Periodontitis promotes tumor growth and immune evasion via PD-1/PD-L1
Abstract Background Our study investigated the role of experimental periodontitis on tumor growth, local and systemic immunosuppressive status, and programmed death receptor 1 (PD-1) / programmed death ligand 1 (PD-L1) expression in oral squamous cell carcinoma (OSCC) and prostate cancer. Methods Mo...
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Springer
2024-11-01
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| Series: | Cancer Immunology, Immunotherapy |
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| Online Access: | https://doi.org/10.1007/s00262-024-03865-5 |
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| author | Suli Wang Fujiao Nie Qiuyue Yin Haoyang Tian Pizhang Gong Jinhong Ju Jiayi Liu Pishan Yang Chengzhe Yang |
| author_facet | Suli Wang Fujiao Nie Qiuyue Yin Haoyang Tian Pizhang Gong Jinhong Ju Jiayi Liu Pishan Yang Chengzhe Yang |
| author_sort | Suli Wang |
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| description | Abstract Background Our study investigated the role of experimental periodontitis on tumor growth, local and systemic immunosuppressive status, and programmed death receptor 1 (PD-1) / programmed death ligand 1 (PD-L1) expression in oral squamous cell carcinoma (OSCC) and prostate cancer. Methods Mouse oral or prostate cancer xenograft models were divided into control, periodontitis and periodontitis + anti-PD-1 groups. Tumor volume and weight were recorded and the levels of relevant immune-suppressive cells and T cells were detected by flow cytometry or immunofluorescence. THP-1 cells were stimulated using conditioned media of LPS-stimulated Cal-27 cells and PD-L1 expression was measured by quantitative real-time PCR, western blotting and immunofluorescence. Tumor specimens from OSCC patients with or without periodontitis were also collected for immunofluorescence. Results Periodontitis significantly promoted tumor volume and weight. Compared to the control, the proportions of tumor-associated macrophages (TAMs), regulatory T cells (Tregs), PD-L1+TAMs and PD-1+CD8+T cells increased, while CD8+T cells decreased in the periodontitis group. Immunofluorescence demonstrated that there was an increase in PD-L1+TAMs and PD-1+CD8+T cells, but a decrease in IFN-γ+CD8+T cells in both xenografts and clinical OSCC samples with periodontitis. In vitro, LPS-stimulated Cal-27 cells had a stronger potential to induce PD-L1 expression in macrophages compared with unstimulated Cal-27 cells. And the promoting effect of periodontitis on tumor growth and immune evasion was significantly attenuated after anti-PD-1 therapy. Conclusion Periodontitis may facilitate tumor growth and immune escape evidenced by the increased immune-suppressive cells and the decreased functional T cells, via enhancing PD-1/PD-L1 expression in the tumor microenvironment. |
| format | Article |
| id | doaj-art-bc5b560ddfa740b0a80519123a6c0d73 |
| institution | Kabale University |
| issn | 1432-0851 |
| language | English |
| publishDate | 2024-11-01 |
| publisher | Springer |
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| series | Cancer Immunology, Immunotherapy |
| spelling | doaj-art-bc5b560ddfa740b0a80519123a6c0d732025-02-02T12:26:32ZengSpringerCancer Immunology, Immunotherapy1432-08512024-11-0174111510.1007/s00262-024-03865-5Periodontitis promotes tumor growth and immune evasion via PD-1/PD-L1Suli Wang0Fujiao Nie1Qiuyue Yin2Haoyang Tian3Pizhang Gong4Jinhong Ju5Jiayi Liu6Pishan Yang7Chengzhe Yang8Department of Periodontology, School and Hospital of Stomatology, Cheeloo College of Medicine, Shandong University & Shandong Key Laboratory of Oral Tissue Regeneration & Shandong Engineering Research Center of Dental Materials and Oral Tissue Regeneration & Shandong Provincial Clinical Research Center for Oral DiseasesDepartment of Periodontology, School and Hospital of Stomatology, Cheeloo College of Medicine, Shandong University & Shandong Key Laboratory of Oral Tissue Regeneration & Shandong Engineering Research Center of Dental Materials and Oral Tissue Regeneration & Shandong Provincial Clinical Research Center for Oral DiseasesDepartment of Periodontology, School and Hospital of Stomatology, Cheeloo College of Medicine, Shandong University & Shandong Key Laboratory of Oral Tissue Regeneration & Shandong Engineering Research Center of Dental Materials and Oral Tissue Regeneration & Shandong Provincial Clinical Research Center for Oral DiseasesDepartment of Periodontology, School and Hospital of Stomatology, Cheeloo College of Medicine, Shandong