Proteolytic maturation of replicase polyprotein pp1a by the nsp4 main proteinase is essential for equine arteritis virus replication and includes internal cleavage of nsp7

Journal of General Virology

Volumn 87, Issue 12, 2006, Pages 3473-3482

  van Aken, Danny ^a   Zevenhoven Dobbe, Jessika ^a   Gorbalenya, Alexander E ^a   Snijder, Eric J ^a  

^a LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENTARY DNA; NONSTRUCTURAL PROTEIN 4; NONSTRUCTURAL PROTEIN 7; POLYPROTEIN; PROTEIN PP1A; PROTEINASE; UNCLASSIFIED DRUG; VIRUS PROTEIN;

AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; EQUINE VIRAL ARTERITIS VIRUS; MOLECULAR CLONING; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROCESSING; SITE DIRECTED MUTAGENESIS; VIRAL GENETICS; VIRUS GENOME; VIRUS REPLICATION;

ANIMALS; ARTERITIS VIRUS, EQUINE; CELL LINE; CRICETINAE; GENE PRODUCTS, POL; MUTAGENESIS, SITE-DIRECTED; PEPTIDE HYDROLASES; PROTEIN PROCESSING, POST-TRANSLATIONAL; RNA, VIRAL; VIRAL NONSTRUCTURAL PROTEINS; VIRUS REPLICATION;

ARTERIVIRUS; EQUINE ARTERITIS VIRUS; NIDOVIRALES;

EID: 33751405956     PISSN: 00221317     EISSN: None     Source Type: Journal    
DOI: 10.1099/vir.0.82269-0     Document Type: Article

References (53)

