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Article(id=1226956555166331727, tenantId=1146029695717560320, journalId=1192105938417971205, issueId=1226956547847275311, articleNumber=null, orderNo=null, doi=10.13343/j.cnki.wsxb.20250126, pmid=null, cstr=null, oa=null, hot=null, price=null, onlineType=0, articleFormat=0, articleType=null, articleTypeStr=research-article, receivedDate=1740067200000, receivedDateStr=2025-02-21, revisedDate=null, revisedDateStr=null, acceptedDate=1744992000000, acceptedDateStr=2025-04-19, onlineDate=1770458838501, onlineDateStr=2026-02-07, pubDate=1756915200000, pubDateStr=2025-09-04, doiRegisterDate=null, doiRegisterDateStr=null, onlineIssueDate=1770458838501, onlineIssueDateStr=2026-02-07, onlineJustAcceptDate=null, onlineJustAcceptDateStr=null, onlineFirstDate=null, onlineFirstDateStr=null, sourceXml=null, magXml=null, createTime=1770458838501, creator=13701087609, updateTime=1770458838501, updator=13701087609, issue=Issue{id=1226956547847275311, tenantId=1146029695717560320, journalId=1192105938417971205, year='2025', volume='65', issue='9', pageStart='3821', pageEnd='4232', issueExtLink='null', onlineDate='null', pubDate='null', beforeIssueId=null, nextIssueId=null, price=null, status=1, issueComplete=1, articleOrder=1, issueType=-1, specialIssue=null, createTime=1770458836757, creator=13701087609, updateTime=1770459153781, updator=13701087609, preIssue=null, nextIssue=null, ext={EN=IssueExt(id=1226957877613605816, tenantId=1146029695717560320, journalId=1192105938417971205, issueId=1226956547847275311, language=EN, specialIssueTitle=, coverIllustrator=null, specialIssueEditor=, specialIssueAbout=), CN=IssueExt(id=1226957877613605817, tenantId=1146029695717560320, journalId=1192105938417971205, issueId=1226956547847275311, language=CN, specialIssueTitle=, coverIllustrator=null, specialIssueEditor=, specialIssueAbout=)}, issueFiles=null}, startPage=4001, endPage=4013, ext={EN=ArticleExt(id=1226956558102344653, articleId=1226956555166331727, tenantId=1146029695717560320, journalId=1192105938417971205, language=EN, title=Fusobacterium nucleatum promotes lung cancer development and influences the lung microbiota, columnId=1192149543992045670, journalTitle=Acta Microbiologica Sinica, columnName=Research Article, runingTitle=null, highlight=null, articleAbstract=

[Objective] To investigate whether Fusobacterium nucleatum promotes the development of lung cancer and find out the underlying mechanisms. [Methods] The cell experiment proved that F. nucleatum can promote the proliferation and metastasis of lung cancer cells; Animal experiments showed that F. nucleatum can promote the development of lung cancer; 16S rRNA gene sequencing of alveolar lavage fluid and transcriptome sequencing of lung tissue were performed to analyze the effects of F. nucleatum on the lung flora of mice with lung cancer and the activation of relevant pathways in lung tissue. [Results] The cell experiment showed that F. nucleatum significantly promoted the proliferation and metastasis of A549 cells. The animal experiments confirmed that F. nucleatum infection in the lungs increased the number of nodules and enhanced the fluorescence intensity in the lung tissue. The 16S rRNA gene sequencing revealed the enrichment of Muribaculum and Simplicispira in the lung of infected mice. The transcriptome sequencing results showed that the mouse model of lung cancer activated the interleukin-17 signaling pathway, cytokine-cytokine receptor interactions, Staphylococcus aureus infection pathway, tumor necrosis factor signaling pathway, and other signaling pathways related to inflammation or immunity after being infected with F. nucleatum. [Conclusion] F. nucleatum infection in mice with lung cancer disrupts the microbiota and activates the immunity- and inflammation-related signaling pathways in the lung, thereby promoting the metastasis of lung cancer in mice.

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*E-mail:
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#These authors contributed equally to this work.

