Cutibacterium acnes strains associated with bone prosthesis infections cannot evade the host immune system
IntroductionCutibacterium acnes is a commensal skin bacterium that is involved in bone prosthesis infections (BPIs) and presents low-grade clinical symptoms. C. acnes has been thought to escape the immune system at bone sites.Material and methodsOur study was carried out on a laboratory strain and t...
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Frontiers Media S.A.
2024-11-01
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| Series: | Frontiers in Immunology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fimmu.2024.1468709/full |
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| author | Léa Thoraval Min Tang-Fichaux Christine Guillaume Jennifer Varin-Simon Claire Dumortier Johan Sergheraert Fabien Lamret Mélanie Bonhomme Frédéric Laurent Jérôme Josse Sophie C. Gangloff Céline Mongaret Fany Reffuveille Frédéric Velard |
| author_facet | Léa Thoraval Min Tang-Fichaux Christine Guillaume Jennifer Varin-Simon Claire Dumortier Johan Sergheraert Fabien Lamret Mélanie Bonhomme Frédéric Laurent Jérôme Josse Sophie C. Gangloff Céline Mongaret Fany Reffuveille Frédéric Velard |
| author_sort | Léa Thoraval |
| collection | DOAJ |
| description | IntroductionCutibacterium acnes is a commensal skin bacterium that is involved in bone prosthesis infections (BPIs) and presents low-grade clinical symptoms. C. acnes has been thought to escape the immune system at bone sites.Material and methodsOur study was carried out on a laboratory strain and two BPI-related clinical strains, one of which surprisingly induced clinical symptoms of inflammation in the patient. We investigated the ability of these C. acnes strains to trigger in vitro human primary neutrophils (PMN) response through inflammatory mediators measurements (antibody arrays, ELISA, RT-qPCR, zymography) and activation status assessment (flow cytometry), and to induce in vivo PMN recruitment from the bloodstream in mice air-pouch model. PMN-mediated inflammation was also studied in an original in vitro model mimetic of an infected bone site that combine titanium alloy, human primary osteoblasts, human primary neutrophils and C. acnes strains.ResultsWe demonstrated for the first time that both C. acnes planktonic and biofilm cultures, triggered an effective immune response by neutrophils in vitro and their recruitment in vivo. This host response was enhanced when using a strain from a patient with inflammatory signs. In an original infected prosthesis mimetic model, osteoblasts and neutrophils were able to detect C. acnes, but their response to the clinical C. acnes inflammatory strain decreased.ConclusionThis work provides the first evidence showing that the immune cell response to pathogenic C. acnes may be tuned by nonimmune cells at the infected site, such as osteoblasts, which may promote bacterial persistence. |
| format | Article |
| id | doaj-art-408e6ef96f3e4def80f36e118262ac0d |
| institution | OA Journals |
| issn | 1664-3224 |
| language | English |
| publishDate | 2024-11-01 |
| publisher | Frontiers Media S.A. |
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| series | Frontiers in Immunology |
| spelling | doaj-art-408e6ef96f3e4def80f36e118262ac0d2025-08-20T02:05:21ZengFrontiers Media S.A.Frontiers in Immunology1664-32242024-11-011510.3389/fimmu.2024.14687091468709Cutibacterium acnes strains associated with bone prosthesis infections cannot evade the host immune systemLéa Thoraval0Min Tang-Fichaux1Christine Guillaume2Jennifer Varin-Simon3Claire Dumortier4Johan Sergheraert5Fabien Lamret6Mélanie Bonhomme7Frédéric Laurent8Jérôme Josse9Sophie C. Gangloff10Céline Mongaret11Fany Reffuveille12Frédéric Velard13Université de Reims Champagne-Ardenne, BIOS, Reims, FranceUniversité de Reims Champagne-Ardenne, BIOS, Reims, FranceUniversité de Reims Champagne-Ardenne, BIOS, Reims, FranceUniversité de Reims Champagne-Ardenne, BIOS, Reims, FranceUniversité de Reims Champagne-Ardenne, BIOS, Reims, FranceUniversité de Reims Champagne-Ardenne, CHU Reims, BIOS, Pôle de Médecine Bucco-Dentaire, UFR