Symbiotic microbiome Staphylococcus epidermidis restricts IL-33 production in allergic nasal epithelium via limiting the cellular necroptosis
Abstract Background Allergic rhinitis (AR) is characterized by airway inflammation in nasal mucosa from inhaled allergens and interleukin (IL)-33 is the potent inducer of Th2 inflammation in allergic nasal epithelium. Staphylococcus epidermidis is one of the most abundant colonizers of the healthy h...
| Main Authors: | , , , , |
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| Format: | Article |
| Language: | English |
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BMC
2023-05-01
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| Series: | BMC Microbiology |
| Subjects: | |
| Online Access: | https://doi.org/10.1186/s12866-023-02898-7 |
| _version_ | 1797801594125811712 |
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| author | Yung Jin Jeon Chan Hee Gil Jina Won Ara Jo Hyun Jik Kim |
| author_facet | Yung Jin Jeon Chan Hee Gil Jina Won Ara Jo Hyun Jik Kim |
| author_sort | Yung Jin Jeon |
| collection | DOAJ |
| description | Abstract Background Allergic rhinitis (AR) is characterized by airway inflammation in nasal mucosa from inhaled allergens and interleukin (IL)-33 is the potent inducer of Th2 inflammation in allergic nasal epithelium. Staphylococcus epidermidis is one of the most abundant colonizers of the healthy human nasal mucosa and might impact the allergen-induced inflammatory responses in the nasal epithelium. Thus, we sought to characterize the mechanism of S. epidermidis regulating Th2 inflammation and IL-33 production in AR nasal mucosa. Results The AR symptoms were alleviated and eosinophilic infiltration, serum IgE levels, and Th2 cytokines were significantly decreased in OVA-sensitized AR mice in response to human nasal commensal S. epidermidis. The inoculation of S. epidermidis to normal human nasal epithelial cells reduced IL-33 and GATA3 transcriptions and also reduced IL-33 and GATA3 expression in AR nasal epithelial (ARNE) cells and the nasal mucosa of AR mice. Our data exhibited that the cellular necroptosis of ARNE cells might be involved in IL-33 production and inoculation of S. epidermidis decreased the phosphorylation of necroptosis enzymes in ARNE cells, which was related to the reduction of IL-33 production. Conclusions We present that human nasal commensal S. epidermidis reduces allergic inflammation by suppressing IL-33 production in nasal epithelium. Our findings indicate that S. epidermidis serves a role in blocking allergen-induced cellular necroptosis in allergic nasal epithelium which might be a key mechanism of reduction of IL-33 and Th2 inflammation. |
| first_indexed | 2024-03-13T04:52:29Z |
| format | Article |
| id | doaj.art-b77ff13034664740ba97841ad6e71138 |
| institution | Directory Open Access Journal |
| issn | 1471-2180 |
| language | English |
| last_indexed | 2024-03-13T04:52:29Z |
| publishDate | 2023-05-01 |
| publisher | BMC |
| record_format | Article |
| series | BMC Microbiology |
| spelling | doaj.art-b77ff13034664740ba97841ad6e711382023-06-18T11:08:16ZengBMCBMC Microbiology1471-21802023-05-0123111110.1186/s12866-023-02898-7Symbiotic microbiome Staphylococcus epidermidis restricts IL-33 production in allergic nasal epithelium via limiting the cellular necroptosisYung Jin Jeon0Chan Hee Gil1Jina Won2Ara Jo3Hyun Jik Kim4Department of Otorhinolaryngology, Gyeongsang National University HospitalDepartment of Otorhinolaryngology, Seoul National University College of MedicineDepartment of Otorhinolaryngology, Seoul National University College of MedicineDepartment of Otorhinolaryngology, Seoul National University College of MedicineDepartment of Otorhinolaryngology, Seoul National University College of MedicineAbstract Background Allergic rhinitis (AR) is characterized by airway inflammation in nasal mucosa from inhaled allergens and interleukin (IL)-33 is the potent inducer of Th2 inflammation in allergic nasal epithelium. Staphylococcus epidermidis is one of the most abundant colonizers of the healthy human nasal mucosa and might impact the allergen-induced inflammatory responses in the nasal epithelium. Thus, we sought to characterize the mechanism of S. epidermidis regulating Th2 inflammation and IL-33 production in AR nasal mucosa. Results The AR symptoms were alleviated and eosinophilic infiltration, serum IgE levels, and Th2 cytokines were significantly decreased in OVA-sensitized AR mice in response to human nasal commensal S. epidermidis. The inoculation of S. epidermidis to normal human nasal epithelial cells reduced IL-33 and GATA3 transcriptions and also reduced IL-33 and GATA3 expression in AR nasal epithelial (ARNE) cells and the nasal mucosa of AR mice. Our data exhibited that the cellular necroptosis of ARNE cells might be involved in IL-33 production and inoculation of S. epidermidis decreased the phosphorylation of necroptosis enzymes in ARNE cells, which was related to the reduction of IL-33 production. Conclusions We present that human nasal commensal S. epidermidis reduces allergic inflammation by suppressing IL-33 production in nasal epithelium. Our findings indicate that S. epidermidis serves a role in blocking allergen-induced cellular necroptosis in allergic nasal epithelium which might be a key mechanism of reduction of IL-33 and Th2 inflammation.https://doi.org/10.1186/s12866-023-02898-7Staphylococcus epidermidisAllergic rhinitisInterleukin-33NecroptosisNasal epithelium |
| spellingShingle | Yung Jin Jeon Chan Hee Gil Jina Won Ara Jo Hyun Jik Kim Symbiotic microbiome Staphylococcus epidermidis restricts IL-33 production in allergic nasal epithelium via limiting the cellular necroptosis BMC Microbiology Staphylococcus epidermidis Allergic rhinitis Interleukin-33 Necroptosis Nasal epithelium |
| title | Symbiotic microbiome Staphylococcus epidermidis restricts IL-33 production in allergic nasal epithelium via limiting the cellular necroptosis |
| title_full | Symbiotic microbiome Staphylococcus epidermidis restricts IL-33 production in allergic nasal epithelium via limiting the cellular necroptosis |
| title_fullStr | Symbiotic microbiome Staphylococcus epidermidis restricts IL-33 production in allergic nasal epithelium via limiting the cellular necroptosis |
| title_full_unstemmed | Symbiotic microbiome Staphylococcus epidermidis restricts IL-33 production in allergic nasal epithelium via limiting the cellular necroptosis |
| title_short | Symbiotic microbiome Staphylococcus epidermidis restricts IL-33 production in allergic nasal epithelium via limiting the cellular necroptosis |
| title_sort | symbiotic microbiome staphylococcus epidermidis restricts il 33 production in allergic nasal epithelium via limiting the cellular necroptosis |
| topic | Staphylococcus epidermidis Allergic rhinitis Interleukin-33 Necroptosis Nasal epithelium |
| url | https://doi.org/10.1186/s12866-023-02898-7 |
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