Does form meet function in the coronavirus replicative organelle?

Trends in Microbiology

Volumn 22, Issue 11, 2014, Pages 642-647

  Neuman, Benjamin W ^a   Angelini, Megan M ^b   Buchmeier, Michael J ^b,c  

^a UNIVERSITY OF READING   (United Kingdom)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Membrane rearrangement; Replicative organelle; RNA virus replication; Virus factory

Indexed keywords

NONSTRUCTURAL PROTEIN 3; NONSTRUCTURAL PROTEIN 4; RNA DIRECTED RNA POLYMERASE; RNA POLYMERASE;

CELL FUNCTION; CELL ORGANELLE; CORONAVIRUS; NIDOVIRALES; NONHUMAN; ORGANELLE SHAPE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN SYNTHESIS; REVIEW; VIRUS CELL INTERACTION; VIRUS REPLICATION; VIRUS TRANSCRIPTION; CORONAVIRIDAE; GENETIC TRANSCRIPTION; PHYSIOLOGY; ULTRASTRUCTURE; VIROLOGY;

CORONAVIRUS; RNA VIRUSES;

CORONAVIRUS; ORGANELLES; TRANSCRIPTION, GENETIC; VIRUS REPLICATION;

EID: 84927034590     PISSN: 0966842X     EISSN: 18784380     Source Type: Journal    
DOI: 10.1016/j.tim.2014.06.003     Document Type: Review

References (78)