, authorsList=Dong LI, Jianghui TONG, Yitong LI, Yifan SUN, Jianjie LI, Ziping WANG, Yafang TAN, Ruifu YANG, Yujing BI), CN=ArticleExt(id=1226956561055133841, articleId=1226956555166331727, tenantId=1146029695717560320, journalId=1192105938417971205, language=CN, title=具核梭杆菌促进肺癌发展及其对肺部微生态的影响, columnId=1192149544164012138, journalTitle=微生物学报, columnName=研究报告, runingTitle=null, highlight=null, articleAbstract=

【目的】 探究具核梭杆菌是否会促进肺癌的发展及其潜在机制。 【方法】 通过细胞实验证实具核梭杆菌能促进肺癌细胞的增殖和转移；通过动物实验验证具核梭杆菌能促进肺癌的发展。对肺癌小鼠的肺泡灌洗液进行16S rRNA基因测序，以及对肺组织进行转录组测序，分析具核梭杆菌对肺癌小鼠肺部菌群的影响及肺组织相关通路的激活情况。 【结果】 具核梭杆菌促进了肺癌上皮细胞A549的增殖和转移。在体内动物实验中，具核梭杆菌感染肺部后肺部结节数量增加，肺组织荧光强度增强。16S rRNA基因测序结果显示，感染小鼠肺部鼠杆状菌属(Muribaculum)、简单螺旋形菌属(Simplicispira)等富集。肺组织转录组结果显示，肺癌小鼠感染具核梭杆菌后激活了IL-17信号通路、细胞因子-细胞因子受体相互作用、金黄色葡萄球菌感染通路、TNF信号通路等与炎症或免疫相关的信号通路。 【结论】 具核梭杆菌感染导致肺部微生物群紊乱，肺组织中多个与炎症和免疫相关的信号通路被激活，从而促进了小鼠肺癌的转移。

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作者贡献声明

李东：进行实验和撰写文章；童江辉：进行实验和数据分析；李奕彤：进行实验；孙一凡：数据分析；李俭杰：样本收集和数据分析；王子平：文章编辑与修改；谭亚芳：实验设计与统筹；杨瑞馥：实验设计与文章审阅；毕玉晶：实验设计与文章撰写。

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A: Growth curves of two strains of F. nucleatum; B: MTT assay of cell proliferation; C, D: Transwell assay of cell transfer; E, F: Comparison of the pro-inflammatory capacity of two strains of F. nucleatum and Escherichia coli DH5α. ns: Not statistically significant; *: P<0.05; **: P<0.01; ***: P<0.001. 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Data are expressed as mean±SD., figureFileSmall=zU7ZhNJxHmhW4si5sLttSA==, figureFileBig=o4mMDEey+jXAiO4hw7dLRw==, tableContent=null), ArticleFig(id=1226964060302918656, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1226956555166331727, language=CN, label=图2, caption=具核梭杆菌促进小鼠肺癌转移。A：实验流程图；B、C：Fn-9、Fn-ATCC和PBS 3组荧光强度比较；D、E：3组肺结节数量和肺器官系数。, figureFileSmall=zU7ZhNJxHmhW4si5sLttSA==, figureFileBig=o4mMDEey+jXAiO4hw7dLRw==, tableContent=null), ArticleFig(id=1226964060474884105, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1226956555166331727, language=EN, label=Figure 3, caption=Pathologic section diagrams and quantitative polymerase chain reaction (qPCR). A: Lung tissue sections of three groups of Fn-9, Fn-ATCC, and PBS; B-D: Expression of IL-1β, TNF-α, and IL-6 in mouse lung tissue. ns: Not statistically significant; *: P<0.05; **: P<0.01. Data are expressed as mean±SD., figureFileSmall=+VvkguUjVRh8mRHfvZbmsA==, figureFileBig=95IIN+M1n8ig3wj1rQPDBw==, tableContent=null), ArticleFig(id=1226964060583936018, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1226956555166331727, language=CN, label=图3, caption=病理切片图和定量聚合酶链反应(qPCR)。A：Fn-9、Fn-ATCC和PBS 3组肺组织切片；B-D：IL-1β、TNF-α和IL-6在小鼠肺组织中的表达(ns：无统计学意义；*：P<0.05；**：P<0.01。数据以平均值±SD表示)。