Expression and functions of SARS coronavirus replicative proteins

Molecular Biology of the SARS-Coronavirus

Volumn , Issue , 2010, Pages 75-98

  Ulferts, Rachel ^b   Imbert, Isabelle ^b   Canard, Bruno ^b   Ziebuhr, John ^a  

^a QUEEN'S UNIVERSITY BELFAST   (United Kingdom)

^b NONE

Author keywords

[No Author keywords available]

Indexed keywords

EID: 78651385196     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1007/978-3-642-03683-5_6     Document Type: Chapter

References (126)

1. Allen MD, Buckle AM, Cordell SC, Lowe J, Bycroft M (2003) The crystal structure of AF1521 a protein from Archaeoglobus fulgidus with homology to the non-histone domain of macroH2A. J Mol Biol 330:503-511
2. Almazan F, Galan C, Enjuanes L (2004) The nucleoprotein is required for efficient coronavirus genome replication. J Virol 78:12683-12688
3. Almazan F, Dediego ML, Galan C, Escors D, Alvarez E, Ortego J, Sola I, Zuniga S, Alonso S, Moreno JL, Nogales A, Capiscol C, Enjuanes L (2006) Construction of a severe acute respiratory syndrome coronavirus infectious cDNA clone and a replicon to study coronavirus RNA synthesis. J Virol 80:10900-10906
4. Almeida MS, Johnson MA, Herrmann T, Geralt M, Wuthrich K (2007) Novel beta-barrel fold in the NMR Structure of the replicase nonstructural protein 1 from the SARS coronavirus. J Virol 81:3151-3161
5. Anand K, Palm GJ, Mesters JR, Siddell SG, Ziebuhr J, Hilgenfeld R (2002) Structure of coronavirus main proteinase reveals combination of a chymotrypsin fold with an extra alpha-helical domain. EMBO J 21:3213-3224
6. Anand K, Ziebuhr J, Wadhwani P, Mesters JR, Hilgenfeld R (2003) Coronavirus main proteinase (3CLpro) structure: basis for design of anti-SARS drugs. Science 300:1763-1767
7. Barretto N, Jukneliene D, Ratia K, Chen Z, Mesecar AD, Baker SC (2005) The papain-like protease of severe acute respiratory syndrome coronavirus has deubiquitinating activity. J Virol 79:15189-15198
8. Beese LS, Steitz TA (1991) Structural basis for the 30-50 exonuclease activity of Escherichia coli DNA polymerase I: a two metal ion mechanism. EMBO J 10:25-33
9. Bhardwaj K, Guarino L, Kao CC (2004) The severe acute respiratory syndrome coronavirus Nsp15 protein is an endoribonuclease that prefers manganese as a cofactor. J Virol 78:12218-12224
10. Bhardwaj K, Sun J, Holzenburg A, Guarino LA, Kao CC (2006) RNA recognition and cleavage by the SARS coronavirus endoribonuclease. J Mol Biol 361:243-256
11. Brierley I (1995) Ribosomal frameshifting viral RNAs. J Gen Virol 76:1885-1892
12. Brockway SM, Denison MR (2005) Mutagenesis of the murine hepatitis virus nsp1-coding region identifies residues important for protein processing, viral RNA synthesis, and viral replication. Virology 340:209-223
13. Brockway SM, Lu XT, Peters TR, Dermody TS, Denison MR (2004) Intracellular localization and protein interactions of the gene 1 protein p28 during mouse hepatitis virus replication. J Virol 78:11551-11562
14. Cao J, Wu CC, Lin TL (2008) Turkey coronavirus non-structure protein NSP15-an endoribonuclease. Intervirology 51:342-351
15. Chatterjee A, Johnson MA, Serrano P, Pedrini B, Joseph JS, Neuman BW, Saikatendu K, Buchmeier MJ, Kuhn P, Wuthrich K (2009) Nuclear magnetic resonance structure shows that the severe acute respiratory syndrome coronavirus-unique domain contains a macrodomain fold. J Virol 83:1823-1836
