Ultrastructural characterization of membranous torovirus replication factories

Cellular Microbiology

Volumn 18, Issue 12, 2016, Pages 1691-1708

  Ávila Pérez, Ginés ^a   Rejas, María Teresa ^b   Rodríguez, Dolores ^a  

^a CENTRO NACIONAL DE BIOTECNOLOGÍA   (Spain)

^b CENTRO DE BIOLOGÍA MOLECULAR SEVERO OCHOA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

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

ARTICLE; BERNE VIRUS; CELL VACUOLE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CYTOPLASM; DOUBLE MEMBRANE VESICLE; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; TOROVIRUS; TRANSMISSION ELECTRON MICROSCOPY; VIRUS MORPHOLOGY; VIRUS REPLICATION; VIRUS TRANSCRIPTION; AMINO ACID SEQUENCE; ANIMAL; CELL MEMBRANE; CYTOPLASM VESICLE; DERMIS; EPITHELIUM CELL; FIBROBLAST; GENE EXPRESSION REGULATION; GENETICS; HORSE; HOST PATHOGEN INTERACTION; HUMAN; INTRACELLULAR MEMBRANE; METABOLISM; SIGNAL TRANSDUCTION; ULTRASTRUCTURE; VIROLOGY;

AMINO ACID SEQUENCE; ANIMALS; CELL MEMBRANE; CYTOPLASMIC VESICLES; DERMIS; EPITHELIAL CELLS; FIBROBLASTS; GENE EXPRESSION REGULATION, VIRAL; HORSES; HOST-PATHOGEN INTERACTIONS; HUMANS; INTRACELLULAR MEMBRANES; MICROSCOPY, ELECTRON, TRANSMISSION; RNA REPLICASE; RNA, DOUBLE-STRANDED; RNA, VIRAL; SIGNAL TRANSDUCTION; TOROVIRUS; VIRAL PROTEINS; VIRUS REPLICATION;

EID: 84978151032     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/cmi.12620     Document Type: Article

References (65)