, figureFileSmall=+VvkguUjVRh8mRHfvZbmsA==, figureFileBig=95IIN+M1n8ig3wj1rQPDBw==, tableContent=null), ArticleFig(id=1226964060701376538, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1226956555166331727, language=EN, label=Figure 4, caption=Effect of Fusobacterium nucleatum on the lung microbiota. A: Community bar plots for the top 20 abundant genera in level for the four groups; B: Chao1 index of the four groups of alveolar lavage fluid (P-value calculated by Kruskal-Wallis test, *: P<0.05); C: PCoA plots of the four groups of alveolar lavage fluid (ANOSIM was used to statistically evaluate significant differences); D: MetagenomeSeq detects differential species between the four groups (*: P<0.05)., figureFileSmall=dX3+XKoOj5KG+JdB5nZOgw==, figureFileBig=urx65Ewds3HiGdzoYfY7eA==, tableContent=null), ArticleFig(id=1226964060827205665, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1226956555166331727, language=CN, label=图4, caption=具核梭杆菌对肺部微生物群的影响。A：4组菌属水平前20个丰度的群落条形图；B：4组肺泡灌洗液的Chao1指数(P值通过Kruskal-Wallis检验计算，*：P<0.05)；C：4组肺泡灌洗液的PCoA图(ANOSIM用于统计评估显著差异)；D：MetagenomeSeq检测4组之间的差异物种(*：P<0.05)。, figureFileSmall=dX3+XKoOj5KG+JdB5nZOgw==, figureFileBig=urx65Ewds3HiGdzoYfY7eA==, tableContent=null), ArticleFig(id=1226964060994977838, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1226956555166331727, language=EN, label=Figure 5, caption=Transcriptome of infected lung cancer tissues. A: Principal component analysis between three groups of samples; B, C: Volcano plots of differential gene expression analysis; D: KEGG pathway enrichment analysis of differential genes in RNA-seq data between Fn-ATCC and PBS; E: KEGG pathway enrichment analysis of differential genes in RNA-seq data between Fn-9 and PBS., figureFileSmall=3+AqUAsyNEPU3dGK2vym8Q==, figureFileBig=RQwpfUMUOgoin6vDMmW8kA==, tableContent=null), ArticleFig(id=1226964061120806964, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1226956555166331727, language=CN, label=图5, caption=感染后肺癌组织的转录组。A：3组样本间的主成分分析；B、C：差异基因表达分析的火山图；D：Fn-ATCC与PBS之间RNA-seq数据中差异基因的KEGG通路富集分析；E：Fn-9与PBS之间RNA-seq数据中差异基因的KEGG通路富集分析。, figureFileSmall=3+AqUAsyNEPU3dGK2vym8Q==, figureFileBig=RQwpfUMUOgoin6vDMmW8kA==, tableContent=null), ArticleFig(id=1226964061250830394, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1226956555166331727, language=EN, label=Table 1, caption=

Primer sequences of mouse inflammatory factor

, figureFileSmall=null, figureFileBig=null, tableContent=
Primers namePrimer sequences (5′→3′)
GAPDH-FCATCACTGCCACCCAGAAGACTG
GAPDH-RATGCCAGTGAGCTTCCCGTTCAG
IL-1β-FGCAACTGTTCCTGAACCCAACT
IL-1β-RAAGTGCATCATCGTTGTTCATACA
IL-6-FTGTTCTCTGGGAAATCGTGGA
IL-6-RAAGTGCATCATCGTTGTTCATACA
TNF-α-FCCCTCACACTCAGATCATCTTCT
TNF-α-RGCTACGACGTGGGCTACAG
), ArticleFig(id=1226964061376659526, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1226956555166331727, language=CN, label=表1, caption=

小鼠炎症因子的引物序列

, figureFileSmall=null, figureFileBig=null, tableContent=
Primers namePrimer sequences (5′→3′)
GAPDH-FCATCACTGCCACCCAGAAGACTG
GAPDH-RATGCCAGTGAGCTTCCCGTTCAG
IL-1β-FGCAACTGTTCCTGAACCCAACT
IL-1β-RAAGTGCATCATCGTTGTTCATACA
IL-6-FTGTTCTCTGGGAAATCGTGGA
IL-6-RAAGTGCATCATCGTTGTTCATACA
TNF-α-FCCCTCACACTCAGATCATCTTCT
TNF-α-RGCTACGACGTGGGCTACAG
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具核梭杆菌促进肺癌发展及其对肺部微生态的影响
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李东 1, 2 , 童江辉 2 , 李奕彤 1, 2 , 孙一凡 2 , 李俭杰 3 , 王子平 3 , 谭亚芳 2 , 杨瑞馥 2 , 毕玉晶 1, 2
微生物学报 | 研究报告 2025,65(9): 4001-4013
