SARS-coronavirus replication is supported by a reticulovesicular network of modified endoplasmic reticulum

PLoS Biology

Volumn 6, Issue 9, 2008, Pages 1957-1974

  Knoops, Kèvin ^a   Kikkert, Marjolein ^a   Van Den Worm, Sjoerd H E ^a   Zevenhoven Dobbe, Jessika C ^a   Van Der Meer, Yvonne ^a   Koster, Abraham J ^a   Mommaas, A Mieke ^a   Snijder, Eric J ^a  

^a LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

DOUBLE STRANDED RNA; VIRUS RNA; RNA DIRECTED RNA POLYMERASE; VIRUS PROTEIN;

ANTIBODY LABELING; ARTICLE; CELL MEMBRANE; CYTOSOL; ELECTRON MICROSCOPY; ENDOPLASMIC RETICULUM; MEMBRANE VESICLE; NONHUMAN; RNA SYNTHESIS; SARS CORONAVIRUS; THREE DIMENSIONAL IMAGING; VIRUS REPLICATION; ANIMAL; BIOLOGICAL MODEL; CELL LINE; CRYOELECTRON MICROSCOPY; GENETICS; HUMAN; IMMUNOHISTOCHEMISTRY; INTRACELLULAR MEMBRANE; MACROMOLECULE; METABOLISM; PHYSIOLOGY; PROTEIN SUBUNIT; ULTRASTRUCTURE;

CORONAVIRUS; DASHEEN MOSAIC VIRUS; RNA VIRUSES; SARS CORONAVIRUS;

ANIMALS; CELL LINE; CRYOELECTRON MICROSCOPY; ENDOPLASMIC RETICULUM; HUMANS; IMAGING, THREE-DIMENSIONAL; IMMUNOHISTOCHEMISTRY; INTRACELLULAR MEMBRANES; MACROMOLECULAR SUBSTANCES; MODELS, BIOLOGICAL; PROTEIN SUBUNITS; RNA REPLICASE; RNA, DOUBLE-STRANDED; RNA, VIRAL; SARS VIRUS; VIRAL PROTEINS; VIRUS REPLICATION;

EID: 54749157085     PISSN: 15449173     EISSN: 15457885     Source Type: Journal    
DOI: 10.1371/journal.pbio.0060226     Document Type: Article

References (79)

