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牙龈卟啉单胞菌感染的口腔癌预后风险与DOK3及浸润性肿瘤相关巨噬细胞的关联：来自中国乌鲁木齐一家三级教学医院200例患者的12年数据分析

Association of DOK3 and infiltrated tumor-associated macrophages with risk for the prognosis of Porphyromonas gingivalis-infected oral cancer: a 12-year data analysis of 200 patients from a tertiary teaching hospital, Urumqi, China.

作者信息

Li Chenxi, Li Muqiu, Wei Wei, Wang Zhengye, Yu Jingwen, Gong Zhongcheng

机构信息

Department of Oral and Maxillofacial Oncology & Surgery, School / Hospital of Stomatology, the First Affiliated Hospital of Xinjiang Medical University, No. 137 Liyushan South Road, Urumqi, 830054, P.R. China.

Stomatological Research Institute of Xinjiang Uygur Autonomous Region, Urumqi, 830054, China.

出版信息

BMC Cancer. 2024 Apr 26;24(1):534. doi: 10.1186/s12885-024-12300-y.

DOI:10.1186/s12885-024-12300-y
PMID:38671413
原文链接:https://pmc.ncbi.nlm.nih.gov/articles/PMC11055382/
Abstract

BACKGROUND: While there is an understanding of the association between the expression of Porphyromonas gingivalis (P. gingivalis) and prognosis of oral squamous cell carcinoma (OSCC), significance specially to address the relevance between different immunohistochemical intensities of P. gingivalis and tumor-associated macrophages (TAMs) in OSCC tissue and related clinicopathologic characteristics has not been well investigated. The present study aimed to investigate the pathological features related to M2-TAM in P. gingivalis-infected OSCC and ascertain its clinical relevance with patients' prognosis. METHODS: A prospective cohort study was designed to comparatively analyze 200 patients from June 2008 to June 2020. Bioinformatics analyses were implemented to identify DOK3 as a key molecule and to appraise immunocyte infiltration using Gene Expression Omnibus and The Cancer Genome Atlas databases. Immunohistochemical evaluation was performed to analyze the association between the expression levels of P. gingivalis, DOK3, and M2-TAM and clinicopathological variables using Fisher's exact test or Pearson's chi-square test. Cox analysis was used to calculate hazard ratios (HR) with corresponding 95% confidence interval (CI) for various clinicopathological features. The Kaplan-Meier approach and log-rank test were used to plot the survival curves. RESULTS: The expression level of P. gingivalis was positively associated with DOK3 and M2-TAMs expression level (P < 0.001). Parameters, including body mass index, clinical stage, recurrence, tumor differentiation, and P. gingivalis, DOK3, and M2-TAM immunoexpression levels, affected the prognosis of patients with OSCC (all P < 0.05). In addition, P. gingivalis (HR = 1.674, 95%CI 1.216-4.142, P = 0.012), DOK3 (HR = 1.881, 95%CI 1.433-3.457, P = 0.042), and M2-TAM (HR = 1.649, 95%CI 0.824-3.082, P = 0.034) were significantly associated with the 10-year cumulative survival rate. CONCLUSIONS: Elevated expression of P. gingivalis and DOK3 indicates M2-TAM infiltration and unfavorable prognosis of OSCC, and could be considered as three novel independent risk factors for predicting the prognosis of OSCC.