16. Chen P, Jiang M, Hu T, Liu Q, Chen XS, Guo D (2007a) Biochemical characterization of exoribonuclease encoded by SARS coronavirus. J Biochem Mol Biol 40:649-655
17. Chen Z, Wang Y, Ratia K, Mesecar AD, Wilkinson KD, Baker SC (2007b) Proteolytic processing and deubiquitinating activity of papain-like proteases of human coronavirus NL63. J Virol 81:6007-6018
18. Cheng A, Zhang W, Xie Y, Jiang W, Arnold E, Sarafianos SG, Ding J (2005) Expression, purification, and characterization of SARS coronavirus RNA polymerase. Virology 335:165-176
19. Clementz MA, Kanjanahaluethai A, O'Brien TE, Baker SC (2008) Mutation in murine coronavirus replication protein nsp4 alters assembly of double membrane vesicles. Virology 375:118-129
20. Connor RF, Roper RL (2007) Unique SARS-CoV protein nsp1: bioinformatics, biochemistry and potential effects on virulence. Trends Microbiol 15:51-53
21. Decroly E, Imbert I, Coutard B, Bouvet M, Selisko B, Alvarez K, Gorbalenya AE, Snijder EJ, Canard B (2008) Coronavirus nonstructural protein 16 is a cap-0 binding enzyme possessing (nucleoside-2'O)-methyltransferase activity. J Virol 82:8071-8084
22. Deming DJ, Graham RL, Denison MR, Baric RS (2007) Processing of open reading frame 1a replicase proteins nsp7 to nsp10 in murine hepatitis virus strain A59 replication. J Virol 81:10280-10291
23. Devaraj SG, Wang N, Chen Z, Chen Z, Tseng M, Barretto N, Lin R, Peters CJ, Tseng CT, Baker SC, Li K (2007) Regulation of IRF-3-dependent innate immunity by the papain-like protease domain of the severe acute respiratory syndrome coronavirus. J Biol Chem 282:32208-32221
24. Donaldson EF, Graham RL, Sims AC, Denison MR, Baric RS (2007) Analysis of murine hepatitis virus strain A59 temperature-sensitive mutant TS-LA6 suggests that nsp10 plays a critical role in polyprotein processing. J Virol 81:7086-7098
25. Dong H, Ray D, Ren S, Zhang B, Puig-Basagoiti F, Takagi Y, Ho CK, Li H, Shi PY (2007) Distinct RNA elements confer specificity to flavivirus RNA cap methylation events. J Virol 81:4412-4421
26. Dong H, Ren S, Zhang B, Zhou Y, Puig-Basagoiti F, Li H, Shi PY (2008) West Nile virus methyltransferase catalyzes two methylations of the viral RNA cap through a substraterepositioning mechanism. J Virol 82:4295-4307
27. Dos Ramos F, Carrasco M, Doyle T, Brierley I (2004) Programmed-1 ribosomal frameshifting in the SARS coronavirus. Biochem Soc Trans 32:1081-1083
28. Dougherty WG, Semler BL (1993) Expression of virus-encoded proteinases: functional and structural similarities with cellular enzymes. Microbiol Rev 57:781-822
29. Draker R, Roper RL, Petric M, Tellier R (2006) The complete sequence of the bovine torovirus genome. Virus Res 115:56-68
30. Eckerle LD, Lu X, Sperry SM, Choi L, Denison MR (2007) High fidelity of murine hepatitis virus replication is decreased in nsp14 exoribonuclease mutants. J Virol 81:12135-12144
31. Egloff MP, Ferron F, Campanacci V, Longhi S, Rancurel C, Dutartre H, Snijder EJ, Gorbalenya AE, 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 USA 101:3792-3796
