The crystal structure of hepatitis C virus NS3 proteinase reveals a trypsin-like fold and a structural zinc binding site

Cell

Volumn 87, Issue 2, 1996, Pages 331-342

  Love, Robert A ^a   Parge, Hans E ^a   Wickersham, John A ^a   Hostomsky, Zdenek ^a   Habuka, Noriyuki ^b,c   Moomaw, Ellen W ^a   Adachi, Tsuyoshi ^b,c   Hostomska, Zuzana ^a  

^a AGOURON PHARMACEUTICALS INC   (United States)

^b JAPAN TOBACCO INC   (Japan)

^c UNIVERSITY OF TSUKUBA   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEINASE; VIRUS ENZYME; ZINC;

AMINO TERMINAL SEQUENCE; ARTICLE; BINDING SITE; CRYSTAL STRUCTURE; ENZYME ACTIVE SITE; ENZYME STRUCTURE; ENZYME SUBSTRATE; HEPATITIS C VIRUS; HYDROPHOBICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN FOLDING; VIRUS REPLICATION; X RAY CRYSTALLOGRAPHY;

HEPATITIS C VIRUS;

EID: 0030592514     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0092-8674(00)81350-1     Document Type: Article

References (51)

1. Allaire, M., Chernala, M.M., Malcolm, B.A., and James, M.N.G. (1994). Picornaviral 3C cysteine proteinases have a fold similar to chymotrypsin-like serine proteinases. Nature 369, 72-76.
2. Bartenschlager, R., Ahlborn-Laake, L., Mous, J., and Jacobsen, H. (1994). Kinetic and structural analyses of hepatitis C virus polyprotein processing. J. Virol. 68, 5045-5055.
3. Bartenschlager, R., Ahlborn-Laake, L., Yasargil, K., Mous, J., and Jacobsen, H. (1995). Substrate determinants for cleavage in cis and in trans by the hepatitis C virus NS3 proteinase. J. Virol. 69, 198-205.
4. Bazan, J.F., and Fletterick, R.J. (1988). Viral cysteine proteases are homologous to the trypsin-like family of serine proteases: structural and functional implications. Proc. Natl. Acad. Sci. USA 85, 7872-7876.
5. Brünger, A. (1992a). Free R-value: a novel statistical quantity for assessing the accuracy of crystal structures. Nature 355, 472-475.
6. Brünger, A. (1992b). XPLOR Version 3.1: A System for X-Ray Crystallography and NMR. (New Haven, Connecticut: Yale University).
7. Burley, S.K., and Petsko, G.A. (1986). Amino-aromatic interactions in proteins. FEBS Lett. 203, 139-143.
8. Carson, M. (1991). Ribbons 2.0. J. Appl. Cryst. 24, 958-961.
9. Choi, H.-K., Tong, L., Minor, W., Dumas, P., Boege, U., Rossman, M.G., and Wengler, G. (1991). Structure of Sindbis virus coat protein reveals a chymotrypsin-like serine proteinase and the organization of the virion. Nature 354, 37-43.
10. Choo, Q.L., Kuo, G., Weiner, A.J., Overby, L.R., Bradley, D.W., and Houghton, M. (1989). Isolation of a cDNA clone derived from blood-borne non-A, non-B viral hepatitis. Science 244, 359-362.
11. Choo, Q.L., Richman, K.H., Han, J.H., Berger, K., Lee, C., Dong, C., Gallegos, C., Coit, D., Medina-Selby, R., Barr, P.J., Weiner, A.J., Bradley, D.W., Kuo, G., and Houghton, M. (1991). Genetic organization and diversity of the hepatitis C virus. Proc. Natl. Acad. Sci. USA 88, 2451-2455.
12. Connolly, M.L. (1983). Solvent-accessible surfaces of proteins and nucleic acids. Science 221, 709-713.
13. D'Souza, E.D.A., Grace, K., Sangar, D.V., Rowlands, D.J.,and Clarke, B.E. (1995). In vitro cleavage of hepatitis C virus polyprotein substrates by purified recombinant NS3 protease. J. Gen. Virol. 76, 1729-1736.
14. Engh, R.A., and Huber, R. (1991). Accurate bond and angle parameters for X-ray protein structure refinement. Acta Cryst. A47, 392-400.
15. Failla, C., Tomei, L., and De Francesco, R. (1994). Both NS3 and NS4A are required for proteolytic processing of hepatitis C virus nonstructural proteins. J. Virol. 68, 3753-3760.
16. Fujinaga, M., Delbaere, T.J., Brayer, G.D., and James, M.N.G. (1985). Refined structure of α-lytic protease at 1.7 Å resolution: analysis of hydrogen bonding and solvent structure. J. Mol. Biol. 183, 479-502.