University & Shandong Key Laboratory of Oral Tissue Regeneration & Shandong Engineering Research Center of Dental Materials and Oral Tissue Regeneration & Shandong Provincial Clinical Research Center for Oral DiseasesDepartment of Periodontology, School and Hospital of Stomatology, Cheeloo College of Medicine, Shandong University & Shandong Key Laboratory of Oral Tissue Regeneration & Shandong Engineering Research Center of Dental Materials and Oral Tissue Regeneration & Shandong Provincial Clinical Research Center for Oral DiseasesDepartment of Periodontology, School and Hospital of Stomatology, Cheeloo College of Medicine, Shandong University & Shandong Key Laboratory of Oral Tissue Regeneration & Shandong Engineering Research Center of Dental Materials and Oral Tissue Regeneration & Shandong Provincial Clinical Research Center for Oral DiseasesDepartment of Periodontology, School and Hospital of Stomatology, Cheeloo College of Medicine, Shandong University & Shandong Key Laboratory of Oral Tissue Regeneration & Shandong Engineering Research Center of Dental Materials and Oral Tissue Regeneration & Shandong Provincial Clinical Research Center for Oral DiseasesDepartment of Periodontology, School and Hospital of Stomatology, Cheeloo College of Medicine, Shandong University & Shandong Key Laboratory of Oral Tissue Regeneration & Shandong Engineering Research Center of Dental Materials and Oral Tissue Regeneration & Shandong Provincial Clinical Research Center for Oral DiseasesDepartment of Oral and Maxillofacial Surgery, Qilu Hospital of Shandong UniversityAbstract Background Our study investigated the role of experimental periodontitis on tumor growth, local and systemic immunosuppressive status, and programmed death receptor 1 (PD-1) / programmed death ligand 1 (PD-L1) expression in oral squamous cell carcinoma (OSCC) and prostate cancer. Methods Mouse oral or prostate cancer xenograft models were divided into control, periodontitis and periodontitis + anti-PD-1 groups. Tumor volume and weight were recorded and the levels of relevant immune-suppressive cells and T cells were detected by flow cytometry or immunofluorescence. THP-1 cells were stimulated using conditioned media of LPS-stimulated Cal-27 cells and PD-L1 expression was measured by quantitative real-time PCR, western blotting and immunofluorescence. Tumor specimens from OSCC patients with or without periodontitis were also collected for immunofluorescence. Results Periodontitis significantly promoted tumor volume and weight. Compared to the control, the proportions of tumor-associated macrophages (TAMs), regulatory T cells (Tregs), PD-L1+TAMs and PD-1+CD8+T cells increased, while CD8+T cells decreased in the periodontitis group. Immunofluorescence demonstrated that there was an increase in PD-L1+TAMs and PD-1+CD8+T cells, but a decrease in IFN-γ+CD8+T cells in both xenografts and clinical OSCC samples with periodontitis. In vitro, LPS-stimulated Cal-27 cells had a stronger potential to induce PD-L1 expression in macrophages compared with unstimulated Cal-27 cells. And the promoting effect of periodontitis on tumor growth and immune evasion was significantly attenuated after anti-PD-1 therapy. Conclusion Periodontitis may facilitate tumor growth and immune escape evidenced by the increased immune-suppressive cells and the decreased functional T cells, via enhancing PD-1/PD-L1 expression in the tumor microenvironment.https://doi.org/10.1007/s00262-024-03865-5PeriodontitisOral cancerProstate cancerTumor immunosuppression microenvironmentPD-1/PD-L1 |
| spellingShingle | Suli Wang Fujiao Nie Qiuyue Yin Haoyang Tian Pizhang Gong Jinhong Ju Jiayi Liu Pishan Yang Chengzhe Yang Periodontitis promotes tumor growth and immune evasion via PD-1/PD-L1 Cancer Immunology, Immunotherapy Periodontitis Oral cancer Prostate cancer Tumor immunosuppression microenvironment PD-1/PD-L1 |
| title | Periodontitis promotes tumor growth and immune evasion via PD-1/PD-L1 |
| title_full | Periodontitis promotes tumor growth and immune evasion via PD-1/PD-L1 |
| title_fullStr | Periodontitis promotes tumor growth and immune evasion via PD-1/PD-L1 |
| title_full_unstemmed | Periodontitis promotes tumor growth and immune evasion via PD-1/PD-L1 |
| title_short | Periodontitis promotes tumor growth and immune evasion via PD-1/PD-L1 |
| title_sort | periodontitis promotes tumor growth and immune evasion via pd 1 pd l1 |
| topic | Periodontitis Oral cancer Prostate cancer Tumor immunosuppression microenvironment PD-1/PD-L1 |
| url | https://doi.org/10.1007/s00262-024-03865-5 |
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