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EsiB, a Novel Pathogenic Escherichia coli Secretory Immunoglobulin A-Binding Protein Impairing Neutrophil Activation

In this study, we have characterized the functional properties of a novel Escherichia coli antigen named EsiB (E. coli secretory immunoglobulin A-binding protein), recently reported to protect mice from sepsis. Gene distribution analysis of a panel of 267 strains representative of different E. coli...

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Autores principales: Pastorello, Ilaria, Rossi Paccani, Silvia, Rosini, Roberto, Mattera, Rossella, Ferrer Navarro, Mario, Urosev, Dunja, Nesta, Barbara, Lo Surdo, Paola, Del Vecchio, Mariangela, Rippa, Valentina, Bertoldi, Isabella, Gomes Moriel, Danilo, Laarman, Alexander J., van Strijp, Jos A. G., Daura, Xavier, Pizza, Mariagrazia, Serino, Laura, Soriani, Marco
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society of Microbiology 2013
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3735183/
https://www.ncbi.nlm.nih.gov/pubmed/23882011
http://dx.doi.org/10.1128/mBio.00206-13
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author Pastorello, Ilaria
Rossi Paccani, Silvia
Rosini, Roberto
Mattera, Rossella
Ferrer Navarro, Mario
Urosev, Dunja
Nesta, Barbara
Lo Surdo, Paola
Del Vecchio, Mariangela
Rippa, Valentina
Bertoldi, Isabella
Gomes Moriel, Danilo
Laarman, Alexander J.
van Strijp, Jos A. G.
Daura, Xavier
Pizza, Mariagrazia
Serino, Laura
Soriani, Marco
author_facet Pastorello, Ilaria
Rossi Paccani, Silvia
Rosini, Roberto
Mattera, Rossella
Ferrer Navarro, Mario
Urosev, Dunja
Nesta, Barbara
Lo Surdo, Paola
Del Vecchio, Mariangela
Rippa, Valentina
Bertoldi, Isabella
Gomes Moriel, Danilo
Laarman, Alexander J.
van Strijp, Jos A. G.
Daura, Xavier
Pizza, Mariagrazia
Serino, Laura
Soriani, Marco
author_sort Pastorello, Ilaria
collection PubMed
description In this study, we have characterized the functional properties of a novel Escherichia coli antigen named EsiB (E. coli secretory immunoglobulin A-binding protein), recently reported to protect mice from sepsis. Gene distribution analysis of a panel of 267 strains representative of different E. coli pathotypes revealed that esiB is preferentially associated with extraintestinal strains, while the gene is rarely found in either intestinal or nonpathogenic strains. These findings were supported by the presence of anti-EsiB antibodies in the sera of patients affected by urinary tract infections (UTIs). By solving its crystal structure, we observed that EsiB adopts a superhelical fold composed of Sel1-like repeats (SLRs), a feature often associated with bacterial proteins possessing immunomodulatory functions. Indeed, we found that EsiB interacts with secretory immunoglobulin A (SIgA) through a specific motif identified by an immunocapturing approach. Functional assays showed that EsiB binding to SIgA is likely to interfere with productive FcαRI signaling, by inhibiting both SIgA-induced neutrophil chemotaxis and respiratory burst. Indeed, EsiB hampers SIgA-mediated signaling events by reducing the phosphorylation status of key signal-transducer cytosolic proteins, including mitogen-activated kinases. We propose that the interference with such immune events could contribute to the capacity of the bacterium to avoid clearance by neutrophils, as well as reducing the recruitment of immune cells to the infection site.
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spelling pubmed-37351832013-08-08 EsiB, a Novel Pathogenic Escherichia coli Secretory Immunoglobulin A-Binding Protein Impairing Neutrophil Activation Pastorello, Ilaria Rossi Paccani, Silvia Rosini, Roberto Mattera, Rossella Ferrer Navarro, Mario Urosev, Dunja Nesta, Barbara Lo Surdo, Paola Del Vecchio, Mariangela Rippa, Valentina Bertoldi, Isabella Gomes Moriel, Danilo Laarman, Alexander J. van Strijp, Jos A. G. Daura, Xavier Pizza, Mariagrazia Serino, Laura Soriani, Marco mBio Research Article In this study, we have characterized the functional properties of a novel Escherichia coli antigen named EsiB (E. coli secretory immunoglobulin A-binding protein), recently reported to protect mice from sepsis. Gene distribution analysis of a panel of 267 strains representative of different E. coli pathotypes revealed that esiB is preferentially associated with extraintestinal strains, while the gene is rarely found in either intestinal or nonpathogenic strains. These findings were supported by the presence of anti-EsiB antibodies in the sera of patients affected by urinary tract infections (UTIs). By solving its crystal structure, we observed that EsiB adopts a superhelical fold composed of Sel1-like repeats (SLRs), a feature often associated with bacterial proteins possessing immunomodulatory functions. Indeed, we found that EsiB interacts with secretory immunoglobulin A (SIgA) through a specific motif identified by an immunocapturing approach. Functional assays showed that EsiB binding to SIgA is likely to interfere with productive FcαRI signaling, by inhibiting both SIgA-induced neutrophil chemotaxis and respiratory burst. Indeed, EsiB hampers SIgA-mediated signaling events by reducing the phosphorylation status of key signal-transducer cytosolic proteins, including mitogen-activated kinases. We propose that the interference with such immune events could contribute to the capacity of the bacterium to avoid clearance by neutrophils, as well as reducing the recruitment of immune cells to the infection site. American Society of Microbiology 2013-07-23 /pmc/articles/PMC3735183/ /pubmed/23882011 http://dx.doi.org/10.1128/mBio.00206-13 Text en Copyright © 2013 Pastorello et al. http://creativecommons.org/licenses/by-nc-sa/3.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution-Noncommercial-ShareAlike 3.0 Unported license (http://creativecommons.org/licenses/by-nc-sa/3.0/) , which permits unrestricted noncommercial use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Pastorello, Ilaria
Rossi Paccani, Silvia
Rosini, Roberto
Mattera, Rossella
Ferrer Navarro, Mario
Urosev, Dunja
Nesta, Barbara
Lo Surdo, Paola
Del Vecchio, Mariangela
Rippa, Valentina
Bertoldi, Isabella
Gomes Moriel, Danilo
Laarman, Alexander J.
van Strijp, Jos A. G.
Daura, Xavier
Pizza, Mariagrazia
Serino, Laura
Soriani, Marco
EsiB, a Novel Pathogenic Escherichia coli Secretory Immunoglobulin A-Binding Protein Impairing Neutrophil Activation
title EsiB, a Novel Pathogenic Escherichia coli Secretory Immunoglobulin A-Binding Protein Impairing Neutrophil Activation
title_full EsiB, a Novel Pathogenic Escherichia coli Secretory Immunoglobulin A-Binding Protein Impairing Neutrophil Activation
title_fullStr EsiB, a Novel Pathogenic Escherichia coli Secretory Immunoglobulin A-Binding Protein Impairing Neutrophil Activation
title_full_unstemmed EsiB, a Novel Pathogenic Escherichia coli Secretory Immunoglobulin A-Binding Protein Impairing Neutrophil Activation
title_short EsiB, a Novel Pathogenic Escherichia coli Secretory Immunoglobulin A-Binding Protein Impairing Neutrophil Activation
title_sort esib, a novel pathogenic escherichia coli secretory immunoglobulin a-binding protein impairing neutrophil activation
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3735183/
https://www.ncbi.nlm.nih.gov/pubmed/23882011
http://dx.doi.org/10.1128/mBio.00206-13
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