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微生物学报 | 研究报告 2025, 65(9): 4001-4013
具核梭杆菌促进肺癌发展及其对肺部微生态的影响
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李东1, 2, 童江辉2, 李奕彤1, 2, 孙一凡2, 李俭杰3, 王子平3, 谭亚芳2, 杨瑞馥2, 毕玉晶1, 2
作者信息
  • 1 安徽医科大学 基础医学院，安徽 合肥
  • 2 军事医学研究院，病原微生物与生物安全全国重点实验室，北京
  • 3 北京大学肿瘤医院 胸部肿瘤内一科，北京
Fusobacterium nucleatum promotes lung cancer development and influences the lung microbiota
Dong LI1, 2, Jianghui TONG2, Yitong LI1, 2, Yifan SUN2, Jianjie LI3, Ziping WANG3, Yafang TAN2, Ruifu YANG2, Yujing BI1, 2
Affiliations
  • 1 School of Basic Medical Sciences, Anhui Medical University, Hefei, Anhui, China
  • 2 State Key Laboratory of Pathogen and Biosecurity, Academy of Military Medical Sciences, Beijing, China
  • 3 Department of Thoracic Oncology, Peking University Cancer Hospital, Beijing, China
出版时间: 2025-09-04 doi: 10.13343/j.cnki.wsxb.20250126
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摘要
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【目的】 探究具核梭杆菌是否会促进肺癌的发展及其潜在机制。 【方法】 通过细胞实验证实具核梭杆菌能促进肺癌细胞的增殖和转移；通过动物实验验证具核梭杆菌能促进肺癌的发展。对肺癌小鼠的肺泡灌洗液进行16S rRNA基因测序，以及对肺组织进行转录组测序，分析具核梭杆菌对肺癌小鼠肺部菌群的影响及肺组织相关通路的激活情况。 【结果】 具核梭杆菌促进了肺癌上皮细胞A549的增殖和转移。在体内动物实验中，具核梭杆菌感染肺部后肺部结节数量增加，肺组织荧光强度增强。16S rRNA基因测序结果显示，感染小鼠肺部鼠杆状菌属(Muribaculum)、简单螺旋形菌属(Simplicispira)等富集。肺组织转录组结果显示，肺癌小鼠感染具核梭杆菌后激活了IL-17信号通路、细胞因子-细胞因子受体相互作用、金黄色葡萄球菌感染通路、TNF信号通路等与炎症或免疫相关的信号通路。 【结论】 具核梭杆菌感染导致肺部微生物群紊乱，肺组织中多个与炎症和免疫相关的信号通路被激活，从而促进了小鼠肺癌的转移。

具核梭杆菌  /  肺癌  /  肺部微生物群  /  16S rRNA基因测序  /  转录组

[Objective] To investigate whether Fusobacterium nucleatum promotes the development of lung cancer and find out the underlying mechanisms. [Methods] The cell experiment proved that F. nucleatum can promote the proliferation and metastasis of lung cancer cells; Animal experiments showed that F. nucleatum can promote the development of lung cancer; 16S rRNA gene sequencing of alveolar lavage fluid and transcriptome sequencing of lung tissue were performed to analyze the effects of F. nucleatum on the lung flora of mice with lung cancer and the activation of relevant pathways in lung tissue. [Results] The cell experiment showed that F. nucleatum significantly promoted the proliferation and metastasis of A549 cells. The animal experiments confirmed that F. nucleatum infection in the lungs increased the number of nodules and enhanced the fluorescence intensity in the lung tissue. The 16S rRNA gene sequencing revealed the enrichment of Muribaculum and Simplicispira in the lung of infected mice. The transcriptome sequencing results showed that the mouse model of lung cancer activated the interleukin-17 signaling pathway, cytokine-cytokine receptor interactions, Staphylococcus aureus infection pathway, tumor necrosis factor signaling pathway, and other signaling pathways related to inflammation or immunity after being infected with F. nucleatum. [Conclusion] F. nucleatum infection in mice with lung cancer disrupts the microbiota and activates the immunity- and inflammation-related signaling pathways in the lung, thereby promoting the metastasis of lung cancer in mice.