32. Egloff MP, Malet H, Putics A, Heinonen M, Dutartre H, Frangeul A, Gruez A, Campanacci V, Cambillau C, Ziebuhr J, Ahola T, Canard B (2006) Structural and functional basis for ADP-ribose and poly (ADP-ribose) binding by viral macro domains. J Virol 80:8493-8502
33. Eriksson KK, Cervantes-Barragan L, Ludewig B, Thiel V (2008) Mouse hepatitis virus liver pathology is dependent on ADP-ribose-1′′- phosphatase, a viral function conserved in the alphalike supergroup. J Virol 82:12325-12334
34. Fan K, Wei P, Feng Q, Chen S, Huang C, Ma L, Lai B, Pei J, Liu Y, Chen J, Lai L (2004) Biosynthesis, purification, and substrate specificity of severe acute respiratory syndrome coronavirus 3C-like proteinase. J Biol Chem 279:1637-1642
35. Fan K, Ma L, Han X, Liang H, Wei P, Liu Y, Lai L (2005) The substrate specificity of SARS coronavirus 3C-like proteinase. Biochem Biophys Res Commun 329:934-940
36. Feder M, Pas J, Wyrwicz LS, Bujnicki JM (2003) Molecular phylogenetics of the RrmJ/fibrillarin superfamily of ribose 2'-O-methyltransferases. Gene 302:129-138
37. Gadlage MJ, Graham RL, Denison MR (2008) Murine coronaviruses encoding nsp2 at different genomic loci have altered replication, protein expression, and localization. J Virol 82:11964-11969
38. Gorbalenya AE, Koonin EV, Donchenko AP, Blinov VM (1989a) Two related superfamilies of putative helicases involved in replication, recombination, repair and expression of DNA and RNA genomes. Nucleic Acids Res 17:4713-4730
39. Gorbalenya AE, Koonin EV, Donchenko AP, Blinov VM (1989b) Coronavirus genome: prediction of putative functional domains in the non-structural polyprotein by comparative amino acid sequence analysis. Nucleic Acids Res 17:4847-4861
40. Gorbalenya AE, Koonin EV, Lai MM (1991) Putative papain-related thiol proteases of positivestrand 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
41. Gorbalenya AE, Enjuanes L, Ziebuhr J, Snijder EJ (2006) Nidovirales: evolving the largest RNA virus genome. Virus Res 117:17-37
42. Gosert R, Kanjanahaluethai A, Egger D, Bienz K, Baker SC (2002) RNA replication of mouse hepatitis virus takes place at double-membrane vesicles. J Virol 76:3697-3708
43. Graham RL, Sims AC, Brockway SM, Baric RS, Denison MR (2005) The nsp2 replicase proteins of murine hepatitis virus and severe acute respiratory syndrome coronavirus are dispensable for viral replication. J Virol 79:13399-13411
44. Guarino LA, Bhardwaj K, Dong W, Sun J, Holzenburg A, Kao C (2005) Mutational analysis of the SARS virus Nsp15 endoribonuclease: identification of residues affecting hexamer formation. J Mol Biol 353:1106-1117
45. Harcourt BH, Jukneliene D, Kanjanahaluethai A, Bechill J, Severson KM, Smith CM, Rota PA, Baker SC (2004) Identification of severe acute respiratory syndrome coronavirus replicase products and characterization of papain-like protease activity. J Virol 78:13600-13612
46. Herold J, Siddell SG (1993) An 'elaborated' pseudoknot is required for high frequency frameshifting during translation of HCV 229E polymerase mRNA. Nucleic Acids Res 21:5838-5842
47. Heusipp G, Harms U, Siddell SG, Ziebuhr J (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
48. Imbert I, Guillemot JC, Bourhis JM, Bussetta C, Coutard B, Egloff MP, Ferron F, Gorbalenya AE, Canard B (2006) A second, non-canonical RNA-dependent RNA polymerase in SARS coronavirus. EMBO J 25:4933-4942