1. Aita, T., Kuwabara, M., Murayama, K., Sasagawa, Y., Yabe, S., Higuchi, R., et al. (2012) Characterization of epidemic diarrhea outbreaks associated with bovine torovirus in adult cows. Arch Virol 157: 423–431.
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 double-membrane vesicles. mBio 4: e00524–00513.
3. Barrette-Ng, I.H., Ng, K.K., Mark, B.L., van Aken, D., Cherney, M.M., Garen, C., et al. (2002) Structure of arterivirus nsp4: the smallest chymotrypsin-like proteinase with an α/β C-terminal extension and alternate conformations of the oxyanion hole. J Biol Chem 277: 39960–39966.
4. Bolte, S., and Cordelières, F.P. (2006) A guided tour into subcellular colocalization analysis in light microscopy. J Microsc 224: 213–232.
5. 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.
6. den Boon, J.A., Snijder, E.J., Chirnside, E.D., de Vries, A.A., Horzinek, M.C., and Spaan, W.J. (1991) Equine arteritis virus is not a togavirus but belongs to the coronaviruslike superfamily. J Virol 65: 2910–2920.
7. Brierley, I., Digard, P., and Inglis, S.C. (1989) Characterization of an efficient coronavirus ribosomal frameshifting signal: requirement for an RNA pseudoknot. Cell 57: 537–547.
8. Brockway, S.M., Clay, C.T., Lu, X.T., and Denison, M.R. (2003) Characterization of the expression, intracellular localization, and replication complex association of the putative mouse hepatitis virus RNA-dependent RNA polymerase. J Virol 77: 10515–10527.
9. Clementz, M.A., Kanjanahaluethai, A., O'Brien, T.E., and Baker, S.C. (2008) Mutation in murine coronavirus replication protein nsp4 alters assembly of double membrane vesicles. Virology 375: 118–129.
10. Cottam, E.M., Maier, H.J., Manifava, M., Vaux, L.C., Chandra-Schoenfelder, P., Gerner, W., et al. (2011) Coronavirus nsp6 proteins generate autophagosomes from the endoplasmic reticulum via an omegasome intermediate. Autophagy 7: 1335–1347.
11. de Groot, R.J. (2008) Chapter 9: Molecular biology and evolution of torovirus. In Nidoviruses. Perlman, S., Gallagher, T., and Snijder, E.J. (eds). Washington, DC: ASM Press, pp. 133–146.
12. De Diego, M.L., Alvarez, E., Almazan, F., Rejas, M.T., Lamirande, E., Roberts, A., et al. (2007) A severe acute respiratory syndrome coronavirus that lacks the E gene is attenuated in vitro and in vivo. J Virol 81: 1701–1713.
13. Draker, R., Roper, R.L., Petric, M., and Tellier, R. (2006) The complete sequence of the bovine torovirus genome. Virus Res 115: 56–68.
14. Friesland, M., Mingorance, L., Chung, J., Chisari, F.V., and Gastaminza, P. (2013) Sigma-1 receptor regulates early steps of viral RNA replication at the onset of hepatitis C virus infection. J Virol 87: 6377–6390.
15. 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.
16. Garzon, A., Maestre, A.M., Pignatelli, J., Rejas, M.T., and Rodriguez, D. (2006) New insights on the structure and morphogenesis of Berne virus. Adv Exp Med Biol 581: 175–180.
17. Gorbalenya, A.E., Enjuanes, L., Ziebuhr, J., and Snijder, E.J. (2006) Nidovirales: evolving the largest RNA virus genome. Virus Res 117: 17–37.
18. 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.
19. Hagemeijer, M.C., Vonk, A.M., Monastyrska, I., Rottier, P.J., and de Haan, C.A. (2012) Visualizing coronavirus RNA synthesis in time by using click chemistry. J Virol 86: 5808–5816.
20. Harak, C., and Lohmann, V. (2015) Ultrastructure of the replication sites of positive-strand RNA viruses. Virology 479–480: 418–433.
21. Hegyi, A., Friebe, A., Gorbalenya, A.E., and Ziebuhr, J. (2002) Mutational analysis of the active centre of coronavirus 3C-like proteases. J Gen Virol 83: 581–593.
22. van Hemert, M.J., van den Worm, S.H., Knoops, K., Mommaas, A.M., Gorbalenya, A.E., and Snijder, E.J. (2008) SARS-coronavirus replication/transcription complexes are membrane-protected and need a host factor for activity in vitro. PLoS Pathog 4: e1000054.
