Tracking the Antigenic Evolution of Foot-and-Mouth Disease Virus.

Quantifying and predicting the antigenic characteristics of a virus is something of a holy grail for infectious disease research because of its central importance to the emergence of new strains, the severity of outbreaks, and vaccine selection. However, these characteristics are defined by a comple...

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Main Authors: Richard Reeve, Daryl W Borley, Francois F Maree, Sasmita Upadhyaya, Azwidowi Lukhwareni, Jan J Esterhuysen, William T Harvey, Belinda Blignaut, Elizabeth E Fry, Satya Parida, David J Paton, Mana Mahapatra
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2016-01-01
Series:PLoS ONE
Online Access:https://journals.plos.org/plosone/article/file?id=10.1371/journal.pone.0159360&type=printable
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author Richard Reeve
Daryl W Borley
Francois F Maree
Sasmita Upadhyaya
Azwidowi Lukhwareni
Jan J Esterhuysen
William T Harvey
Belinda Blignaut
Elizabeth E Fry
Satya Parida
David J Paton
Mana Mahapatra
author_facet Richard Reeve
Daryl W Borley
Francois F Maree
Sasmita Upadhyaya
Azwidowi Lukhwareni
Jan J Esterhuysen
William T Harvey
Belinda Blignaut
Elizabeth E Fry
Satya Parida
David J Paton
Mana Mahapatra
author_sort Richard Reeve
collection DOAJ
description Quantifying and predicting the antigenic characteristics of a virus is something of a holy grail for infectious disease research because of its central importance to the emergence of new strains, the severity of outbreaks, and vaccine selection. However, these characteristics are defined by a complex interplay of viral and host factors so that phylogenetic measures of viral similarity are often poorly correlated to antigenic relationships. Here, we generate antigenic phylogenies that track the phenotypic evolution of two serotypes of foot-and-mouth disease virus by combining host serology and viral sequence data to identify sites that are critical to their antigenic evolution. For serotype SAT1, we validate our antigenic phylogeny against monoclonal antibody escape mutants, which match all of the predicted antigenic sites. For serotype O, we validate it against known sites where available, and otherwise directly evaluate the impact on antigenic phenotype of substitutions in predicted sites using reverse genetics and serology. We also highlight a critical and poorly understood problem for vaccine selection by revealing qualitative differences between assays that are often used interchangeably to determine antigenic match between field viruses and vaccine strains. Our approach provides a tool to identify naturally occurring antigenic substitutions, allowing us to track the genetic diversification and associated antigenic evolution of the virus. Despite the hugely important role vaccines have played in enhancing human and animal health, vaccinology remains a conspicuously empirical science. This study advances the field by providing guidance for tuning vaccine strains via site-directed mutagenesis through this high-resolution tracking of antigenic evolution of the virus between rare major shifts in phenotype.
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spelling doaj-art-b9ad828d94c84c1a9ca4a2b4d1f096f12025-08-20T02:31:58ZengPublic Library of Science (PLoS)PLoS ONE1932-62032016-01-01117e015936010.1371/journal.pone.0159360Tracking the Antigenic Evolution of Foot-and-Mouth Disease Virus.Richard ReeveDaryl W BorleyFrancois F MareeSasmita UpadhyayaAzwidowi LukhwareniJan J EsterhuysenWilliam T HarveyBelinda BlignautElizabeth E FrySatya ParidaDavid J PatonMana MahapatraQuantifying and predicting the antigenic characteristics of a virus is something of a holy grail for infectious disease research because of its central importance to the emergence of new strains, the severity of outbreaks, and vaccine selection. However, these characteristics are defined by a complex interplay of viral and host factors so that phylogenetic measures of viral similarity are often poorly correlated to antigenic relationships. Here, we generate antigenic phylogenies that track the phenotypic evolution of two serotypes of foot-and-mouth disease virus by combining host serology and viral sequence data to identify sites that are critical to their antigenic evolution. For serotype SAT1, we validate our antigenic phylogeny against monoclonal antibody escape mutants, which match all of the predicted antigenic sites. For serotype O, we validate it against known sites where available, and otherwise directly evaluate the impact on antigenic phenotype of substitutions in predicted sites using reverse genetics and serology. We also highlight a critical and poorly understood problem for vaccine selection by revealing qualitative differences between assays that are often used interchangeably to determine antigenic match between field viruses and vaccine strains. Our approach provides a tool to identify naturally occurring antigenic substitutions, allowing us to track the genetic diversification and associated antigenic evolution of the virus. Despite the hugely important role vaccines have played in enhancing human and animal health, vaccinology remains a conspicuously empirical science. This study advances the field by providing guidance for tuning vaccine strains via site-directed mutagenesis through this high-resolution tracking of antigenic evolution of the virus between rare major shifts in phenotype.https://journals.plos.org/plosone/article/file?id=10.1371/journal.pone.0159360&type=printable
spellingShingle Richard Reeve
Daryl W Borley
Francois F Maree
Sasmita Upadhyaya
Azwidowi Lukhwareni
Jan J Esterhuysen
William T Harvey
Belinda Blignaut
Elizabeth E Fry
Satya Parida
David J Paton
Mana Mahapatra
Tracking the Antigenic Evolution of Foot-and-Mouth Disease Virus.
PLoS ONE
title Tracking the Antigenic Evolution of Foot-and-Mouth Disease Virus.
title_full Tracking the Antigenic Evolution of Foot-and-Mouth Disease Virus.
title_fullStr Tracking the Antigenic Evolution of Foot-and-Mouth Disease Virus.
title_full_unstemmed Tracking the Antigenic Evolution of Foot-and-Mouth Disease Virus.
title_short Tracking the Antigenic Evolution of Foot-and-Mouth Disease Virus.
title_sort tracking the antigenic evolution of foot and mouth disease virus
url https://journals.plos.org/plosone/article/file?id=10.1371/journal.pone.0159360&type=printable
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