Architecture of torovirus replicative organelles.
double membrane vesicles
electron microscopy
electron tomography
replication complexes
replication organelles
torovirus
viral factories
Journal
Molecular microbiology
ISSN: 1365-2958
Titre abrégé: Mol Microbiol
Pays: England
ID NLM: 8712028
Informations de publication
Date de publication:
04 2022
04 2022
Historique:
revised:
20
12
2021
received:
02
12
2021
accepted:
22
12
2021
pubmed:
31
12
2021
medline:
20
4
2022
entrez:
30
12
2021
Statut:
ppublish
Résumé
Plus-stranded RNA viruses replicate in the cytosol of infected cells, in membrane-bound replication complexes. We previously identified double membrane vesicles (DMVs) in the cytoplasm of cells infected with Berne virus (BEV), the prototype member of the Torovirus genus (Nidovirales Order). Our previous analysis by transmission electron microscopy suggested that the DMVs form a reticulovesicular network (RVN) analogous those described for the related severe acute respiratory syndrome coronavirus (SARS-CoV-1). Here, we used serial sectioning and electron tomography to characterize the architecture of torovirus replication organelles, and to learn about their biogenesis and dynamics during the infection. The formation of a RVN in BEV infected cells was confirmed, where the outer membranes of the DMVs are interconnected with each other and with the ER. Paired or zippered ER membranes connected with the DMVs were also observed, and likely represent early structures that evolve to give rise to DMVs. Also, paired membranes forming small spherule-like invaginations were observed at late time post-infection. Although resembling in size, the tomographic analysis show that these structures are clearly different from the true spherules described previously for coronaviruses. Hence, BEV shows important similarities, but also some differences, in the architecture of the replication organelles with other nidoviruses.
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
837-850Informations de copyright
© 2021 John Wiley & Sons Ltd.
Références
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. Archives of Virology, 157, 423-431. https://doi.org/10.1007/s00705-011-1183-9
Almsherqi, Z.A. , Kohlwein, S.D. & Deng, Y. (2006) Cubic membranes: a legend beyond the Flatland* of cell membrane organization. Journal of Cell Biology, 173, 839-844. https://doi.org/10.1083/jcb.200603055
Al-Mulla, H.M. , Turrell, L. , Smith, N.M. , Payne, L. , Baliji, S. , Zust, R. et al. (2014) Competitive fitness in coronaviruses is not correlated with size or number of double-membrane vesicles under reduced-temperature growth conditions. MBio, 5, e01107-13. https://doi.org/10.1128/mBio.01107-13
Alonso-Padilla, J. , Pignatelli, J. , Simon-Grife, M. , Plazuelo, S. , Casal, J. & Rodriguez, D. (2012) Seroprevalence of porcine torovirus (PToV) in Spanish farms. BMC Research Notes, 5, 675. https://doi.org/10.1186/1756-0500-5-675
Ávila-Pérez, G. , Diaz-Beneitez, E. , Cubas-Gaona, L.L. , Nieves-Molina, G. , Rodríguez, J.R. , Rodríguez, J.F. et al. (2019) Activation of the autophagy pathway by Torovirus infection is irrelevant for virus replication. PLoS One, 14, e0219428. https://doi.org/10.1371/journal.pone.0219428
Ávila-Pérez, G. , Rejas, M.T. & Rodríguez, D. (2016) Ultrastructural characterization of membranous torovirus replication factories. Cellular Microbiology, 18, 1691-1708. https://doi.org/10.1111/cmi.12620
Cortese, M. , Lee, J.Y. , Cerikan, B. , Neufeldt, C.J. , Oorschot, V.M.J. , Köhrer, S. et al. (2020) Integrative imaging reveals SARS-CoV-2-induced reshaping of subcellular morphologies. Cell Host and Microbe, 28, 853-866.e5.
De Groot, R.J. (2008) Chapter 9: Molecular biology and evolution of torovirus. In: Perlman, S. , Gallagher, T. and Snijder, E.J. (Eds.) Nidoviruses. ASM Press, pp. 133-146.
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. Journal of General Virology, 94, 1749-1760.
