High-throughput screening identifies inhibitors of the SARS coronavirus main proteinase

Chemistry and Biology

Volumn 11, Issue 10, 2004, Pages 1445-1453

  Blanchard, Jan E ^a   Elowe, Nadine H ^a   Huitema, Carly ^b   Fortin, Pascal D ^b   Cechetto, Jonathan D ^a   Eltis, Lindsay D ^b   Brown, Eric D ^a  

^a MCMASTER UNIVERSITY   (Canada)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CORONAVIRUS; SARS CORONAVIRUS;

EID: 5544272766     PISSN: 10745521     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.chembiol.2004.08.011     Document Type: Article

References (52)

1. World Health Organization (August 14, 2003). Alert, verification and public health management of SARS in the post-outbreak period (http://www.who.int.csr/sars/postoutbreak/en/).
2. World Heath Organization (August 15, 2003). Summary table of SARS cases by country, 1 November 2002 to 31 July 2003 (http://www.who.int/csr/sars/ country/2003_08_15/en/).
3. Ksiazek T.G., Erdman D., Goldsmith C.S., Zaki S.R., Peret T., Emery S., Tong S., Urbani C., Comer J.A., Lim W., Rollin P.E., et al. A novel coronavirus associated with Severe Acute Respiratory Syndrome. N. Engl. J. Med. 348:2003;1953-1966
4. Drosten C., Günther S., Preiser W., van der Werf S., Brodt H.-R., Becker S., Rabenau H., Panning M., Kolesnikova L., Fouchier R.A.M., et al. Identification of a novel coronavirus in patients with Severe Acute Respiratory Syndrome. N. Engl. J. Med. 348:2003;1967-1976
5. Fouchier R.A.M., Kuiken T., Schutten M., van Amerongen G., van Doornum G.J.J., van den Hoogen B.G., Peiris M., Lim W., Stöhr K., Osterhaus A.D.M.E. Koch's postulates fulfilled for SARS virus. Nature. 423:2003;240
6. Marra M.A., Jones S.J.M., Astell C.R., Holt R.A., Brooks-Wilson A., Butterfield Y.S.N., Khattra J., Asano J.K., Barber S.A., Chan S.Y., et al. The genome sequence of the SARS-associated coronavirus. Science. 300:2003;1399-1404
7. Rota P.A., Oberste M.S., Monroe S.S., Nix W.A., Campagnoli R., Icenogle J.P., Peñaranda S., Bankamp B., Maher K., Chen M.-H., et al. Characterization of a novel coronavirus associated with Severe Acute Respiratory Syndrome. Science. 300:2003;1394-1399
8. World Health Organization (January 31, 2004). New case of laboratory-confirmed SARS in Guangdong, China, update 5 (http://www.who.int/csr/ don/2004_01_31/en/).
9. World Health Organization (April 30, 2004). China confirms SARS infection in another previously reported case; summary of cases to date, update 5 (http://www.who.int/csr/don/2004_04_30/en/).
10. Thiel V., Herold J., Schelle B., Siddell S.G. Viral replicase gene products suffice for coronavirus discontinuous transcription. J. Virol. 75:2001;6676-6681
11. Thiel V., Ivanov K.A., Putics Á., Hertzig T., Schelle B., Bayer S., Weißbrich B., Snijder E.J., Rabenau H., Doerr H.W., et al. Mechanisms and enzymes involved in SARS coronavirus genome expression. J. Gen. Virol. 84:2003;2305-2315
12. pro) structure. basis for design of anti-SARS drugs Science. 300:2003;1763-1767
13. Yang H., Yang M., Ding Y., Liu Y., Lou Z., Zhou Z., Sun L., Mo L., Ye S., Pang H., et al. The crystal structures of severe acute respiratory syndrome virus main protease and its complex with an inhibitor. Proc. Natl. Acad. Sci. USA. 100:2003;13190-13195
14. Ziebuhr J., Snijder E.J., Gorbalenya A.E. Virus-encoded proteinases and proteolytic processing in the Nidovirales. J. Gen. Virol. 81:2000;853-879
15. Jenwitheesuk E., Samudrala R. Identifying inhibitors of the SARS coronavirus proteinase. Bioorg. Med. Chem. Lett. 13:2003;3989-3992