Fusobacterium nucleatum  /  lung cancer  /  lung microbiota  /  16S rRNA gene sequencing  /  transcriptome
李东, 童江辉, 李奕彤, 孙一凡, 李俭杰, 王子平, 谭亚芳, 杨瑞馥, 毕玉晶. 具核梭杆菌促进肺癌发展及其对肺部微生态的影响. 微生物学报, 2025 , 65 (9) : 4001 -4013 . DOI: 10.13343/j.cnki.wsxb.20250126
Dong LI, Jianghui TONG, Yitong LI, Yifan SUN, Jianjie LI, Ziping WANG, Yafang TAN, Ruifu YANG, Yujing BI. Fusobacterium nucleatum promotes lung cancer development and influences the lung microbiota[J]. Acta Microbiologica Sinica, 2025 , 65 (9) : 4001 -4013 . DOI: 10.13343/j.cnki.wsxb.20250126
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肺癌严重威胁着人类的身体健康。每年有100万至800万人被诊断出患有肺癌，其中约100万至600万人死于肺癌[1]。虽然导致肺癌的原因很多，但吸烟仍是主要的风险因素。其他非吸烟因素包括环境和职业暴露、慢性肺部疾病、肺部感染以及不良生活方式等[2]。相关研究发现，在非吸烟人群中肺癌与以慢性气道炎症为特征的疾病密切相关，如慢性阻塞性肺疾病、肺炎衣原体感染、结核分枝杆菌引起的肺结核和呼吸道病毒感染等[3]。这些结果表明，肺部微生物可能在肺癌的发生和发展中发挥重要作用。具核梭杆菌是口腔中常见的革兰氏阴性厌氧菌。它与牙龈卟啉单胞菌及其他微生物共同破坏宿主与微生物之间的平衡，诱发牙周炎[4-5]。随着测序技术的发展，研究人员发现具核梭杆菌也能在结直肠癌组织中富集。进一步研究表明，具核梭杆菌能够促进结直肠癌的发展[6-7]。在ApcMin/+ 小鼠模型中，通过灌胃方式将具核梭杆菌引入小鼠体内，结果显示其会促进结直肠癌的发生[8]。此外，研究人员利用培养组学技术从肺癌患者的肺泡灌洗液中分离出具核梭杆菌，并通过分析口腔微生物、牙周病与肺癌之间的关联，发现具核梭杆菌可能是肺癌标志物的潜在微生物之一[9-11]。
本研究探讨了具核梭杆菌促进肺癌发展的潜在机制。
1 材料与方法
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1.1 实验菌株与细胞
具核梭杆菌(Fusobacterium nucleatum) ATCC 25586购自广东省微生物菌种保藏中心。具核梭杆菌(Fusobacterium nucleatum) strain-9从北京大学肿瘤医院肺癌患者的肺泡灌洗液中分离并在本实验室保存[9]。以上菌株分别命名为Fn-ATCC和Fn-9。
肺癌上皮细胞A549、人单核细胞白血病THP-1细胞、带有绿色荧光蛋白的小鼠Lewis肺癌细胞(LLC-GFP)均为本实验室保存。
1.2 实验动物
选择8周龄、雌性野生型无特定病原体(specific-pathogen-free, SPF)级C57BL/6N小鼠(北京维通利华实验动物技术有限公司)，饲养于军事医学研究院实验动物中心。
1.3 主要试剂和仪器
MTT试剂盒购自北京索莱宝科技有限公司；Transwell孔板购自康宁公司；ELISA试剂盒购自达科为生物技术股份有限公司；RNA提取试剂盒FastPure Cell/Tissue Total RNA Isolation Kit V2、逆转录试剂盒Taq Pro Universal SYBR qPCR Master Mix、HiScript III RT SuperMix for qPCR试剂盒和SYBR Green qPCR Master Mix均购自南京诺唯赞生物科技股份有限公司。
