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Biofilm-forming strains of P. aeruginosa and S. aureus isolated from cystic fibrosis patients differently affect inflammatory phenotype of macrophages

OBJECTIVE: Lung cystic fibrosis (CF) is characterized by chronic infections and hyperinflammatory response of neutrophils and macrophages. P. aeruginosa (PA) and S. aureus (MSSA, MRSA) are major pathogens of advanced CF. The main goal of this study was to compare the inflammatory phenotype of murine...

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Autores principales: Ciszek-Lenda, Marta, Majka, Grzegorz, Suski, Maciej, Walczewska, Maria, Górska, Sabina, Golińska, Edyta, Fedor, Angelika, Gamian, Andrzej, Olszanecki, Rafał, Strus, Magdalena, Marcinkiewicz, Janusz
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Springer International Publishing 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10279583/
https://www.ncbi.nlm.nih.gov/pubmed/37253897
http://dx.doi.org/10.1007/s00011-023-01743-x
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author Ciszek-Lenda, Marta
Majka, Grzegorz
Suski, Maciej
Walczewska, Maria
Górska, Sabina
Golińska, Edyta
Fedor, Angelika
Gamian, Andrzej
Olszanecki, Rafał
Strus, Magdalena
Marcinkiewicz, Janusz
author_facet Ciszek-Lenda, Marta
Majka, Grzegorz
Suski, Maciej
Walczewska, Maria
Górska, Sabina
Golińska, Edyta
Fedor, Angelika
Gamian, Andrzej
Olszanecki, Rafał
Strus, Magdalena
Marcinkiewicz, Janusz
author_sort Ciszek-Lenda, Marta
collection PubMed
description OBJECTIVE: Lung cystic fibrosis (CF) is characterized by chronic infections and hyperinflammatory response of neutrophils and macrophages. P. aeruginosa (PA) and S. aureus (MSSA, MRSA) are major pathogens of advanced CF. The main goal of this study was to compare the inflammatory phenotype of murine C57BL/6 macrophages exposed to PA57 with that exposed to MSSA60, both strains isolated from the same patient with severe CF. In the present study, we used C57BL/6 mice sensitive to lung infection with P. aeruginosa. METHODS: We measured the release of cytokines and the expression of phenotypic markers of murine neutrophils and macrophages exposed to bacterial cells and biofilm components (i.e., EPS) of the selected bacteria. In addition, a quantitative proteomic approach was used for the characterization of proteome-wide changes in macrophages. RESULTS: Neutrophils stimulated with PA57 and MSSA60 strains produced hyperinflammatory pattern of cytokines. The pro-inflammatory impact of PA57 was significantly higher than that of MSSA60 (IL-6/IL-10 ratio: PA57 = 9.3 vs. MSSA60 = 1.7). Macrophages produced significantly lower amount of cytokines, but showed classical pattern of M1 markers (iNOS-High; arginase-1 and mannose receptor MRC1-Low). Importantly, as evidenced by proteomic analysis, PA57 and PA57-EPS were stronger inducers of M1 macrophage polarization than the MSSA60 counterparts. CONCLUSIONS: Our study demonstrated that strong biofilm P. aeruginosa strains, CF isolates, are dominant inducers of M1 macrophages, termed biofilm-associated macrophages (BAMs). We suggest that repolarization of detrimental BAMs might be a new therapeutic strategy to ameliorate the airway damage in CF. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1007/s00011-023-01743-x.
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spelling pubmed-102795832023-06-21 Biofilm-forming strains of P. aeruginosa and S. aureus isolated from cystic fibrosis patients differently affect inflammatory phenotype of macrophages Ciszek-Lenda, Marta Majka, Grzegorz Suski, Maciej Walczewska, Maria Górska, Sabina Golińska, Edyta Fedor, Angelika Gamian, Andrzej Olszanecki, Rafał Strus, Magdalena Marcinkiewicz, Janusz Inflamm Res Original Research Paper OBJECTIVE: Lung cystic fibrosis (CF) is characterized by chronic infections and hyperinflammatory response of neutrophils and macrophages. P. aeruginosa (PA) and S. aureus (MSSA, MRSA) are major pathogens of advanced CF. The main goal of this study was to compare the inflammatory phenotype of murine C57BL/6 macrophages exposed to PA57 with that exposed to MSSA60, both strains isolated from the same patient with severe CF. In the present study, we used C57BL/6 mice sensitive to lung infection with P. aeruginosa. METHODS: We measured the release of cytokines and the expression of phenotypic markers of murine neutrophils and macrophages exposed to bacterial cells and biofilm components (i.e., EPS) of the selected bacteria. In addition, a quantitative proteomic approach was used for the characterization of proteome-wide changes in macrophages. RESULTS: Neutrophils stimulated with PA57 and MSSA60 strains produced hyperinflammatory pattern of cytokines. The pro-inflammatory impact of PA57 was significantly higher than that of MSSA60 (IL-6/IL-10 ratio: PA57 = 9.3 vs. MSSA60 = 1.7). Macrophages produced significantly lower amount of cytokines, but showed classical pattern of M1 markers (iNOS-High; arginase-1 and mannose receptor MRC1-Low). Importantly, as evidenced by proteomic analysis, PA57 and PA57-EPS were stronger inducers of M1 macrophage polarization than the MSSA60 counterparts. CONCLUSIONS: Our study demonstrated that strong biofilm P. aeruginosa strains, CF isolates, are dominant inducers of M1 macrophages, termed biofilm-associated macrophages (BAMs). We suggest that repolarization of detrimental BAMs might be a new therapeutic strategy to ameliorate the airway damage in CF. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1007/s00011-023-01743-x. Springer International Publishing 2023-05-31 2023 /pmc/articles/PMC10279583/ /pubmed/37253897 http://dx.doi.org/10.1007/s00011-023-01743-x Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/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 licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence 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 licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Original Research Paper
Ciszek-Lenda, Marta
Majka, Grzegorz
Suski, Maciej
Walczewska, Maria
Górska, Sabina
Golińska, Edyta
Fedor, Angelika
Gamian, Andrzej
Olszanecki, Rafał
Strus, Magdalena
Marcinkiewicz, Janusz
Biofilm-forming strains of P. aeruginosa and S. aureus isolated from cystic fibrosis patients differently affect inflammatory phenotype of macrophages
title Biofilm-forming strains of P. aeruginosa and S. aureus isolated from cystic fibrosis patients differently affect inflammatory phenotype of macrophages
title_full Biofilm-forming strains of P. aeruginosa and S. aureus isolated from cystic fibrosis patients differently affect inflammatory phenotype of macrophages
title_fullStr Biofilm-forming strains of P. aeruginosa and S. aureus isolated from cystic fibrosis patients differently affect inflammatory phenotype of macrophages
title_full_unstemmed Biofilm-forming strains of P. aeruginosa and S. aureus isolated from cystic fibrosis patients differently affect inflammatory phenotype of macrophages
title_short Biofilm-forming strains of P. aeruginosa and S. aureus isolated from cystic fibrosis patients differently affect inflammatory phenotype of macrophages
title_sort biofilm-forming strains of p. aeruginosa and s. aureus isolated from cystic fibrosis patients differently affect inflammatory phenotype of macrophages
topic Original Research Paper
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10279583/
https://www.ncbi.nlm.nih.gov/pubmed/37253897
http://dx.doi.org/10.1007/s00011-023-01743-x
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