Multiple enzymatic activities associated with severe acute respiratory syndrome coronavirus helicase

Journal of Virology

Volumn 78, Issue 11, 2004, Pages 5619-5632

  Ivanov, A ^a   Thiel, Volker ^a,c   Dobbe, Jessika C ^b   Van Der Meer, Yvonne ^b   Snijder, Eric J ^b   Ziebuhrl, John ^a  

^a UNIVERSITY OF WÜRZBURG   (Germany)

^b LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^c CANTONAL HOSPITAL ST GALLEN   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; CYTIDINE TRIPHOSPHATE; DEOXYRIBONUCLEOTIDE; GUANOSINE TRIPHOSPHATE; HELICASE; HYBRID PROTEIN; NONSTRUCTURAL PROTEIN 13; NUCLEOSIDE TRIPHOSPHATASE; NUCLEOTIDE; PROTEINASE; RNA POLYMERASE; UNCLASSIFIED DRUG; URIDINE TRIPHOSPHATE; VIRUS RNA;

ANIMAL CELL; ARTICLE; CORONAVIRUS; DNA DENATURATION; ENZYME ACTIVITY; ENZYME ASSAY; NONHUMAN; NUCLEOTIDE SEQUENCE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; RESPIRATORY TRACT INFECTION; RNA SYNTHESIS; SARS CORONAVIRUS; SEVERE ACUTE RESPIRATORY SYNDROME; VERO CELL; VIRUS INFECTION;

ACID ANHYDRIDE HYDROLASES; AMINO ACID SEQUENCE; ANIMALS; CERCOPITHECUS AETHIOPS; DNA HELICASES; MOLECULAR SEQUENCE DATA; RNA HELICASES; SARS VIRUS; VERO CELLS; VIRUS REPLICATION;

EID: 2442679084     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.78.11.5619-5632.2004     Document Type: Article

References (92)

1. Ahlquist, P., A. O. Noueiry, W. M. Lee, D. B. Kushner, and B. T. Dye. 2003. Host factors in positive-strand RNA virus genome replication. J. Virol. 77:8181-8186.
2. Almazán, F., J. M. González, Z. Pénzes, A. Izeta, E. Calvo, J. Plana-Durán, and L. Enjuanes. 2000. Engineering the largest RNA virus genome as an infectious bacterial artificial chromosome. Proc. Natl. Acad. Sci. USA 97: 5516-5521.
3. pro) structure: basis for design of anti-SARS drugs. Science 300:1763-1767.
4. Bautista, E. M., K. S. Faaberg, D. Mickelson, and E. D. McGruder. 2002. Functional properties of the predicted helicase of porcine reproductive and respiratory syndrome virus. Virology 298:258-270.
5. Bird, L. E., H. S. Subramanya, and D. B. Wigley. 1998. Helicases: a unifying structural theme? Curr. Opin. Struct. Biol. 8:14-18.
6. Bisaillon, M., J. Bergeron, and G. Lemay. 1997. Characterization of the nucleoside triphosphate phosphohydrolase and helicase activities of the reovirus lambda1 protein. J. Biol. Chem. 272:18298-18303.
7. Bisaillon, M., and G. Lemay. 1997. Characterization of the reovirus lambda1 protein RNA 5′-triphosphatase activity. J. Biol. Chem. 272:29954-29957.
8. Bost, A. G., R. H. Carnahan, X. T. Lu, and M. R. Denison. 2000. Four proteins processed from the replicase gene polyprotein of mouse hepatitis virus colocalize in the cell periphery and adjacent to sites of virion assembly. J. Virol. 74:3379-3387.
9. Bost, A. G., E. Prentice, and M. R. Denison. 2001. Mouse hepatitis virus replicase protein complexes are translocated to sites of M protein accumulation in the ERGIC at late times of infection. Virology 285:21-29.