49. Imbert I, Snijder EJ, Dimitrova M, Guillemot JC, Lecine P, Canard B (2008) The SARS-Coronavirus PLnc domain of nsp3 as a replication/transcription scaffolding protein. Virus Res 133:136-148
50. Ivanov KA, Ziebuhr J (2004) Human coronavirus 229E nonstructural protein 13: characterization of duplex-unwinding, nucleoside triphosphatase, and RNA 50-triphosphatase activities. J Virol 78:7833-7838
51. Ivanov KA, Thiel V, Dobbe JC, van der Meer Y, Snijder EJ, Ziebuhr J (2004a) Multiple enzymatic activities associated with severe acute respiratory syndrome coronavirus helicase. J Virol 78:5619-5632
52. Ivanov KA, Hertzig T, Rozanov M, Bayer S, Thiel V, Gorbalenya AE, Ziebuhr J (2004b) Major genetic marker of nidoviruses encodes a replicative endoribonuclease. Proc Natl Acad Sci USA 101:12694-12699
53. Joseph JS, Saikatendu KS, Subramanian V, Neuman BW, Brooun A, Griffith M, Moy K, Yadav MK, Velasquez J, Buchmeier MJ, Stevens RC, Kuhn P (2006) Crystal structure of nonstructural protein 10 from the severe acute respiratory syndrome coronavirus reveals a novel fold with two zinc-binding motifs. J Virol 80:7894-7901
54. Kamitani W, Narayanan K, Huang C, Lokugamage K, Ikegami T, Ito N, Kubo H, Makino S (2006) Severe acute respiratory syndrome coronavirus nsp1 protein suppresses host gene expression by promoting host mRNA degradation. Proc Natl Acad Sci USA 103:12885-12890
55. Kang H, Bhardwaj K, Li Y, Palaninathan S, Sacchettini J, Guarino L, Leibowitz JL, Kao CC (2007) Biochemical and genetic analyses of murine hepatitis virus Nsp15 endoribonuclease. J Virol 81:13587-13597
56. Karras GI, Kustatscher G, Buhecha HR, Allen MD, Pugieux C, Sait F, Bycroft M, Ladurner AG (2005) The macro domain is an ADP-ribose binding module. EMBO J 24:1911-1920
57. Knoops K, Kikkert M, Worm SH, Zevenhoven-Dobbe JC, van der Meer Y, Koster AJ, Mommaas AM, Snijder EJ (2008) SARS-coronavirus replication is supported by a reticulovesicular network of modified endoplasmic reticulum. PLoS Biol 6:e226
58. Koonin EV (1991) The phylogeny of RNA-dependent RNA polymerases of positive-strand RNA viruses. J Gen Virol 72:2197-2206
59. Lai MM, Patton CD, Stohlman SA (1982) Further characterization of mRNA's of mouse hepatitis virus: presence of common 5'-end nucleotides. J Virol 41:557-565
60. Laneve P, Altieri F, Fiori ME, Scaloni A, Bozzoni I, Caffarelli E (2003) Purification, cloning, and characterization of XendoU, a novel endoribonuclease involved in processing of intronencoded small nucleolar RNAs in Xenopus laevis. J Biol Chem 278:13026-13032
61. Langberg SR, Moss B (1981) Post-transcriptional modifications of mRNA. Purification and characterization of cap I and cap II RNA (nucleoside-2'-)- methyltransferases from HeLa cells. J Biol Chem 256:10054-10060
62. Lindner HA, Fotouhi-Ardakani N, Lytvyn V, Lachance P, Sulea T, Menard R (2005) The papainlike protease from the severe acute respiratory syndrome coronavirus is a deubiquitinating enzyme. J Virol 79:15199-15208
63. Lindner HA, Lytvyn V, Qi H, Lachance P, Ziomek E, Menard R (2007) Selectivity in ISG15 and ubiquitin recognition by the SARS coronavirus papain-like protease. Arch Biochem Biophys 466:8-14
