Dynamics of macrophage polarization support Salmonella persistence in a whole living organism
Numerous intracellular bacterial pathogens interfere with macrophage function, including macrophage polarization, to establish a niche and persist. However, the spatiotemporal dynamics of macrophage polarization during infection within host remain to be investigated. Here, we implement a model of pe...
| Main Authors: | , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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eLife Sciences Publications Ltd
2024-01-01
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| Series: | eLife |
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| Online Access: | https://elifesciences.org/articles/89828 |
| _version_ | 1827367638000467968 |
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| author | Jade Leiba Tamara Sipka Christina Begon-Pescia Matteo Bernardello Sofiane Tairi Lionello Bossi Anne-Alicia Gonzalez Xavier Mialhe Emilio J Gualda Pablo Loza-Alvarez Anne Blanc-Potard Georges Lutfalla Mai E Nguyen-Chi |
| author_facet | Jade Leiba Tamara Sipka Christina Begon-Pescia Matteo Bernardello Sofiane Tairi Lionello Bossi Anne-Alicia Gonzalez Xavier Mialhe Emilio J Gualda Pablo Loza-Alvarez Anne Blanc-Potard Georges Lutfalla Mai E Nguyen-Chi |
| author_sort | Jade Leiba |
| collection | DOAJ |
| description | Numerous intracellular bacterial pathogens interfere with macrophage function, including macrophage polarization, to establish a niche and persist. However, the spatiotemporal dynamics of macrophage polarization during infection within host remain to be investigated. Here, we implement a model of persistent Salmonella Typhimurium infection in zebrafish, which allows visualization of polarized macrophages and bacteria in real time at high resolution. While macrophages polarize toward M1-like phenotype to control early infection, during later stages, Salmonella persists inside non-inflammatory clustered macrophages. Transcriptomic profiling of macrophages showed a highly dynamic signature during infection characterized by a switch from pro-inflammatory to anti-inflammatory/pro-regenerative status and revealed a shift in adhesion program. In agreement with this specific adhesion signature, macrophage trajectory tracking identifies motionless macrophages as a permissive niche for persistent Salmonella. Our results demonstrate that zebrafish model provides a unique platform to explore, in a whole organism, the versatile nature of macrophage functional programs during bacterial acute and persistent infections. |
| first_indexed | 2024-03-08T09:12:05Z |
| format | Article |
| id | doaj.art-3af0b99d3e344f90b3211f34a283ae51 |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-03-08T09:12:05Z |
| publishDate | 2024-01-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj.art-3af0b99d3e344f90b3211f34a283ae512024-01-31T20:15:48ZengeLife Sciences Publications LtdeLife2050-084X2024-01-011310.7554/eLife.89828Dynamics of macrophage polarization support Salmonella persistence in a whole living organismJade Leiba0Tamara Sipka1Christina Begon-Pescia2Matteo Bernardello3Sofiane Tairi4Lionello Bossi5Anne-Alicia Gonzalez6Xavier Mialhe7Emilio J Gualda8Pablo Loza-Alvarez9https://orcid.org/0000-0002-3129-1213Anne Blanc-Potard10Georges Lutfalla11Mai E Nguyen-Chi12https://orcid.org/0000-0003-2672-2426LPHI, Université de Montpellier, CNRS, INSERM, Montpellier, FranceLPHI, Université de Montpellier, CNRS, INSERM, Montpellier, FranceLPHI, Université de Montpellier, CNRS, INSERM, Montpellier, FranceICFO - Institute of Photonic Sciences, The Barcelona Institute of Science and Technology, Castelldefels, Barcelona, SpainLPHI, Université de Montpellier, CNRS, INSERM, Montpellier, FranceInstitute for Integrative Biology of the Cell-I2BC, Université Paris-Saclay, CEA, CNRS, Gif-sur-Yvette, FranceMGX-Montpellier GenomiX, Université de Montpellier, CNRS, INSERM, Montpellier, FranceMGX-Montpellier GenomiX, Université de Montpellier, CNRS, INSERM, Montpellier, FranceICFO - Institute of Photonic Sciences, The Barcelona Institute of Science and Technology, Castelldefels, Barcelona, SpainICFO - Institute of Photonic Sciences, The Barcelona Institute of Science and Technology, Castelldefels, Barcelona, SpainLPHI, Université de Montpellier, CNRS, INSERM, Montpellier, FranceLPHI, Université de Montpellier, CNRS, INSERM, Montpellier, FranceLPHI, Université de Montpellier, CNRS, INSERM, Montpellier, FranceNumerous intracellular bacterial pathogens interfere with macrophage function, including macrophage polarization, to establish a niche and persist. However, the spatiotemporal dynamics of macrophage polarization during infection within host remain to be investigated. Here, we implement a model of persistent Salmonella Typhimurium infection in zebrafish, which allows visualization of polarized macrophages and bacteria in real time at high resolution. While macrophages polarize toward M1-like phenotype to control early infection, during later stages, Salmonella persists inside non-inflammatory clustered macrophages. Transcriptomic profiling of macrophages showed a highly dynamic signature during infection characterized by a switch from pro-inflammatory to anti-inflammatory/pro-regenerative status and revealed a shift in adhesion program. In agreement with this specific adhesion signature, macrophage trajectory tracking identifies motionless macrophages as a permissive niche for persistent Salmonella. Our results demonstrate that zebrafish model provides a unique platform to explore, in a whole organism, the versatile nature of macrophage functional programs during bacterial acute and persistent infections.https://elifesciences.org/articles/89828macrophagesSalmonellabacterial persistencemacrophage polarizationinnate immunity |
| spellingShingle | Jade Leiba Tamara Sipka Christina Begon-Pescia Matteo Bernardello Sofiane Tairi Lionello Bossi Anne-Alicia Gonzalez Xavier Mialhe Emilio J Gualda Pablo Loza-Alvarez Anne Blanc-Potard Georges Lutfalla Mai E Nguyen-Chi Dynamics of macrophage polarization support Salmonella persistence in a whole living organism eLife macrophages Salmonella bacterial persistence macrophage polarization innate immunity |
| title | Dynamics of macrophage polarization support Salmonella persistence in a whole living organism |
| title_full | Dynamics of macrophage polarization support Salmonella persistence in a whole living organism |
| title_fullStr | Dynamics of macrophage polarization support Salmonella persistence in a whole living organism |
| title_full_unstemmed | Dynamics of macrophage polarization support Salmonella persistence in a whole living organism |
| title_short | Dynamics of macrophage polarization support Salmonella persistence in a whole living organism |
| title_sort | dynamics of macrophage polarization support salmonella persistence in a whole living organism |
| topic | macrophages Salmonella bacterial persistence macrophage polarization innate immunity |
| url | https://elifesciences.org/articles/89828 |
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