The Porcine Deltacoronavirus Replication Organelle Comprises Double-Membrane Vesicles and Zippered Endoplasmic Reticulum with Double-Membrane Spherules

Porcine deltacoronavirus (PDCoV) was first identified in Hong Kong in 2012 from samples taken from pigs in 2009. PDCoV was subsequently identified in the USA in 2014 in pigs with a history of severe diarrhea. The virus has now been detected in pigs in several countries around the world. Following th...

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Main Authors: Nicole Doyle, Philippa C. Hawes, Jennifer Simpson, Lorin H. Adams, Helena J. Maier
Format: Article
Language:English
Published: MDPI AG 2019-11-01
Series:Viruses
Subjects:
Online Access:https://www.mdpi.com/1999-4915/11/11/1030
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author Nicole Doyle
Philippa C. Hawes
Jennifer Simpson
Lorin H. Adams
Helena J. Maier
author_facet Nicole Doyle
Philippa C. Hawes
Jennifer Simpson
Lorin H. Adams
Helena J. Maier
author_sort Nicole Doyle
collection DOAJ
description Porcine deltacoronavirus (PDCoV) was first identified in Hong Kong in 2012 from samples taken from pigs in 2009. PDCoV was subsequently identified in the USA in 2014 in pigs with a history of severe diarrhea. The virus has now been detected in pigs in several countries around the world. Following the development of tissue culture adapted strains of PDCoV, it is now possible to address questions regarding virus&#8722;host cell interactions for this genera of coronavirus. Here, we presented a detailed study of PDCoV-induced replication organelles. All positive-strand RNA viruses induce the rearrangement of cellular membranes during virus replication to support viral RNA synthesis, forming the replication organelle. Replication organelles for the <i>Alpha-</i>, <i>Beta</i>-, and <i>Gammacoronavirus</i> genera have been characterized. All coronavirus genera induced the formation of double-membrane vesicles (DMVs). In addition, <i>Alpha</i>- and <i>Betacoronaviruses</i> induce the formation of convoluted membranes, while <i>Gammacoronaviruses</i> induce the formation of zippered endoplasmic reticulum (ER) with tethered double-membrane spherules. However, the structures induced by <i>Deltacoronaviruses</i>, particularly the presence of convoluted membranes or double-membrane spherules, are unknown. Initially, the dynamics of PDCoV strain OH-FD22 replication were assessed with the onset of viral RNA synthesis, protein synthesis, and progeny particle release determined. Subsequently, virus-induced membrane rearrangements were identified in infected cells by electron microscopy. As has been observed for all other coronaviruses studied to date, PDCoV replication was found to induce the formation of double-membrane vesicles. Significantly, however, PDCoV replication was also found to induce the formation of regions of zippered endoplasmic reticulum, small associated tethered vesicles, and double-membrane spherules. These structures strongly resemble the replication organelle induced by avian <i>Gammacoronavirus</i> infectious bronchitis virus.
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spelling doaj.art-715efa7323e741e588743524312457c12022-12-22T00:52:54ZengMDPI AGViruses1999-49152019-11-011111103010.3390/v11111030v11111030The Porcine Deltacoronavirus Replication Organelle Comprises Double-Membrane Vesicles and Zippered Endoplasmic Reticulum with Double-Membrane SpherulesNicole Doyle0Philippa C. Hawes1Jennifer Simpson2Lorin H. Adams3Helena J. Maier4The Pirbright Institute, Ash Road, Woking, Surrey GU24 0NF, UKThe Pirbright Institute, Ash Road, Woking, Surrey GU24 0NF, UKThe Pirbright Institute, Ash Road, Woking, Surrey GU24 0NF, UKThe Pirbright Institute, Ash Road, Woking, Surrey GU24 0NF, UKThe Pirbright Institute, Ash Road, Woking, Surrey GU24 0NF, UKPorcine deltacoronavirus (PDCoV) was first identified in Hong Kong in 2012 from samples taken from pigs in 2009. PDCoV was subsequently identified in the USA in 2014 in pigs with a history of severe diarrhea. The virus has now been detected in pigs in several countries around the world. Following the development of tissue culture adapted strains of PDCoV, it is now possible to address questions regarding virus&#8722;host cell interactions for this genera of coronavirus. Here, we presented a detailed study of PDCoV-induced replication organelles. All positive-strand RNA viruses induce the rearrangement of cellular membranes during virus replication to support viral RNA synthesis, forming the replication organelle. Replication organelles for the <i>Alpha-</i>, <i>Beta</i>-, and <i>Gammacoronavirus</i> genera have been characterized. All coronavirus genera induced the formation of double-membrane vesicles (DMVs). In addition, <i>Alpha</i>- and <i>Betacoronaviruses</i> induce the formation of convoluted membranes, while <i>Gammacoronaviruses</i> induce the formation of zippered endoplasmic reticulum (ER) with tethered double-membrane spherules. However, the structures induced by <i>Deltacoronaviruses</i>, particularly the presence of convoluted membranes or double-membrane spherules, are unknown. Initially, the dynamics of PDCoV strain OH-FD22 replication were assessed with the onset of viral RNA synthesis, protein synthesis, and progeny particle release determined. Subsequently, virus-induced membrane rearrangements were identified in infected cells by electron microscopy. As has been observed for all other coronaviruses studied to date, PDCoV replication was found to induce the formation of double-membrane vesicles. Significantly, however, PDCoV replication was also found to induce the formation of regions of zippered endoplasmic reticulum, small associated tethered vesicles, and double-membrane spherules. These structures strongly resemble the replication organelle induced by avian <i>Gammacoronavirus</i> infectious bronchitis virus.https://www.mdpi.com/1999-4915/11/11/1030porcine deltacoronaviruscoronavirusreplication organelledouble-membrane vesicledmvzippered erspheruledouble-membrane spherule
spellingShingle Nicole Doyle
Philippa C. Hawes
Jennifer Simpson
Lorin H. Adams
Helena J. Maier
The Porcine Deltacoronavirus Replication Organelle Comprises Double-Membrane Vesicles and Zippered Endoplasmic Reticulum with Double-Membrane Spherules
Viruses
porcine deltacoronavirus
coronavirus
replication organelle
double-membrane vesicle
dmv
zippered er
spherule
double-membrane spherule
title The Porcine Deltacoronavirus Replication Organelle Comprises Double-Membrane Vesicles and Zippered Endoplasmic Reticulum with Double-Membrane Spherules
title_full The Porcine Deltacoronavirus Replication Organelle Comprises Double-Membrane Vesicles and Zippered Endoplasmic Reticulum with Double-Membrane Spherules
title_fullStr The Porcine Deltacoronavirus Replication Organelle Comprises Double-Membrane Vesicles and Zippered Endoplasmic Reticulum with Double-Membrane Spherules
title_full_unstemmed The Porcine Deltacoronavirus Replication Organelle Comprises Double-Membrane Vesicles and Zippered Endoplasmic Reticulum with Double-Membrane Spherules
title_short The Porcine Deltacoronavirus Replication Organelle Comprises Double-Membrane Vesicles and Zippered Endoplasmic Reticulum with Double-Membrane Spherules
title_sort porcine deltacoronavirus replication organelle comprises double membrane vesicles and zippered endoplasmic reticulum with double membrane spherules
topic porcine deltacoronavirus
coronavirus
replication organelle
double-membrane vesicle
dmv
zippered er
spherule
double-membrane spherule
url https://www.mdpi.com/1999-4915/11/11/1030
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