IVIS Spectrum小动物活体光学成像系统、PerkinElmer Operetta CLSTM高内涵成像分析系统均购自PerkinElmer公司。
1.4 细菌生长曲线的测定
将Fn-9和Fn-ATCC菌液的OD600值调至1.0时，菌液浓度分别为5×107 CFU/mL和1×108 CFU/mL。在24孔板中加入2 mL BHI (脑心浸液肉汤)培养基，并加入50 μL上述调好的菌液。培养12 h后取出菌液检测OD600值，之后每隔2 h取出孔板中的菌液测量OD600值，直至36 h结束。将数据导入GraphPad Prism软件中绘制曲线图。
1.5 MTT细胞增殖实验
每孔培养2×104个A549细胞，在37 ℃、5% CO2条件下培养4 h。在平板中分别加入感染复数(multiplicity of infection, MOI)为20或40的Fn-ATCC或Fn-9菌株。细胞与细菌共培养48 h后，使用MTT细胞增殖和细胞毒性检测试剂盒检测细胞，并在酶联免疫测定仪上以490 nm波长测量各孔的吸光度值。PBS用作空白对照。
1.6 Transwell实验
使用带有8 μm孔径膜的24孔Transwell小室评估细胞迁移能力。在Transwell小室的上室加入200 μL A549细胞悬液，下室分别加入800 μL含Fn-9或Fn-ATCC的细菌溶液(细菌重悬于含10%胎牛血清的1640培养基中，MOI为100)、800 μL含10%胎牛血清的1640培养基或200 μL 10 μg/mL脂多糖溶液以吸引细胞迁移。将Transwell小室置于37 ℃、5% CO2培养箱中培养48 h。随后用4%甲醇固定穿透膜的细胞30 min。随用0.1%结晶紫染色25 min，最后在显微镜下拍照。通过观察并拍摄每个孔的5个随机区域，统计每个孔中迁移细胞的数量。每个实验设置4个技术重复孔。4孔计数的平均值作为一次生物实验的结果。生物重复实验重复3次。
1.7 ELISA检测炎症因子的表达
用PMA试剂刺激THP-1细胞48 h后，分别加入Fn-9和Fn-ATCC 2种菌株的上清液，继续培养4 h。按照试剂盒说明书使用ELISA试剂盒检测IL-1β和TNF-α细胞因子的表达水平。
1.8 动物实验
将8周龄雌性C57BL/6N小鼠混养1周后随机分为3组：Fn-ATCC组、Fn-9组和PBS组。将LLC-GFP细胞分别与Fn-ATCC和Fn-9 2种具核梭杆菌的上清液或PBS共同培养12 h。收集细胞后，通过经尾静脉将2.5×106个细胞/只注射到小鼠体内。造模后第7天和第14天使用小动物微喷雾化器将Fn-9、Fn-ATCC或PBS雾化至小鼠支气管分叉处。第21天处死小鼠，提取血清用于细胞因子检测，利用IVIS Spectrum系统检测肺部荧光强度，并对小鼠肺结节进行计数，同时收集肺泡灌洗液。
本研究所有动物实验通过军事医学研究院伦理委员会批准，编号为IACUC-DWZX-2024-015。
1.9 病理检测
将新鲜肺组织在4%多聚甲醛中固定24 h，随后将肺组织包埋于石蜡块中，切成薄片，经苏木精-伊红染色(HE染色)后进行肺组织病理学诊断。
1.10 实时定量聚合酶链式反应(qPCR)
提取肺组织总RNA，使用逆转录试剂盒将RNA逆转录为cDNA。在LightCycler 480 II实时荧光定量PCR系统中，使用SYBR Green qPCR Master Mix进行qPCR检测。数据以2-ΔΔCt方法表示相对表达量的变化倍数。所用引物序列如表1所示。
1.11 小鼠肺泡灌洗液16S rRNA基因测序
动物实验结束后，立即收集小鼠新鲜肺泡灌洗液，迅速放入-80 ℃冰箱保存。将样本送至北京诺禾致源科技股份有限公司进行16S rRNA基因测序。
1.12 肺组织转录组测序
将肺组织样本保存于-80 ℃冰箱，随后送至北京诺禾致源科技股份有限公司进行转录组测序。
1.13 数据分析
对于多组数据的比较，首先确认每组数据是否符合正态分布及方差齐性。若数据呈正态分布且方差齐性，则采用单因素方差分析(analysis of variance, ANOVA)或双尾非配对t检验(two-tailed unpaired t-test)；若数据不符合正态分布或方差不齐，则采用Kruskal-Wallis检验进行分析。显著性水平设定为P<0.05。所有统计分析均使用GraphPad Prism软件(v9.0.0)完成。