64. Marra MA, Jones SJ, Astell CR, Holt RA, Brooks-Wilson A, Butterfield YS, Khattra J, Asano JK, Barber SA, Chan SY, Cloutier A, Coughlin SM, Freeman D, Girn N, Griffith OL, Leach SR, Mayo M, McDonald H, Montgomery SB, Pandoh PK, Petrescu AS, Robertson AG, Schein JE, Siddiqui A, Smailus DE, Stott JM, Yang GS, Plummer F, Andonov A, Artsob H, Bastien N, Bernard K, Booth TF, Bowness D, Czub M, Drebot M, Fernando L, Flick R, Garbutt M, Gray M, Grolla A, Jones S, Feldmann H, Meyers A, Kabani A, Li Y, Normand S, Stroher U, Tipples GA, Tyler S, Vogrig R, Ward D, Watson B, Brunham RC, Krajden M, Petric M, Skowronski DM, Upton C, Roper RL (2003) The Genome sequence of the SARS-associated coronavirus. Science 300:1399-1404
65. Masters PS (2006) The molecular biology of coronaviruses. Adv Virus Res 66:193-292
66. Miknis ZJ, Donaldson EF, Umland TC, Rimmer RA, Baric RS, Schultz LW (2009) SARS-CoV nsp9 dimerization is essential for efficient viral growth. J Virol Jan 19 (Epub ahead of print)
67. Minskaia E, Hertzig T, Gorbalenya AE, Campanacci V, Cambillau C, Canard B, Ziebuhr J (2006) Discovery of an RNA virus 3'->5' exoribonuclease that is critically involved in coronavirus RNA synthesis. Proc Natl Acad Sci USA 103:5108-5113
68. Namy O, Moran SJ, Stuart DI, Gilbert RJ, Brierley I (2006) A mechanical explanation of RNA pseudoknot function in programmed ribosomal frameshifting. Nature 441:244-247
69. Narayanan K, Huang C, Lokugamage K, Kamitani W, Ikegami T, Tseng CT, Makino S (2008) Severe acute respiratory syndrome coronavirus nsp1 suppresses host gene expression, including that of type I interferon, in infected cells. J Virol 82:4471-4479
70. Neuman BW, Joseph JS, Saikatendu KS, Serrano P, Chatterjee A, Johnson MA, Liao L, Klaus JP, Yates JR 3 rd, Wuthrich K, Stevens RC, Buchmeier MJ, Kuhn P (2008) Proteomics analysis unravels the functional repertoire of coronavirus nonstructural protein 3. J Virol 82:5279-5294
71. Neuvonen M, Ahola T (2009) Differential activities of cellular and viral macro domain proteins in binding of ADP-ribose metabolites. J Mol Biol 385:212-225
72. Oostra M, te Lintelo EG, Deijs M, Verheije MH, Rottier PJ, de Haan CA (2007) Localization and membrane topology of coronavirus nonstructural protein 4: involvement of the early secretory pathway in replication. J Virol 81:12323-12336
73. Oostra M, Hagemeijer MC, van Gent M, Bekker CP, te Lintelo EG, Rottier PJ, De Haan CA (2008) Topology and membrane anchoring of the coronavirus replication complex: not all hydrophobic domains of nsp3 and nsp6 are membrane spanning. J Virol 82:12392-12405
74. Palmenberg AC (1990) Proteolytic processing of picornaviral polyprotein. Annu Rev Microbiol 44:603-623
75. Pasternak AO, Spaan W J M, Snijder EJ (2006) Nidovirus transcription: how to make sense...? J Gen Virol 87:1403-1421
76. Plotch SJ, Bouloy M, Ulmanen I, Krug RM (1981) A unique cap (m7G pppXm)-dependent influenza virion endonuclease cleaves capped RNAs to generate the primers that initiate viral RNA transcription. Cell 23:847-858
77. Prentice E, McAuliffe J, Lu X, Subbarao K, Denison MR (2004) Identification and characterization of severe acute respiratory syndrome coronavirus replicase proteins. J Virol 78:9977-9986