10. Caruthers, J. M., and D. B. McKay. 2002. Helicase structure and mechanism. Curr. Opin. Struct. Biol. 12:123-133.
11. Casais, R., V. Thiel, S. G. Siddell, D. Cavanagh, and P. Britton. 2001. Reverse genetics system for the avian coronavirus infectious bronchitis virus. J. Virol. 75:12359-12369.
12. Delagoutte, E., and P. H. von Hippel. 2002. Helicase mechanisms and the coupling of helicases within macromolecular machines. I. Structures and properties of isolated helicases. Q. Rev. Biophys. 35:431-478.
13. Denison, M. R., W. J. Spaan, Y. van der Meer, C. A. Gibson, A. C. Sims, E. Prentice, and X. T. Lu. 1999. The putative helicase of the coronavirus mouse hepatitis virus is processed from the replicase gene polyprotein and localizes in complexes that are active in viral RNA synthesis. J. Virol. 73:6862-6871.
14. Drosten, C., S. Günther, W. Preiser, S. van der Werf, H. R. Brodt, S. Becker, H. Rabenau, M. Panning, L. Kolesnikova, R. A. Fouchier, A. Berger, A. M. Burguière, J. Cinatl, M. Eickmann, N. Escriou, K. Grywna, S. Kramme, J. C. Manuguerra, S. Müller, V. Rickerts, M. Stürmer, S. Vieth, H. D. Klenk, A. D. Osterhaus, H. Schmitz, and H. W. Doerr. 2003. Identification of a novel coronavirus in patients with severe acute respiratory syndrome. N. Engl. J. Med. 348:1967-1976.
15. Fan, K., P. Wei, Q. Feng, S. Chen, C. Huang, L. Ma, B. Lai, J. Pei, Y. Liu, J. Chen, and L. Lai. 2003. Biosynthesis, purification and substrate specificity of SARS coronavirus 3C-like proteinase. J. Biol. Chem. 279:1637-1642.
16. Fouchier, R. A., T. Kuiken, M. Schutten, G. van Amerongen, G. J. van Doornum, B. G. van den Hoogen, M. Peiris, W. Lim, K. Stöhr, and A. D. Osterhaus. 2003. Aetiology: Koch's postulates fulfilled for SARS virus. Nature 423:240.
17. Gorbalenya, A. E. 2001. Big nidovirus genome. When count and order of domains matter. Adv. Exp. Med. Biol. 494:1-17.
18. Gorbalenya, A. E., and E. V. Koonin. 1993. Helicases: amino acid sequence comparisons and structure-function relationships. Curr. Opin. Struct. Biol. 3:419-429.
19. Gorbalenya, A. E., E. V. Koonin, A. P. Donchenko, and V. M. Blinov. 1989. Coronavirus genome: prediction of putative functional domains in the non-structural polyprotein by comparative amino acid sequence analysis. Nucleic Acids Res. 17:4847-4861.
20. Gorbalenya, A. E., E. V. Koonin, A. P. Donchenko, and V. M. Blinov. 1989. Two related superfamilies of putative helicases involved in replication, recombination, repair and expression of DNA and RNA genomes. Nucleic Acids Res. 17:4713-4730.
21. Gorbalenya, A. E., E. V. Koonin, and M. M. Lai. 1991. Putative papain-related thiol proteases of positive-strand RNA viruses. Identification of rubi- and aphthovirus proteases and delineation of a novel conserved domain associated with proteases of rubi-, alpha- and coronaviruses. FEBS Lett. 288:201-205.
22. Gosert, R., A. Kanjanahaluethai, D. Egger, K. Bienz, and S. C. Baker. 2002. RNA replication of mouse hepatitis virus takes place at double-membrane vesicles. J. Virol. 76:3697-3708.
23. Hegyi, A., A. Friebe, A. E. Gorbalenya, and J. Ziebuhr. 2002. Mutational analysis of the active centre of coronavirus 3C-like proteases. J. Gen. Virol. 83:581-593.
24. Herold, J., S. Siddell, and J. Ziebuhr. 1996. Characterization of coronavirus RNA polymerase gene products. Methods Enzymol. 275:68-89.
