Ultrastructural Characterization of Arterivirus Replication Structures: Reshaping the Endoplasmic Reticulum To Accommodate Viral RNA Synthesis
Identifieur interne : 000028 ( PascalFrancis/Checkpoint ); précédent : 000027; suivant : 000029Ultrastructural Characterization of Arterivirus Replication Structures: Reshaping the Endoplasmic Reticulum To Accommodate Viral RNA Synthesis
Auteurs : Kèvin Knoops [Pays-Bas] ; Montserrat Barcena [Pays-Bas] ; Ronald W. A. L. Limpens [Pays-Bas] ; Abraham J. Koster [Pays-Bas] ; A. Mieke Mommaas [Pays-Bas] ; Eric J. Snijder [Pays-Bas]Source :
- Journal of virology [ 0022-538X ] ; 2012.
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- Pascal (Inist)
English descriptors
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Abstract
Virus-induced membrane structures support the assembly and function of positive-strand RNA virus replication complexes. The replicase proteins of arteriviruses are associated with double-membrane vesicles (DMVs), which were previously proposed to derive from the endoplasmic reticulum (ER). Using electron tomography, we performed an in-depth ultrastructural analysis of cells infected with the prototypic arterivirus equine arteritis virus (EAV). We established that the outer membranes of EAV-induced DMVs are interconnected with each other and with the ER, thus forming a reticulovesicular network (RVN) resembling that previously described for the distantly related severe acute respiratory syndrome (SARS) coronavirus. Despite significant morphological differences, a striking parallel between the two virus groups, and possibly all members of the order Nidovirales, is the accumulation in the DMV interior of double-stranded RNA, the presumed intermediate of viral RNA synthesis. In our electron tomograms, connections between the DMV interior and cytosol could not be unambiguously identified, suggesting that the double-stranded RNA is compartmentalized by the DMV membranes. As a novel approach to visualize and quantify the RNA content of viral replication structures, we explored electron spectroscopic imaging of DMVs, which revealed the presence of phosphorus in amounts equaling on average a few dozen copies of the EAV RNA genome. Finally, our electron tomograms revealed a network of nucleocapsid protein-containing protein tubules that appears to be intertwined with the RVN. This potential intermediate in nucleocapsid formation, which was not observed in coronavirus-infected cells, suggests that arterivirus RNA synthesis and assembly are coordinated in intracellular space.
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A. L." last="Limpens">Ronald W. A. L. Limpens</name><affiliation wicri:level="3"><inist:fA14 i1="01"><s1>Electron Microscopy Section, Department of Molecular Cell Biology, Leiden University Medical Center</s1><s2>Leiden</s2><s3>NLD</s3><sZ>1 aut.</sZ><sZ>2 aut.</sZ><sZ>3 aut.</sZ><sZ>4 aut.</sZ><sZ>5 aut.</sZ></inist:fA14><country>Pays-Bas</country><placeName><settlement type="city">Leyde</settlement><region nuts="2" type="province">Hollande-Méridionale</region></placeName></affiliation></author><author><name sortKey="Koster, Abraham J" sort="Koster, Abraham J" uniqKey="Koster A" first="Abraham J." last="Koster">Abraham J. Koster</name><affiliation wicri:level="3"><inist:fA14 i1="01"><s1>Electron Microscopy Section, Department of Molecular Cell Biology, Leiden University Medical Center</s1><s2>Leiden</s2><s3>NLD</s3><sZ>1 aut.</sZ><sZ>2 aut.</sZ><sZ>3 aut.</sZ><sZ>4 aut.</sZ><sZ>5 aut.</sZ></inist:fA14><country>Pays-Bas</country><placeName><settlement type="city">Leyde</settlement><region nuts="2" type="province">Hollande-Méridionale</region></placeName></affiliation></author><author><name sortKey="Mieke Mommaas, A" sort="Mieke Mommaas, A" uniqKey="Mieke Mommaas A" first="A." last="Mieke Mommaas">A. Mieke Mommaas</name><affiliation wicri:level="3"><inist:fA14 i1="01"><s1>Electron Microscopy Section, Department of Molecular Cell Biology, Leiden University Medical Center</s1><s2>Leiden</s2><s3>NLD</s3><sZ>1 aut.</sZ><sZ>2 aut.</sZ><sZ>3 aut.</sZ><sZ>4 aut.</sZ><sZ>5 aut.