Heat-killed Prevotella intermedia promotes the progression of oral squamous cell carcinoma by inhibiting the expression of tumor suppressors and affecting the tumor microenvironment
Abstract Background Oral microbial dysbiosis contributes to the development of oral squamous cell carcinoma (OSCC). Our previous study showed that Prevotella intermedia (P. intermedia) were enriched in the oral mucosal surface, plaque, and saliva of patients with OSCC. Intratumoral microbiome could...
| Main Authors: | , , , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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BMC
2024-03-01
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| Series: | Experimental Hematology & Oncology |
| Subjects: | |
| Online Access: | https://doi.org/10.1186/s40164-024-00500-y |
| _version_ | 1797247442447499264 |
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| author | Yifan Zhou Yao Qin Jingjing Ma Zhiyuan Li Weiwei Heng Lei Zhang Hong Liu Ruowei Li Miaomiao Zhang Qiao Peng Pei Ye Ning Duan Ting Liu Wenmei Wang Xiang Wang |
| author_facet | Yifan Zhou Yao Qin Jingjing Ma Zhiyuan Li Weiwei Heng Lei Zhang Hong Liu Ruowei Li Miaomiao Zhang Qiao Peng Pei Ye Ning Duan Ting Liu Wenmei Wang Xiang Wang |
| author_sort | Yifan Zhou |
| collection | DOAJ |
| description | Abstract Background Oral microbial dysbiosis contributes to the development of oral squamous cell carcinoma (OSCC). Our previous study showed that Prevotella intermedia (P. intermedia) were enriched in the oral mucosal surface, plaque, and saliva of patients with OSCC. Intratumoral microbiome could reshape the immune system and influence the development of various tumors. However, the invasion status of human OSCC tissues by P. intermedia and the pathway through which intratumoral P. intermedia potentiates tumor progression remain unexplored. Methods P. intermedia in human OSCC or normal tissues was detected by FISH. A mouse OSCC cell line SCC7 was adopted to investigate the effects of heat-killed P. intermedia treatment on cell proliferation, invasion, and cytokine release by using CCK-8 assay, transwell invasion assay and ELISA. Moreover, we established a mouse transplanted tumor model by using SCC7 cells, injected heat-killed P. intermedia into tumor tissues, and investigated the effects of heat-killed P. intermedia on tumor growth, invasion, cytokine levels, immune cell infiltrations, and expression levels by using gross observation, H&E staining, ELISA, immunohistochemistry, mRNA sequencing, and transcriptomic analysis. Results Our results indicated that P. intermedia were abundant in OSCC and surrounding muscle tissues. Heat-killed P. intermedia promoted SCC7 cell proliferation, invasion and proinflammatory cytokine secretions, accelerated transplanted tumor growth in mice, exacerbate muscle and perineural invasion of OSCC, elevated the serum levels of IL-17A, IL-6, TNF-α, IFN-γ, and PD-L1, induced Treg cells M2 type macrophages in mouse transplanted tumors. The data of transcriptomic analysis revealed that heat-killed P. intermedia increased the expression levels of inflammatory cytokines and chemokines while reduced the expression levels of some tumor suppressor genes in mouse transplanted tumors. Additionally, IL-17 signaling pathway was upregulated whereas GABAergic system was downregulated by heat-killed P. intermedia treatment. Conclusions Taken together, our results suggest that P. intermedia could inhibit the expression of tumor suppressors, alter the tumor microenvironment, and promote the progression of OSCC. |
| first_indexed | 2024-04-24T19:58:46Z |
| format | Article |
| id | doaj.art-fab09bda8ecf42c99dd9fcded707db0c |
| institution | Directory Open Access Journal |
| issn | 2162-3619 |
| language | English |
| last_indexed | 2024-04-24T19:58:46Z |
| publishDate | 2024-03-01 |
| publisher | BMC |
| record_format | Article |
| series | Experimental Hematology & Oncology |
| spelling | doaj.art-fab09bda8ecf42c99dd9fcded707db0c2024-03-24T12:12:42ZengBMCExperimental Hematology & Oncology2162-36192024-03-0113112010.1186/s40164-024-00500-yHeat-killed Prevotella intermedia promotes the progression of oral squamous cell carcinoma by inhibiting the expression of tumor suppressors and affecting the tumor microenvironmentYifan Zhou0Yao Qin1Jingjing Ma2Zhiyuan Li3Weiwei Heng4Lei Zhang5Hong Liu6Ruowei Li7Miaomiao Zhang8Qiao Peng9Pei Ye10Ning Duan11Ting Liu12Wenmei Wang13Xiang Wang14Nanjing Stomatological Hospital, Affiliated Hospital of Medical School, Institute of Stomatology, Nanjing UniversityNanjing Stomatological Hospital, Affiliated Hospital of Medical School, Institute of Stomatology, Nanjing UniversityNanjing Stomatological Hospital, Affiliated Hospital of Medical School, Institute of Stomatology, Nanjing UniversityNanjing Stomatological Hospital, Affiliated Hospital of Medical School, Institute of Stomatology, Nanjing UniversityNanjing Stomatological Hospital, Affiliated Hospital of Medical School, Institute of Stomatology, Nanjing UniversityNanjing Stomatological Hospital, Affiliated Hospital of Medical School, Institute of Stomatology, Nanjing UniversityNanjing Stomatological Hospital, Affiliated Hospital of Medical School, Institute of Stomatology, Nanjing UniversityNanjing