Porphyromonas gingivalis infection of oral keratinocytes drives the release of pro-inflammatory extracellular vesicles
Abstract Periodontitis is an inflammatory disease caused by bacterial infection. Recent studies have identified extracellular vesicles (EVs) as potential mediators of inflammation. This study aimed to evaluate the pro-inflammatory properties and miRNA content of EVs secreted in response to Porphyrom...
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Nature Portfolio
2025-07-01
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| Online Access: | https://doi.org/10.1038/s41598-025-10078-y |
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| author | Pierre-Yves Gegout Benjamin Mary Céline Stutz Vincent Hyenne Ofir Ginesin Hadar Zigdon-Giladi Olivier Huck |
| author_facet | Pierre-Yves Gegout Benjamin Mary Céline Stutz Vincent Hyenne Ofir Ginesin Hadar Zigdon-Giladi Olivier Huck |
| author_sort | Pierre-Yves Gegout |
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| description | Abstract Periodontitis is an inflammatory disease caused by bacterial infection. Recent studies have identified extracellular vesicles (EVs) as potential mediators of inflammation. This study aimed to evaluate the pro-inflammatory properties and miRNA content of EVs secreted in response to Porphyromonas gingivalis infection. Oral epithelial cells (ECs) were infected with P. gingivalis (MOI 100) for 24 h. EVs from infected (P.g.-ECs-EVs) and uninfected cells (ECs-EVs) were isolated, characterized, and tested on naive ECs. Cellular activity, inflammatory markers (TNF-α, IL-1β), and miRNA content of the secreted EVs were evaluated. Bioinformatic analysis was subsequently performed to identify potential targets of differentially expressed miRNAs. P. gingivalis infection increased EV production by 102-fold. P.g.-ECs-EVs exhibited distinct properties compared to ECs-EVs, including higher metabolic activity and elevated TNF-α and IL-1β expression and secretion levels in exposed ECs. Several inflammation-related miRNAs were highly upregulated in P.g.-ECs-EVs (11- to 142-fold; p < 0.001). P. gingivalis promotes the secretion of pro-inflammatory EVs by ECs, suggesting their role as key mediators in P. gingivalis-induced inflammation and periodontal tissue destruction. |
| format | Article |
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| institution | Kabale University |
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| language | English |
| publishDate | 2025-07-01 |
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| spelling | doaj-art-28b155f456e447c09a3dbe3bce4d9b8c2025-08-20T03:45:56ZengNature PortfolioScientific Reports2045-23222025-07-0115111110.1038/s41598-025-10078-yPorphyromonas gingivalis infection of oral keratinocytes drives the release of pro-inflammatory extracellular vesiclesPierre-Yves Gegout0Benjamin Mary1Céline Stutz2Vincent Hyenne3Ofir Ginesin4Hadar Zigdon-Giladi5Olivier Huck6INSERM, UMR 1260Tumor Biomechanics, INSERM UMR_S1109, Université de Strasbourg, Fédération de Médecine Translationnelle de Strasbourg (FMTS)INSERM, UMR 1260Tumor Biomechanics, INSERM UMR_S1109, Université de Strasbourg, Fédération de Médecine Translationnelle de Strasbourg (FMTS)Department of Periodontology, School of Graduate Dentistry, Faculty of Medicine, Rambam Health Care Campus, Technion (Israel Institute of Technology)Department of Periodontology, School of Graduate Dentistry, Faculty of Medicine, Rambam Health Care Campus, Technion (Israel Institute of Technology)INSERM, UMR 1260Abstract Periodontitis is an inflammatory disease caused by bacterial infection. Recent studies have identified extracellular vesicles (EVs) as potential mediators of inflammation. This study aimed to evaluate the pro-inflammatory properties and miRNA content of EVs secreted in response to Porphyromonas gingivalis infection. Oral epithelial cells (ECs) were infected with P. gingivalis (MOI 100) for 24 h. EVs from infected (P.g.-ECs-EVs) and uninfected cells (ECs-EVs) were isolated, characterized, and tested on naive ECs. Cellular activity, inflammatory markers (TNF-α, IL-1β), and miRNA content of the secreted EVs were evaluated. Bioinformatic analysis was subsequently performed to identify potential targets of differentially expressed miRNAs. P. gingivalis infection increased EV production by 102-fold. P.g.-ECs-EVs exhibited distinct properties compared to ECs-EVs, including higher metabolic activity and elevated TNF-α and IL-1β expression and secretion levels in exposed ECs. Several inflammation-related miRNAs were highly upregulated in P.g.-ECs-EVs (11- to 142-fold; p < 0.001). P. gingivalis promotes the secretion of pro-inflammatory EVs by ECs, suggesting their role as key mediators in P. gingivalis-induced inflammation and periodontal tissue destruction.https://doi.org/10.1038/s41598-025-10078-yExosomesExtracellular vesicles (EVs)InflammationPeriodontitisMicroRNA (miRNA)Porphyromonas gingivalis (P. gingivalis) |
| spellingShingle | Pierre-Yves Gegout Benjamin Mary Céline Stutz Vincent Hyenne Ofir Ginesin Hadar Zigdon-Giladi Olivier Huck Porphyromonas gingivalis infection of oral keratinocytes drives the release of pro-inflammatory extracellular vesicles Scientific Reports Exosomes Extracellular vesicles (EVs) Inflammation Periodontitis MicroRNA (miRNA) Porphyromonas gingivalis (P. gingivalis) |
| title | Porphyromonas gingivalis infection of oral keratinocytes drives the release of pro-inflammatory extracellular vesicles |
| title_full | Porphyromonas gingivalis infection of oral keratinocytes drives the release of pro-inflammatory extracellular vesicles |
| title_fullStr | Porphyromonas gingivalis infection of oral keratinocytes drives the release of pro-inflammatory extracellular vesicles |
| title_full_unstemmed | Porphyromonas gingivalis infection of oral keratinocytes drives the release of pro-inflammatory extracellular vesicles |
| title_short | Porphyromonas gingivalis infection of oral keratinocytes drives the release of pro-inflammatory extracellular vesicles |
| title_sort | porphyromonas gingivalis infection of oral keratinocytes drives the release of pro inflammatory extracellular vesicles |
| topic | Exosomes Extracellular vesicles (EVs) Inflammation Periodontitis MicroRNA (miRNA) Porphyromonas gingivalis (P. gingivalis) |
| url | https://doi.org/10.1038/s41598-025-10078-y |
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