Odontologie, Reims, FranceUniversité de Reims Champagne-Ardenne, BIOS, Reims, FranceCentre International de Recherche en Infectiologie (CIRI), Université de Lyon, Inserm, U1111, Université Claude Bernard Lyon 1, CNRS, UMR5308, ENS de Lyon, Lyon, FranceCentre International de Recherche en Infectiologie (CIRI), Université de Lyon, Inserm, U1111, Université Claude Bernard Lyon 1, CNRS, UMR5308, ENS de Lyon, Lyon, FranceCentre International de Recherche en Infectiologie (CIRI), Université de Lyon, Inserm, U1111, Université Claude Bernard Lyon 1, CNRS, UMR5308, ENS de Lyon, Lyon, FranceUniversité de Reims Champagne-Ardenne, BIOS, UFR Pharmacie, Reims, FranceUniversité de Reims Champagne-Ardenne, CHU Reims, BIOS, Service Pharmacie, Reims, FranceUniversité de Reims Champagne-Ardenne, BIOS, UFR Pharmacie, Reims, FranceUniversité de Reims Champagne-Ardenne, BIOS, Reims, FranceIntroductionCutibacterium acnes is a commensal skin bacterium that is involved in bone prosthesis infections (BPIs) and presents low-grade clinical symptoms. C. acnes has been thought to escape the immune system at bone sites.Material and methodsOur study was carried out on a laboratory strain and two BPI-related clinical strains, one of which surprisingly induced clinical symptoms of inflammation in the patient. We investigated the ability of these C. acnes strains to trigger in vitro human primary neutrophils (PMN) response through inflammatory mediators measurements (antibody arrays, ELISA, RT-qPCR, zymography) and activation status assessment (flow cytometry), and to induce in vivo PMN recruitment from the bloodstream in mice air-pouch model. PMN-mediated inflammation was also studied in an original in vitro model mimetic of an infected bone site that combine titanium alloy, human primary osteoblasts, human primary neutrophils and C. acnes strains.ResultsWe demonstrated for the first time that both C. acnes planktonic and biofilm cultures, triggered an effective immune response by neutrophils in vitro and their recruitment in vivo. This host response was enhanced when using a strain from a patient with inflammatory signs. In an original infected prosthesis mimetic model, osteoblasts and neutrophils were able to detect C. acnes, but their response to the clinical C. acnes inflammatory strain decreased.ConclusionThis work provides the first evidence showing that the immune cell response to pathogenic C. acnes may be tuned by nonimmune cells at the infected site, such as osteoblasts, which may promote bacterial persistence.https://www.frontiersin.org/articles/10.3389/fimmu.2024.1468709/fullinflammationCutibacterium acnesbiofilmbone and joint infectionhuman primary neutrophils |
| spellingShingle | Léa Thoraval Min Tang-Fichaux Christine Guillaume Jennifer Varin-Simon Claire Dumortier Johan Sergheraert Fabien Lamret Mélanie Bonhomme Frédéric Laurent Jérôme Josse Sophie C. Gangloff Céline Mongaret Fany Reffuveille Frédéric Velard Cutibacterium acnes strains associated with bone prosthesis infections cannot evade the host immune system Frontiers in Immunology inflammation Cutibacterium acnes biofilm bone and joint infection human primary neutrophils |
| title | Cutibacterium acnes strains associated with bone prosthesis infections cannot evade the host immune system |
| title_full | Cutibacterium acnes strains associated with bone prosthesis infections cannot evade the host immune system |
| title_fullStr | Cutibacterium acnes strains associated with bone prosthesis infections cannot evade the host immune system |
| title_full_unstemmed | Cutibacterium acnes strains associated with bone prosthesis infections cannot evade the host immune system |
| title_short | Cutibacterium acnes strains associated with bone prosthesis infections cannot evade the host immune system |
| title_sort | cutibacterium acnes strains associated with bone prosthesis infections cannot evade the host immune system |
| topic | inflammation Cutibacterium acnes biofilm bone and joint infection human primary neutrophils |
| url | https://www.frontiersin.org/articles/10.3389/fimmu.2024.1468709/full |
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