25. Heusipp, G., U. Harms, S. G. Siddell, and J. Ziebuhr. 1997. Identification of an ATPase activity associated with a 71-kilodalton polypeptide encoded in gene 1 of the human coronavirus 229E. J. Virol. 71:5631-5634.
26. Hofstee, B. H., M. Dixon, and E. C. Webb. 1959. Non-inverted versus inverted plots in enzyme kinetics. Nature 184:1296-1298.
27. Kadaré, G., and A. L. Haenni. 1997. Virus-encoded RNA helicases. J. Virol. 71:2583-2590.
28. Kalinina, N. O., D. V. Rakitina, A. G. Solovyev, J. Schiemann, and S. Y. Morozov. 2002. RNA helicase activity of the plant virus movement proteins encoded by the first gene of the triple gene block. Virology 296:321-329.
29. Koonin, E. V. 1991. The phylogeny of RNA-dependent RNA polymerases of positive-strand RNA viruses. J. Gen. Virol. 72:2197-2206.
30. Koonin, E. V., and V. V. Dolja. 1993. Evolution and taxonomy of positive-strand RNA viruses: implications of comparative analysis of amino acid sequences. Crit. Rev. Biochem. Mol. Biol. 28:375-430.
31. Korolev, S., J. Hsieh, G. H. Gauss, T. M. Lohman, and G. Waksman. 1997. Major domain swiveling revealed by the crystal structures of complexes of E. coli Rep helicase bound to single-stranded DNA and ADP. Cell 90:635-647.
32. Ksiazek, T. G., D. Erdman, C. S. Goldsmith, S. R. Zaki, T. Peret, S. Emery, S. Tong, C. Urbani, J. A. Comer, W. Lim, P. E. Rollin, S. F. Dowell, A. E. Ling, C. D. Humphrey, W. J. Shieh, J. Guarner, C. D. Paddock, P. Rota, B. Fields, J. DeRisi, J. Y. Yang, N. Cox, J. M. Hughes, J. W. LeDuc, W. J. Bellini, and L. J. Anderson. 2003. A novel coronavirus associated with severe acute respiratory syndrome. N. Engl. J. Med. 348:1953-1966.
33. Kwong, A. D., J. L. Kim, and C. Lin. 2000. Structure and function of hepatitis C virus NS3 helicase. Curr. Top. Microbiol. Immunol. 242:171-196.
34. Lai, M. M., and D. Cavanagh. 1997. The molecular biology of coronaviruses. Adv. Virus Res. 48:1-100.
35. Lai, M. M., C. D. Patton, and S. A. Stohlman. 1982. Further characterization of mRNAs of mouse hepatitis virus: presence of common 5′-end nucleotides. J. Virol. 41:557-565.
36. Lai, M. M., and S. A. Stohlman. 1981. Genome structure of mouse hepatitis virus: comparative analysis by oligonucleotide mapping. Adv. Exp. Med. Biol. 142:69-82.
37. Lai, M. M. C., and K. V. Holmes. 2001. Coronaviridae: the viruses and their replication, p. 1163-1185. In D. M. Knipe and P. M. Howley (ed.), Fields virology, 4th ed., vol. 1. Lippincott Williams & Wilkins, Philadelphia, Pa.
38. Lee, C. G., and J. Hurwitz. 1992. A new RNA helicase isolated from HeLa cells that catalytically translocates in the 3′ to 5′ direction. J. Biol. Chem. 267:4398-4407.
39. Li, H., S. Clum, S. You, K. E. Ebner, and R. Padmanabhan. 1999. The serine protease and RNA-stimulated nucleoside triphosphatase and RNA helicase functional domains of dengue virus type 2 NS3 converge within a region of 20 amino acids. J. Virol. 73:3108-3116.
