace AC, Laskowski RA, Thornton JM. 1995. LIGPLOT: a program to generate schematic diagrams of protein-ligand interactions. Protein Eng. 8:127-134. http://dx.doi.org/10.1093/protein/8.2.127.
24. Prichard MN, Shipman C, Jr. 1990. A three-dimensional model to analyze drug-drug interactions. Antiviral Res. 14:181-205. http://dx.doi.org/10.1016/ 0166-3542(90)90001-N.
25. Vliegen I, Delang L, Neyts J. 2013. Selecting and characterizing drugresistant hepatitis C virus replicon. Methods Mol. Biol. 1030:93-103. http://dx.doi.org/10.1007/978-1-62703-484-5-8.
26. Leen EN, Baeza G, Curry S. 2012. Structure of a murine norovirus NS6 protease-product complex revealed by adventitious crystallisation. PLoS On. 7:e38723. http://dx.doi.org/10.1371/journal.pone.0038723.
27. Wobus CE, Thackray LB, Virgin HW. 2006. Murine norovirus: a model system to study norovirus biology and pathogenesis. J. Virol. 80:5104-5112. http://dx.doi.org/10.1128/JVI.02346-05.
28. Cuerrier D, Moldoveanu T, Davies PL. 2005. Determination of peptide substrate specificity for mu-calpain by a peptide library-based approach: the importance of primed side interactions. J. Biol. Chem. 280:40632-40641. http://dx.doi.org/10.1074/jbc.M506870200.
29. Jaulent AM, Fahy AS, Knox SR, Birtley JR, Roque-Rosell N, Curry S, Leatherbarrow RJ. 2007. A continuous assay for foot-and-mouth disease virus 3C protease activity. Anal. Biochem. 368:130-137. http://dx.doi.org/10.1016/j.ab. 2007.05.026.
30. Matthews DA, Dragovich PS, Webber SE, Fuhrman SA, Patick AK, Zalman LS, Hendrickson TF, Love RA, Prins TJ, Marakovits JT, Zhou R, Tikhe J, Ford CE, Meador JW, Ferre RA, Brown EL, Binford SL, Brothers MA, DeLisle DM, Worland ST. 1999. Structure-assisted design of mechanism-based irreversible inhibitors of human rhinovirus 3C protease with potent antiviral activity against multiple rhinovirus serotypes. Proc. Natl. Acad. Sci. U. S. A. 96:11000-11007. http://dx.doi.org/10.1073/pnas.96.20.11000.
31. Tan J, George S, Kusov Y, Perbandt M, Anemuller S, Mesters JR, Norder H, Coutard B, Lacroix C, Leyssen P, Neyts J, Hilgenfeld R. 2013. 3C protease of enterovirus 68: structure-based design of Michael acceptor inhibitors and their broad-spectrum antiviral effects against picornaviruses. J. Virol. 87:4339-4351. http://dx.doi.org/10.1128/JVI.01123-12.
32. Rocha-Pereira J, Jochmans D, Dallmeier K, Leyssen P, Cunha R, Costa I, Nascimento MS, Neyts J. 2012. Inhibition of norovirus replication by the nucleoside analogue 2'-C-methylcytidine. Biochem. Biophys. Res. Commun. 427:796-800. http://dx.doi.org/10.1016/j.bbrc.2012.10.003.
33. Rocha-Pereira J, Jochmans D, Debing Y, Verbeken E, Nascimento MS, Neyts J. 2013. The viral polymerase inhibitor 2'-C-methylcytidine inhibits Norwalk virus replication and protects against norovirus-induced diarrhea and mortality in a mouse model. J. Virol. 87:11798-11805. http://dx.doi.org/10.1128/JVI.02064- 13.
34. Hall AJ, Curns AT, McDonald LC, Parashar UD, Lopman BA. 2012. The roles of Clostridium difficile and norovirus among gastroenteritisassociated deaths in the United States, 1999-2007. Clin. Infect. Dis. 55:216-223. http://dx.doi.org/10.1093/cid/cis386.
35. Lopman BA, Hall AJ, Curns AT, Parashar UD. 2011. Increasing rates of gastroenteritis hospital discharges in U. S. adults and the contribution of norovirus, 1996-2007. Clin. Infect. Dis. 52:466-474. http://dx.doi.org/10.1093/ cid/ciq163.