1. den Boon J.A., Ahlquist P. Organelle-like membrane compartmentalization of positive-strand RNA virus replication factories. Annu. Rev. Microbiol. 2010, 64:241-256.
2. Knoops K., et al. SARS-coronavirus replication is supported by a reticulovesicular network of modified endoplasmic reticulum. PLoS Biol. 2008, 6:e226.
3. Gosert R., et al. RNA replication of mouse hepatitis virus takes place at double-membrane vesicles. J. Virol. 2002, 76:3697-3708.
4. Stokes H.L., et al. A new cistron in the murine hepatitis virus replicase gene. J. Virol. 2010, 84:10148-10158.
5. Verheije M.H., et al. Mouse hepatitis coronavirus RNA replication depends on GBF1-mediated ARF1 activation. PLoS Pathog. 2008, 4:e1000088.
6. Hagemeijer M.C., et al. Visualizing coronavirus RNA synthesis in time by using click chemistry. J. Virol. 2012, 86:5808-5816.
7. Ulasli M., et al. Qualitative and quantitative ultrastructural analysis of the membrane rearrangements induced by coronavirus. Cell. Microbiol. 2010, 12:844-861.
8. Al-Mulla H.M.N., et al. Competitive fitness in coronaviruses is not correlated with size or number of double-membrane vesicles under reduced-temperature growth conditions. mBio 2014, 5:e01107-e01113.
9. Hagemeijer M.C., et al. Dynamics of coronavirus replication-transcription complexes. J. Virol. 2010, 84:2134-2149.
10. de Haan C.A., et al. Autophagy-independent LC3 function in vesicular traffic. Autophagy 2010, 6:994-996.
11. Maier H.J., et al. Infectious bronchitis virus generates spherules from zippered endoplasmic reticulum membranes. mBio 2013, 4:e00801-e00813.
12. Koonin E.V., et al. The ancient virus world and evolution of cells. Biol. Direct 2006, 1:29. 10.1186/1745-6150-1-29.
13. Richards A.L., et al. Generation of unique poliovirus RNA replication organelles. MBio 2014, 5. e00833-00813, http://dx.doi.org/10.1128/mBio.00833-13.
14. Teterina N.L., et al. Induction of intracellular membrane rearrangements by HAV proteins 2C and 2BC. Virology 1997, 237:66-77.
15. Suhy D.A., et al. Remodeling the endoplasmic reticulum by poliovirus infection and by individual viral proteins: an autophagy-like origin for virus-induced vesicles. J. Virol. 2000, 74:8953-8965.
16. Short J.R., Dorrington R.A. Membrane targeting of an alpha-like tetravirus replicase is directed by a region within the RNA-dependent RNA polymerase domain. J. Gen. Virol. 2012, 93:1706-1716.
17. Nishihara T. Various morphological aspects of Escherichia coli lysis by RNA bacteriophage MS2 observed by transmission and scanning electron microscopes. New Microbiol. 2003, 26:163-168.
18. Bolduc B., et al. Identification of novel positive-strand RNA viruses by metagenomic analysis of archaea-dominated Yellowstone hot springs. J. Virol. 2012, 86:5562-5573.
19. Lauber C., et al. The footprint of genome architecture in the largest genome expansion in RNA viruses. PLoS Pathog. 2013, 9:e1003500.
20. Angelini M.M., et al. Severe acute respiratory syndrome coronavirus nonstructural proteins 3, 4, and 6 induce double-membrane vesicles. MBio 2013, 4. e00524-00513, http://dx.doi.org/10.1128/mBio.00524-13.
21. Posthuma C.C., et al. Formation of the arterivirus replication/transcription complex: a key role for nonstructural protein 3 in the remodeling of intracellular membranes. J. Virol. 2008, 82:4480-4491.
22. Ziebuhr J., et al. Virus-encoded proteinases and proteolytic processing in the Nidovirales. J. Gen. Virol. 2000, 81:853-879.
23. Manolaridis I., et al. Structure of the C-terminal domain of nsp4 from feline coronavirus. Acta Crystallogr. D: Biol. Crystallogr. 2009, 65:839-846.
24. Sparks J.S., et al. Genetic analysis of murine hepatitis virus nsp4 in virus replication. J. Virol. 2007, 81:12554-12563.
25. Neuman B.W., et al. Proteomics analysis unravels the functional repertoire of coronavirus nonstructural protein 3. J. Virol. 2008, 82:5279-5294.
26. Bouvet M., et al. In vitro reconstitution of SARS-coronavirus mRNA cap methylation. PLoS Pathog. 2010, 6:e1000863.
27. de Wilde A.H., et al. MERS-coronavirus replication induces severe in vitro cytopathology and is strongly inhibited by cyclosporin A or interferon-alpha treatment. J. Gen. Virol. 2013, 94:1749-1760.
28. Orenstein J.M., et al. Morphogenesis of coronavirus HCoV-NL63 in cell culture: a transmission electron microscopic study. Open Infect. Dis. J. 2008, 2:52-58.
29. Snijder E.J., et al. Non-structural proteins 2 and 3 interact to modify host cell membranes during the formation of the arterivirus replication complex. J. Gen. Virol. 2001, 82:985-994.
30. Wood O., et al. Electron microscopic study of tissue cultures infected with simian haemorrhagic fever virus. J. Gen. Virol. 1970, 7:129-136.
31. Cottam E.M., et al. Coronavirus nsp6 proteins generate autophagosomes from the endoplasmic reticulum via an omegasome intermediate. Autophagy 2011, 7:1335-1347.
32. Hagemeijer M.C., et al. Mobility and interactions of coronavirus nonstructural protein 4. J. Virol. 2011, 85:4572-4577.
33. Hagemeijer M.C., et al. Biogenesis and dynamics of the coronavirus replicative structures. Viruses 2012, 4:3245-3269.
34. Zirkel F., et al. An insect nidovirus emerging from a primary tropical rainforest. MBio 2011, 2. e00077-00011, http://dx.doi.org/10.1128/mBio.00077-11.
35. Spann K.M., et al. Lymphoid organ virus of Penaeus monodon from Australia. Dis. Aquat. Organ. 1995, 23:127-134.
36. Gauthier L., et al. Viruses associated with ovarian degeneration in Apis mellifera L. queens. PLoS ONE 2011, 6:e16217.
37. Takao Y., et al. Isolation and characterization of a novel single-stranded RNA virus infectious to a marine fungoid protist, Schizochytrium sp. (Thraustochytriaceae, Labyrinthulea). Appl. Environ. Microbiol. 2005, 71:4516-4522.
38. Hsu N.Y., et al. Viral reorganization of the secretory pathway generates distinct organelles for RNA replication. Cell 2010, 141:799-811.
39. Roberts I.M., Harrison B.D. Inclusion bodies and tubular structures in Chenopodium amaranticolor plants infected with strawberry latent ringspot virus. J. Gen. Virol. 1970, 7:47-54.
40. Tilsner J., et al. The TGB1 movement protein of Potato virus X reorganizes actin and endomembranes into the X-body, a viral replication factory. Plant Physiol. 2012, 158:1359-1370.