40. Li, Y. I., T. W. Shih, Y. H. Hsu, Y. T. Han, Y. L. Huang, and M. Meng. 2001. The helicase-like domain of plant potexvirus replicase participates in formation of RNA 5′ cap structure by exhibiting RNA 5′ -triphosphatase activity. J. Virol. 75:12114-12120.
41. Lohman, T. M., and K. P. Bjornson. 1996. Mechanisms of helicase-catalyzed DNA unwinding. Annu. Rev. Biochem. 65:169-214.
42. Mackenzie, J. M., M. K. Jones, and E. G. Westaway. 1999. Markers for trans-Golgi membranes and the intermediate compartment localize to induced membranes with distinct replication functions in flavivirus-infected cells. J. Virol. 73:9555-9567.
43. Marra, M. A., S. J. Jones, C. R. Astell, R. A. Holt, A. Brooks-Wilson, Y. S. Butterfield, J. Khattra, J. K. Asano, S. A. Barber, S. Y. Chan, A. Cloutier, S. M. Coughlin, D. Freeman, N. Girn, O. L. Griffith, S. R. Leach, M. Mayo, H. McDonald, S. B. Montgomery, P. K. Pandoh, A. S. Petrescu, A. G. Robertson, J. E. Schein, A. Siddiqui, D. E. Smailus, J. M. Stott, G. S. Yang, F. Plummer, A. Andonov, H. Artsob, N. Bastien, K. Bernard, T. F. Booth, D. Bowness, M. Czub, M. Drebot, L. Fernando, R. Flick, M. Garbutt, M. Gray, A. Grolla, S. Jones, H. Feldmann, A. Meyers, A. Kabani, Y. Li, S. Normand, U. Stroher, G. A. Tipples, S. Tyler, R. Vogrig, D. Ward, B. Watson, R. C. Brunham, M. Krajden, M. Petric, D. M. Skowronski, C. Upton, and R. L. Roper. 2003. The genome sequence of the SARS-associated coronavirus. Science 300:1399-1404.
44. Morgenstern, K. A., J. A. Landro, K. Hsiao, C. Lin, Y. Gu, M. S. Su, and J. A. Thomson. 1997. Polynucleotide modulation of the protease, nucleoside triphosphatase, and helicase activities of a hepatitis C virus NS3-NS4A complex isolated from transfected COS cells. J. Virol. 71:3767-3775.
45. Pang, P. S., E. Jankowsky, P. J. Planet, and A. M. Pyle. 2002. The hepatitis C viral NS3 protein is a processive DNA helicase with cofactor enhanced RNA unwinding. EMBO J. 21:1168-1176.
46. Pasternak, A. O., E. van den Born, W. J. Spaan, and E. J. Snijder. 2001. Sequence requirements for RNA strand transfer during nidovirus discontinuous subgenomic RNA synthesis. EMBO J. 20:7220-7228.
47. Pedersen, K. W., Y. van der Meer, N. Roos, and E. J. Snijder. 1999. Open reading frame 1a-encoded subunits of the arterivirus replicase induce endoplasmic reticulum-derived double-membrane vesicles which carry the viral replication complex. J. Virol. 73:2016-2026.
48. Peiris, J. S., C. M. Chu, V. C. Cheng, K. S. Chan, I. F. Hung, L. L. Poon, K. I. Law, B. S. Tang, T. Y. Hon, C. S. Chan, K. H. Chan, J. S. Ng, B. J. Zheng, W. L. Ng, R. W. Lai, Y. Guan, and K. Y. Yuen. 2003. Clinical progression and viral load in a community outbreak of coronavirus-associated SARS pneumonia: a prospective study. Lancet 361:1767-1772.
49. Peiris, J. S., S. T. Lai, L. L. Poon, Y. Guan, L. Y. Yam, W. Lim, J. Nicholls, W. K. Yee, W. W. Yan, M. T. Cheung, V. C. Cheng, K. H. Chan, D. N. Tsang, R. W. Yung, T. K. Ng, and K. Y. Yuen. 2003. Coronavirus as a possible cause of severe acute respiratory syndrome. Lancet 361:1319-1325.