DeDiego, 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. Journal of Virology, 81, 1701-1713. https://doi.org/10.1128/JVI.01467-06
den Boon, J.A. & Ahlquist, P. (2010) Organelle-like membrane compartmentalization of positive-strand RNA virus replication factories. Annual Review of Microbiology, 64, 241-256. https://doi.org/10.1146/annurev.micro.112408.134012
Dhama, K. , Pawaiya, R.V.S. , Chakraborty, S. , Tiwari, R. & Verma, A.K. (2014) Toroviruses affecting animals and humans: a review. Asian Journal of Animal and Veterinary Advances, 9, 190-201. https://doi.org/10.3923/ajava.2014.190.201
Doyle, N. , Hawes, P.C. , Simpson, J. , Adams, L.H. & Maier, H.J. (2019) The porcine deltacoronavirus replication organelle comprises double-membrane vesicles and zippered endoplasmic reticulum with double-membrane spherules. Viruses, 11, 1030.
Draker, R. , Roper, R.L. , Petric, M. & Tellier, R. (2006) The complete sequence of the bovine torovirus genome. Virus Research, 115, 56-68. https://doi.org/10.1016/j.virusres.2005.07.005
Duckmanton, L. , Luan, B. , Devenish, J. , Tellier, R. & Petric, M. (1997) Characterization of torovirus from human fecal specimens. Virology, 239, 158-168. https://doi.org/10.1006/viro.1997.8879
Fiala, J.C. (2005) Reconstruct: a free editor for serial section microscopy. Journal of Microscopy, 218, 52-61. https://doi.org/10.1111/j.1365-2818.2005.01466.x
Garzon, A. , Maestre, A.M. , Pignatelli, J. , Rejas, M.T. & Rodriguez, D. (2006) New insights on the structure and morphogenesis of Berne virus. Advances in Experimental Medicine and Biology, 581, 175-180.
Gosert, R. , Kanjanahaluethai, A. , Egger, D. , Bienz, K. & Baker, S.C. (2002) RNA replication of mouse hepatitis virus takes place at double-membrane vesicles. Journal of Virology, 76, 3697-3708. https://doi.org/10.1128/JVI.76.8.3697-3708.2002
Hagemeijer, M.C. , Verheije, M.H. , Ulasli, M. , Shaltiel, I.A. , de Vries, L.A. , Reggiori, F. et al. (2010) Dynamics of coronavirus replication-transcription complexes. Journal of Virology, 84, 2134-2149. https://doi.org/10.1128/JVI.01716-09
Harak, C. & Lohmann, V. (2015) Ultrastructure of the replication sites of positive-strand RNA viruses. Virology, 479-480, 418-433. https://doi.org/10.1016/j.virol.2015.02.029
Hoet, A.E. , Nielsen, P.R. , Hasoksuz, M. , Thomas, C. , Wittum, T.E. & Saif, L.J. (2003) Detection of bovine torovirus and other enteric pathogens in feces from diarrhea cases in cattle. Journal of Veterinary Diagnostic Investigation, 15, 205-212. https://doi.org/10.1177/104063870301500301
Hoet, A.E. & Saif, L.J. (2004) Bovine torovirus (Breda virus) revisited. Animal Health Research Reviews, 5, 157-171. https://doi.org/10.1079/AHR200498
Hu, Z.M. , Yang, Y.L. , Xu, L.D. , Wang, B. , Qin, P. & Huang, Y.W. (2019) Porcine torovirus (PToV)-a brief review of etiology, diagnostic assays and current epidemiology. Frontiers in Veterinary Science, 6, 120.
Ito, T. , Katayama, S. , Okada, N. , Masubuchi, K. , Fukuyama, S. & Shimizu, M. (2010) Genetic and antigenic characterization of newly isolated bovine toroviruses from Japanese cattle. Journal of Clinical Microbiology, 48, 1795-1800. https://doi.org/10.1128/JCM.02339-09
Jamieson, F.B. , Wang, E.E. , Bain, C. , Good, J. , Duckmanton, L. & Petric, M. (1998) Human torovirus: a new nosocomial gastrointestinal pathogen. Journal of Infectious Diseases, 178, 1263-1269. https://doi.org/10.1086/314434
Knoops, K. , Barcena, M. , Limpens, R.W. , Koster, A.J. , Mommaas, A.M. & Snijder, E.J. (2012) Ultrastructural characterization of arterivirus replication structures: reshaping the endoplasmic reticulum to accommodate viral RNA synthesis. Journal of Virology, 86, 2474-2487. https://doi.org/10.1128/JVI.06677-11
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 Biology, 6, e226. https://doi.org/10.1371/journal.pbio.0060226
Koopmans, M.P. , Goosen, E.S. , Lima, A.A. , McAuliffe, I.T. , Nataro, J.P. , Barrett, L.J. et al. (1997) Association of torovirus with acute and persistent diarrhea in children. The Pediatric Infectious Disease Journal, 16, 504-507. https://doi.org/10.1097/00006454-199705000-00010
Koopmans, M. & Horzinek, M.C. (1994) Toroviruses of animals and humans: a review. Advances in Virus Research, 43, 233-273.