41. Linnik O., et al. Unraveling the structure of viral replication complexes at super-resolution. Front. Plant Sci. 2013, 4:6. 10.3389/fpls.2013.00006.
42. Edwardson J.R., Christie R.G. Use of virus-induced inclusions in classification and diagnosis. Ann. Rev. Phytopathol. 1978, 16:31-55.
43. Rudzinska-Langwald A. Cytological changes in phloem parenchyma cells of Solanum rostratum (Dunal.) related to the replication of potato virus M (PVM). Acta Societatis Botanicorum Poloniae 1990, 59:45-53.
44. Boine B., et al. Recombinant expression of the coat protein of Botrytis virus X and development of an immunofluorescence detection method to study its intracellular distribution in Botrytis cinerea. J. Gen. Virol. 2012, 93:2502-2511.
45. Lesemann D.E. Virus group-specific and virus-specific cytological alterations induced by members of the tymovirus group. J. Phytopathol. 1977, 90:315-336.
46. Tomaru Y., et al. Isolation and characterization of two distinct types of HcRNAV, a single-stranded RNA virus infecting the bivalve-killing microalga Heterocapsa circularisquama. Aquat. Microb. Ecol. 2004, 34:207-218.
47. Guix S., et al. C-terminal nsP1a protein of human astrovirus colocalizes with the endoplasmic reticulum and viral RNA. J. Virol. 2004, 78:13627-13636.
48. Mendez E., et al. Association of the astrovirus structural protein VP90 with membranes plays a role in virus morphogenesis. J. Virol. 2007, 81:10649-10658.
49. Moreira A.G., et al. Identification and partial characterization of a Carica papaya-infecting isolate of Alfalfa mosaic virus in Brazil. J. Gen. Plant Pathol. 2010, 76:172-175.
50. Schwartz M., et al. A positive-strand RNA virus replication complex parallels form and function of retrovirus capsids. Mol. Cell 2002, 9:505-514.
51. Bailey D., et al. Feline calicivirus p32, p39 and p30 proteins localize to the endoplasmic reticulum to initiate replication complex formation. J. Gen. Virol. 2010, 91:739-749.
52. Pringle F.M., et al. Providence virus: a new member of the Tetraviridae that infects cultured insect cells. Virology 2003, 306:359-370.
53. Medina V., et al. Specific inclusion bodies are associated with replication of lettuce infectious yellows virus RNAs in Nicotiana benthamiana protoplasts. J. Gen. Virol. 1998, 79(Pt 10):2325-2329.
54. Gillespie L.K., et al. The endoplasmic reticulum provides the membrane platform for biogenesis of the flavivirus replication complex. J. Virol. 2010, 84:10438-10447.
55. Welsch S., et al. Composition and three-dimensional architecture of the dengue virus replication and assembly sites. Cell Host Microbe 2009, 5:365-375.
56. Romero-Brey I., et al. Three-dimensional architecture and biogenesis of membrane structures associated with hepatitis C virus replication. PLoS Pathog. 2012, 8:e1003056.
57. Miller S., et al. The non-structural protein 4A of dengue virus is an integral membrane protein inducing membrane alterations in a 2K-regulated manner. J. Biol. Chem. 2007, 282:8873-8882.
58. Roosendaal J., et al. Regulated cleavages at the West Nile virus NS4A-2K-NS4B junctions play a major role in rearranging cytoplasmic membranes and Golgi trafficking of the NS4A protein. J. Virol. 2006, 80:4623-4632.
59. Egger D., et al. Expression of hepatitis C virus proteins induces distinct membrane alterations including a candidate viral replication complex. J. Virol. 2002, 76:5974-5984.
60. Rehman S., et al. Subcellular localization of hepatitis E virus (HEV) replicase. Virology 2008, 370:77-92.
61. Gill C.C., Chong J. Cytopathological evidence for the division of barley yellow dwarf virus isolates into two subgroups. Virology 1979, 95:59-69.
62. Kopek B.G., et al. Nodavirus-induced membrane rearrangement in replication complex assembly requires replicase protein a, RNA templates, and polymerase activity. J. Virol. 2010, 84:12492-12503.
63. Kopek B.G., et al. Three-dimensional analysis of a viral RNA replication complex reveals a virus-induced mini-organelle. PLoS Biol. 2007, 5:e220.
64. Schaad M.C., et al. Formation of plant RNA virus replication complexes on membranes: role of an endoplasmic reticulum-targeted viral protein. EMBO J. 1997, 16:4049-4059.
65. Grangeon R., et al. Impact on the endoplasmic reticulum and Golgi apparatus of turnip mosaic virus infection. J. Virol. 2012, 86:9255-9265.
66. Wei T., Wang A. Biogenesis of cytoplasmic membranous vesicles for plant potyvirus replication occurs at endoplasmic reticulum exit sites in a COPI- and COPII-dependent manner. J. Virol. 2008, 82:12252-12264.
67. Magliano D., et al. Rubella virus replication complexes are virus-modified lysosomes. Virology 1998, 240:57-63.
68. Fontana J., et al. Three-dimensional structure of rubella virus factories. Virology 2010, 405:579-591.
69. Salonen A., et al. Properly folded nonstructural polyprotein directs the Semliki Forest virus replication complex to the endosomal compartment. J. Virol. 2003, 77:1691-1702.
70. Sharma M., et al. Inhibition of phospholipid biosynthesis decreases the activity of the tombusvirus replicase and alters the subcellular localization of replication proteins. Virology 2011, 415:141-152.
71. Barajas D., et al. A unique role for the host ESCRT proteins in replication of Tomato bushy stunt virus. PLoS Pathog. 2009, 5:e1000705.
72. Kawakami S., et al. Tobacco mosaic virus infection spreads cell to cell as intact replication complexes. Proc. Natl. Acad. Sci. U.S.A. 2004, 101:6291-6296.
73. Reichel C., et al. The role of the ER and cytoskeleton in plant viral trafficking. Trends Plant Sci. 1999, 4:458-462.
74. Batts W.N., et al. Genetic analysis of a novel nidovirus from fathead minnows. J. Gen. Virol. 2012, 93:1247-1252.
75. Krogh A., et al. Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J. Mol. Biol. 2001, 305:567-580.
76. Kanjanahaluethai A., et al. Membrane topology of murine coronavirus replicase nonstructural protein 3. Virology 2007, 361:391-401.
77. Oostra M., et al. Topology and membrane anchoring of the coronavirus replication complex: not all hydrophobic domains of nsp3 and nsp6 are membrane spanning. J. Virol. 2008, 82:12392-12405.
78. Oostra M., et al. Localization and membrane topology of coronavirus nonstructural protein 4: involvement of the early secretory pathway in replication. J. Virol. 2007, 81:12323-12336.