16. Huang C., Wei P., Fan K., Liu Y., Lai L. 3C-like proteinase from SARS coronavirus catalyzes substrate hydrolysis by a general base mechanism. Biochemistry. 43:2004;4568-4574
17. Fan K., Wei P., Feng Q., Chen S., Huang C., Ma L., Lai B., Pei J., Liu Y., Chen J., et al. Biosynthesis, purification, and substrate specificity of severe acute respiratory syndrome coronavirus 3C-like proteinase. J. Biol. Chem. 279:2004;1637-1642
18. Chou K.-C., Wei D.-Q., Zhong W.-Z. Binding mechanism of coronavirus main proteinase with ligands and its implication to drug design against SARS. Biochem. Biophys. Res. Commun. 308:2003;148-151
19. Xiong B., Gui C.-S., Xu X.-Y., Luo C., Chen J., Luo H.-B., Chen L.-L., Li G.-W., Sun T., Yu C.-Y., et al. A 3D model of SARS-CoV 3CL proteinase and its inhibitors design by virtual screening. Acta Pharmacol. Sin. 24:2003;497-504
20. Lee V.S., Wittayanarakul K., Remsungnen T., Parasuk V., Sompornpisut P., Chantratita W., Sangma C., Vannarat S., Srichaikul P., Hannongbua S., et al. Structure and dynamics of SARS coronavirus proteinase. the primary key to the designing and screening for anti-SARS drugs ScienceAsia. 29:2003;181-188
21. Toney J.H., Navas-Martin S., Weiss S.R., Koeller A. Sabadinine. a potential non-peptide anti-Severe Acute-Respiratory-Syndrome agent identified using structure-aided design J. Med. Chem. 47:2004;1079-1080
22. Sirois S., Wei D.-Q., Du Q., Chou K.-C. Virtual screening for SARS-CoV protease based on KZ7088 pharmacophore points. J. Chem. Inf. Comput. Sci. 44:2004;1111-1122
23. Tan E.L.C., Ooi E.E., Lin C.-Y., Tan H.C., Ling A.E., Lim B., Stanton L.W. Inhibition of SARS coronavirus infection in vitro with clinically approved antiviral drugs. Emerg. Infect. Dis. 10:2004;581-586
24. Vastag B. Old drugs for a new bug; influenza, HIV drugs enlisted to fight SARS. JAMA. 290:2003;1695-1696
25. Lee N., Hui D., Wu A., Chan P., Cameron P., Joynt G.M., Ahuja A., Yung M.Y., Leung C.B., To K.F., Lui S.F., Szeto C.C., Chung S., Sung J.J.Y. A major outbreak of Severe Acute Respiratory Syndrome in Hong Kong. N. Engl. J. Med. 348:2003;1986-1994
26. Knowles S.R., Phillips E.J., Dresser L., Matukas L. Common adverse events associated with the use of ribavirin for Severe Acute Respiratory Syndrome in Canada. Clin. Infect. Dis. 37:2003;1139-1142
27. Lau A.C.-W., So L.K.-Y., Miu F.P.-L., Yung R.W.-H., Poon E., Cheung T.M.-T., Yam L.Y.-C. Outcome of coronavirus-associated severe acute respiratory syndrome using a standard treatment protocol. Respirology. 9:2004;173-183
28. Yamamoto N., Yang R., Yoshinaka Y., Amari S., Nakano T., Cinatl J., Rabenau H., Doerr H.W., Hunsmann G., Otaka A., et al. HIV protease inhibitor nelfinavir inhibits replication of SARS-associated coronavirus. Biochem. Biophys. Res. Commun. 318:2004;719-725
29. Wu C.-Y., Jan J.-T., Ma S.-H., Kuo C.-J., Juan H.-F., Cheng Y.-S.E., Hsu H.-H., Huang H.-C., Wu D., Brik A., et al. Small molecules targeting severe acute respiratory syndrome human coronavirus. Proc. Natl. Acad. Sci. USA. 101:2004;10012-10017
30. Gershkovich A.A., Kholodovych V.V. Fluorogenic substrates for proteases based on intramolecular fluorescence energy transfer (IFETS). J. Biochem. Biophys. Methods. 33:1996;135-162
31. Liu Y., Kati W., Chen C.-M., Tripathi R., Molla A., Kohlbrenner W. Use of a fluorescence plate reader for measuring kinetic parameters with inner filter effect correction. Anal. Biochem. 267:1999;331-335
32. Shi J., Wei Z., Song J. Dissection study on the Severe Acute Respiratory Syndrome 3C-like protease reveals the critical role of the extra domain in dimerization of the enzyme. J. Biol. Chem. 279:2004;24765-24773
