Porphyromonas gingivalis outer membrane vesicles augments proliferation and metastasis of oral squamous cell carcinoma cells

Abstract Background Porphyromonas gingivalis (P. gingivalis) is closely related to Oral squamous cell carcinoma (OSCC), and P. gingivalis outer membrane vesicles (OMVs) is the main pathogenic factor, which is associated with periodontitis, atherosclerosis and other diseases. However, few studies hav...

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Main Authors: Yanru Zeng, Yiyang Wang, Xiaona Shi, Yuanhao Zhao, Yue Tang, Shanshan Liu, Xiaofeng Zhu
Format: Article
Language:English
Published: BMC 2025-05-01
Series:BMC Oral Health
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Online Access:https://doi.org/10.1186/s12903-025-05937-z
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author Yanru Zeng
Yiyang Wang
Xiaona Shi
Yuanhao Zhao
Yue Tang
Shanshan Liu
Xiaofeng Zhu
author_facet Yanru Zeng
Yiyang Wang
Xiaona Shi
Yuanhao Zhao
Yue Tang
Shanshan Liu
Xiaofeng Zhu
author_sort Yanru Zeng
collection DOAJ
description Abstract Background Porphyromonas gingivalis (P. gingivalis) is closely related to Oral squamous cell carcinoma (OSCC), and P. gingivalis outer membrane vesicles (OMVs) is the main pathogenic factor, which is associated with periodontitis, atherosclerosis and other diseases. However, few studies have reported an association between P. gingivalis OMVs and OSCC. The purpose of this study was to establish the clinical relationship between P. gingivalis and OSCC based on clinical samples. Further, the effect of P. gingivalis OMVs on OSCC was observed with cell model in vitro, and the possible molecular mechanism was discussed. Methods Immunohistochemistry was used to detect the abundance of P. gingivalis in OSCC and its paired paracancer tissues, and to analyze the correlation between P. gingivalis and clinicopathological parameters of patients. P. gingivalis OMVs were isolated to observe its effects on the proliferation and migration of OSCC cell lines. RNA-seq was performed and the expression of differentially expressed genes (DEGs) was detected by real-time quantitative PCR (RT-qPCR) to explore the potential mechnism of P. gingivalis OMVs on OSCC progression. Results The abundance of P. gingivalis in OSCC was higher than that in para-cancerous tissues, and was positively correlated with the degree of tissue differentiation (P = 0.028), T stage (P < 0.001), and clinical stage (P = 0.011). P. gingivalis OMVs promoted the proliferation and migration of HN6 cells, and promoted the proliferation of CAL27 cells, but had no significant effect on its migration. P. gingivalis OMVs treatment attenuated the expressions of TNFSF15, ZNF292, ATRX, ASPM and KIF20B in CAL27 and HN6 cells. Conclusion This study suggests that P. gingivalis may be an indicator of poor prognosis for OSCC. P. gingivalis OMVs may down-regulate the expression of TNFSF15, ZNF292, ATRX, ASPM, KIF20B and participate in the occurrence and development of OSCC.