</sZ></inist:fA14><country>Pays-Bas</country><placeName><settlement type="city">Leyde</settlement><region nuts="2" type="province">Hollande-Méridionale</region></placeName></affiliation></author><author><name sortKey="Snijder, Eric J" sort="Snijder, Eric J" uniqKey="Snijder E" first="Eric J." last="Snijder">Eric J. Snijder</name><affiliation wicri:level="3"><inist:fA14 i1="02"><s1>Molecular Virology Laboratory, Department of Medical Microbiology, Center of Infectious Diseases, Leiden University Medical Center</s1><s2>Leiden</s2><s3>NLD</s3><sZ>1 aut.</sZ><sZ>6 aut.</sZ></inist:fA14><country>Pays-Bas</country><placeName><settlement type="city">Leyde</settlement><region nuts="2" type="province">Hollande-Méridionale</region></placeName></affiliation></author></analytic><series><title level="j" type="main">Journal of virology</title><title level="j" type="abbreviated">J. virol.</title><idno type="ISSN">0022-538X</idno><imprint><date when="2012">2012</date></imprint></series></biblStruct></sourceDesc><seriesStmt><title level="j" type="main">Journal of virology</title><title level="j" type="abbreviated">J. virol.</title><idno type="ISSN">0022-538X</idno></seriesStmt></fileDesc><profileDesc><textClass><keywords scheme="KwdEn" xml:lang="en"><term>Arterivirus</term><term>Endoplasmic reticulum</term><term>Replication</term></keywords><keywords scheme="Pascal" xml:lang="fr"><term>Arterivirus</term><term>Réplication</term><term>Réticulum endoplasmique</term></keywords></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">Virus-induced membrane structures support the assembly and function of positive-strand RNA virus replication complexes. The replicase proteins of arteriviruses are associated with double-membrane vesicles (DMVs), which were previously proposed to derive from the endoplasmic reticulum (ER). Using electron tomography, we performed an in-depth ultrastructural analysis of cells infected with the prototypic arterivirus equine arteritis virus (EAV). We established that the outer membranes of EAV-induced DMVs are interconnected with each other and with the ER, thus forming a reticulovesicular network (RVN) resembling that previously described for the distantly related severe acute respiratory syndrome (SARS) coronavirus. Despite significant morphological differences, a striking parallel between the two virus groups, and possibly all members of the order Nidovirales, is the accumulation in the DMV interior of double-stranded RNA, the presumed intermediate of viral RNA synthesis. In our electron tomograms, connections between the DMV interior and cytosol could not be unambiguously identified, suggesting that the double-stranded RNA is compartmentalized by the DMV membranes. As a novel approach to visualize and quantify the RNA content of viral replication structures, we explored electron spectroscopic imaging of DMVs, which revealed the presence of phosphorus in amounts equaling on average a few dozen copies of the EAV RNA genome. Finally, our electron tomograms revealed a network of nucleocapsid protein-containing protein tubules that appears to be intertwined with the RVN. This potential intermediate in nucleocapsid formation, which was not observed in coronavirus-infected cells, suggests that arterivirus RNA synthesis and assembly are coordinated in intracellular space.</div></front></TEI><inist><standard h6="B"><pA><fA01 i1="01" i2="1"><s0>0022-538X</s0></fA01><fA03 i2="1"><s0>J. virol.</s0></fA03><fA05><s2>86</s2></fA05><fA06><s2>5</s2></fA06><fA08 i1="01" i2="1" l="ENG"><s1>Ultrastructural Characterization of Arterivirus Replication Structures: Reshaping the Endoplasmic Reticulum To Accommodate Viral RNA Synthesis</s1></fA08><fA11 i1="01" i2="1"><s1>KNOOPS (Kèvin)</s1></fA11><fA11 i1="02" i2="1"><s1>BARCENA (Montserrat)</s1></fA11><fA11 i1="03" i2="1"><s1>LIMPENS (Ronald W. A. 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All rights reserved.</s1></fA44><fA45><s0>67 ref.