Protein A-mediated multicellular behavior in Staphylococcus aureus

The capacity of Staphylococcus aureus to form biofilms on host tissues and implanted medical devices is one of the major virulence traits underlying persistent and chronic infections. The matrix in which S. aureus cells are encased in a biofilm often consists of the polysaccharide intercellular adhe...

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Autores: Merino Barberá, Nekane, Toledo Arana, Alejandro, Vergara Irigaray, Marta, Valle Turrillas, Jaione, Solano Goñi, Cristina, Calvo, Enrique, Lopez, Juan Antonio, Foster, Timothy J., Penadés, José R., Lasa Uzcudun, Íñigo
Tipo de documento: artigo
Estado:Versão publicada
Data de publicação:2008
País:España
Recursos:Universidad Pública de Navarra
Repositório:Academica-e. Repositorio Institucional de la Universidad Pública de Navarra
OAI Identifier:oai:academica-e.unavarra.es:2454/32086
Acesso em linha:https://hdl.handle.net/2454/32086
Access Level:Acceso aberto
Palavra-chave:Staphylococcus aureus
Staphylococcal protein
Multicellular behavior
Biofilms
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spelling Protein A-mediated multicellular behavior in Staphylococcus aureusMerino Barberá, NekaneToledo Arana, AlejandroVergara Irigaray, MartaValle Turrillas, JaioneSolano Goñi, CristinaCalvo, EnriqueLopez, Juan AntonioFoster, Timothy J.Penadés, José R.Lasa Uzcudun, ÍñigoStaphylococcus aureusStaphylococcal proteinMulticellular behaviorBiofilmsThe capacity of Staphylococcus aureus to form biofilms on host tissues and implanted medical devices is one of the major virulence traits underlying persistent and chronic infections. The matrix in which S. aureus cells are encased in a biofilm often consists of the polysaccharide intercellular adhesin (PIA) or poly-N-acetyl glucosamine (PNAG). However, surface proteins capable of promoting biofilm development in the absence of PIA/PNAG exopolysaccharide have been described. Here, we used two-dimensional nano-liquid chromatography and mass spectrometry to investigate the composition of a proteinaceous biofilm matrix and identified protein A (spa) as an essential component of the biofilm; protein A induced bacterial aggregation in liquid medium and biofilm formation under standing and flow conditions. Exogenous addition of synthetic protein A or supernatants containing secreted protein A to growth media induced biofilm development, indicating that protein A can promote biofilm development without being covalently anchored to the cell wall. Protein A-mediated biofilm formation was completely inhibited in a dose-dependent manner by addition of serum, purified immunoglobulin G, or anti-protein A-specific antibodies. A murine model of subcutaneous catheter infection unveiled a significant role for protein A in the development of biofilm-associated infections, as the amount of protein A-deficient bacteria recovered from the catheter was significantly lower than that of wild-type bacteria when both strains were used to coinfect the implanted medical device. Our results suggest a novel role for protein A complementary to its known capacity to interact with multiple immunologically important eukaryotic receptors.This work was supported by the BIO2005-08399 and ERA-Net pathogenomics GEN2006-27792-C2-1-E/PAT grants from the Spanish Ministerio de Educación y Ciencia and grant LSHM-CT-2006-019064 from the European Union.American Society for MicrobiologyIdAB. Instituto de Agrobiotecnología / Agrobioteknologiako Institutua2008info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionapplication/pdfhttps://hdl.handle.net/2454/32086reponame:Academica-e. Repositorio Institucional de la Universidad Pública de Navarrainstname:Universidad Pública de NavarraInglés© 2009, American Society for Microbiology. All Rights Reserved.info:eu-repo/semantics/openAccessoai:academica-e.unavarra.es:2454/320862026-06-17T12:41:47Z
dc.title.none.fl_str_mv Protein A-mediated multicellular behavior in Staphylococcus aureus
title Protein A-mediated multicellular behavior in Staphylococcus aureus
spellingShingle Protein A-mediated multicellular behavior in Staphylococcus aureus
Merino Barberá, Nekane
Staphylococcus aureus
Staphylococcal protein
Multicellular behavior
Biofilms
title_short Protein A-mediated multicellular behavior in Staphylococcus aureus
title_full Protein A-mediated multicellular behavior in Staphylococcus aureus
title_fullStr Protein A-mediated multicellular behavior in Staphylococcus aureus
title_full_unstemmed Protein A-mediated multicellular behavior in Staphylococcus aureus
title_sort Protein A-mediated multicellular behavior in Staphylococcus aureus
dc.creator.none.fl_str_mv Merino Barberá, Nekane
Toledo Arana, Alejandro
Vergara Irigaray, Marta
Valle Turrillas, Jaione
Solano Goñi, Cristina
Calvo, Enrique
Lopez, Juan Antonio
Foster, Timothy J.