50. Preugschat, F., D. R. Averett, B. E. Clarke, and D. J. Porter. 1996. A steady-state and pre-steady-state kinetic analysis of the NTPase activity associated with the hepatitis C virus NS3 helicase domain. J. Biol. Chem. 271:24449-24457.
51. Rogers, G. W., Jr., W. F. Lima, and W. C. Merrick. 2001. Further characterization of the helicase activity of eIF4A. Substrate specificity. J. Biol. Chem. 276:12598-12608.
52. Rota, P. A., M. S. Oberste, S. S. Monroe, W. A. Nix, R. Campagnoli, J. P. Icenogle, S. Penaranda, B. Bankamp, K. Maher, M. H. Chen, S. Tong, A. Tamin, L. Lowe, M. Frace, J. L. DeRisi, Q. Chen, D. Wang, D. D. Erdman, T. C. Peret, C. Burns, T. G. Ksiazek, P. E. Rollin, A. Sanchez, S. Liffick, B. Holloway, J. Limor, K. McCaustland, M. Olsen-Rasmussen, R. Fouchier, S. Günther, A. D. Osterhaus, C. Drosten, M. A. Pallansch, L. J. Anderson, and W. J. Bellini. 2003. Characterization of a novel coronavirus associated with severe acute respiratory syndrome. Science 300:1394-1399.
53. Ruan, Y. J., C. L. Wei, A. L. Ee, V. B. Vega, H. Thoreau, S. T. Su, J. M. Chia, P. Ng, K. P. Chiu, L. Lim, T. Zhang, C. K. Peng, E. O. Lin, N. M. Lee, S. L. Yee, L. F. Ng, R. E. Chee, L. W. Stanton, P. M. Long, and E. T. Liu. 2003. Comparative full-length genome sequence analysis of 14 SARS coronavirus isolates and common mutations associated with putative origins of infection. Lancet 361:1779-1785.
54. Rust, R. C., L. Landmann, R. Gosert, B. L. Tang, W. Hong, H. P. Hauri, D. Egger, and K. Bienz. 2001. Cellular COPII proteins are involved in production of the vesicles that form the poliovirus replication complex. J. Virol. 75:9808-9818.
55. Salonen, A., L. Vasiljeva, A. Merits, J. Magden, E. Jokitalo, and L. Kääriäinen. 2003. Properly folded nonstructural polyprotein directs the Semliki Forest virus replication complex to the endosomal compartment. J. Virol. 77:1691-1702.
56. Sawicki, S. G., and D. L. Sawicki. 1995. Coronaviruses use discontinuous extension for synthesis of subgenome-length negative strands. Adv. Exp. Med. Biol. 380:499-506.
57. Sawicki, S. G., and D. L. Sawicki. 1998. A new model for coronavirus transcription. Adv. Exp. Med. Biol. 440:215-219.
58. Seybert, A., A. Hegyi, S. G. Siddell, and J. Ziebuhr. 2000. The human coronavirus 229E superfamily 1 helicase has RNA and DNA duplex-unwinding activities with 5′-to-3′ polarity. RNA 6:1056-1068.
59. Seybert, A., L. C. van Dinten, E. J. Snijder, and J. Ziebuhr. 2000. Biochemical characterization of the equine arteritis virus helicase suggests a close functional relationship between arterivirus and coronavirus helicases. J. Virol. 74:9586-9593.
60. Seybert, A., and J. Ziebuhr. 2001. Guanosine triphosphatase activity of the human coronavirus helicase. Adv. Exp. Med. Biol. 494:255-260.
61. Shi, S. T., J. J. Schiller, A. Kanjanahaluethai, S. C. Baker, J. W. Oh, and M. M. Lai. 1999. Colocalization and membrane association of murine hepatitis virus gene 1 products and De novo-synthesized viral RNA in infected cells. J. Virol. 73:5957-5969.