Koopmans, M. , Petric, M. , Glass, R.I. & Monroe, S.S. (1993) Enzyme-linked immunosorbent assay reactivity of torovirus-like particles in fecal specimens from humans with diarrhea. Journal of Clinical Microbiology, 31, 2738-2744. https://doi.org/10.1128/jcm.31.10.2738-2744.1993
Koopmans, M. , van Wuijckhuise-Sjouke, L. , Schukken, Y.H. , Cremers, H. & Horzinek, M.C. (1991) Association of diarrhea in cattle with torovirus infections on farms. American Journal of Veterinary Research, 52, 1769-1773.
Kremer, J.R. , Mastronarde, D.N. & McIntosh, J.R. (1996) Computer visualization of three-dimensional image data using IMOD. Journal of Structural Biology, 116, 71-76. https://doi.org/10.1006/jsbi.1996.0013
Kroneman, A. , Cornelissen, L.A. , Horzinek, M.C. , de Groot, R.J. & Egberink, H.F. (1998) Identification and characterization of a porcine torovirus. Journal of Virology, 72, 3507-3511. https://doi.org/10.1128/JVI.72.5.3507-3511.1998
Kuwabara, M. , Wada, K. , Maeda, Y. , Miyazaki, A. & Tsunemitsu, H. (2007) First isolation of cytopathogenic bovine torovirus in cell culture from a calf with diarrhea. Clinical and Vaccine Immunology, 14, 998-1004. https://doi.org/10.1128/CVI.00475-06
Limpens, R.W. , van der Schaar, H.M. , Kumar, D. , Koster, A.J. , Snijder, E.J. , van Kuppeveld, F.J.M. et al. (2011) The transformation of enterovirus replication structures: a three-dimensional study of single- and double-membrane compartments. MBio, 2, e00166-11. https://doi.org/10.1128/mBio.00166-11
Lodha, A. , de Silva, N. , Petric, M. & Moore, A.M. (2005) Human torovirus: a new virus associated with neonatal necrotizing enterocolitis. Acta Paediatrica, 94, 1085-1088. https://doi.org/10.1111/j.1651-2227.2005.tb02049.x
Maestre, A.M. , Garzón, A. & Rodríguez, D. (2011) Equine torovirus (BEV) induces caspase-mediated apoptosis in infected cells. PLoS One, 6, e20972. https://doi.org/10.1371/journal.pone.0020972
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, e00801-13. https://doi.org/10.1128/mBio.00801-13
Maier, H.J. , Neuman, B.W. , Bickerton, E. , Keep, S.M. , Alrashedi, H. , Hall, R. et al. (2016) Extensive coronavirus-induced membrane rearrangements are not a determinant of pathogenicity. Scientific Reports, 6, 27126. https://doi.org/10.1038/srep27126
Metwally, S. , Mohamed, F. , Faaberg, K. , Burrage, T. , Prarat, M. , Moran, K. et al. (2010) Pathogenicity and molecular characterization of emerging porcine reproductive and respiratory syndrome virus in Vietnam in 2007. Transboundary and Emerging Diseases, 57, 315-329. https://doi.org/10.1111/j.1865-1682.2010.01152.x
Mihelc, E.M. , Baker, S.C. & Lanman, J.K. (2021) Coronavirus infection induces progressive restructuring of the endoplasmic reticulum involving the formation and degradation of double membrane vesicles. Virology, 556, 9-22. https://doi.org/10.1016/j.virol.2020.12.007
Miller, S. & Krijnse-Locker, J. (2008) Modification of intracellular membrane structures for virus replication. Nature Reviews Microbiology, 6, 363-374. https://doi.org/10.1038/nrmicro1890
Orenstein, J.M. , Banach, B. & Baker, S.C. (2008) Morphogenesis of coronavirus HCoV-NL63 in cell culture: a transmission electron microscopic study. The Open Infectious Diseases Journal, 2, 52-58. https://doi.org/10.2174/1874279300802010052
Oudshoorn, D. , van der Hoeven, B. , Limpens, R.W. , Beugeling, C. , Snijder, E.J. , Barcena, M. et al. (2016) Antiviral innate immune response interferes with the formation of replication-associated membrane structures induced by a positive-strand RNA virus. MBio, 7, e01991-16. https://doi.org/10.1128/mBio.01991-16
