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Evidence of involvement of the mannose receptor in the internalization of Streptococcus pneumoniae by Schwann cells

BACKGROUND: The ability of S. pneumoniae to generate infections depends on the restrictions imposed by the host’s immunity, in order to prevent the bacterium from spreading from the nasopharynx to other tissues, such as the brain. Some authors claim that strains of S. pneumoniae, which fail to survi...

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Autores principales: Macedo-Ramos, Hugo, Batista, Andre F, Carrier-Ruiz, Alvaro, Alves, Lucineia, Allodi, Silvana, Ribeiro-Resende, Victor T, Teixeira, Lucia M, Baetas-da-Cruz, Wagner
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4236529/
https://www.ncbi.nlm.nih.gov/pubmed/25085553
http://dx.doi.org/10.1186/s12866-014-0211-9
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author Macedo-Ramos, Hugo
Batista, Andre F
Carrier-Ruiz, Alvaro
Alves, Lucineia
Allodi, Silvana
Ribeiro-Resende, Victor T
Teixeira, Lucia M
Baetas-da-Cruz, Wagner
author_facet Macedo-Ramos, Hugo
Batista, Andre F
Carrier-Ruiz, Alvaro
Alves, Lucineia
Allodi, Silvana
Ribeiro-Resende, Victor T
Teixeira, Lucia M
Baetas-da-Cruz, Wagner
author_sort Macedo-Ramos, Hugo
collection PubMed
description BACKGROUND: The ability of S. pneumoniae to generate infections depends on the restrictions imposed by the host’s immunity, in order to prevent the bacterium from spreading from the nasopharynx to other tissues, such as the brain. Some authors claim that strains of S. pneumoniae, which fail to survive in the bloodstream, can enter the brain directly from the nasal cavity by axonal transport through the olfactory and/or trigeminal nerves. However, from the immunological point of view, glial cells are far more responsive to bacterial infections than are neurons. This hypothesis is consistent with several recent reports showing that bacteria can infect glial cells from the olfactory bulb and trigeminal ganglia. Since our group previously demonstrated that Schwann cells (SCs) express a functional and appropriately regulated mannose receptor (MR), we decided to test whether SCs are involved in the internalization of S. pneumoniae via MR. RESULTS: Immediately after the interaction step, as well as 3 h later, the percentage of association was approximately 56.5%, decreasing to 47.2% and 40.8% after 12 and 24 h, respectively. Competition assays by adding a 100-fold excess of mannan prior to the S. pneumoniae infection reduced the number of infected cells at 3 and 24 h. A cytochemistry assay with Man/BSA-FITC binding was performed in order to verify a possible overlap between mannosylated ligands and internalized bacteria. Incubation of the SCs with Man/BSA-FITC resulted in a large number of intracellular S. pneumoniae, with nearly complete loss of the capsule. Moreover, the anti-pneumococcal antiserum staining colocalized with the internalized man/BSA-FITC, suggesting that both markers are present within the same endocytic compartment of the SC. CONCLUSIONS: Our data offer novel evidence that SCs could be essential for pneumococcal cells to escape phagocytosis and killing by innate immune cells. On the other hand, the results also support the idea that SCs are immunocompetent cells of the PNS that can mediate an efficient immune response against pathogens via MR.
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spelling pubmed-42365292014-11-19 Evidence of involvement of the mannose receptor in the internalization of Streptococcus pneumoniae by Schwann cells Macedo-Ramos, Hugo Batista, Andre F Carrier-Ruiz, Alvaro Alves, Lucineia Allodi, Silvana Ribeiro-Resende, Victor T Teixeira, Lucia M Baetas-da-Cruz, Wagner BMC Microbiol Research Article BACKGROUND: The ability of S. pneumoniae to generate infections depends on the restrictions imposed by the host’s immunity, in order to prevent the bacterium from spreading from the nasopharynx to other tissues, such as the brain. Some authors claim that strains of S. pneumoniae, which fail to survive in the bloodstream, can enter the brain directly from the nasal cavity by axonal transport through the olfactory and/or trigeminal nerves. However, from the immunological point of view, glial cells are far more responsive to bacterial infections than are neurons. This hypothesis is consistent with several recent reports showing that bacteria can infect glial cells from the olfactory bulb and trigeminal ganglia. Since our group previously demonstrated that Schwann cells (SCs) express a functional and appropriately regulated mannose receptor (MR), we decided to test whether SCs are involved in the internalization of S. pneumoniae via MR. RESULTS: Immediately after the interaction step, as well as 3 h later, the percentage of association was approximately 56.5%, decreasing to 47.2% and 40.8% after 12 and 24 h, respectively. Competition assays by adding a 100-fold excess of mannan prior to the S. pneumoniae infection reduced the number of infected cells at 3 and 24 h. A cytochemistry assay with Man/BSA-FITC binding was performed in order to verify a possible overlap between mannosylated ligands and internalized bacteria. Incubation of the SCs with Man/BSA-FITC resulted in a large number of intracellular S. pneumoniae, with nearly complete loss of the capsule. Moreover, the anti-pneumococcal antiserum staining colocalized with the internalized man/BSA-FITC, suggesting that both markers are present within the same endocytic compartment of the SC. CONCLUSIONS: Our data offer novel evidence that SCs could be essential for pneumococcal cells to escape phagocytosis and killing by innate immune cells. On the other hand, the results also support the idea that SCs are immunocompetent cells of the PNS that can mediate an efficient immune response against pathogens via MR. BioMed Central 2014-08-02 /pmc/articles/PMC4236529/ /pubmed/25085553 http://dx.doi.org/10.1186/s12866-014-0211-9 Text en Copyright © 2014 Macedo-Ramos et al.; licensee BioMed Central Ltd http://creativecommons.org/licenses/by/4.0 This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Macedo-Ramos, Hugo
Batista, Andre F
Carrier-Ruiz, Alvaro
Alves, Lucineia
Allodi, Silvana
Ribeiro-Resende, Victor T
Teixeira, Lucia M
Baetas-da-Cruz, Wagner
Evidence of involvement of the mannose receptor in the internalization of Streptococcus pneumoniae by Schwann cells
title Evidence of involvement of the mannose receptor in the internalization of Streptococcus pneumoniae by Schwann cells
title_full Evidence of involvement of the mannose receptor in the internalization of Streptococcus pneumoniae by Schwann cells
title_fullStr Evidence of involvement of the mannose receptor in the internalization of Streptococcus pneumoniae by Schwann cells
title_full_unstemmed Evidence of involvement of the mannose receptor in the internalization of Streptococcus pneumoniae by Schwann cells
title_short Evidence of involvement of the mannose receptor in the internalization of Streptococcus pneumoniae by Schwann cells
title_sort evidence of involvement of the mannose receptor in the internalization of streptococcus pneumoniae by schwann cells
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4236529/
https://www.ncbi.nlm.nih.gov/pubmed/25085553
http://dx.doi.org/10.1186/s12866-014-0211-9
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