17. Furey, W., and Swaminathan, S. (1990). "PHASES" - a program package for the processing and analysis of diffraction data from macromolecules. ACA Meeting Summaries 73 (New York: American Crystallographic Association).
18. Grakoui, A., McCourt, D.W., Wychowski, C., Feinstone, S.M., and Rice, C.M. (1993). Characterization of the hepatitis C virus-encoded serine proteinase: determination of proteinase-dependent polyprotein cleavage sites. J. Virol. 67, 2832-2843.
19. Han, D.S., Hahm, B., Rho, H.-M., and Jang, S.K. (1995). Identification of the protease domain in NS3 of hepatitis C virus. J. Gen. Virol. 76, 985-993.
20. Hijikata, M., Mizushima, H., Akagi, T., Mori, S., Kakiuchi, N., Kato, N., Tanaka, T., Kimura, K., and Shimotohno, K. (1993). Two distinct proteinase activities required for the processing of a putative non-structural precursor protein of hepatitis C virus. J. Virol. 67, 4665-4675.
21. Houghton, M. (1996). Hepatitis C viruses. In Fields Virology, Third Edition, B.N. Fields, D.M. Knipe, and P.M. Howley, eds. (New York: Raven Press), pp. 1035-1058.
22. Ji, X., Zhang, P., Armstrong, R.N., and Gilliland, G.L. (1992). The three-dimensional structure of a glutathione S-transferase from the Mu class: structural analysis of the binary complex of isoenzyme 3-3 and glutathione at 2.2 Å resolution. Biochemistry 31, 10169-10184.
23. Jones, T.A. (1978). A graphics model building and refinement system for macromolecules. J. Appl. Cryst. 11, 268-272.
24. Kato, N., Hijikata, M., Ootsuyama, Y., Nakagawa, M., Ohkoshi, S., Sugimura, T., and Shimotohno, K. (1990). Molecular cloning of the human hepatitis C virus genome from Japanese patients with non-A, non-B hepatitis. Proc. Natl. Acad. Sci. USA 87, 9524-9528.
25. Koch, J.O., Lohman, V., Herian, U., and Bartenschlager, R. (1996). In vitro studies on the activation of the hepatitis C virus NS3 proteinase by the NS4A cofactor. Virology 221, 54-66.
26. Laskowski, R.J., MacArthur, M.W., Moss, D.S., and Thornton, J.M. (1993). PROCHECK: a program to check the stereochemical quality of protein structures. J Appl. Cryst. 26, 283-291.
27. Levitt, M., and Perutz, M.F. (1988). Aromatic rings as hydrogen bond acceptors. J. Mol. Biol. 201, 751-754.
28. Lin, C. and Rice, C.R. (1995). The hepatitis C virus NS3 serine proteinase and NS4A cofactor: establishment of a cell-free trans-processing assay. Proc. Natl. Acad. Sci. USA 92, 7622-7626.
29. Lin, C., Pragai, B.M., Grakoui, A., Xu, J., and Rice, C.M. (1994). Hepatitis C virus NS3 serine proteinase: trans-cleavage requirements and processing kinetics. J. Virol. 68, 8147-8157.
30. Linnen, J., Wages, J., Jr., Zhang-Keck, Z.-Y., Fry, K.E., Krawczynski, K.Z., Alter, H., Koonin, E., Gallagher, M., Alter, M., Hadziyannis, S., Karayiannis, P., Fung, K., Nakatsuji, Y., Shih, J.W.-K., Young, L., Piatak, M., Jr., Hoover, C., Fernandez, J., Chen, S., Zou, J.-C., Morris, T., Hyams, K.C., Ismay, S., Lifson, J.D., Hess, G., Foung, S.K.H., Thomas, H., Bradley, D., Margolis, H., and Kim, J.P. (1996). Molecular cloning and disease association of hepatitis G virus: a transfusiontransmissible agent. Science 271, 505-508.
31. Liu, S., Ji, X., Gilliland, G.L., Stevens, W.J., and Armstrong, R.N. (1993). Second-sphere electrostatic effects in the active site of glutathione S-transferase: observation of an on-face hydrogen bond between the side chain of threonine 13 and the π-cloud of tyrosine 6 and its influence on catalysis. J. Am. Chem. Soc. 115, 7910-7911.
32. Matthews, D.A., Smith, W.W., Ferre, R.A., Condon, B., Budahazi, G., Sisson, W., Villafranca, J.E., Janson, C.A., McElroy, H.E., Gribskov, C.L., and Worland, S. (1994). Structure of human rhinovirus 3C protease reveals a trypsin-like polypeptide fold, RNA-binding site, and means for cleaving precursor polyprotein. Cell 77, 761-771.