Paul, D. & Bartenschlager, R. (2013) Architecture and biogenesis of plus-strand RNA virus replication factories. World Journal of Virology, 2, 32-48. https://doi.org/10.5501/wjv.v2.i2.32
Pedersen, K.W. , van der Meer, Y. , Roos, N. & 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. Journal of Virology, 73, 2016-2026. https://doi.org/10.1128/JVI.73.3.2016-2026.1999
Pignatelli, J. , Alonso-Padilla, J. & Rodriguez, D. (2013) Lineage specific antigenic differences in porcine torovirus hemagglutinin-esterase (PToV-HE) protein. Veterinary Research, 44, 126. https://doi.org/10.1186/1297-9716-44-126
Pignatelli, J. , Grau-Roma, L. , Jimenez, M. , Segales, J. & Rodriguez, D. (2010a) Longitudinal serological and virological study on porcine torovirus (PToV) in piglets from Spanish farms. Veterinary Microbiology, 146, 260-268. https://doi.org/10.1016/j.vetmic.2010.05.023
Pignatelli, J. , Jimenez, M. , Grau-Roma, L. & Rodriguez, D. (2010b) Detection of porcine torovirus by real time RT-PCR in piglets from a Spanish farm. Journal of Virological Methods, 163, 398-404. https://doi.org/10.1016/j.jviromet.2009.10.031
Pignatelli, J. , Jimenez, M. , Luque, J. , Rejas, M.T. , Lavazza, A. & Rodriguez, D. (2009) Molecular characterization of a new PToV strain. Evolutionary implications. Virus Research, 143, 33-43.
Pohlenz, J.F. , Cheville, N.F. , Woode, G.N. & Mokresh, A.H. (1984) Cellular lesions in intestinal mucosa of gnotobiotic calves experimentally infected with a new unclassified bovine virus (Breda virus). Veterinary Pathology, 21, 407-417. https://doi.org/10.1177/030098588402100407
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 Path, 8, e1003056. https://doi.org/10.1371/journal.ppat.1003056
Scott, F.M. , Holliman, A. , Jones, G.W. , Gray, E.W. & Fitton, J. (1996) Evidence of torovirus infection in diarrhoeic cattle. The Veterinary Record, 138, 284-285. https://doi.org/10.1136/vr.138.12.284
Smits, S.L. , Snijder, E.J. & de Groot, R.J. (2006) Characterization of a torovirus main proteinase. Journal of Virology, 80, 4157-4167. https://doi.org/10.1128/JVI.80.8.4157-4167.2006
Smits, S.L. , van Vliet, A.L. , Segeren, K. , el Azzouzi, H. , van Essen, M. & de Groot, R.J. (2005) Torovirus non-discontinuous transcription: mutational analysis of a subgenomic mRNA promoter. Journal of Virology, 79, 8275-8281. https://doi.org/10.1128/JVI.79.13.8275-8281.2005
Snapp, E.L. , Hegde, R.S. , Francolini, M. , Lombardo, F. , Colombo, S. , Pedrazzini, E. et al. (2003) Formation of stacked ER cisternae by low affinity protein interactions. Journal of Cell Biology, 163, 257-269. https://doi.org/10.1083/jcb.200306020
Snijder, E.J. , den Boon, J.A. , Bredenbeek, P.J. , Horzinek, M.C. , Rijnbrand, R. & Spaan, W.J. (1990a) 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 Research, 18, 4535-4542.
Snijder, E.J. , den Boon, J.A. , Horzinek, M.C. & 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. https://doi.org/10.1016/0042-6822(91)90056-H
Snijder, E.J. , Den Boon, J.A. , Spaan, W.J. , Weiss, M. & Horzinek, M.C. (1990b) Primary structure and post-translational processing of the Berne virus peplomer protein. Virology, 178, 355-363. https://doi.org/10.1016/0042-6822(90)90332-L
Snijder, E.J. & Horzinek, M.C. (1993) Toroviruses: replication, evolution and comparison with other members of the coronavirus-like superfamily. Journal of General Virology, 74, 2305-2316.
