Untangling membrane rearrangement in the nidovirales

DNA and Cell Biology

Volumn 33, Issue 3, 2014, Pages 122-127

  Angelini, Megan Mary ^a   Neuman, Benjamin William ^b   Buchmeier, Michael J ^a,c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF READING   (United Kingdom)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; NIDOVIRALES; NONHUMAN; PRIORITY JOURNAL;

MEMBRANE FUSION; MODELS, BIOLOGICAL; NIDOVIRALES;

EID: 84895728398     PISSN: 10445498     EISSN: 15577430     Source Type: Journal    
DOI: 10.1089/dna.2013.2304     Document Type: Article

References (73)

1. Ahlquist, P. (2006). Parallels among positive-strand RNA viruses, reverse-transcribing viruses and double-stranded RNA viruses. Nat Rev Microbiol 4, 371-382.
2. Angelini, M.M., Akhlaghpour, M., Neuman, B.W., and Buchmeier, M.J. (2013). Severe acute respiratory syndrome coronavirus nonstructural proteins 3, 4, and 6 induce doublemembrane vesicles. MBio 4, e00524-13.
3. Bacia, K., Schwille, P., and Kurzchalia, T. (2005). Sterol structure determines the separation of phases and the curvature of the liquid-ordered phase in model membranes. Proc Natl Acad Sci U S A 102, 3272-3277.
4. Baumgart, T., Hess, S.T., and Webb, W.W. (2003). Imaging coexisting fluid domains in biomembrane models coupling curvature and line tension. Nature 425, 821-824.
5. Belov, G.A., Nair, V., Hansen, B.T., Hoyt, F.H., Fischer, E.R., and Ehrenfeld, E. (2012). Complex dynamic development of poliovirus membranous replication complexes. J Virol 86, 302-312.
6. Brian, D.A., and Baric, R.S. (2005). Coronavirus genome structure and replication. Curr Top Microbiol Immunol 287, 1-30.
7. Britton, P., and Cavanagh, D. (2008). Nidovirus genome organization and expression mechanisms. In Nidoviruses. S. Perlman, T. Gallagher, and E.J. Snijder, eds. (ASM Press, Washington, DC), pp. 29-46.
8. Cal T., Galli, C., Olivari, S., and Molinari, M. (2008). Segregation and rapid turnover of EDEM1 by an autophagy-like mechanism modulates standard ERAD and folding activities. Biochem Biophys Res Commun 371, 405-410.
9. Cottam, E.M., Maier, H.J., Manifava, M., Vaux, L.C., Chandra- Schoenfelder, P., Gerner, W., Britton, P., Ktistakis, N.T., and Wileman, T. (2011). Coronavirus nsp6 proteins generate autophagosomes from the endoplasmic reticulum via an omegasome intermediate. Autophagy 7, 1335-1347.
10. Cowley, J.A., Dimmock, C.M. Spann, K.M., and Walker, P.J. (2000). Gill-associated virus of Penaeus monodon prawns: an invertebrate virus with ORF1a and ORF1b genes related to arteri- and coronaviruses. J Gen Virol 81, 1473-1484.
11. David-Ferreira, J.F., and Manaker, R.A. (1965). An electron microscope study of the development of a mouse hepatitis virus in tissue culture cells. J Cell Biol 24, 57-78.
12. de Haan, C.A., and Reggiori, F. (2008). Are nidoviruses hijacking the autophagy machinery? Autophagy 4, 276-279.
13. de Wilde, A.H., Raj, V.S., Oudshoorn, D., Bestebroer, T.M., van Nieuwkoop, S., Limpens, R.W., Posthuma, C.C., van der Meer, Y., Barcena, M., Haagmans, B.L., Snijder, E.J., and van den Hoogen, B.G. (2013). MERS-coronavirus replication induces severe in vitro cytopathology and is strongly inhibited by cyclosporinAor interferon-a treatment. J GenVirol 94, 1749-1760.
14. den Boon, J.A., and Ahlquist, P. (2010). Organelle-like membrane compartmentalization of positive-strand RNA virus replication factories. Annu Rev Microbiol 64, 241-256.
15. Denison, M.R. (2008). Seeking membranes: positive-strand RNA virus replication complexes. PLoS Biol 6, e270.
16. Faaberg, K.S. (2008). Arterivirus structural proteins and assembly. In Nidoviruses. S. Perlman, T. Gallagher, and E.J. Snijder, eds. (ASM Press, Washington DC), pp. 211-234.
