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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...
Autores principales: | , , , , , , , , , , , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
American Society of Microbiology
2013
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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. |
format | Online Article Text |
id | pubmed-3735183 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2013 |
publisher | American Society of Microbiology |
record_format | MEDLINE/PubMed |
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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