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spelling doaj-art-7b8f7dee19674622919fc57bde7c7ab82025-08-20T02:15:15ZengBMCBMC Oral Health1472-68312025-05-0125111810.1186/s12903-025-05937-zPorphyromonas gingivalis outer membrane vesicles augments proliferation and metastasis of oral squamous cell carcinoma cellsYanru Zeng0Yiyang Wang1Xiaona Shi2Yuanhao Zhao3Yue Tang4Shanshan Liu5Xiaofeng Zhu6Department of Oral Maxillo-Facial Surgery, The First Affiliated Hospital, Fujian Medical UniversityDepartment of Oral Maxillo-Facial Surgery, The First Affiliated Hospital, Fujian Medical UniversityFujian Key Laboratory of Oral Diseases & Fujian Provincial Engineering Research Center of Oral Biomaterial & Stomatological Key Lab of Fujian College and University, School and Hospital of Stomatology, Fujian Medical UniversityFujian Key Laboratory of Oral Diseases & Fujian Provincial Engineering Research Center of Oral Biomaterial & Stomatological Key Lab of Fujian College and University, School and Hospital of Stomatology, Fujian Medical UniversityFujian Key Laboratory of Oral Diseases & Fujian Provincial Engineering Research Center of Oral Biomaterial & Stomatological Key Lab of Fujian College and University, School and Hospital of Stomatology, Fujian Medical UniversityDepartment of Oral Maxillo-Facial Surgery, The First Affiliated Hospital, Fujian Medical UniversityDepartment of Oral Maxillo-Facial Surgery, The First Affiliated Hospital, Fujian Medical UniversityAbstract Background Porphyromonas gingivalis (P. gingivalis) is closely related to Oral squamous cell carcinoma (OSCC), and P. gingivalis outer membrane vesicles (OMVs) is the main pathogenic factor, which is associated with periodontitis, atherosclerosis and other diseases. However, few studies have reported an association between P. gingivalis OMVs and OSCC. The purpose of this study was to establish the clinical relationship between P. gingivalis and OSCC based on clinical samples. Further, the effect of P. gingivalis OMVs on OSCC was observed with cell model in vitro, and the possible molecular mechanism was discussed. Methods Immunohistochemistry was used to detect the abundance of P. gingivalis in OSCC and its paired paracancer tissues, and to analyze the correlation between P. gingivalis and clinicopathological parameters of patients. P. gingivalis OMVs were isolated to observe its effects on the proliferation and migration of OSCC cell lines. RNA-seq was performed and the expression of differentially expressed genes (DEGs) was detected by real-time quantitative PCR (RT-qPCR) to explore the potential mechnism of P. gingivalis OMVs on OSCC progression. Results The abundance of P. gingivalis in OSCC was higher than that in para-cancerous tissues, and was positively correlated with the degree of tissue differentiation (P = 0.028), T stage (P < 0.001), and clinical stage (P = 0.011). P. gingivalis OMVs promoted the proliferation and migration of HN6 cells, and promoted the proliferation of CAL27 cells, but had no significant effect on its migration. P. gingivalis OMVs treatment attenuated the expressions of TNFSF15, ZNF292, ATRX, ASPM and KIF20B in CAL27 and HN6 cells. Conclusion This study suggests that P. gingivalis may be an indicator of poor prognosis for OSCC. P. gingivalis OMVs may down-regulate the expression of TNFSF15, ZNF292, ATRX, ASPM, KIF20B and participate in the occurrence and development of OSCC.https://doi.org/10.1186/s12903-025-05937-zSquamous cell carcinoma of head and neckPorphyromonas gingivalisExtracelular vesicles
spellingShingle Yanru Zeng
Yiyang Wang
Xiaona Shi
Yuanhao Zhao
Yue Tang
Shanshan Liu
Xiaofeng Zhu
Porphyromonas gingivalis outer membrane vesicles augments proliferation and metastasis of oral squamous cell carcinoma cells
BMC Oral Health
Squamous cell carcinoma of head and neck
Porphyromonas gingivalis
Extracelular vesicles
title Porphyromonas gingivalis outer membrane vesicles augments proliferation and metastasis of oral squamous cell carcinoma cells
title_full Porphyromonas gingivalis outer membrane vesicles augments proliferation and metastasis of oral squamous cell carcinoma cells
title_fullStr Porphyromonas gingivalis outer membrane vesicles augments proliferation and metastasis of oral squamous cell carcinoma cells
title_full_unstemmed Porphyromonas gingivalis outer membrane vesicles augments proliferation and metastasis of oral squamous cell carcinoma cells
title_short Porphyromonas gingivalis outer membrane vesicles augments proliferation and metastasis of oral squamous cell carcinoma cells
title_sort porphyromonas gingivalis outer membrane vesicles augments proliferation and metastasis of oral squamous cell carcinoma cells
topic Squamous cell carcinoma of head and neck
Porphyromonas gingivalis
Extracelular vesicles
url https://doi.org/10.1186/s12903-025-05937-z
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