78. Putics A, Filipowicz W, Hall J, Gorbalenya AE, Ziebuhr J (2005) ADP-ribose-1′′-monophosphatase: a conserved coronavirus enzyme that is dispensable for viral replication in tissue culture. J Virol 79:12721-12731
79. Putics A, Gorbalenya AE, Ziebuhr J (2006) Identification of protease and ADP-ribose 1′′-monophosphatase activities associated with transmissible gastroenteritis virus non-structural protein 3. J Gen Virol 87:651-656
80. Ratia K, Saikatendu KS, Santarsiero BD, Barretto N, Baker SC, Stevens RC, Mesecar AD (2006) Severe acute respiratory syndrome coronavirus papain-like protease: structure of a viral deubiquitinating enzyme. Proc Natl Acad Sci USA 103:5717-5722
81. Ray D, Shah A, Tilgner M, Guo Y, Zhao Y, Dong H, Deas TS, Zhou Y, Li H, Shi PY (2006) West Nile virus 5'-cap structure is formed by sequential guanine N-7 and ribose 2'-O methylations by nonstructural protein 5. J Virol 80:8362-8370
82. Ricagno S, Egloff MP, Ulferts R, Coutard B, Nurizzo D, Campanacci V, Cambillau C, Ziebuhr J, Canard B (2006) Crystal structure and mechanistic determinants of SARS coronavirus nonstructural protein 15 define an endoribonuclease family. Proc Natl Acad Sci USA 103:11892-11897
83. Rota PA, Oberste MS, Monroe SS, Nix WA, Campagnoli R, Icenogle JP, Penaranda S, Bankamp B, Maher K, Chen MH, Tong S, Tamin A, Lowe L, Frace M, DeRisi JL, Chen Q, Wang D, Erdman DD, Peret TC, Burns C, Ksiazek TG, Rollin PE, Sanchez A, Liffick S, Holloway B, Limor J, McCaustland K, Olsen-Rasmussen M, Fouchier R, Gunther S, Osterhaus AD, Drosten C, Pallansch MA, Anderson LJ, Bellini WJ (2003) Characterization of a novel coronavirus associated with severe acute respiratory syndrome. Science 300:1394-1399
84. Saikatendu KS, Joseph JS, Subramanian V, Clayton T, Griffith M, Moy K, Velasquez J, Neuman BW, Buchmeier MJ, Stevens RC, Kuhn P (2005) Structural basis of severe acute respiratory syndrome coronavirus ADP-ribose-1′′- phosphate dephosphorylation by a conserved domain of nsP3. Structure 13:1665-1675
85. Salonen A, Ahola T, Kaariainen L (2005) Viral RNA replication in association with cellular membranes. Curr Top Microbiol Immunol 285:139-173
86. Sawicki SG, Sawicki DL (1986) Coronavirus minus-strand RNA synthesis and effect of cycloheximide on coronavirus RNA synthesis. J Virol 57:328-334
87. Sawicki SG, Sawicki DL, Siddell SG (2007) A contemporary view of coronavirus transcription. J Virol 81:20-29
88. Schelle B, Karl N, Ludewig B, Siddell SG, Thiel V (2005) Selective replication of coronavirus genomes that express nucleocapsid protein. J Virol 79:6620-6630
89. Schiller JJ, Kanjanahaluethai A, Baker SC (1998) Processing of the coronavirus MHV-JHM polymerase polyprotein: identification of precursors and proteolytic products spanning 400 kilodaltons of ORF1a. Virology 242:288-302
90. Schütze H, Ulferts R, Schelle B, Bayer S, Granzow H, Hoffmann B, Mettenleiter TC, Ziebuhr J (2006) Characterization of White bream virus reveals a novel genetic cluster of nidoviruses. J Virol 80:11598-11609
91. Serrano P, Johnson MA, Almeida MS, Horst R, Herrmann T, Joseph JS, Neuman BW, Subramanian V, Saikatendu KS, Buchmeier MJ, Stevens RC, Kuhn P, Wuthrich K (2007) Nuclear magnetic resonance structure of the N-terminal domain of nonstructural protein 3 from the severe acute respiratory syndrome coronavirus. J Virol 81:12049-12060