17. Froshauer, S., Kartenbeck, J., and Helenius, A. (1988). Alphavirus RNA replicase is located on the cytoplasmic surface of endosomes and lysosomes. J Cell Biol 107, 2075-2086.
18. Gadlage, M.J., Sparks, J.S., Beachboard, D.C., Cox, R.G., Doyle, J.D., Stobart, C.C., and Denison, M.R. (2010). Murine hepatitis virus nonstructural protein 4 regulates virus-induced membrane modifications and replication complex function. J Virol 84, 280-290.
19. Gillespie, L.K., Hoenen, A., Morgan, G., and Mackenzie, J.M. (2010). The endoplasmic reticulum provides the membrane platform for biogenesis of the flavivirus replication complex. J Virol 84, 10438-10447.
20. Goldsmith, C.S., Tatti, K.M., Ksiazek, T.G., Rollin, P.E., Comer, J.A., Lee, W.W., Rota, P.A., Bankamp, B., Bellini, W.J., and Zaki, S.R. (2004). Ultrastructural characterization of SARS coronavirus. Emerg Infect Dis 10, 320-326.
21. Gonzalez, J.M., Gomez-Puertas, P., Cavanagh, D., Gorbalenya, A.E., and Enjuanes, L. (2003). A comparative sequence analysis to revise the current taxonomy of the family Coronaviridae. Arch Virol 148, 2207-2235.
22. Gorbalenya, A.E., Enjuanes, L., Ziebuhr, J., and Snijder, E.J. (2006). Nidovirales: evolving the largest RNA virus genome. Virus Res 117, 17-37.
23. Gosert, R., Kanjanahaluethai, A., Egger, D., Bienz, K., and Baker, S.C. (2002). RNA replication of mouse hepatitis virus takes place at double-membrane vesicles. J Virol 76, 3697- 3708.
24. Hagemeijer, M.C., Ulasli, M., Vonk, A.M., Reggiori, F., Rottier, P.J., and de Haan, C.A. (2011). Mobility and interactions of coronavirus nonstructural protein 4. J Virol 85, 4572-4577.
25. Hagemeijer, M.C., Verheije, M.H., Ulasli, M., Shaltiel, I.A., de Vries, L.A., Reggiori, F., Rottier, P.J., and de Haan, C.A. (2010). Dynamics of coronavirus replication-transcription complexes. J Virol 84, 2134-2149.
26. Hogue, B.G., and Machamer, C.E. (2008). Coronavirus structural proteins and virus assembly. In Nidoviruses. S. Perlman, T. Gallagher, and E.J. Snijder, eds. (ASM Press, Washington DC), pp. 179-200.
27. Imbert, I., Snijder, E.J., Dimitrova, M., Guillemot, J.C., Lecine, P., and Canard, B. (2008). The SARS-Coronavirus PLnc domain of nsp3 as a replication/transcription scaffolding protein. Virus Res 133, 136-148.
28. Kirkegaard, K., and Jackson, W.T. (2005). Topology of doublemembraned vesicles and the opportunity for non-lytic release of cytoplasm. Autophagy 1, 182-184.
29. Knoops, K., Barcena, M., Limpens, R.W., Koster, A.J., Mommaas, A.M., and Snijder, E.J. (2012). Ultrastructural characterization of arterivirus replication structures: reshaping the endoplasmic reticulum to accommodate viral RNA synthesis. J Virol 86, 2474-2487.
30. Knoops, K., Kikkert, M., Worm, S.H., Zevenhoven-Dobbe, J.C., van der Meer, Y., Koster, A.J., Mommaas, A.M., and Snijder, E.J. (2008). SARS-coronavirus replication is supported by a reticulovesicular network of modified endoplasmic reticulum. PLoS Biol 6, e226.
31. Kopek, B.G., Perkins, G., Miller, D.J., Ellisman, M.H., and Ahlquist, P. (2007). Three-dimensional analysis of a viral RNA replication complex reveals a virus-induced miniorganelle. PLoS Biol 5, e220.
32. Kopek, B.G., Settles, E.W., Friesen, P.D., and Ahlquist, P. (2010). Nodavirus-induced membrane rearrangement in replication complex assembly requires replicase protein a, RNA templates, and polymerase activity. J Virol 84, 12492-12503.
33. Krogh, A., Larsson, B., von Heijne, G., and Sonnhammer, E.L. (2001). Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol 305, 567-580.
34. Lauber, C., Goeman, J.J., Parquet, M.E.C., Thi Nga, P., Snijder, E.J., Morita, K., and Gorbalenya, A.E. (2013). The footprint of genome architecture in the largest genome expansion in RNA viruses. PLoS Pathog 9, e1003500.