Penadés, José R.
Lasa Uzcudun, Íñigo
author Merino Barberá, Nekane
author_facet Merino Barberá, Nekane
Toledo Arana, Alejandro
Vergara Irigaray, Marta
Valle Turrillas, Jaione
Solano Goñi, Cristina
Calvo, Enrique
Lopez, Juan Antonio
Foster, Timothy J.
Penadés, José R.
Lasa Uzcudun, Íñigo
author_role author
author2 Toledo Arana, Alejandro
Vergara Irigaray, Marta
Valle Turrillas, Jaione
Solano Goñi, Cristina
Calvo, Enrique
Lopez, Juan Antonio
Foster, Timothy J.
Penadés, José R.
Lasa Uzcudun, Íñigo
author2_role author
author
author
author
author
author
author
author
author
dc.contributor.none.fl_str_mv IdAB. Instituto de Agrobiotecnología / Agrobioteknologiako Institutua
dc.subject.none.fl_str_mv Staphylococcus aureus
Staphylococcal protein
Multicellular behavior
Biofilms
topic Staphylococcus aureus
Staphylococcal protein
Multicellular behavior
Biofilms
description The capacity of Staphylococcus aureus to form biofilms on host tissues and implanted medical devices is one of the major virulence traits underlying persistent and chronic infections. The matrix in which S. aureus cells are encased in a biofilm often consists of the polysaccharide intercellular adhesin (PIA) or poly-N-acetyl glucosamine (PNAG). However, surface proteins capable of promoting biofilm development in the absence of PIA/PNAG exopolysaccharide have been described. Here, we used two-dimensional nano-liquid chromatography and mass spectrometry to investigate the composition of a proteinaceous biofilm matrix and identified protein A (spa) as an essential component of the biofilm; protein A induced bacterial aggregation in liquid medium and biofilm formation under standing and flow conditions. Exogenous addition of synthetic protein A or supernatants containing secreted protein A to growth media induced biofilm development, indicating that protein A can promote biofilm development without being covalently anchored to the cell wall. Protein A-mediated biofilm formation was completely inhibited in a dose-dependent manner by addition of serum, purified immunoglobulin G, or anti-protein A-specific antibodies. A murine model of subcutaneous catheter infection unveiled a significant role for protein A in the development of biofilm-associated infections, as the amount of protein A-deficient bacteria recovered from the catheter was significantly lower than that of wild-type bacteria when both strains were used to coinfect the implanted medical device. Our results suggest a novel role for protein A complementary to its known capacity to interact with multiple immunologically important eukaryotic receptors.
publishDate 2008
dc.date.none.fl_str_mv 2008
dc.type.none.fl_str_mv info:eu-repo/semantics/article
info:eu-repo/semantics/publishedVersion
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv https://hdl.handle.net/2454/32086
url https://hdl.handle.net/2454/32086
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.rights.none.fl_str_mv © 2009, American Society for Microbiology. All Rights Reserved.
info:eu-repo/semantics/openAccess
rights_invalid_str_mv © 2009, American Society for Microbiology. All Rights Reserved.
eu_rights_str_mv openAccess
dc.format.none.fl_str_mv application/pdf
dc.publisher.none.fl_str_mv American Society for Microbiology
publisher.none.fl_str_mv American Society for Microbiology
dc.source.none.fl_str_mv reponame:Academica-e. Repositorio Institucional de la Universidad Pública de Navarra
instname:Universidad Pública de Navarra
instname_str Universidad Pública de Navarra
reponame_str Academica-e. Repositorio Institucional de la Universidad Pública de Navarra
collection Academica-e. Repositorio Institucional de la Universidad Pública de Navarra
repository.name.fl_str_mv
repository.mail.fl_str_mv
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