92. Seybert A, Hegyi A, Siddell SG, Ziebuhr J (2000) The human coronavirus 229E superfamily 1 helicase has RNA and DNA duplex-unwinding activities with 5'-to-3' polarity. RNA 6:1056-1068
93. Seybert A, Posthuma CC, van Dinten LC, Snijder EJ, Gorbalenya AE, Ziebuhr J (2005) A complex zinc finger controls the enzymatic activities of nidovirus helicases. J Virol 79:696-704
94. Shi ST, Lai MM (2005) Viral and cellular proteins involved in coronavirus replication. Curr Top Microbiol Immunol 287:95-131
95. Shuman S (2001) Structure, mechanism, and evolution of the mRNA capping apparatus. Prog Nucleic Acid Res Mol Biol 66:1-40
96. Snijder EJ, van Tol H, Roos N, Pedersen KW (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
97. Snijder EJ, Bredenbeek PJ, Dobbe JC, Thiel V, Ziebuhr J, Poon LL, Guan Y, Rozanov M, Spaan WJ, Gorbalenya AE (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
98. Spaan W, Delius H, Skinner M, Armstrong J, Rottier P, Smeekens S, van der Zeijst BA, Siddell SG (1983) Coronavirus mRNA synthesis involves fusion of non-contiguous sequences. EMBO J 2:1839-1844
99. Sparks JS, Lu X, Denison MR (2007) Genetic analysis of Murine hepatitis virus nsp4 in virus replication. J Virol 81:12554-12563
100. Su D, Lou Z, Sun F, Zhai Y, Yang H, Zhang R, Joachimiak A, Zhang XC, Bartlam M, Rao Z (2006) Dodecamer structure of severe acute respiratory syndrome coronavirus nonstructural protein nsp10. J Virol 80:7902-7908
101. Sulea T, Lindner HA, Purisima EO, Menard R (2005) Deubiquitination, a new function of the severe acute respiratory syndrome coronavirus papain-like protease? J Virol 79:4550-4551
102. Sutton G, Fry E, Carter L, Sainsbury S, Walter T, Nettleship J, Berrow N, Owens R, Gilbert R, Davidson A, Siddell S, Poon LL, Diprose J, Alderton D, Walsh M, Grimes JM, Stuart DI (2004) The nsp9 replicase protein of SARS-coronavirus, structure and functional insights. Structure 12:341-353
103. Tan J, Verschueren KH, Anand K, Shen J, Yang M, Xu Y, Rao Z, Bigalke J, Heisen B, Mesters JR, Chen K, Shen X, Jiang H, Hilgenfeld R (2005) pH-dependent conformational flexibility of the SARS-CoV main proteinase (M (pro)) dimer: molecular dynamics simulations and multiple X-ray structure analyses. J Mol Biol 354:25-40
104. Tan J, Kusov Y, Mutschall D, Tech S, Nagarajan K, Hilgenfeld R, Schmidt CL (2007) The "SARS-unique domain" (SUD) of SARS coronavirus is an oligo (G)-binding protein. Biochem Biophys Res Commun 364:877-882
105. Tanner JA, Watt RM, Chai YB, Lu LY, Lin MC, Peiris JS, Poon LL, Kung HF, Huang JD (2003) The severe acute respiratory syndrome (SARS) coronavirus NTPase/helicase belongs to a distinct class of 50 to 30 viral helicases. J Biol Chem 278:39578-39582
106. Thiel V, Ivanov KA, Putics A, Hertzig T, Schelle B, Bayer S, Weissbrich B, Snijder EJ, Rabenau H, Doerr HW, Gorbalenya AE, Ziebuhr J (2003) Mechanisms and enzymes involved in SARS coronavirus genome expression. J Gen Virol 84:2305-2315
107. van Dinten LC, van Tol H, Gorbalenya AE, Snijder EJ (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
108. van Hemert MJ, van den Worm SH, Knoops K, Mommaas AM, Gorbalenya AE, Snijder EJ (2008) SARS-coronavirus replication/transcription complexes are membrane-protected and need a host factor for activity in vitro. PLoS Pathog 4:e1000054