33. McRee, D.E. (1992). XtalView: a visual protein crystallographic system for X11/Xview. J. Mol. Graph. 10, 44-47.
34. Meyer, E., Cole, G., Radhakrishnan, R., and Pepp, O. (1988). Structure of native porcine pancreatic elastase at 1.65 Å resolution. Acta Cryst. B44, 26-38.
35. Miller, R.H., and Purcell, R.H. (1990). Hepatitis C virus shares amino acid sequence similarity with pestiviruses and flaviviruses as well as members of two plant virus supergroups. Proc. Natl. Acad. Sci. USA 87, 2057-2061.
36. Otwinowski, Z., and Minor, W. (1996). Processing of X-ray diffraction data collected in oscillation mode. Meth. Enzymol. 276, 307-326.
37. Pizzi, E., Tramontano, A., Tomei, L., La Monica, N., Failla, C., Sardana, M., Wood, T., and De Francesco, R. (1994). Molecular model of the specificity pocket of the hepatitis C virus protease: implications for substrate recognition. Proc. Natl. Acad. Sci. USA 91, 888-892.
38. Read, R.J., and James, M.N.G. (1986). Introduction to the protein inhibitors: X-ray crystallography. In Proteinase Inhibitors, A.J. Barret and G. Salvesen, eds. (Amsterdam; New York; Oxford: Elsevier Science Publishers BV), pp. 301-336.
39. Schwabe, J.W.R., and Klug, A. (1994). Zinc mining for protein domains. Struct. Biol. 1, 345-349.
40. Simons, J.N., Leary, T.P., Dawson, G.J., Pilot-Matias, TJ., Muerhoff, A.S., Schlauder, G.G., Desai, S.M., and Mushahwar, I.K. (1995). Isolation of novel virus-like sequences associated with human hepatitis. Nature Med. 1, 564-569.
41. Simmonds, P., Smith, D.B., McOmish, F., Yap, P.L., Kolberg, J., Urdea, M.S., and Holmes, E.C. (1994). Identification of genotypes of hepatitis C virus by sequence comparisons in the core, E1 and NS5 regions. J. Gen. Virol. 75, 1053-1061.
42. Sommergruber, W., Casari, G., Fessl, F., Seipelt, J., and Skern, T. (1994). The 2A proteinase of human rhinovirus is a zinc containing enzyme. Virology 204, 815-818.
43. Steinkühler, C., Tomei, L., and De Francesco, R. (1996). In vitro activity of hepatitis C virus protease NS3 purified from recombinant baculovirus-infected SF9 cells. J. Biol. Chem. 277, 6367-6373.
44. Suzich, J.A., Tamura, J.K., Palmer-Hill, F., Warrener, P., Grakoui, A., Rice, C.M., Feinstone, S.M., and Collett, M.S. (1993). Hepatitis C virus NS3 protein polynucleotide-stimulated nucleoside triphosphatase and comparison with related pestivirus and flavivirus enzymes. J. Virol. 67, 6152-6158.
45. Takamizawa, A., Mori, C., Fuke, I., Manabe, S., Murakami, S., Fujita, J., Onishi, E., Andoh, T., Yoshida, I., and Okayama, H. (1991). Structure and organization of the hepatitis C virus genome isolated from human carriers. J. Virol. 65, 1105-1113.
46. Terwilliger, T.C., Kim, S.-H., and Eisenberg, D. (1987). Generalized method of determining heavy-atom positions using the difference Patterson function. Acta Cryst. A43, 1-5.
47. Vallee, B.L., and Auld, D.S. (1990). Zinc coordination, function, and structure of zinc enzymes and other proteins. Biochemistry 29, 5647-5659.
48. van Doorn, L.J. (1994). Review: molecular biology of the hepatitis C virus. J. Med. Virol. 43, 345-356.
49. Voss, T., Meyer, R., and Sommergruber, W. (1995). Spectroscopic characterization of rhinoviral protease 2A: Zn is essential for the structural integrity. Protein Sci. 4, 2526-2531.
50. Wang, B.C. (1985). Resolution of phase ambiguity in macromolecular crystallography. Meth. Enzymol. 115, 90-112.
51. Yu, S.F., and Lloyd, R.E. (1992). Characterization of the roles of conserved cysteine and histidine residues in poliovirus 2A protease. Virology 186, 725-735.