1. Bienz K, Egger D, Pfister T, Troxler M (1992) Structural and functional characterization of the poliovirus replication complex. J Virol 66: 2740-2747.
2. Ahlquist P (2006) Parallels among positive-strand RNA viruses, reverse-transcribing viruses and double-stranded RNA viruses. Nat Rev Microbiol 4: 371-382.
3. Mackenzie J (2005) Wrapping things up about virus RNA replication. Traffic 6: 967-977.
4. Novoa RR, Calderita G, Arranz R, Fontana J, Granzow H, Risco C (2005) Virus factories: associations of cell organelles for viral replication and morphogenesis. Biol Cell 97: 147-172.
5. Netherton C, Moffat K, Brooks E, Wileman T (2007) A guide to viral inclusions, membrane rearrangements, factories, and viroplasm produced during virus replication. Adv Virus Res 70: 101-182.
6. Kirkegaard K, Jackson WT (2005) Topology of double-membraned vesicles and the opportunity for non-lytic release of cytoplasm. Autophagy 1: 182-184.
7. Kopek BG, Perkins G, Miller DJ, Ellisman MH, Ahlquist P (2007) Three-dimensional analysis of a viral RNA replication complex reveals a virusinduced mini-organelle. PLoS Biol 5: e220. doi:10.1371/journal.pbio.0050220
8. Miller S, Krijnse Locker J (2008) Modification of intracellular membrane structures for virus replication. Nat Rev Microbiol 6: 363-374.
9. Haller O, Kochs G, Weber F (2006) The interferon response circuit: induction and suppression by pathogenic viruses. Virology 344: 119-130.
10. Garcia-Sastre A, Biron CA (2006) Type 1 interferons and the virus-host relationship: a lesson in detente. Science 312: 879-882.
11. Peiris JSM, Guan Y, Yuen KY (2004) Severe acute respiratory syndrome. Nat Med 10: S88-S97.
12. Pyrc K, Berkhout B, van der Hoek L (2007) The novel human coronaviruses NL63 and HKU1. J Virol 81: 3051-3057.
13. Ziebuhr J (2004) Molecular biology of severe acute respiratory syndrome coronavirus. Curr Opin Microbiol 7: 412-419.
14. Gorbalenya AE, Enjuanes L, Ziebuhr J, Snijder EJ (2006) Nidovirales: evolving the largest RNA virus genome. Virus Res 117: 17-37.
15. 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.
16. Prentice E, McAuliffe J, Lu XT, Subbarao K, Denison MR (2004) Identification and characterization of severe acute respiratory syndrome coronavirus replicase proteins. J Virol 78: 9977-9986.
17. 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.
18. 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.
19. Pasternak AO, Spaan WJM, Snijder EJ (2006) Nidovirus transcription: how to make sense. . .? J Gen Virol 87: 1403-1421.
20. Sawicki SG, Sawicki DL, Siddell SG (2007) A contemporary view of coronavirus transcription. J Virol 81: 20-29.
21. Krijnse Locker J, Ericsson M, Rottier PJM, Griffiths G (1994) Characterization of the budding compartment of mouse hepatitis virus: evidence that transport from RER to the Golgi complex requires only one vesicular transport step. J Cell Biol 124: 55-70.
22. Masters PS (2006) The molecular biology of coronaviruses. Adv Virus Res 193-292.
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 the coronavirus nonstructural protein 4: involvement of the early secretory pathway in replication. J Virol 81: 13876-13888.
25. Pedersen KW, van der Meer Y, Roos N, Snijder EJ (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.
26. 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.
27. Goldsmith CS, Tatti KM, Ksiazek TG, Rollin PE, Comer JA, et al. (2004) Ultrastructural characterization of SARS coronavirus. Emerging Infect Dis 10: 320-326.
28. Snijder EJ, van der Meer Y, Zevenhoven-Dobbe J, Onderwater JJM, 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.
29. 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.
30. Stertz S, Reichelt M, Spiegel M, Kuri T, Martínez-Sobrido L, et al. (2007) The intracellular sites of early replication and budding of SARS-coronavirus. Virology 361: 304-315.
31. van der Meer Y, Snijder EJ, Dobbe JC, Schleich S, Denison MR, et al. (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.
32. Prentice E, Jerome WG, Yoshimori T, Mizushima N, Denison MR (2004) Coronavirus replication complex formation utilizes components of cellular autophagy. J Biol Chem 279: 10136-10141.
33. Kirkegaard K, Taylor MP, Jackson WT (2004) Cellular autophagy: surrender, avoidance and subversion by microorganisms. Nat Rev Microbiol 2: 301-314.
34. 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.
35. Verheije MH, Raaben M, Mari M, Te Lintelo EG, Reggiori F, et al. (2008) Mouse hepatitis coronavirus RNA replication depends on GBF1-mediated ARF1 activation. PLoS Pathog 4: e1000088. doi:10.1371/journal.ppat.1000088
36. Koster AJ, Grimm R, Typke D, Hegerl R, Stoschek A, et al. (1997) Perspectives of molecular and cellular electron tomography. J Struct Biol 120: 276-308.
37. Frey TG, Perkins GA, Ellisman MH (2006) Electron tomography of membrane-bound cellular organelles. Annu Rev Biophys Biomol Struct 35: 199-224.
38. Walther P, Ziegler A (2002) Freeze substitution of high-pressure frozen samples: the visibility of biological membranes is improved when the substitution medium contains water. J Microsc 208: 3-10.
39. David-Ferreira JF, Manaker RA (1965) An electron microscope study of the development of a mouse hepatitis virus in tissue culture cells. J Cell Biol 24: 57-78.
40. Westaway EG, Mackenzie JM, Kenney MT, Jones MK, Khromykh AA (1997) Ultrastructure of Kunjin virus-infected cells: colocalization of NS1 and NS3 with double-stranded RNA, and of NS2b with NS3, in virus-induced membrane structures. J Virol 71: 6650-6661.
41. Mackenzie JM, Jones MK, Westaway EG (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.
42. Neuman BW, Joseph JS, Saikatendu KS, Serrano P, Chatterjee A, et al. (2008) Proteomics analysis unravels the functional repertoire of coronavirus nonstructural protein 3. J Virol 82: 5279-5294.
43. Ziebuhr J, Snijder EJ, Gorbalenya AE (2000) Virus-encoded proteinases and proteolytic processing in the Nidovirales. J Gen Virol 81: 853-879.