35. Limpens, R.W., van der Schaar, H.M., Kumar, D., Koster, A.J., Snijder, E.J., van Kuppeveld, F.J., and Barcena, M. (2011). The transformation of enterovirus replication structures: a three-dimensional study of single- and double-membrane compartments. MBio 2, e00166-11.
36. Mackenzie, J. (2005). Wrapping things up about virus RNA replication. Traffic 6, 967-977.
37. Maier, H.J., and Britton, P. (2012). Involvement of autophagy in coronavirus replication. Viruses 4, 3440-3451.
38. McMahon, H.T., and Gallop, J.L. (2005). Membrane curvature and mechanisms of dynamic cell membrane remodelling. Nature 438, 590-596.
39. Miller, D.J., Schwartz, M.D., and Ahlquist, P. (2001). Flock house virus RNA replicates on outer mitochondrial membranes in Drosophila cells. J Virol 75, 11664-11676.
40. Miller, S., and Krijnse-Locker, J. (2008). Modification of intracellular membrane structures for virus replication. Nat Rev Microbiol 6, 363-374.
41. Miorin, L., Romero-Brey, I., Maiuri, P., Hoppe, S., Krijnse- Locker, J., Bartenschlager, R., and Marcello, A. (2013). Three-dimensional architecture of tick-borne encephalitis virus replication sites and trafficking of the replicated RNA. J Virol 87, 6469-6481.
42. Monastyrska, I., Ulasli, M., Rottier, P.J., Guan, J.L., Reggiori, F., and de Haan, C.A. (2013). An autophagy-independent role for LC3 in equine arteritis virus replication. Autophagy 9, 164-174.
43. Netherton, C.L., and Wileman, T. (2011). Virus factories, double membrane vesicles and viroplasm generated in animal cells. Curr Opin Virol 1, 381-387.
44. Neuman, B.W., Joseph, J.S., Saikatendu, K.S., Serrano, P., Chatterjee, A., Johnson, M.A., Liao, L., Klaus, J.P., Yates, J.R., Wuthrich, K., Stevens, R.C., Buchmeier, M.J., and Kuhn, P. (2008). Proteomics analysis unravels the functional repertoire of coronavirus nonstructural protein 3. J Virol 82, 5279-5294.
45. Novoa, R.R., Calderita, G., Arranz, R., Fontana, J., Granzow, H., and Risco, C. (2005). Virus factories: associations of cell organelles for viral replication and morphogenesis. Biol Cell 97, 147-172.
46. Oostra, M., Hagemeijer, M.C., van Gent,M., Bekker, C.P., te Lintelo, E.G., Rottier, P.J., and de Haan, C.A. (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.
47. Oostra, M., te Lintelo, E.G., Deijs, M., Verheije, M.H., Rottier, P.J., and de Haan, C.A. (2007). Localization and membrane topology of coronavirus nonstructural protein 4: involvement of the early secretory pathway in replication. J Virol 81, 12323-12336.
48. Pasternak, A.O., Spaan, W.J., and Snijder, E.J. (2006). Nidovirus transcription: how to make sense? J Gen Virol 87, 1403-1421.
49. Pedersen, K.W., van der Meer, Y., Roos, N., and Snijder, E.J. (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.
50. Perera, R., Riley, C., Isaac, G., Hopf-Jannasch, A.S., Moore, R.J., Weitz, K.W., Pasa-Tolic, L., Metz, T.O., Adamec, J., and Kuhn, R.J. (2012). Dengue virus infection perturbs lipid homeostasis in infected mosquito cells. PLoS Pathog 8, e1002584.
51. Posthuma, C.C., Pedersen, K.W., Lu, Z., Joosten, R.G., Roos, N., Zevenhoven-Dobbe, J.C., and Snijder, E.J. (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.
52. Prentice, E., Jerome, W.G., Yoshimori, T., Mizushima, N., and Denison, M.R. (2004). Coronavirus replication complex formation utilizes components of cellular autophagy. J Biol Chem 279, 10136-10141.
53. Reggiori, F., Monastyrska, I., Verheije, M.H., Cal, T., Ulasli, M., Bianchi, S., Bernasconi, R., de Haan, C.A., and Molinari, M. (2010). Coronaviruses hijack the LC3-I-positive EDEMosomes, ER-derived vesicles exporting short-lived ERAD regulators, for replication. Cell Host Microbe 7, 500- 508.