2 结果与分析
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2.1 具核梭杆菌体外促细胞增殖和细胞因子分泌
生长曲线显示，2株具核梭杆菌在生长30 h后达到平稳期(图1A)，处于对数期的细菌被用于后续实验。用2种菌株感染A549细胞48 h，与空白对照组相比，在MOI=40和MOI=20的条件下，Fn-ATCC能显著促进A549细胞的增殖，而当MOI=20时Fn-9和Fn-ATCC均能显著促进A549细胞的增殖(图1B)。在Transwell实验中，当MOI=100时与空白对照组相比，经具核梭杆菌刺激后的A549细胞过膜数量显著增加(图1C、1D)。
THP-1细胞经2株菌株的培养上清刺激后，细胞分泌的TNF-α与对照组(大肠杆菌DH5α刺激组)相比显著增加(图1E)，而IL-1β的分泌量差异无统计学意义(图1F)。这些结果表明，在体外实验中具核梭杆菌可促进肺上皮细胞的增殖和转移，并刺激免疫细胞分泌细胞因子。
2.2 具核梭杆菌促进小鼠肺癌转移
采用C57小鼠进行尾静脉注射造模实验，通过肺部递送2种具核梭杆菌或PBS (图2A)。造模成功后收集3组小鼠的肺组织，并使用IVIS Spectrum系统进行拍照(图2B)。结果显示，Fn-9组和Fn-ATCC组肺组织的荧光强度显著高于PBS组(图2C)。统计肺结节数量发现，Fn-9组和Fn-ATCC组的数量显著高于对照组(图2D)。同时，2组的肺器官系数也均高于PBS组(图2E)。这些结果表明，具核梭杆菌可能促进了肿瘤细胞的增殖与转移。
为了进一步了解3组小鼠的肺损伤情况，对肺切片进行了HE染色分析。病理结果显示，3组小鼠的肺部均有炎症细胞浸润，但Fn-9组和Fn-ATCC组的肺泡间隔破坏更为严重，部分气道黏膜上皮也出现萎缩(图3A)。值得注意的是，2组的肺肿瘤面积明显增大，肺结节数量明显增多(图3A)。同样地，qPCR检测3组小鼠肺组织中炎症因子的表达发现，Fn-9组和Fn-ATCC组的IL-1β和TNF-α表达量更高(图3B、3C)，而IL-6的表达在3组之间无显著差异(图3D)。综上所述，在动物水平上证明了具核梭杆菌促进了肺癌的转移和进展。
2.3 具核梭杆菌对小鼠肺部微生物群的影响
收集上述各组及正常小鼠的肺泡灌洗液，探讨具核梭杆菌对肺微生物群的影响。在属水平，Fn-9组和Fn-ATCC组细菌组成明显不同于PBS组(图4A)。Chao1指数表明，Fn-9组的α多样性显著高于空白组(图4B)。然而，4组间的β多样性无显著差异(图4C)。MetagenomeSeq分析显示，Fn-9组和Fn-ATCC组中Muribaculum的丰度显著低于PBS组，而Fn-9组中Simplicispira的丰度显著高于PBS组(图4D)。
2.4 肺组织转录组分析
转录组测序用于描述肺组织变化的特征。主成分分析(principal components analysis, PCA)结果显示，Fn-9组、Fn-ATCC组和PBS组的转录组基因存在显著差异(图5A)。进一步通过火山图比较其差异基因的变化，发现与PBS组相比，Fn-ATCC组共有1 855个差异基因表达上调，1 185个差异基因表达下调(图5B)；而在Fn-9组与PBS组的比较中，Fn-9组共有864个差异基因表达上调，640个差异基因表达下调(图5C)。随后，分析了3组小鼠肺组织中KEGG通路差异基因的富集情况。在Fn-9组、Fn-ATCC组和PBS组的比较中，差异基因主要富集在IL-17信号通路、细胞因子-细胞因子受体相互作用、细胞周期和运动蛋白等信号通路上，这提示Fn-9组和Fn-ATCC组2种菌株可能通过调节免疫反应来促进肺癌的进展(图5D、5E)。
3 讨论与结论
