SARS-coronavirus replication/transcription complexes are membrane-protected and need a host factor for activity in vitro

PLoS Pathogens

Volumn 4, Issue 5, 2008, Pages

  Van Hemert, Martijn J ^a   Van Den Worm, Sjoerd H E ^a   Knoops, Kèvin ^a   Mommaas, A Mieke ^a   Gorbalenya, Alexander E ^a   Snijder, Eric J ^a  

^a LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

DETERGENT; GENOMIC RNA; MESSENGER RNA; NONSTRUCTURAL PROTEIN 1; NUCLEASE; PROTEINASE; RNA DIRECTED RNA POLYMERASE; TRANSCRIPTASE; DACTINOMYCIN; MATRIX PROTEIN; VIRUS RNA;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; CYTOPLASM; MEMBRANE STRUCTURE; NONHUMAN; PROTEIN PROCESSING; PROTEIN SYNTHESIS; RNA DEGRADATION; RNA SYNTHESIS; SARS CORONAVIRUS; VIRUS GENOME; VIRUS REPLICATION; VIRUS TRANSCRIPTION; ANIMAL; BIOSYNTHESIS; CERCOPITHECUS; DRUG EFFECT; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; HOST PATHOGEN INTERACTION; METABOLISM; PATHOGENICITY; PHYSIOLOGY; RABBIT; RNA PROCESSING; ULTRASTRUCTURE; VERO CELL;

SARS CORONAVIRUS;

ANIMALS; CERCOPITHECUS AETHIOPS; CYTOPLASM; DACTINOMYCIN; GENE EXPRESSION REGULATION, VIRAL; GENOME, VIRAL; HOST-PATHOGEN INTERACTIONS; RABBITS; RNA PROCESSING, POST-TRANSCRIPTIONAL; RNA, MESSENGER; RNA, VIRAL; SARS VIRUS; TRANSCRIPTION, GENETIC; VERO CELLS; VIRAL MATRIX PROTEINS; VIRUS REPLICATION;

EID: 44449098281     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1000054     Document Type: Article

References (51)