54. Salonen, A., Ahola, T., and Kaariainen, L. (2005). Viral RNA replication in association with cellular membranes. Curr Top Microbiol Immunol 285, 139-173.
55. Schley, D., Whittaker, R.J., and Neuman, B.W. (2013). Arenavirus budding resulting from viral-protein-associated cell membrane curvature. J R Soc Interface 10, 20130403.
56. Schwartz, M., Chen, J., Janda, M., Sullivan, M., den Boon, J., and Ahlquist, P. (2002). A positive-strand RNA virus replication complex parallels form and function of retrovirus capsids. Mol Cell 9, 505-514.
57. Shibata, Y., Hu, J., Kozlov, M.M., and Rapoport, T.A. (2009). Mechanisms shaping the membranes of cellular organelles. Annu Rev Cell Dev Biol 25, 329-354.
58. Snijder, E.J., Kikkert, M., and Fang, Y. (2013). Arterivirus molecular biology and pathogenesis. J Gen Virol 94(Pt 10), 2141-2163.
59. Snijder, E.J., van der Meer, Y., Zevenhoven-Dobbe, J., Onderwater, J.J., van der Meulen, J., Koerten, H.K., and 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.
60. Snijder, E.J., van Tol, H., Roos, N., and Pedersen, K.W. (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.
61. Sonnhammer, E.L., von Heijne, G., and Krogh, A. (1998). A hidden Markov model for predicting transmembrane helices in protein sequences. Proc Int Conf Intell Syst Mol Biol 6, 175-182.
62. Spuul, P., Balistreri, G., Kaariainen, L., and Ahola, T. (2010). Phosphatidylinositol 3-kinase-, actin-, and microtubuledependent transport of Semliki Forest Virus replication complexes from the plasma membrane to modified lysosomes. J Virol 84, 7543-7557.
63. Stokes, H.L., Baliji, S., Hui, C.G., Sawicki, S.G., Baker, S.C., and Siddell, S.G. (2010). A new cistron in the murine hepatitis virus replicase gene. J Virol 84, 10148-10158.
64. Subramaniam, S. (2005). Bridging the imaging gap: visualizing subcellular architecture with electron tomography. Curr Opin Microbiol 8, 316-322.
65. Subramaniam, S., Bartesaghi, A., Liu, J., Bennett, A.E., and Sougrat, R. (2007). Electron tomography of viruses. Curr Opin Struct Biol 17, 596-602.
66. Suhy, D.A., Giddings, T.H., and Kirkegaard, K. (2000). Remodeling the endoplasmic reticulum by poliovirus infection and by individual viral proteins: an autophagy-like origin for virus-induced vesicles. J Virol 74, 8953-8965.
67. Ulasli, M., Verheije, M.H., de Haan, C.A., and Reggiori, F. (2010). Qualitative and quantitative ultrastructural analysis of the membrane rearrangements induced by coronavirus. Cell Microbiol 12, 844-861.
68. van der Meer, Y., van Tol, H., Locker, J.K., and Snijder, E.J. (1998). ORF1a-encoded replicase subunits are involved in the membrane association of the arterivirus replication complex. J Virol 72, 6689-6698.
69. van Hemert, M.J., de Wilde, A.H., Gorbalenya, A.E., and Snijder, E.J. (2008). The in vitro RNA synthesizing activity of the isolated arterivirus replication/transcription complex is dependent on a host factor. J Biol Chem 283, 16525-16536.
70. von Brunn, A., Teepe, C., Simpson, J.C., Pepperkok, R., Friedel, C.C., Zimmer, R., Roberts, R., Baric, R., and Haas, J. (2007). Analysis of intraviral protein-protein interactions of the SARS coronavirus ORFeome. PLoS One 2, e459.
71. Welsch, S., Miller, S., Romero-Brey, I., Merz, A., Bleck, C.K., Walther, P., Fuller, S.D., Antony, C., Krijnse-Locker, J., and Bartenschlager, R. (2009). Composition and three-dimensional architecture of the dengue virus replication and assembly sites. Cell Host Microbe 5, 365-375.
72. Zhao, Z., Thackray, L.B., Miller, B.C., Lynn, T.M., Becker, M.M., Ward, E., Mizushima, N.N., Denison, M.R., and Virgin, H.W. (2007). Coronavirus replication does not require the autophagy gene ATG5. Autophagy 3, 581-585.
73. Ziebuhr, J. (2006). The coronavirus replicase: insights into a sophisticated enzyme machinery. Adv Exp Med Biol 581, 3-11.