33. Copeland R.A. Mechanistic considerations in high-throughput screening. Anal. Biochem. 320:2003;1-12
34. Lipinski C.A., Lombardo F., Dominy B.W., Feeny P.J. Experimental and computational approaches to estimate solubility and permeability in drug discovery and development settings. Adv. Drug Deliv. Rev. 23:1996;3-25
35. Zolli-Juran M., Cechetto J.D., Hartlen R., Daigle D.M., Brown E.D. High-throughput screening identifies novel inhibitors of Escherichia coli dihydrofolate reductase that are competitive with dihydrofolate. Bioorg. Med. Chem. Lett. 13:2003;2493-2496
36. Zhang J.-H., Chung T.D.Y., Oldenburg K.R. A simple statistical parameter for use in evaluation and validation of high-throughput screening assays. J. Biomol. Screen. 4:1999;67-73
37. Hawkins D.M., Kass G.V. In. Hawkins D.M. Topics in Applied Multivariate Analysis. 1982;269-302 Cambridge University Press, New York
38. Breiman L., Friedman J.H., Olshen R.A., Stone C.J. Classification and Regression Trees. 1984;Chapman & Hall, New York
39. McGovern S.L., Caselli E., Grigorieff N., Shoichet B.K. A common mechanism underlying promiscuous inhibitors from virtual and high-throughput screening. J. Med. Chem. 45:2002;1712-1722
40. Dragovich P.S., Webber S.E., Babine R.E., Fuhrman S.A., Patick A.K., Matthews D.A., Lee C.A., Reich S.H., Prins T.J., Marakovits J.T., et al. Structure-based design, synthesis, and biological evaluation of irreversible human rhinovirus 3C protease inhibitors. 1. Michael acceptor structure-activity studies. J. Med. Chem. 41:1998;2806-2818
41. Matthews D.A., Dragovich P.S., Webber S.E., Fuhrman S.A., Patick A.K., Zalman L.S., Hendrickson T.F., Love R.A., Prins T.J., Marakovits J.T., et al. 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. USA. 96:1999;11000-11007
42. 13C NMR evidence for a thioimidate ester adduct. J. Am. Chem. Soc. 108:1986;1350-1351
43. Webb J.L. Enzyme and Metabolic Inhibitors. Volume. 3 (New(York: Academic Press):1966;. Inc
44. Otto H.-H., Schirmeister T. Cysteine proteases and their inhibitors. Chem. Rev. 97:1997;133-171
45. Allaire M., Chernaia M.M., Malcolm B.A., James M.N.G. Picornaviral 3C cysteine proteinases have a fold similar to chymotrypsin-like serine proteinases. Nature. 369:1994;72-76
46. Richer M.J., Juliano L., Hashimoto C., Jean F. Serpin mechansim of Hepatitis C virus Nonstructural 3 (NS3) protease inhibition. J. Biol. Chem. 279:2004;10222-10227
47. Téllez-Valencia A., Ávila-Ríos S., Pérez-Montfort R., Rodríguez-Romero A., de Gómez-Puyou M.T., López-Calahorra F., Gómez-Puyou A. Highly specific inactivation of triosphosphate isomerase from Trypanosoma cruzi. Biochem. Biophys. Res. Commun. 295:2002;958-963
48. Bhandari P., Gowrishankar J. An Escherichia coli host strain useful for efficient overproduction of cloned gene products with NaCl as the inducer. J. Bacteriol. 179:1997;4403-4406
49. Tabor S., Richardson C. A bacteriophage T7 RNA polymerase/promotor system for controlled exclusive expression of specific genes. Proc. Natl. Acad. Sci. USA. 82:1985;1074-1078
50. Ausubel F.M., Brent R., Kingston R.E., Moore D.D., Seidman J.G., Smith J.A., Struhl K. Current Protocols in Molecular Biology. 1991;Greene Publishing Associates, New York
51. Eltis L.D., Iwagami S.G., Smith M. Hyperexpression of a synthetic gene encoding a high potential iron sulfur protein. Protein Eng. 7:1994;1145-1150
52. Malcolm B.A., Chin S.M., Jewell D.A., Stratton-Thomas J.R., Thudium K.B., Ralston R., Rosenberg S. Expression and characterization of recombinant Hepatitis A virus 3C proteinase. Biochemistry. 31:1992;3358-3363