摘要

背景：虽然人们已经了解牙龈卟啉单胞菌（P. gingivalis）的表达与口腔鳞状细胞癌（OSCC）预后之间的关联，但对于OSCC组织中P. gingivalis不同免疫组化强度与肿瘤相关巨噬细胞（TAMs）之间的相关性及其相关临床病理特征的意义尚未进行充分研究。本研究旨在探讨P. gingivalis感染的OSCC中与M2-TAM相关的病理特征，并确定其与患者预后的临床相关性。 方法：设计一项前瞻性队列研究，对2008年6月至2020年6月期间的200例患者进行比较分析。利用基因表达综合数据库和癌症基因组图谱数据库进行生物信息学分析，以确定DOK3为关键分子并评估免疫细胞浸润情况。采用Fisher精确检验或Pearson卡方检验进行免疫组化评估，以分析P. gingivalis、DOK3和M2-TAM的表达水平与临床病理变量之间的关联。使用Cox分析计算各种临床病理特征的风险比（HR）及其相应的95%置信区间（CI）。采用Kaplan-Meier法和对数秩检验绘制生存曲线。 结果：P. gingivalis的表达水平与DOK3和M2-TAMs的表达水平呈正相关（P < 0.001）。包括体重指数、临床分期、复发、肿瘤分化以及P. gingivalis、DOK3和M2-TAM免疫表达水平等参数影响OSCC患者的预后（均P < 0.05）。此外，P. gingivalis（HR = 1.674，95%CI 1.216 - 4.142，P = 0.012）、DOK3（HR = 1.881，95%CI 1.433 - 3.457，P = 0.042）和M2-TAM（HR = 1.649，95%CI 0.824 - 3.082，P = 0.034）与10年累积生存率显著相关。 结论：P. gingivalis和DOK3表达升高表明M2-TAM浸润及OSCC预后不良，可被视为预测OSCC预后的三个新的独立危险因素。

https://cdn.ncbi.nlm.nih.gov/pmc/blobs/fca1/11055382/f95e6e225bc8/12885_2024_12300_Fig7_HTML.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/fca1/11055382/8683063974d2/12885_2024_12300_Fig1_HTML.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/fca1/11055382/428bb9183780/12885_2024_12300_Fig2_HTML.jpg
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https://cdn.ncbi.nlm.nih.gov/pmc/blobs/fca1/11055382/95f02f60bcc1/12885_2024_12300_Fig4_HTML.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/fca1/11055382/b3e47cc9000e/12885_2024_12300_Fig5_HTML.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/fca1/11055382/0b7a98b5a17b/12885_2024_12300_Fig6_HTML.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/fca1/11055382/f95e6e225bc8/12885_2024_12300_Fig7_HTML.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/fca1/11055382/8683063974d2/12885_2024_12300_Fig1_HTML.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/fca1/11055382/428bb9183780/12885_2024_12300_Fig2_HTML.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/fca1/11055382/17b78c33367d/12885_2024_12300_Fig3_HTML.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/fca1/11055382/95f02f60bcc1/12885_2024_12300_Fig4_HTML.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/fca1/11055382/b3e47cc9000e/12885_2024_12300_Fig5_HTML.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/fca1/11055382/0b7a98b5a17b/12885_2024_12300_Fig6_HTML.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/fca1/11055382/f95e6e225bc8/12885_2024_12300_Fig7_HTML.jpg

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Med Oral Patol Oral Cir Bucal. 2025-7-1

[2]
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[3]
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[4]
Deliberation concerning the role of M1-type macrophage subset in oral carcinogenesis.

J Exp Clin Cancer Res. 2024-8-8

[5]
Probability Regarding the Tumor-Promoter Role of Porphyromonas gingivalis for the Gastric Carcinogenesis.

Dig Dis Sci. 2024-6

本文引用的文献

[1]
Effect of Prognostic Factors of Postoperative Radiotherapy in Oral Squamous Cell Carcinoma: A SEER-Based Study.

Ear Nose Throat J. 2023-11-23

[2]
Reprogramming tumour-associated macrophages to outcompete cancer cells.

Nature. 2023-7

[3]
Oral Microbiome Community Composition in Head and Neck Squamous Cell Carcinoma.

Cancers (Basel). 2023-4-29

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Considerations regarding the tumor-suppressor role of naringenin as a novel agent for the treatment of oral squamous cell carcinoma.

Cancer Immunol Immunother. 2023-9

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Cureus. 2022-12-30

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Porphyromonas gingivalis promotes the progression of oral squamous cell carcinoma by activating the neutrophil chemotaxis in the tumour microenvironment.

Cancer Immunol Immunother. 2023-6

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Porphyromonas gingivalis Activation of Tumor-Associated Macrophages via DOK3 Promotes Recurrence of Oral Squamous Cell Carcinoma.

Med Sci Monit. 2022-10-10

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What is the Potential Interplay between Microbiome and Tumor Microenvironment in Oral Squamous Cell Carcinomas?

Asian Pac J Cancer Prev. 2022-7-1

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CD206+ tumor-associated macrophages cross-present tumor antigen and drive antitumor immunity.

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