62. Shuman, S. 1995. Capping enzyme in eukaryotic mRNA synthesis. Prog. Nucleic Acid Res. Mol. Biol. 50:101-129.
63. Shuman, S. 2001. Structure, mechanism, and evolution of the mRNA capping apparatus. Prog. Nucleic Acid Res. Mol. Biol. 66:1-40.
64. Singleton, M. R., and D. B. Wigley. 2002. Modularity and specialization in superfamily 1 and 2 helicases. J. Bacteriol. 184:1819-1826.
65. Snijder, E. J., P. J. Bredenbeek, J. C. Dobbe, V. Thiel, J. Ziebuhr, L. L. Poon, Y. Guan, M. Rozanov, W. J. Spaan, and A. E. Gorbalenya. 2003. Unique and conserved features of genome and proteome of SARS-coronavirus, an early split-off from the coronavirus group 2 lineage. J. Mol. Biol. 331:991-1004.
66. Snijder, E. J., H. van Tol, N. Roos, and K. W. Pedersen. 2001. Non-structural proteins 2 and 3 interact to modify host cell membranes during the formation of the arterivirus replication complex. J. Gen. Virol. 82:985-994.
67. Snijder, E. J., A. L. Wassenaar, and W. J. Spaan. 1994. Proteolytic processing of the replicase ORF1a protein of equine arteritis virus. J. Virol. 68: 5755-5764.
68. Soultanas, P., M. S. Dillingham, S. S. Velankar, and D. B. Wigley. 1999. DNA binding mediates conformational changes and metal ion coordination in the active site of PcrA helicase. J. Mol. Biol. 290:137-148.
69. Tanner, J. A., R. M. Watt, Y. B. Chai, L. Y. Lu, M. C. Lin, J. S. Peiris, L. L. Poon, H. F. Kung, and J. D. Huang. 2003. The severe acute respiratory syndrome (SARS) coronavirus NTPase/helicase belongs to a distinct class of 5′ to 3′ viral helicases. J. Biol. Chem. 278:39578-39582.
70. Thiel, V., J. Herold, B. Schelle, and S. G. Siddell. 2001. Infectious RNA transcribed in vitro from a cDNA copy of the human coronavirus genome cloned in vaccinia virus. J. Gen. Virol. 82:1273-1281.
71. Thiel, V., J. Herold, B. Schelle, and S. G. Siddell. 2001. Viral replicase gene products suffice for coronavirus discontinuous transcription. J. Virol. 75: 6676-6681.
72. Thiel, V., K. A. Ivanov, Á. Putics, T. Hertzig, B. Schelle, S. Bayer, B. Weißbrich, E. J. Snijder, H. Rabenau, H. W. Doerr, A. E. Gorbalenya, and J. Ziebuhr. 2003. Mechanisms and enzymes involved in SARS coronavirus genome expression. J. Gen. Virol. 84:2305-2315.
73. Thiel, V., N. Karl, B. Schelle, P. Disterer, I. Klagge, and S. G. Siddell. 2003. Multigene RNA vector based on coronavirus transcription. J. Virol. 77:9790-9798.
74. van der Meer, Y., E. J. Snijder, J. C. Dobbe, S. Schleich, M. R. Denison, W. J. Spaan, and J. Krijnse Locker. 1999. Localization of mouse hepatitis virus nonstructural proteins and RNA synthesis indicates a role for late endosomes in viral replication. J. Virol. 73:7641-7657.
75. van der Meer, Y., H. van Tol, J. Krijnse Locker, and E. J. Snijder. 1998. ORF1a-encoded replicase subunits are involved in the membrane association of the arterivirus replication complex. J. Virol. 72:6689-6698.
76. van Dinten, L. C., J. A. den Boon, A. L. Wassenaar, W. J. Spaan, and E. J. Snijder. 1997. An infectious arterivirus cDNA clone: identification of a replicase point mutation that abolishes discontinuous mRNA transcription. Proc. Natl. Acad. Sci. USA 94:991-996.