1. Anand, K., Palm, G. J., Mesters, J. R., Siddell, S. G., Ziebuhr, J. & Hilgenfeld, R. (2002). Structure of coronavirus main proteinase reveals combination of a chymotrypsin fold with an extra α-helical domain. EMBO J 21, 3213-3224.
2. Barrette-Ng, I. H., Ng, K. K.-S., Mark B. L., van Aken, D., Cherney, M. M., Garen, C., Kolodenko, Y., Gorbalenya, A. E., Snijder, E. J. & James, M. N. G. (2002). Structure of arterivirus nsp4: the smallest chymotrypsin-like proteinase with an α/ab C-terminal extension and alternate conformations of the oxyanion hole. J Biol Chem 277, 39960-39966.
3. Bartenschlager, R., Ahlborn-Laake, L., Mous, J. & Jacobsen, H. (1994). Kinetic and structural analyses of hepatitis C virus polyprotein processing. J Virol 68, 5045-5055.
4. Bost, A. G., Carnahan, R. H., Lu, X. T. & Denison, M. R. (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.
5. den Boon, J. A., Snijder, E. J., Chirnside, E. D., de Vries, A. A. F., HorzineK M. C. & Spaan, W. J. M. (1991). Equine arter virus is not a togavirus but belongs to the coronaviruslike superfamily. J Virol 65, 2910-2920.
6. Denison, M. R., Yount, B., Brockway, S. M., Graham, R. L., Sims, A. C., Lu, X. & Baric, R. S. (2004). Cleavage between replicase proteins p28 and p65 of mouse hepatitis virus is not required for virus replication. J Virol 78, 5957-5965.
7. de Vries, A. A. F., Chirnside, E. D., Horzinek, M. C. & Rottler, P. J. M. (1992). Structural proteins of equine arteritis virus. J Virol 66, 6294-6303.
8. Ding, M. & Schlesinger, M. J. (1989). Evidence that Sindbis virus NSP2 is an autoprotease which processes the virus nonstructural polyprotein. Virology 171, 280-284.
9. Doll, E. R., Bryans, J. T., McCollum, W. H. & Wallace, M. E. (1957). Isolation of a filterable agent causing arteritis of horses and abortion by mares: its differentiation from the equine abortion (influenza) virus. Cornell Vet 47, 3-41.
10. Edgar, R. C. (2004). MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32, 1792-1797.
11. Egloff, M.-P., Ferron, F., Campanacci, V., Longhl, S., Rancurel, C., Dutartre, H., Snijder, E. J., Gorbalenya, A. E., Cambillau, C. & Canard, B. (2004). The severe acute respiratory syndrome-coronavirus replicative protein nsp9 is a single-stranded RNA-binding subunit unique in the RNA virus world. Proc Natl Acad Sci U S A 101, 3792-3796.
12. Fuerst, T. R., Niles, E. G., Studier, F. W. & Moss, B. (1986). Eukaryotic transient-expression system based on recombinant vaccinia virus that synthesizes bacteriophage T7 RNA polymerase. Proc Natl Acad Sci U S A 83, 8122-8126.
13. Godeny, E. K., Chen, L., Kumar, S. N., Methven, S. L., Koonin, E. V. & Brinton, M. A. (1993). Complete genomic sequence and phylogenetic analysis of the lactate dehydrogenase-elevating virus (LDV). Virology 194, 585-596.
14. Gorbalenya, A. E. & Snijder, E. J. (1996). Viral cysteine proteases. Perspect Drug Discov Des 6, 64-86.
15. Gorbalenya, A. E., Enjuanes, L., Ziebuhr, J. & Snijder, E. J. (2006). Nidovirales: evolving the largest RNA virus genome. Virus Res 117, 17-37.
16. Hardy, M. E., Crone, T. J., Brower, J. E. & Ettayebi, K. (2002). Substrate specificity of the Norwalk virus 3C-like proteinase. Virus Res 89, 29-39.
17. Jore, J., De Geus, B., Jackson, R. J., Pouwels, P. H. & Enger-Valk, B. E. (1988). Poliovirus protein 3CD is the active protease for processing of the precursor protein P1 in vitro. J Gen Virol 69, 1627-1636.
18. Kim, J. C., Spence, R. A., Currier, P. F., Lu, X. & Denison, M. R. (1995). Coronavirus protein processing and RNA synthesis is inhibited by the cysteine proteinase inhibitor E64d. Virology 208, 1-8.
19. Laemmil, U. K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685.
20. Landt O., Grunert, H.-P. & Hahn, U. (1990). A general method for rapid site-directed mutagenesis using the polymerase chain reaction. Gene 96, 125-128.
21. Ropp, S. L., Wees, C. E. M., Fang, Y. & 10 other authors (2004). Characterization of emerging European-like porcine reproductive and respiratory syndrome virus isolates in the United States. J Virol 78, 3684-3703.
22. Rosé, J. R., Babé, L. M. & Cralk, C. S. (1995). Defining the level of human immunodeficiency virus type 1 (HIV-1) protease activity required for HIV-1 particle maturation and infectivity. J Virol 69, 2751-2758.
23. Ryan, M. D. & Flint, M. (1997). Virus-encoded proteinases of the picornavirus super-group. J Gen Virol 78, 699-723.
24. Sambrook J., Fritsch, E. F. & Maniatis, T. (1989). Molecular Cloning: a Laboratory Manual, 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
25. Sawicki, S. G., Sawicki, D. L., Younker, D., Meyer, Y., Thiel, V., Stokes, H. & Siddell, S. G. (2005). Functional and genetic analysis of coronavirus replicase-transcriptase proteins. PLoS Pathog 1, e39.
26. Schechter, I. & Berger, A. (1967). On the size of the active site in proteases. I. Papain. Biochem Biophys Res Commun 27, 157-162.
27. Shen, S., Kwang, J., Liu, W. & Liu, D. X. (2000). Determination of the complete nucleotide sequence of a vaccine strain of porcine reproductive and respiratory syndrome virus and identification of the Nsp2 gene with a unique insertion. Arch Virol 145, 871-883.
28. Siddell, S. G., Ziebuhr, J. & Snijder, E. J. (2005). Coronaviruses, toroviruses and arteriviruses. In Topley and Wilson's Microbiology and Microbial Infections, 10th edn, Virology volume, pp. 823-856. Edited by B. W. Mahy & V. ter Meulen. London: Hodder Arnold.
29. Smits, S. L., Snjjder, E. J. & de Groot R. J. (2006). Characterization of a torovirus main proteinase. J Virol 80, 4157-4167.