23. Hoet, E.A., and Linda, J.F. (2008) Chapter 23: Torovirus pathogenesis and immune response. In Nidoviruses. Perlman, S., Gallagher, T., and Snijder, E.J. (eds). Washington, DC: ASM Press, pp. 351–359.
24. Ito, T., Katayama, S., Okada, N., Masubuchi, K., Fukuyama, S., and Shimizu, M. (2010) Genetic and antigenic characterization of newly isolated bovine toroviruses from Japanese cattle. J Clin Microbiol 48: 1795–1800.
25. Ivanov, K.A., Thiel, V., Dobbe, J.C., van der Meer, Y., Snijder, E.J., and Ziebuhr, J. (2004) Multiple enzymatic activities associated with severe acute respiratory syndrome coronavirus helicase. J Virol 78: 5619–5632.
26. King, A.M.Q., Adams, M.J., Carstens, E.B., and Lefkowitz, E.J. (2012) Order – Nidovirales. In Virus Taxonomy. King, A.M.Q., Adams, M.J., Carstens, E.B., and Lefkowitz, E.J. (eds). San Diego: Elsevier, pp. 784–794.
27. Knoops, K., Kikkert, M., Worm, S.H.E., Zevenhoven-Dobbe, J.C., van der Meer, Y., Koster, A.J., et al. (2008) SARS-coronavirus replication is supported by a reticulovesicular network of modified endoplasmic reticulum. PLoS Biol 6: e226.
28. Knoops, K., Swett-Tapia, C., van den Worm, S.H.E., te Velthuis, A.J.W., Koster, A.J., Mommaas, A.M., et al. (2010) Integrity of the early secretory pathway promotes, but is not required for, severe acute respiratory syndrome coronavirus RNA synthesis and virus-induced remodeling of endoplasmic reticulum membranes. J Virol 84: 833–846.
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. Kuwabara, M., Wada, K., Maeda, Y., Miyazaki, A., and Tsunemitsu, H. (2007) First isolation of cytopathogenic bovine torovirus in cell culture from a calf with diarrhea. Clin Vaccine Immunol 14: 998–1004.
31. Lee, J.Y., Marshall, J.A., and Bowden, D.S. (1994) Characterization of rubella virus replication complexes using antibodies to double-stranded RNA. Virology 200: 307–312.
32. Limpens, R.W., van der Schaar, H.M., Kumar, D., Koster, A.J., Snijder, E.J., van Kuppeveld, F.J.M., and Bárcena, M. (2011) The transformation of enterovirus replication structures: a three-dimensional study of single- and double-membrane compartments. mBio 2: e00166–00111.
33. Mackenzie, J.M., Jones, M.K., and Young, P.R. (1996) Immunolocalization of the dengue virus nonstructural glycoprotein NS1 suggests a role in viral RNA replication. Virology 220: 232–240.
34. Maestre, A.M., Garzón, A., and Rodríguez, D. (2011) Equine torovirus (BEV) induces caspase-mediated apoptosis in infected cells. PLoS One 6: e20972.
35. Maier, H.J., Hawes, P.C., Cottam, E.M., Mantell, J., Verkade, P., Monaghan, P., et al. (2013) Infectious bronchitis virus generates spherules from zippered endoplasmic reticulum membranes. mBio 4: e00801–00813.
36. Miller, S., and Krijnse-Locker, J. (2008) Modification of intracellular membrane structures for virus replication. Nat Rev Micro 6: 363–374.
37. Netherton, C.L., and Wileman, T. (2011) Virus factories, double membrane vesicles and viroplasm generated in animal cells. Curr Opin Virol 1: 381–387.
38. Orenstein, J.M., Banach, B., and Baker, S.C. (2008) Morphogenesis of coronavirus HCoV-NL63 in cell culture: a transmission electron microscopic study. Open Infect Dis J 2: 52–58.
39. Patterson, G.H., and Lippincott-Schwartz, J. (2002) A photoactivatable GFP for selective photolabeling of proteins and cells. Science 297: 1873–1877.
40. 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.
41. 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.
42. Raturi, A., and Simmen, T. (2013) Where the endoplasmic reticulum and the mitochondrion tie the knot: the mitochondria-associated membrane (MAM). Biochimic et Biophys Acta (BBA) – Mol Cell Res 1833: 213–224.
43. Romero-Brey, I., Merz, A., Chiramel, A., Lee, J.Y., Chlanda, P., Haselman, U., et al. (2012) Three-dimensional architecture and biogenesis of membrane structures associated with hepatitis C virus replication. PLoS Pathog 8: e1003056.