</s0></fA45><fA47 i1="01" i2="1"><s0>12-0114301</s0></fA47><fA60><s1>P</s1></fA60><fA61><s0>A</s0></fA61><fA64 i1="01" i2="1"><s0>Journal of virology</s0></fA64><fA66 i1="01"><s0>USA</s0></fA66><fC01 i1="01" l="ENG"><s0>Virus-induced membrane structures support the assembly and function of positive-strand RNA virus replication complexes. The replicase proteins of arteriviruses are associated with double-membrane vesicles (DMVs), which were previously proposed to derive from the endoplasmic reticulum (ER). Using electron tomography, we performed an in-depth ultrastructural analysis of cells infected with the prototypic arterivirus equine arteritis virus (EAV). We established that the outer membranes of EAV-induced DMVs are interconnected with each other and with the ER, thus forming a reticulovesicular network (RVN) resembling that previously described for the distantly related severe acute respiratory syndrome (SARS) coronavirus. Despite significant morphological differences, a striking parallel between the two virus groups, and possibly all members of the order Nidovirales, is the accumulation in the DMV interior of double-stranded RNA, the presumed intermediate of viral RNA synthesis. In our electron tomograms, connections between the DMV interior and cytosol could not be unambiguously identified, suggesting that the double-stranded RNA is compartmentalized by the DMV membranes. As a novel approach to visualize and quantify the RNA content of viral replication structures, we explored electron spectroscopic imaging of DMVs, which revealed the presence of phosphorus in amounts equaling on average a few dozen copies of the EAV RNA genome. Finally, our electron tomograms revealed a network of nucleocapsid protein-containing protein tubules that appears to be intertwined with the RVN. This potential intermediate in nucleocapsid formation, which was not observed in coronavirus-infected cells, suggests that arterivirus RNA synthesis and assembly are coordinated in intracellular space.</s0></fC01><fC02 i1="01" i2="X"><s0>002A05C10</s0></fC02><fC03 i1="01" i2="X" l="FRE"><s0>Arterivirus</s0><s2>NW</s2><s5>01</s5></fC03><fC03 i1="01" i2="X" l="ENG"><s0>Arterivirus</s0><s2>NW</s2><s5>01</s5></fC03><fC03 i1="01" i2="X" l="SPA"><s0>Arterivirus</s0><s2>NW</s2><s5>01</s5></fC03><fC03 i1="02" i2="X" l="FRE"><s0>Réplication</s0><s5>05</s5></fC03><fC03 i1="02" i2="X" l="ENG"><s0>Replication</s0><s5>05</s5></fC03><fC03 i1="02" i2="X" l="SPA"><s0>Replicación</s0><s5>05</s5></fC03><fC03 i1="03" i2="X" l="FRE"><s0>Réticulum endoplasmique</s0><s5>06</s5></fC03><fC03 i1="03" i2="X" l="ENG"><s0>Endoplasmic reticulum</s0><s5>06</s5></fC03><fC03 i1="03" i2="X" l="SPA"><s0>Retículo endoplásmico</s0><s5>06</s5></fC03><fC07 i1="01" i2="X" l="FRE"><s0>Arteriviridae</s0><s2>NW</s2></fC07><fC07 i1="01" i2="X" l="ENG"><s0>Arteriviridae</s0><s2>NW</s2></fC07><fC07 i1="01" i2="X" l="SPA"><s0>Arteriviridae</s0><s2>NW</s2></fC07><fC07 i1="02" i2="X" l="FRE"><s0>Nidovirales</s0><s2>NW</s2></fC07><fC07 i1="02" i2="X" l="ENG"><s0>Nidovirales</s0><s2>NW</s2></fC07><fC07 i1="02" i2="X" l="SPA"><s0>Nidovirales</s0><s2>NW</s2></fC07><fC07 i1="03" i2="X" l="FRE"><s0>Virus</s0><s2>NW</s2></fC07><fC07 i1="03" i2="X" l="ENG"><s0>Virus</s0><s2>NW</s2></fC07><fC07 i1="03" i2="X" l="SPA"><s0>Virus</s0><s2>NW</s2></fC07><fN21><s1>086</s1></fN21><fN44 i1="01"><s1>OTO</s1></fN44><fN82><s1>OTO</s1></fN82></pA></standard></inist><affiliations><list><country><li>Pays-Bas</li></country><region><li>Hollande-Méridionale</li></region><settlement><li>Leyde</li></settlement></list><tree><country name="Pays-Bas"><region name="Hollande-Méridionale"><name sortKey="Knoops, Kevin" sort="Knoops, Kevin" uniqKey="Knoops K" first="Kèvin" last="Knoops">Kèvin Knoops</name></region><name sortKey="Barcena, Montserrat" sort="Barcena, Montserrat" uniqKey="Barcena M" first="Montserrat" last="Barcena">Montserrat Barcena</name><name sortKey="Knoops, Kevin" sort="Knoops, Kevin" uniqKey="Knoops K" first="Kèvin" last="Knoops">Kèvin Knoops</name><name sortKey="Koster, Abraham J" sort="Koster, Abraham J" uniqKey="Koster A" first="Abraham J." last="Koster">Abraham J. Koster</name><name sortKey="Limpens, Ronald W A L" sort="Limpens, Ronald W A L" uniqKey="Limpens R" first="Ronald W. A. L." last="Limpens">Ronald W. A. L. Limpens</name><name sortKey="Mieke Mommaas, A" sort="Mieke Mommaas, A" uniqKey="Mieke Mommaas A" first="A." last="Mieke Mommaas">A. Mieke Mommaas</name><name sortKey="Snijder, Eric J" sort="Snijder, Eric J" uniqKey="Snijder E" first="Eric J." last="Snijder">Eric J. Snijder</name></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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