30. Snijder, E. J. & Meulenberg, J. J. M. (1998). The molecular biology of arteriviruses. J Gen Virol 79, 961-979.
31. Snijder, E. J. & Meulenberg, J. J. M. (2001). Arteriviruses. In Fields Virology, 4th edn, pp. 1205-1220. Edited by D. M. Knipe & P. M. Howley. Philadelphia, PA: Lippincott Williams & Wilkins.
32. Snijder, E. J., Wassenaar, A. L. M. & Spaan, W. J. M. (1994). Proteolytic processing of the replicase ORF1a protein of equine arteritis virus. J Virol 68, 5755-5764.
33. Snijder, E. J., Wassenaar, A. L. M., van Dinten, L. C., Spaan, W. J. M. & Gorbalenya, A. E. (1996). The arterivirus nsp4 protease is the prototype of a novel group of chymotrypsin-like enzymes, the 3C-like serine proteases. J Biol Chem 271, 4864-4871.
34. Snijder, E. J., Dobbe, J. C. & Spean, W. J. M. (2003). Heterodimerization of the two major envelope proteins is essential for arterivirus infectivity. J Virol 77, 97-104.
35. Snijder, E. J., Brinton, M. A., Faaberg, K. S., Godeny, E. K., Gorbalenya, A. E., MacLachlan, N. J., Mengeling, W. L. & Plagemann, P. G. W. (2005). Family Arteriviridae. In Virus Taxonomy. Eighth Report of the International Committee on Taxonomy of Viruses, pp. 965-974. Edited by C. M. Fauqet, M. A. Mayo, J. Maniloff, U. Desselberger & L. A. Ball. London: Elsevier/Academic Press.
36. Snijder, E. J., van der Meer, Y., Zevenhoven-Dobbe, J., Onderwater, J. J. M., van der Meulen, J., Koerten, H. K. & Mommaas, A. M. (2006). Ultrastructure and origin of membrane vesicles associated with the severe acute respiratory syndrome coronavirus replication complex. J Virol 80, 5927-5940.
37. Spaan, W. J. M., Cavanagh, D., de Groot R. J., Enjuanes, L., Gorbalenya, A. E., Snijder, E. J. & Walker, P. J. (2005). Order Nidovirales. In Virus Taxonomy. Eighth Report of the International Committee on Taxonomy of Viruses, pp. 937-945. Edited by C. M. Fauqet, M. A. Mayo, J. Maniloff, U. Desselberger & L. A. Ball. London: Elsevier/Academic Press.
38. Sutton, G., Fry, E., Carter, L & 14 other authors (2004). The nsp9 replicase protein of SARS-coronavirus, structure and functional insights. Structure 12, 341-353.
39. Tijms, M. A., van Dinten, L C., Gorbalenya, A. E. & Snijder, E. J. (2001). A zinc finger-containing papain-like protease couples subgenomic mRNA synthesis to genome translation in a positive-stranded RNA virus. Proc Natl Acad Sci U S A 98, 1889-1894.
40. van Akenn, D., Benckhuijsen, W. E., Drijfhout, J. W., Wassenaar, A. L. M., Gorbalenya, A. E. & Snijder, E. J. (2006a). Expression, purification, and in vitro activity of an arterivirus main proteinase. Virus Res 120, 97-106.
41. van Aken, D., Snijder, E. J. & Gorbalenya, A. E. (2006b). Mutagenesis analysis of the nsp4 main proteinase reveals determinants of arterivirus replicase polyprotein autoprocessing. J Virol 80, 3428-3437.
42. van der Meer, Y., van Tol, H., Locker, J. K. & Snijder, E. J. (1998). ORF1a-encoded replicase subunits are involved in the membrane association of the arterivirus replication complex. J Virol 72, 6689-6698.
43. van Dinten, L. C., Wassenaar, A. L. M., Gorbalenya, A. E., Spaan, W. J. M. & Snijder, E. J. (1996). Processing of the equine arteritis virus replicase ORF1b protein: identification of cleavage products containing the putative viral polymerase and helicase domains. J Virol 70, 6625-6633.
44. van Dinten, L. C., den Boon, J. A., Wassenaar, A. L. M., Spaan, W. J. M. & Snijder, E. J. (1997). An infectious arterivirus cDNA clone: identification of a replicase point mutation that abolishes discontinuous mRNA transcription. Proc Natl Acad Sci U S A 94, 991-996.
45. van Dinten, L. C., Rensen, S., Gorbalenya, A. E. & Snijder, E. J. (1999). Proteolytic processing of the open reading frame 1b-encoded part of arterivirus replicase is mediated by nsp4 serine protease and is essential for virus replication. J Virol 73, 2027-2037.
46. Wassenaar, A. L. M., Spaan, W. J. M., Gorbalenya, A. E. & Snijder, E. J. (1997). Alternative proteolytic processing of the arterivirus replicase ORF1a polyprotein: evidence that NSP2 acts as a cofactor for the NSP4 serine protease. J Virol 71, 9313-9322.
47. Yang, H., Yang, M., Ding, Y., Liu, Y., Lou, Z., Zhou, Z., Sun, L., Mo, L., Ye, S. & other authors (2003). The crystal structures of severe acute respiratory syndrome virus main protease and its complex with an inhibitor. Proc Natl Acad Sci U S A 100, 13190-13195.
48. Yang, H., Xie, W., Xue, X. & 16 other authors (2005). Design of wide-spectrum inhibitors targeting coronavirus main proteases. PLoS Biol 3, e324.
49. Ypma-Wong, M. F., Dewalt, P. G., Johnson, V. H., Lamb, J. G. & Semler, B. L. (1988). Protein 3CD is the major poliovirus proteinase responsible for cleavage of the P1 capsid precursor. Virology 166, 265-270.
50. Zeng, L, Godeny, E. K, Methven, S. L. & Brinton, M. A. (1995). Analysis of simian hemorrhagic fever virus (SHFV) subgenomic RNAs, junction sequences, and 5′ leader. Virology 207, 543-548.
51. Zhai, Y., Sun, F., Li, X., Pang, H., Xu, X., Bartlam, M. & Rao, Z. (2005). Insights into SARS-CoV transcription and replication from the structure of the nsp7-nsp8 hexadecamer. Nat Struct Mol Biol 12, 990-986.
52. Ziebuhr, J., Snijder, E. J. & Gorbalenya, A. E. (2000). Virus-encoded proteinases and proteolytic processing in the Nidovirales. J Gen Virol 81, 853-879.
53. Ziebuhr, J., Bayer, S., Cowley, J. A. & Gorbalenya, A. E. (2003). The 3C-like proteinase of an invertebrate nidovirus links coronavirus and potyvirus homologs. J Virol 77, 1415-1426.