44. Schneider, M., Ackermann, K., Stuart, M., Wex, C., Protzer, U., Schatzl, H.M., and Gilch, S. (2012) Severe acute respiratory syndrome coronavirus replication is severely impaired by MG132 due to proteasome-independent inhibition of M-calpain. J Virol 86: 10112–10122.
45. Shi, S.T., Schiller, J.J., Kanjanahaluethai, A., Baker, S.C., Oh, J.W., and Lai, M.M.C. (1999) Colocalization and membrane association of murine hepatitis virus gene 1 products and de novo-synthesized viral RNA in infected cells. J Virol 73: 5957–5969.
46. Siddell, S.G., Ziebuhr, J., and Snijder, E.J. (2010) Coronaviruses, toroviruses, and arteriviruses. In Topley & Wilson's Microbiology and Microbial Infections. Mahy, B.W.J., and Meulen, V. ter (eds). London: Hodder Arnold.
47. Sims, A.C., Ostermann, J., and Denison, M.R. (2000) Mouse hepatitis virus replicase proteins associate with two distinct populations of intracellular membranes. J Virol 74: 5647–5654.
48. Slot, J.W., and Geuze, H.J. (2007) Cryosectioning and immunolabeling. Nat Protocols 2: 2480–2491.
49. Smits, S.L., Snijder, E.J., and de Groot, R.J. (2006) Characterization of a torovirus main proteinase. J Virol 80: 4157–4167.
50. Snijder, E.J., and Horzinek, M.C. (1993) Toroviruses: replication, evolution and comparison with other members of the coronavirus-like superfamily. J Gen Virol 74: 2305–2316.
51. Snijder, E.J., den Boon, J.A., Bredenbeek, P.J., Horzinek, M.C., Rijnbrand, R., and Spaan, W.J. (1990) The carboxyl-terminal part of the putative Berne virus polymerase is expressed by ribosomal frameshifting and contains sequence motifs which indicate that toro- and coronaviruses are evolutionarily related. Nucleic Acids Res 18: 4535–4542.
52. Snijder, E.J., den Boon, J.A., Horzinek, M.C., and Spaan, W.J. (1991) Comparison of the genome organization of toro- and coronaviruses: evidence for two nonhomologous RNA recombination events during Berne virus evolution. Virology 180: 448–452.
53. Snijder, E.J., Wassenaar, A.L.M., van Dinten, L.C., Spaan, W.J.M., and Gorbalenya, A.E. (1996) The arterivirus nsp4 protease is the prototype of a novel group of chymotrypsin-like enzymes, the 3C-like serine proteases. J Biol Chem 271: 4864–4871.
54. 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.
55. 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.
56. Targett-Adams, P., Boulant, S., and McLauchlan, J. (2008) Visualization of double-stranded RNA in cells supporting hepatitis C virus RNA replication. J Virol 82: 2182–2195.
57. 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.
58. Ulferts, R., Mettenleiter, T.C., and Ziebuhr, J. (2011) Characterization of Bafinivirus main protease autoprocessing activities. J Virol 85: 1348–1359.
59. Weiss, M., and Horzinek, M.C. (1986) Morphogenesis of Berne virus (proposed family Toroviridae). J Gen Virol 67: 1305–1314.
60. Weiss, M., Steck, F., and Horzinek, M.C. (1983) Purification and partial characterization of a new enveloped RNA virus (Berne virus). J Gen Virol 64: 1849–1858.
61. Westaway, E.G., Mackenzie, J.M., Kenney, M.T., Jones, M.K., and Khromykh, A.A. (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.
62. Westaway, E.G., Khromykh, A.A., and Mackenzie, J.M. (1999) Nascent Flavivirus RNA colocalized in situ with double-stranded RNA in stable replication complexes. Virology 258: 108–117.
63. de Wilde, A.H., Raj, V.S., Oudshoorn, D., Bestebroer, T.M., van Nieuwkoop, S., Limpens, R.W., et al. (2013) MERS-coronavirus replication induces severe in vitro cytopathology and is strongly inhibited by cyclosporin A or interferon-alpha treatment. J Gen Virol 94: 1749–1760.
64. Zhao, Z., Thackray, L.B., Miller, B.C., Lynn, T.M., Becker, M.M., Ward, E., et al. (2007) Coronavirus replication does not require the autophagy gene ATG5. Autophagy 3: 581–585.
65. Ziebuhr, J., Snijder, E.J., and Gorbalenya, A.E. (2000) Virus-encoded proteinases and proteolytic processing in the Nidovirales. J Gen Virol 81: 853–879.