Stomatological Hospital, Affiliated Hospital of Medical School, Institute of Stomatology, Nanjing UniversityNanjing Stomatological Hospital, Affiliated Hospital of Medical School, Institute of Stomatology, Nanjing UniversityNanjing Stomatological Hospital, Affiliated Hospital of Medical School, Institute of Stomatology, Nanjing UniversityNanjing Stomatological Hospital, Affiliated Hospital of Medical School, Institute of Stomatology, Nanjing UniversityNanjing Stomatological Hospital, Affiliated Hospital of Medical School, Institute of Stomatology, Nanjing UniversityNanjing Stomatological Hospital, Affiliated Hospital of Medical School, Institute of Stomatology, Nanjing UniversityNanjing Stomatological Hospital, Affiliated Hospital of Medical School, Institute of Stomatology, Nanjing UniversityNanjing Stomatological Hospital, Affiliated Hospital of Medical School, Institute of Stomatology, Nanjing UniversityAbstract Background Oral microbial dysbiosis contributes to the development of oral squamous cell carcinoma (OSCC). Our previous study showed that Prevotella intermedia (P. intermedia) were enriched in the oral mucosal surface, plaque, and saliva of patients with OSCC. Intratumoral microbiome could reshape the immune system and influence the development of various tumors. However, the invasion status of human OSCC tissues by P. intermedia and the pathway through which intratumoral P. intermedia potentiates tumor progression remain unexplored. Methods P. intermedia in human OSCC or normal tissues was detected by FISH. A mouse OSCC cell line SCC7 was adopted to investigate the effects of heat-killed P. intermedia treatment on cell proliferation, invasion, and cytokine release by using CCK-8 assay, transwell invasion assay and ELISA. Moreover, we established a mouse transplanted tumor model by using SCC7 cells, injected heat-killed P. intermedia into tumor tissues, and investigated the effects of heat-killed P. intermedia on tumor growth, invasion, cytokine levels, immune cell infiltrations, and expression levels by using gross observation, H&E staining, ELISA, immunohistochemistry, mRNA sequencing, and transcriptomic analysis. Results Our results indicated that P. intermedia were abundant in OSCC and surrounding muscle tissues. Heat-killed P. intermedia promoted SCC7 cell proliferation, invasion and proinflammatory cytokine secretions, accelerated transplanted tumor growth in mice, exacerbate muscle and perineural invasion of OSCC, elevated the serum levels of IL-17A, IL-6, TNF-α, IFN-γ, and PD-L1, induced Treg cells M2 type macrophages in mouse transplanted tumors. The data of transcriptomic analysis revealed that heat-killed P. intermedia increased the expression levels of inflammatory cytokines and chemokines while reduced the expression levels of some tumor suppressor genes in mouse transplanted tumors. Additionally, IL-17 signaling pathway was upregulated whereas GABAergic system was downregulated by heat-killed P. intermedia treatment. Conclusions Taken together, our results suggest that P. intermedia could inhibit the expression of tumor suppressors, alter the tumor microenvironment, and promote the progression of OSCC.https://doi.org/10.1186/s40164-024-00500-yOral squamous cell carcinomaPrevotella intermediaIL-17 signal pathwayGABAergic systemTumor suppressor genes |
| spellingShingle | Yifan Zhou Yao Qin Jingjing Ma Zhiyuan Li Weiwei Heng Lei Zhang Hong Liu Ruowei Li Miaomiao Zhang Qiao Peng Pei Ye Ning Duan Ting Liu Wenmei Wang Xiang Wang Heat-killed Prevotella intermedia promotes the progression of oral squamous cell carcinoma by inhibiting the expression of tumor suppressors and affecting the tumor microenvironment Experimental Hematology & Oncology Oral squamous cell carcinoma Prevotella intermedia IL-17 signal pathway GABAergic system Tumor suppressor genes |
| title | Heat-killed Prevotella intermedia promotes the progression of oral squamous cell carcinoma by inhibiting the expression of tumor suppressors and affecting the tumor microenvironment |
| title_full | Heat-killed Prevotella intermedia promotes the progression of oral squamous cell carcinoma by inhibiting the expression of tumor suppressors and affecting the tumor microenvironment |
| title_fullStr | Heat-killed Prevotella intermedia promotes the progression of oral squamous cell carcinoma by inhibiting the expression of tumor suppressors and affecting the tumor microenvironment |
| title_full_unstemmed | Heat-killed Prevotella intermedia promotes the progression of oral squamous cell carcinoma by inhibiting the expression of tumor suppressors and affecting the tumor microenvironment |
| title_short | Heat-killed Prevotella intermedia promotes the progression of oral squamous cell carcinoma by inhibiting the expression of tumor suppressors and affecting the tumor microenvironment |
| title_sort | heat killed prevotella intermedia promotes the progression of oral squamous cell carcinoma by inhibiting the expression of tumor suppressors and affecting the tumor microenvironment |
| topic | Oral squamous cell carcinoma Prevotella intermedia IL-17 signal pathway GABAergic system Tumor suppressor genes |
| url | https://doi.org/10.1186/s40164-024-00500-y |
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