109. Wathelet MG, Orr M, Frieman MB, Baric RS (2007) Severe acute respiratory syndrome coronavirus evades antiviral signaling: role of nsp1 and rational design of an attenuated strain. J Virol 81:11620-11633
110. Xu X, Liu Y, Weiss S, Arnold E, Sarafianos SG, Ding J (2003) Molecular model of SARS coronavirus polymerase: implications for biochemical functions and drug design. Nucleic Acids Res 31:7117-7130
111. Xu X, Zhai Y, Sun F, Lou Z, Su D, Xu Y, Zhang R, Joachimiak A, Zhang XC, Bartlam M, Rao Z (2006) New antiviral target revealed by the hexameric structure of mouse hepatitis virus nonstructural protein nsp15. J Virol 80:7909-7917
112. Xu Y, Cong L, Chen C, Wei L, Zhao Q, Xu X, Ma Y, Bartlam M, Rao Z (2009) Crystal structures of two coronavirus ADP-ribose-1′′- monophosphatases and their complexes with ADP-Ribose: a systematic structural analysis of the viral ADRP domain. J Virol 83:1083-1092
113. Xue X, Yu H, Yang H, Xue F, Wu Z, Shen W, Li J, Zhou Z, Ding Y, Zhao Q, Zhang XC, Liao M, Bartlam M, Rao Z (2008) Structures of two coronavirus main proteases: implications for substrate binding and antiviral drug design. J Virol 82:2515-2527
114. Yang H, Yang M, Ding Y, Liu Y, Lou Z, Zhou Z, Sun L, Mo L, Ye S, Pang H, Gao GF, Anand K, Bartlam M, Hilgenfeld R, Rao Z (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
115. Yang H, Xie W, Xue X, Yang K, Ma J, Liang W, Zhao Q, Zhou Z, Pei D, Ziebuhr J, Hilgenfeld R, Yuen KY, Wong L, Gao G, Chen S, Chen Z, Ma D, Bartlam M, Rao Z (2005) Design of widespectrum inhibitors targeting coronavirus main proteases. PLoS Biol 3:e324
116. 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 12:980-986
117. Zhao Q, Li S, Xue F, Zou Y, Chen C, Bartlam M, Rao Z (2008) Structure of the main protease from a global infectious human coronavirus, HCoV-HKU1. J Virol 82:8647-8655
118. Zheng D, Chen G, Guo B, Cheng G, Tang H (2008) PLP2, a potent deubiquitinase from murine hepatitis virus, strongly inhibits cellular type I interferon production. Cell Res 18:1105-1113
119. Ziebuhr J (2005) The coronavirus replicase. Curr Top Microbiol Immunol 287:57-94
120. Ziebuhr J (2008) Coronavirus replicative proteins. In: Perlman S, Gallagher T, Snijder EJ (eds) Nidoviruses. ASM, Washington, DC, pp 65-81
121. Ziebuhr J, Snijder EJ (2007) The coronavirus replicase gene: special enzymes for special viruses. In: Thiel V (ed) Coronaviruses - molecular and cellular biology. Caister Academic, Norfolk, UK, pp 33-63
122. Ziebuhr J, Herold J, Siddell SG (1995) Characterization of a human coronavirus (strain 229E) 3C-like proteinase activity. J Virol 69:4331-4338
123. Ziebuhr J, Snijder EJ, Gorbalenya AE (2000) Virus-encoded proteinases and proteolytic processing in the Nidovirales. J Gen Virol 81:853-879
124. Ziebuhr J, Thiel V, Gorbalenya AE (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
125. Zuo Y, Deutscher MP (2001) Exoribonuclease superfamilies: structural analysis and phylogenetic distribution. Nucleic Acids Res 29:1017-1026
126. Züst R, Cervantes-Barragan L, Kuri T, Blakqori G, Weber F, Ludewig B, Thiel V (2007) Coronavirus non-structural protein 1 is a major pathogenicity factor: implications for the rational design of coronavirus vaccines. PLoS Pathog 3:e109