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Exfoliative toxin E, a new Staphylococcus aureus virulence factor with host-specific activity

Exfoliative toxins (ETs) are secreted virulence factors produced by staphylococci. These serine proteases specifically cleave desmoglein 1 (Dsg1) in mammals and are key elements in staphylococcal skin infections. We recently identified a new et gene in S. aureus O46, a strain isolated from ovine mas...

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Autores principales: Imanishi, Ichiro, Nicolas, Aurélie, Caetano, Ana-Carolina Barbosa, Castro, Thiago Luiz de Paula, Tartaglia, Natayme Rocha, Mariutti, Ricardo, Guédon, Eric, Even, Sergine, Berkova, Nadia, Arni, Raghuvir K., Seyffert, Nubia, Azevedo, Vasco, Nishifuji, Koji, Le Loir, Yves
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6841975/
https://www.ncbi.nlm.nih.gov/pubmed/31704997
http://dx.doi.org/10.1038/s41598-019-52777-3
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author Imanishi, Ichiro
Nicolas, Aurélie
Caetano, Ana-Carolina Barbosa
Castro, Thiago Luiz de Paula
Tartaglia, Natayme Rocha
Mariutti, Ricardo
Guédon, Eric
Even, Sergine
Berkova, Nadia
Arni, Raghuvir K.
Seyffert, Nubia
Azevedo, Vasco
Nishifuji, Koji
Le Loir, Yves
author_facet Imanishi, Ichiro
Nicolas, Aurélie
Caetano, Ana-Carolina Barbosa
Castro, Thiago Luiz de Paula
Tartaglia, Natayme Rocha
Mariutti, Ricardo
Guédon, Eric
Even, Sergine
Berkova, Nadia
Arni, Raghuvir K.
Seyffert, Nubia
Azevedo, Vasco
Nishifuji, Koji
Le Loir, Yves
author_sort Imanishi, Ichiro
collection PubMed
description Exfoliative toxins (ETs) are secreted virulence factors produced by staphylococci. These serine proteases specifically cleave desmoglein 1 (Dsg1) in mammals and are key elements in staphylococcal skin infections. We recently identified a new et gene in S. aureus O46, a strain isolated from ovine mastitis. In the present study, we characterized the new et gene at a genetic level and the enzymatic activity of the deduced protein. The S. aureus O46 genome was re-assembled, annotated and compared with other publicly available S. aureus genomes. The deduced amino acid sequence of the new et gene shared 40%, 53% and 59% sequence identity to those of ETA, ETB and ETD, respectively. The new et gene shared the same genetic vicinity and was similar in other S. aureus strains bearing this gene. The recombinant enzyme of the new et gene caused skin exfoliation in vivo in neonatal mice. The new et-gene was thus named ete, encoding a new type (type E) of exfoliative toxin. We showed that ETE degraded the extracellular segments of Dsg1 in murine, ovine and caprine epidermis, as well as in ovine teat canal epithelia, but not that in bovine epidermis. We further showed that it directly hydrolyzed human and swine Dsg1 as well as murine Dsg1α and Dsg1β, but not canine Dsg1 or murine Dsg1γ. Molecular modeling revealed a correlation between the preferred orientation of ETE docking on its Dsg1 cleavage site and species-specific cleavage activity, suggesting that the docking step preceding cleavage accounts for the ETE species-specificity. This new virulence factor may contribute to the bacterial colonization on the stratified epithelia in certain ruminants with mastitis.
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spelling pubmed-68419752019-11-14 Exfoliative toxin E, a new Staphylococcus aureus virulence factor with host-specific activity Imanishi, Ichiro Nicolas, Aurélie Caetano, Ana-Carolina Barbosa Castro, Thiago Luiz de Paula Tartaglia, Natayme Rocha Mariutti, Ricardo Guédon, Eric Even, Sergine Berkova, Nadia Arni, Raghuvir K. Seyffert, Nubia Azevedo, Vasco Nishifuji, Koji Le Loir, Yves Sci Rep Article Exfoliative toxins (ETs) are secreted virulence factors produced by staphylococci. These serine proteases specifically cleave desmoglein 1 (Dsg1) in mammals and are key elements in staphylococcal skin infections. We recently identified a new et gene in S. aureus O46, a strain isolated from ovine mastitis. In the present study, we characterized the new et gene at a genetic level and the enzymatic activity of the deduced protein. The S. aureus O46 genome was re-assembled, annotated and compared with other publicly available S. aureus genomes. The deduced amino acid sequence of the new et gene shared 40%, 53% and 59% sequence identity to those of ETA, ETB and ETD, respectively. The new et gene shared the same genetic vicinity and was similar in other S. aureus strains bearing this gene. The recombinant enzyme of the new et gene caused skin exfoliation in vivo in neonatal mice. The new et-gene was thus named ete, encoding a new type (type E) of exfoliative toxin. We showed that ETE degraded the extracellular segments of Dsg1 in murine, ovine and caprine epidermis, as well as in ovine teat canal epithelia, but not that in bovine epidermis. We further showed that it directly hydrolyzed human and swine Dsg1 as well as murine Dsg1α and Dsg1β, but not canine Dsg1 or murine Dsg1γ. Molecular modeling revealed a correlation between the preferred orientation of ETE docking on its Dsg1 cleavage site and species-specific cleavage activity, suggesting that the docking step preceding cleavage accounts for the ETE species-specificity. This new virulence factor may contribute to the bacterial colonization on the stratified epithelia in certain ruminants with mastitis. Nature Publishing Group UK 2019-11-08 /pmc/articles/PMC6841975/ /pubmed/31704997 http://dx.doi.org/10.1038/s41598-019-52777-3 Text en © The Author(s) 2019 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 license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license 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 license, visit http://creativecommons.org/licenses/by/4.0/.
spellingShingle Article
Imanishi, Ichiro
Nicolas, Aurélie
Caetano, Ana-Carolina Barbosa
Castro, Thiago Luiz de Paula
Tartaglia, Natayme Rocha
Mariutti, Ricardo
Guédon, Eric
Even, Sergine
Berkova, Nadia
Arni, Raghuvir K.
Seyffert, Nubia
Azevedo, Vasco
Nishifuji, Koji
Le Loir, Yves
Exfoliative toxin E, a new Staphylococcus aureus virulence factor with host-specific activity
title Exfoliative toxin E, a new Staphylococcus aureus virulence factor with host-specific activity
title_full Exfoliative toxin E, a new Staphylococcus aureus virulence factor with host-specific activity
title_fullStr Exfoliative toxin E, a new Staphylococcus aureus virulence factor with host-specific activity
title_full_unstemmed Exfoliative toxin E, a new Staphylococcus aureus virulence factor with host-specific activity
title_short Exfoliative toxin E, a new Staphylococcus aureus virulence factor with host-specific activity
title_sort exfoliative toxin e, a new staphylococcus aureus virulence factor with host-specific activity
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6841975/
https://www.ncbi.nlm.nih.gov/pubmed/31704997
http://dx.doi.org/10.1038/s41598-019-52777-3
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