1. Peiris JS, Guan Y, Yuen KY (2004) Severe acute respiratory syndrome. Nat Med 10: S88-S97.
2. Gorbalenya AE, Enjuanes L, Ziebuhr J, Snijder EJ (2006) Nidovirales: evolving the largest RNA virus genome. Virus Res 117: 17-37.
3. Pasternak AO, Spaan WJ, Snijder EJ (2006) Nidovirus transcription: how to make sense...? J Gen Virol 87: 1403-1421.
4. Sawicki SG, Sawicki DL, Siddell SG (2007) A contemporary view of coronavirus transcription. J Virol 81: 20-29.
5. Snijder EJ, Bredenbeek PJ, Dobbe JC, Thiel V, Ziebuhr J, et al. (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.
6. Thiel V, Ivanov KA, Putics A, Hertzig T, Schelle B, et al. (2003) Mechanisms and enzymes involved in SARS coronavirus genome expression. J Gen Virol 84: 2305-2315.
7. Lindner HA, Fotouhi-Ardakani N, Lytvyn V, Lachance P, Sulea T, et al. (2005) The papain-like protease from the severe acute respiratory syndrome coronavirus is a deubiquitinating enzyme. J Virol 79: 15199-15208.
8. Harcourt BH, Jukneliene D, Kanjanahaluethai A, Bechill J, Severson KM, et al. (2004) Identification of severe acute respiratory syndrome coronavirus replicase products and characterization of papain-like protease activity. J Virol 78: 13600-13612.
9. Yang H, Yang M, Ding Y, Liu Y, Lou Z, et al. (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.
10. Graziano V, McGrath WJ, DeGruccio AM, Dunn JJ, Mangel WF (2006) Enzymatic activity of the SARS coronavirus main proteinase dimer. FEBS Lett 580: 2577-2583.
11. Tan YJ, Lim SG, Hong W (2005) Characterization of viral proteins encoded by the SARS-coronavirus genome. Antiviral Res 65: 69-78.
12. Ziebuhr J (2004) Molecular biology of severe acute respiratory syndrome coronavirus. Curr Opin Microbiol 7: 412-419.
13. Cheng A, Zhang W, Xie Y, Jiang W, Arnold E, et al. (2005) Expression, purification, and characterization of SARS coronavirus RNA polymerase. Virology 335: 165-176.
14. Ivanov KA, Thiel V, Dobbe JC, van der Meer Y, Snijder EJ, et al. (2004) Multiple enzymatic activities associated with severe acute respiratory syndrome coronavirus helicase. J Virol 78: 5619-5632.
15. Imbert I, Guillemot JC, Bourhis JM, Bussetta C, Coutard B, et al. (2006) A second, non-canonical RNA-dependent RNA polymerase in SARS coronavirus. EMBO J 25: 4933-4942.
16. Zhai Y, Sun F, Li X, Pang H, Xu X, et al. (2005) Insights into SARS-CoV transcription and replication from the structure of the nsp7-nsp8 hexadecamer. Nat Struct Mol Biol 12: 980-986.
17. Minskaia E, Hertzig T, Gorbalenya AE, Campanacci V, Cambillau C, et al. (2006) Discovery of an RNA virus 39-.59 exoribonuclease that is critically involved in coronavirus RNA synthesis. Proc Natl Acad Sci U S A 103: 5108-5113.
18. 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.
19. 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.
20. Ivanov KA, Hertzig T, Rozanov M, Bayer S, Thiel V, et al. (2004) Major genetic marker of nidoviruses encodes a replicative endoribonuclease. Proc Natl Acad Sci U S A 101: 12694-12699.
21. 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.
22. Ricagno S, Egloff MP, Ulferts R, Coutard B, Nurizzo D, et al. (2006) Crystal structure and mechanistic determinants of SARS coronavirus nonstructural protein 15 define an endoribonuclease family. Proc Natl Acad Sci U S A 103: 11892-11897.
23. Kanjanahaluethai A, Chen Z, Jukneliene D, Baker SC (2007) Membrane topology of murine coronavirus replicase nonstructural protein 3. Virology 361: 391-401.
24. Oostra M, te Lintelo EG, Deijs M, Verheije MH, Rottier PJ, et al. (2007) Localization and membrane topology of coronavirus nonstructural protein 4: involvement of the early secretory pathway in replication. J Virol 81: 12323-12336.
25. 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.
26. Snijder EJ, van der Meer Y, Zevenhoven-Dobbe J, Onderwater JJ, van der Meulen J, et al. (2006) Ultrastructure and origin of membrane vesicles associated with the severe acute respiratory syndrome coronavirus replication complex. J Virol 80: 5927-5940.
27. Stertz S, Reichelt M, Spiegel M, Kuri T, Martinez-Sobrido L, et al. (2007) The intracellular sites of early replication and budding of SARS-coronavirus. Virology 361: 304-315.
28. Goldsmith CS, Tatti KM, Ksiazek TG, Rollin PE, Comer JA, et al. (2004) Ultrastructural characterization of SARS coronavirus. Emerg Infect Dis 10: 320-326.
29. Ng ML, Tan SH, See EE, Ooi EE, Ling AE (2003) Proliferative growth of SARS coronavirus in Vero E6 cells. J Gen Virol 84: 3291-3303.
30. Kamitani W, Narayanan K, Huang C, Lokugamage K, Ikegami T, et al. (2006) Severe acute respiratory syndrome coronavirus nsp1 protein suppresses host gene expression by promoting host mRNA degradation. Proc Natl Acad Sci U S A 103: 12885-12890.
31. Mackenzie J (2005) Wrapping things up about virus RNA replication. Traffic 6: 967-977.
32. Salonen A, Ahola T, Kaariainen L (2005) Viral RNA replication in association with cellular membranes. Curr Top Microbiol Immunol 285: 139-173.
33. Novoa RR, Calderita G, Arranz R, Fontana J, Granzow H, et al. (2005) Virus factories: associations of cell organelles for viral replication and morphogenesis. Biol of the Cell 97: 147-172.
34. Ziebuhr J (2005) The coronavirus replicase. Curr Top Microbiol Immunol 287: 57-94.
35. Brayton PR, Lai MM, Patton CD, Stohlman SA (1982) Characterization of two RNA polymerase activities induced by mouse hepatitis virus. J Virol 42: 847-853.
36. Brayton PR, Stohlman SA, Lai MM (1984) Further characterization of mouse hepatitis virus RNA-dependent RNA polymerases. Virology 133: 197-201.
37. Mahy BW, Siddell S, Wege H, ter MV (1983) RNA-dependent RNA polymerase activity in murine coronavirus-infected cells. J Gen Virol 64: 103-111.
38. Compton SR, Rogers DB, Holmes KV, Fertsch D, Remenick J, et al. (1987) In vitro replication of mouse hepatitis virus strain A59. J Virol 61: 1814-1820.
39. Dennis DE, Brian DA (1982) RNA-dependent RNA polymerase activity in coronavirus- infected cells. J Virol 42: 153-164.
40. Leibowitz JL, DeVries JR (1988) Synthesis of virus-specific RNA in permeabilized murine coronavirus-infected cells. Virology 166: 66-75.
41. Sawicki SG, Sawicki DL (1986) Coronavirus minus-strand RNA synthesis and effect of cycloheximide on coronavirus RNA synthesis. J Virol 57: 328-334.
42. Baric RS, Yount B (2000) Subgenomic negative-strand RNA function during mouse hepatitis virus infection. J Virol 74: 4039-4046.
43. Kim JC, Spence RA, Currier PF, Lu X, Denison MR (1995) Coronavirus protein processing and RNA synthesis is inhibited by the cysteine proteinase inhibitor E64d. Virology 208: 1-8.
44. Sparks JS, Lu X, Denison MR (2007) Genetic analysis of Murine hepatitis virus nsp4 in virus replication. J Virol 81: 12554-12563.
45. Sutton G, Fry E, Carter L, Sainsbury S, Walter T, et al. (2004) The nsp9 replicase protein of SARS-coronavirus, structure and functional insights. Structure 12: 341-353.
46. Sethna PB, Brian DA (1997) Coronavirus genomic and subgenomic minus-strand RNAs copartition in membrane-protected replication complexes. J Virol 71: 7744-7749.
47. Aizaki H, Lee KJ, Sung VM, Ishiko H, Lai MM (2004) Characterization of the hepatitis C virus RNA replication complex associated with lipid rafts. Virology 324: 450-461.
48. Shi ST, Lee KJ, Aizaki H, Hwang SB, Lai MM (2003) Hepatitis C virus RNA replication occurs on a detergent-resistant membrane that cofractionates with caveolin-2. J Virol 77: 4160-4168.
49. Miyanari Y, Atsuzawa K, Usuda N, Watashi K, Hishiki T, et al. (2007) The lipid droplet is an important organelle for hepatitis C virus production. Nat Cell Biol 9: 1089-1097.
50. Li GM, Li YG, Yamate M, Li SM, Ikuta K (2007) Lipid rafts play an important role in the early stage of severe acute respiratory syndrome-coronavirus life cycle. Microbes Infect 9: 96-102.
51. van Marle G, van Dinten LC, Spaan WJ, Luytjes W, Snijder EJ (1999) Characterization of an equine arteritis virus replicase mutant defective in subgenomic mRNA synthesis. J Virol 73: 5274-5281.