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A novel capsid protein network allows the characteristic internal membrane structure of Marseilleviridae giant viruses

Marseilleviridae is a family of giant viruses, showing a characteristic internal membrane with extrusions underneath the icosahedral vertices. However, such large objects, with a maximum diameter of 250 nm are technically difficult to examine at sub-nanometre resolution by cryo-electron microscopy....

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Autores principales: Chihara, Akane, Burton-Smith, Raymond N., Kajimura, Naoko, Mitsuoka, Kaoru, Okamoto, Kenta, Song, Chihong, Murata, Kazuyoshi
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9742146/
https://www.ncbi.nlm.nih.gov/pubmed/36504202
http://dx.doi.org/10.1038/s41598-022-24651-2
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author Chihara, Akane
Burton-Smith, Raymond N.
Kajimura, Naoko
Mitsuoka, Kaoru
Okamoto, Kenta
Song, Chihong
Murata, Kazuyoshi
author_facet Chihara, Akane
Burton-Smith, Raymond N.
Kajimura, Naoko
Mitsuoka, Kaoru
Okamoto, Kenta
Song, Chihong
Murata, Kazuyoshi
author_sort Chihara, Akane
collection PubMed
description Marseilleviridae is a family of giant viruses, showing a characteristic internal membrane with extrusions underneath the icosahedral vertices. However, such large objects, with a maximum diameter of 250 nm are technically difficult to examine at sub-nanometre resolution by cryo-electron microscopy. Here, we tested the utility of 1 MV high-voltage cryo-EM (cryo-HVEM) for single particle structural analysis (SPA) of giant viruses using tokyovirus, a species of Marseilleviridae, and revealed the capsid structure at 7.7 Å resolution. The capsid enclosing the viral DNA consisted primarily of four layers: (1) major capsid proteins (MCPs) and penton proteins, (2) minor capsid proteins (mCPs), (3) scaffold protein components (ScPCs), and (4) internal membrane. The mCPs showed a novel capsid lattice consisting of eight protein components. ScPCs connecting the icosahedral vertices supported the formation of the membrane extrusions, and possibly act like tape measure proteins reported in other giant viruses. The density on top of the MCP trimer was suggested to include glycoproteins. This is the first attempt at cryo-HVEM SPA. We found the primary limitations to be the lack of automated data acquisition and software support for collection and processing and thus achievable resolution. However, the results pave the way for using cryo-HVEM for structural analysis of larger biological specimens.
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spelling pubmed-97421462022-12-13 A novel capsid protein network allows the characteristic internal membrane structure of Marseilleviridae giant viruses Chihara, Akane Burton-Smith, Raymond N. Kajimura, Naoko Mitsuoka, Kaoru Okamoto, Kenta Song, Chihong Murata, Kazuyoshi Sci Rep Article Marseilleviridae is a family of giant viruses, showing a characteristic internal membrane with extrusions underneath the icosahedral vertices. However, such large objects, with a maximum diameter of 250 nm are technically difficult to examine at sub-nanometre resolution by cryo-electron microscopy. Here, we tested the utility of 1 MV high-voltage cryo-EM (cryo-HVEM) for single particle structural analysis (SPA) of giant viruses using tokyovirus, a species of Marseilleviridae, and revealed the capsid structure at 7.7 Å resolution. The capsid enclosing the viral DNA consisted primarily of four layers: (1) major capsid proteins (MCPs) and penton proteins, (2) minor capsid proteins (mCPs), (3) scaffold protein components (ScPCs), and (4) internal membrane. The mCPs showed a novel capsid lattice consisting of eight protein components. ScPCs connecting the icosahedral vertices supported the formation of the membrane extrusions, and possibly act like tape measure proteins reported in other giant viruses. The density on top of the MCP trimer was suggested to include glycoproteins. This is the first attempt at cryo-HVEM SPA. We found the primary limitations to be the lack of automated data acquisition and software support for collection and processing and thus achievable resolution. However, the results pave the way for using cryo-HVEM for structural analysis of larger biological specimens. Nature Publishing Group UK 2022-12-11 /pmc/articles/PMC9742146/ /pubmed/36504202 http://dx.doi.org/10.1038/s41598-022-24651-2 Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Chihara, Akane
Burton-Smith, Raymond N.
Kajimura, Naoko
Mitsuoka, Kaoru
Okamoto, Kenta
Song, Chihong
Murata, Kazuyoshi
A novel capsid protein network allows the characteristic internal membrane structure of Marseilleviridae giant viruses
title A novel capsid protein network allows the characteristic internal membrane structure of Marseilleviridae giant viruses
title_full A novel capsid protein network allows the characteristic internal membrane structure of Marseilleviridae giant viruses
title_fullStr A novel capsid protein network allows the characteristic internal membrane structure of Marseilleviridae giant viruses
title_full_unstemmed A novel capsid protein network allows the characteristic internal membrane structure of Marseilleviridae giant viruses
title_short A novel capsid protein network allows the characteristic internal membrane structure of Marseilleviridae giant viruses
title_sort novel capsid protein network allows the characteristic internal membrane structure of marseilleviridae giant viruses
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9742146/
https://www.ncbi.nlm.nih.gov/pubmed/36504202
http://dx.doi.org/10.1038/s41598-022-24651-2
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