Equine rhinitis A virus and its low pH empty particle: clues towards an aphthovirus entry mechanism?

Equine rhinitis A virus (ERAV) is closely related to foot-and-mouth disease virus (FMDV), belonging to the genus Aphthovirus of the Picornaviridae. How picornaviruses introduce their RNA genome into the cytoplasm of the host cell to initiate replication is unclear since they have no lipid envelope t...

Full description

Saved in:
Bibliographic Details
Main Authors: Tobias J Tuthill, Karl Harlos, Thomas S Walter, Nick J Knowles, Elisabetta Groppelli, David J Rowlands, David I Stuart, Elizabeth E Fry
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2009-10-01
Series:PLoS Pathogens
Online Access:https://journals.plos.org/plospathogens/article/file?id=10.1371/journal.ppat.1000620&type=printable
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1850226962926141440
author Tobias J Tuthill
Karl Harlos
Thomas S Walter
Nick J Knowles
Elisabetta Groppelli
David J Rowlands
David I Stuart
Elizabeth E Fry
author_facet Tobias J Tuthill
Karl Harlos
Thomas S Walter
Nick J Knowles
Elisabetta Groppelli
David J Rowlands
David I Stuart
Elizabeth E Fry
author_sort Tobias J Tuthill
collection DOAJ
description Equine rhinitis A virus (ERAV) is closely related to foot-and-mouth disease virus (FMDV), belonging to the genus Aphthovirus of the Picornaviridae. How picornaviruses introduce their RNA genome into the cytoplasm of the host cell to initiate replication is unclear since they have no lipid envelope to facilitate fusion with cellular membranes. It has been thought that the dissociation of the FMDV particle into pentameric subunits at acidic pH is the mechanism for genome release during cell entry, but this raises the problem of how transfer across the endosome membrane of the genome might be facilitated. In contrast, most other picornaviruses form 'altered' particle intermediates (not reported for aphthoviruses) thought to induce membrane pores through which the genome can be transferred. Here we show that ERAV, like FMDV, dissociates into pentamers at mildly acidic pH but demonstrate that dissociation is preceded by the transient formation of empty 80S particles which have released their genome and may represent novel biologically relevant intermediates in the aphthovirus cell entry process. The crystal structures of the native ERAV virus and a low pH form have been determined via highly efficient crystallization and data collection strategies, required due to low virus yields. ERAV is closely similar to FMDV for VP2, VP3 and part of VP4 but VP1 diverges, to give a particle with a pitted surface, as seen in cardioviruses. The low pH particle has internal structure consistent with it representing a pre-dissociation cell entry intermediate. These results suggest a unified mechanism of picornavirus cell entry.
format Article
id doaj-art-66f5b04743c946ecbf6520d017d294da
institution OA Journals
issn 1553-7366
1553-7374
language English
publishDate 2009-10-01
publisher Public Library of Science (PLoS)
record_format Article
series PLoS Pathogens
spelling doaj-art-66f5b04743c946ecbf6520d017d294da2025-08-20T02:04:57ZengPublic Library of Science (PLoS)PLoS Pathogens1553-73661553-73742009-10-01510e100062010.1371/journal.ppat.1000620Equine rhinitis A virus and its low pH empty particle: clues towards an aphthovirus entry mechanism?Tobias J TuthillKarl HarlosThomas S WalterNick J KnowlesElisabetta GroppelliDavid J RowlandsDavid I StuartElizabeth E FryEquine rhinitis A virus (ERAV) is closely related to foot-and-mouth disease virus (FMDV), belonging to the genus Aphthovirus of the Picornaviridae. How picornaviruses introduce their RNA genome into the cytoplasm of the host cell to initiate replication is unclear since they have no lipid envelope to facilitate fusion with cellular membranes. It has been thought that the dissociation of the FMDV particle into pentameric subunits at acidic pH is the mechanism for genome release during cell entry, but this raises the problem of how transfer across the endosome membrane of the genome might be facilitated. In contrast, most other picornaviruses form 'altered' particle intermediates (not reported for aphthoviruses) thought to induce membrane pores through which the genome can be transferred. Here we show that ERAV, like FMDV, dissociates into pentamers at mildly acidic pH but demonstrate that dissociation is preceded by the transient formation of empty 80S particles which have released their genome and may represent novel biologically relevant intermediates in the aphthovirus cell entry process. The crystal structures of the native ERAV virus and a low pH form have been determined via highly efficient crystallization and data collection strategies, required due to low virus yields. ERAV is closely similar to FMDV for VP2, VP3 and part of VP4 but VP1 diverges, to give a particle with a pitted surface, as seen in cardioviruses. The low pH particle has internal structure consistent with it representing a pre-dissociation cell entry intermediate. These results suggest a unified mechanism of picornavirus cell entry.https://journals.plos.org/plospathogens/article/file?id=10.1371/journal.ppat.1000620&type=printable
spellingShingle Tobias J Tuthill
Karl Harlos
Thomas S Walter
Nick J Knowles
Elisabetta Groppelli
David J Rowlands
David I Stuart
Elizabeth E Fry
Equine rhinitis A virus and its low pH empty particle: clues towards an aphthovirus entry mechanism?
PLoS Pathogens
title Equine rhinitis A virus and its low pH empty particle: clues towards an aphthovirus entry mechanism?
title_full Equine rhinitis A virus and its low pH empty particle: clues towards an aphthovirus entry mechanism?
title_fullStr Equine rhinitis A virus and its low pH empty particle: clues towards an aphthovirus entry mechanism?
title_full_unstemmed Equine rhinitis A virus and its low pH empty particle: clues towards an aphthovirus entry mechanism?
title_short Equine rhinitis A virus and its low pH empty particle: clues towards an aphthovirus entry mechanism?
title_sort equine rhinitis a virus and its low ph empty particle clues towards an aphthovirus entry mechanism
url https://journals.plos.org/plospathogens/article/file?id=10.1371/journal.ppat.1000620&type=printable
work_keys_str_mv AT tobiasjtuthill equinerhinitisavirusanditslowphemptyparticlecluestowardsanaphthovirusentrymechanism
AT karlharlos equinerhinitisavirusanditslowphemptyparticlecluestowardsanaphthovirusentrymechanism
AT thomasswalter equinerhinitisavirusanditslowphemptyparticlecluestowardsanaphthovirusentrymechanism
AT nickjknowles equinerhinitisavirusanditslowphemptyparticlecluestowardsanaphthovirusentrymechanism
AT elisabettagroppelli equinerhinitisavirusanditslowphemptyparticlecluestowardsanaphthovirusentrymechanism
AT davidjrowlands equinerhinitisavirusanditslowphemptyparticlecluestowardsanaphthovirusentrymechanism
AT davidistuart equinerhinitisavirusanditslowphemptyparticlecluestowardsanaphthovirusentrymechanism
AT elizabethefry equinerhinitisavirusanditslowphemptyparticlecluestowardsanaphthovirusentrymechanism