44. Zhai Y, Sun F, Li X, Pang H, Xu X3, 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.
45. 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.
46. Sethna PB, Hung SL, Brian DA (1989) Coronavirus subgenomic minus-strand RNAs and the potential for mRNA replicons. Proc Natl Acad Sci U S A 86: 5626-5630.
47. Sawicki D, Wang T, Sawicki S (2001) The RNA structures engaged in replication and transcription of the A59 strain of mouse hepatitis virus. J Gen Virol 82: 385-396.
48. Stollar BD, Stollar V (1970) Immunofluorescent demonstration of double-stranded RNA in the cytoplasm of Sindbis virus-infected cells. Virology 42: 276-280.
49. Weber F, Wagner V, Rasmussen SB, Hartmann R, Paludan SR (2006) Double-stranded RNA is produced by positive-strand RNA viruses and DNA viruses but not in detectable amounts by negative-strand RNA viruses. J Virol 80: 5059-5064.
50. Targett-Adams P, Boulant S, McLauchlan J (2007) Visualization of double-stranded RNA in cells supporting hepatitis C virus RNA replication. J Virol 81: JVI.01565-07v1-Epub.
51. Schonborn J, Oberstrass J, Breyel E, Tittgen J, Schumacher J, et al. (1991) Monoclonal antibodies to double-stranded RNA as probes of RNA structure in crude nucleic acid extracts. Nucleic Acids Res 19: 2993-3000.
52. Salonen A, Ahola T, Kaariainen L (2004) Viral RNA replication in association with cellular membranes. Curr Top Microbiol Immunol 285: 139-173.
53. Wileman T (2006) Aggresomes and autophagy generate sites for virus replication. Science 312: 875-878.
54. Bost AG, Prentice E, Denison MR (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.
55. Froshauer S, Kartenbeck J, Helenius A (1988) Alphavirus RNA replicase is located on the cytoplasmic surface of endosomes and lysosomes. J Cell Biol 107: 2075-2086.
56. Sparks JS, Lu X, Denison MR (2007) Genetic analysis of murine hepatitis virus nsp4 in virus replication. J Virol 81: 12554-12563.
57. Kutik S, Guiard B, Meyer HE, Wiedemann N, Pfanner N (2007) Cooperation of translocase complexes in mitochondrial protein import. J Cell Biol 179: 585-591.
58. Endo T, Yamamoto H, Esaki M (2003) Functional cooperation and separation of translocators in protein import into mitochondria, the double-membrane bounded organelles. J Cell Sci 116: 3259-3267.
59. 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.
60. Posthuma CC, Pedersen KW, Lu Z, Joosten RG, Roos N, et al. (2008) Formation of the arterivirus replication/transcription complex: a key role for nonstructural protein 3 in the remodeling of intracellular membranes. J Virol 82: 4480-4491.
61. Rust RC, Landmann L, Gosert R, Tang BL, Hong WJ, et al. (2001) Cellular COPII proteins are involved in production of the vesicles that form the poliovirus replication complex. J Virol 75: 9808-9818.
62. Egger D, Bienz K (2005) Intracellular location and translocation of silent and active poliovirus replication complexes. J Gen Virol 86: 707-718.
63. Schlegel A, Giddings THJ, Ladinsky MS, Kirkegaard K (1996) Cellular origin and ultrastructure of membranes induced during poliovirus infection. J Virol 70: 6576-6588.
64. Jackson WT, Giddings TH, Taylor MP, Mulinyawe S, Rabinovitch M, et al. (2005) Subversion of cellular autophagosomal machinery by RNA viruses. PLoS Biol 3: 861-871. doi: 10.1371/journal.pbio.0030156
65. Quinkert D, Bartenschlager R, Lohmann V (2005) Quantitative analysis of the hepatitis C virus replication complex. J Virol 79: 13594-13605.
66. 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.
67. van Hemert MJ, van den Worm SHE, Knoops K, Mommaas AM, Gorbalenya AE, et al. (2008) SARS-coronavirus replication/transcription complexes are membrane-enclosed and need a host factor for activity in vitro. PLoS Pathog 4: e1000054. doi:10.1371/journal.ppat.1000054
68. Uchil PD, Satchidanandam V (2003) Architecture of the flaviviral replication complex. J Biol Chem 278: 24388-24398.
69. Westaway EG, Khromykh AA, Mackenzie JM (1999) Nascent flavivirus RNA colocalized in situ with double-stranded RNA in stable replication complexes. Virology 258: 108-117.
70. Bienz K, Egger D, Pasamontes L (1987) Association of polioviral proteins of the P2 genomic region with the viral replication complex and virus-induced membrane synthesis as visualized by electron microscopic immunocytochemistry and autoradiography. Virology 160: 220-226.
71. Versteeg GA, Spaan WJM (2008) Host cell responses to coronavirus infections. In: Perlman S, Gallagher T, Snijder EJ, editors. Nidoviruses. Washington (D.C.): ASM Press. pp. 245-258.
72. Versteeg GA, Bredenbeek PJ, van den Worm SH, Spaan WJ (2007) Group 2 coronaviruses prevent immediate early interferon induction by protection of viral RNA from host cell recognition. Virology 361: 18-26.
73. Zhou H, Perlman S (2007) Mouse hepatitis virus does not induce Beta interferon synthesis and does not inhibit its induction by double-stranded RNA. J Virol 81: 568-574.
74. Roth-Cross JK, Martinez-Sobrido L, Scott EP, Garcia-Sastre A, Weiss SR (2007) Inhibition of the alpha/beta interferon response by mouse hepatitis virus at multiple levels. J Virol 81: 7189-7199.
75. Hornung V, Ellegast J, Kim S, Brzozka K, Jung A, et al. (2006) 59-Triphosphate RNA is the ligand for RIG-I. Science 314: 994-997.
76. Kremer JR, Mastronarde DN, McIntosh JR (1996) Computer visualization of three-dimensional image data using IMOD. J Struct Biol 116: 71-76.
77. Martone ME, Tran J, Wong WW, Sargis J, Fong L, et al. (2008) The cell centered database project: an update on building community resources for managing and sharing 3D imaging data. J Struct Biol 161: 220-231.
78. Frangakis AS, Hegerl R (2001) Noise reduction in electron tomographic reconstructions using nonlinear anisotropic diffusion. J Struct Biol 135: 250.
79. van der Meer Y, van Tol H, Krijnse Locker J, Snijder EJ (1998) ORF1a-encoded replicase subunits are involved in the membrane association of the arterivirus replication complex. J Virol 72: 6689-6698.