Snijder, E.J. , Horzinek, M.C. & Spaan, W.J. (1990c) A 3'-coterminal nested set of independently transcribed mRNAs is generated during Berne virus replication. Journal of Virology, 64, 331-338. https://doi.org/10.1128/jvi.64.1.331-338.1990
Snijder, E.J. , Limpens, R. , de Wilde, A.H. , de Jong, A.W.M. , Zevenhoven-Dobbe, J.C. , Maier, H.J. et al. (2020) A unifying structural and functional model of the coronavirus replication organelle: Tracking down RNA synthesis. PLoS Biology, 18, e3000715. https://doi.org/10.1371/journal.pbio.3000715
Snijder, E.J. , van der Meer, Y. , Zevenhoven-Dobbe, J. , Onderwater, J.J. , van der Meulen, J. , Koerten, H.K. et al. (2006) Ultrastructure and origin of membrane vesicles associated with the severe acute respiratory syndrome coronavirus replication complex. Journal of Virology, 80, 5927-5940. https://doi.org/10.1128/JVI.02501-05
Stewart, H. , Brown, K. , Dinan, A.M. , Irigoyen, N. , Snijder, E.J. & Firth, A.E. (2018) Transcriptional and translational landscape of equine torovirus. Journal of Virology, 92, e00589-18. https://doi.org/10.1128/JVI.00589-18
Stueckemann, J.A. , Ritzi, D.M. , Holth, M. , Smith, M.S. , Swart, W.J. , Cafruny, W.A. et al. (1982) Replication of lactate dehydrogenase-elevating virus in macrophages. Journal of General Virology, 59, 245-262.
Ulasli, M. , Verheije, M.H. , de Haan, C.A. & Reggiori, F. (2010) Qualitative and quantitative ultrastructural analysis of the membrane rearrangements induced by coronavirus. Cellular Microbiology, 12, 844-861. https://doi.org/10.1111/j.1462-5822.2010.01437.x
van der Hoeven, B. , Oudshoorn, D. , Koster, A.J. , Snijder, E.J. , Kikkert, M. & Bárcena, M. (2016) Biogenesis and architecture of arterivirus replication organelles. Virus Research, 220, 70-90. https://doi.org/10.1016/j.virusres.2016.04.001
van Vliet, A.L. , Smits, S.L. , Rottier, P.J. & de Groot, R.J. (2002) Discontinuous and non-discontinuous subgenomic RNA transcription in a nidovirus. EMBO Journal, 21, 6571-6580. https://doi.org/10.1093/emboj/cdf635
Weiss, M. & Horzinek, M.C. (1986) Morphogenesis of Berne virus (proposed family Toroviridae). Journal of General Virology, 67, 1305-1314. https://doi.org/10.1099/0022-1317-67-7-1305
Weiss, M. , Steck, F. & Horzinek, M.C. (1983) Purification and partial characterization of a new enveloped RNA virus (Berne virus). Journal of General Virology, 64, 1849-1858. https://doi.org/10.1099/0022-1317-64-9-1849
Wilhelmi, I. , Roman, E. & Sanchez-Fauquier, A. (2003) Viruses causing gastroenteritis. Clinical Microbiology and Infection, 9, 247-262. https://doi.org/10.1046/j.1469-0691.2003.00560.x
Wolff, G. , Limpens, R. , Zevenhoven-Dobbe, J.C. , Laugks, U. , Zheng, S. , de Jong, A.W.M. et al. (2020a) A molecular pore spans the double membrane of the coronavirus replication organelle. Science, 369, 1395-1398. https://doi.org/10.1126/science.abd3629
Wolff, G. , Melia, C.E. , Snijder, E.J. & Bárcena, M. (2020b) Double-membrane vesicles as platforms for viral replication. Trends in Microbiology, 28, 1022-1033. https://doi.org/10.1016/j.tim.2020.05.009
Wood, O. , Tauraso, N. & Liebhaber, H. (1970) Electron microscopic study of tissue cultures infected with simian haemorrhagic fever virus. Journal of General Virology, 7, 129-136. https://doi.org/10.1099/0022-1317-7-2-129
Zhou, X. , Cong, Y. , Veenendaal, T. , Klumperman, J. , Shi, D. , Mari, M. et al. (2017) Ultrastructural characterization of membrane rearrangements induced by porcine epidemic diarrhea virus infection. Viruses, 9, 251. https://doi.org/10.3390/v9090251