77. van Dinten, L. C., H. van Tol, A. E. Gorbalenya, and E. J. Snijder. 2000. The predicted metal-binding region of the arterivirus helicase protein is involved in subgenomic mRNA synthesis, genome replication, and virion biogenesis. J. Virol. 74:5213-5223.
78. Vasiljeva, L., A. Merits, P. Auvinen, and L. Kääriäinen. 2000. Identification of a novel function of the alphavirus capping apparatus. RNA 5′-triphosphatase activity of Nsp2. J. Biol. Chem. 275:17281-17287.
79. Vaux, D., J. Tooze, and S. Fuller. 1990. Identification by anti-idiotype antibodies of an intracellular membrane protein that recognizes a mammalian endoplasmic reticulum retention signal. Nature 345:495-502.
80. Velankar, S. S., P. Soultanas, M. S. Dillingham, H. S. Subramanya, and D. B. Wigley. 1999. Crystal structures of complexes of PcrA DNA helicase with a DNA substrate indicate an inchworm mechanism. Cell 97:75-84.
81. von Grotthuss, M., L. S. Wyrwicz, and L. Rychlewski. 2003. mRNA cap-1 methyltransferase in the SARS genome. Cell 113:701-702.
82. Walker, J. E., M. Saraste, M. J. Runswick, and N. J. Gay. 1982. Distantly related sequences in the alpha- and beta-subunits of ATP synthase, myosin, kinases and other ATP-requiring enzymes and a common nucleotide binding fold. EMBO J. 1:945-951.
83. Warrener, P., and M. S. Collett. 1995. Pestivirus NS3 (p80) protein possesses RNA helicase activity. J. Virol. 69:1720-1726.
84. Wengler, G. 1993. The NS 3 nonstructural protein of flaviviruses contains an RNA triphosphatase activity. Virology 197:265-273.
85. Yang, H., M. Yang, Y. Ding, Y. Liu, Z. Lou, Z. Zhou, L. Sun, L. Mo, S. Ye, H. Pang, G. F. Gao, K. Anand, M. Bartlam, R. Hilgenfeld, and Z. Rao. 2003. The crystal structures of severe acute respiratory syndrome virus main protease and its complex with an inhibitor. Proc. Natl. Acad. Sci. USA 100: 13190-13195.
86. Yount, B., K. M. Curtis, and R. S. Baric. 2000. Strategy for systematic assembly of large RNA and DNA genomes: transmissible gastroenteritis virus model. J. Virol. 74:10600-10611.
87. Yount, B., K. M. Curtis, E. A. Fritz, L. E. Hensley, P. B. Jahrling, E. Prentice, M. R. Denison, T. W. Geisbert, and R. S. Baric. 2003. Reverse genetics with a full-length infectious cDNA of severe acute respiratory syndrome coronavirus. Proc. Natl. Acad. Sci. USA 100:12995-13000.
88. Yount, B., M. R. Denison, S. R. Weiss, and R. S. Baric. 2002. Systematic assembly of a full-length infectious cDNA of mouse hepatitis virus strain A59. J. Virol. 76:11065-11078.
89. Ziebuhr, J., J. Herold, and S. G. Siddell. 1995. Characterization of a human coronavirus (strain 229E) 3C-like proteinase activity. J. Virol. 69:4331-4338.
90. Ziebuhr, J., G. Heusipp, and S. G. Siddell. 1997. Biosynthesis, purification, and characterization of the human coronavirus 229E 3C-like proteinase. J. Virol. 71:3992-3997.
91. Ziebuhr, J., E. J. Snijder, and A. E. Gorbalenya. 2000. Virus-encoded proteinases and proteolytic processing in the Nidovirales. J. Gen. Virol. 81:853-879.
92. Ziebuhr, J., V. Thiel, and A. E. Gorbalenya. 2001. The autocatalytic release of a putative RNA virus transcription factor from its polyprotein precursor involves two paralogous papain-like proteases that cleave the same peptide bond. J. Biol. Chem. 276:33220-33232.