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传统上，肺一直被认为是一个无菌器官，随着分子测序技术的发展证实肺中实际上存在少量微生物，这可能是由于口腔、上呼吸道、下呼吸道和肺直接接触导致呼吸道或口腔中的微生物进入呼吸道并在肺中定殖[12-14]。根据目前的理论，大多数微生物通过上呼吸道以及微量吸入的方式进入肺部[14-16]。相比之下，某些微生物已被证实会增加患肺癌的风险[17]。作为口腔中常见的条件致病菌，具核梭杆菌已被证明与多种疾病相关[18-20]。具核梭杆菌与牙龈卟啉单胞菌协同作用可诱发牙周炎，并促进口腔癌的发展[4,21-22]。除口腔疾病外，研究人员还在结直肠癌患者的组织中检测到高丰度的具核梭杆菌[23-24]，并进一步证实具核梭杆菌对结直肠癌有促进作用[6,25]。从作用机制上看，具核梭杆菌能激活Apcmin/+ 小鼠的NF-κB信号通路，并诱导TNF、IL-6、IL-8和IL-1β等促癌通路[8,26]。然而，目前尚无直接证据表明具核梭杆菌与肺癌有关。
本研究首先选择了2种不同来源的具核梭杆菌菌株：一种是ATCC 25586标准菌株，另一种是从肺癌患者肺泡灌洗液中提取的具核梭杆菌动物亚种。与其他亚种相比，动物亚种具核梭杆菌在结直肠癌生态区域中占主导地位[27]。在动物实验中，发现向小鼠肺部递送具核梭杆菌可促进肺结节数量的增加，并且实验组的肺组织在荧光成像下比对照组的荧光强度更强。通过qPCR检测发现，小鼠肺组织中TNF-α和IL-1β基因的表达显著增加。研究也表明，TNF-α在肺癌的上皮-间质转化(epithelial-mesenchymal transition, EMT)、侵袭、转移和进展过程中起着重要作用，这在TNFR2-KO小鼠植入Lewis肺癌(LLC)模型中也得到了证实[28-29]。IL-1β也被证实在肿瘤微环境中的表达升高，并在肺癌的转移发展中发挥重要作用[30-31]。
根据肺泡灌洗液的16S rRNA基因测序结果，在实验组和PBS组之间发现了2个不同的属：简单螺旋形菌属(Simplicispira)和鼠杆状菌属(Muribaculum)。简单螺旋形菌属是一种常见于土壤、水库和污泥中的细菌，尚未见与癌症相关的报道[32-33]。鼠杆状菌属与肠道微生物群中的脂质代谢以及结直肠癌中的肠道微生物菌群失调有关[34-35]。肺组织转录组KEGG结果表明，具核梭杆菌可能通过免疫相关信号通路促进肺癌转移。细胞因子-细胞因子受体相互作用通路与肿瘤密切相关，研究证实齐墩果酸可通过调节细胞因子-细胞因子受体相互作用通路来调控乳酸菌抑制肿瘤的发展，TRIM6也通过该通路促进胶质瘤的发展[36-37]。同样地，TNF信号通路也参与了细胞凋亡及其对癌症疾病的影响[38-39]。具核梭杆菌进入小鼠肺部后，激活了金黄色葡萄球菌感染途径，而金黄色葡萄球菌具有很强的促炎能力，能引起肺炎等疾病[40-41]。肺部炎症会诱发肺部微环境的改变，从而导致肺癌病变[42]。此外，尽管在结直肠癌研究中已显示具核梭杆菌能够进入肠上皮细胞发挥作用，但对于具核梭杆菌是否能进入肺上皮细胞尚无相关报道，这也是后续机制研究的方向之一。
综上所述，通过细胞实验验证了具核梭杆菌能促进A549细胞的增殖和转移，并通过体内实验进一步验证了它能促进肺癌的转移和恶化。根据16S rRNA基因测序结果和肺组织转录组结果，具核梭杆菌进入小鼠肺部后扰乱了肺部菌群的组成，激活了肺组织中多个与炎症和免疫相关的信号通路，这可能是具核梭杆菌促进肺癌的潜在机制。
基金
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  • 国家重点研发计划(2022YFC2601200)
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2025年第65卷第9期
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doi: 10.13343/j.cnki.wsxb.20250126
  • 接收时间：2025-02-21
  • 首发时间：2026-02-07
  • 出版时间：2025-09-04
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  • 收稿日期：2025-02-21
  • 录用日期：2025-04-19
基金
National Key Research and Development Program of China(2022YFC2601200)
国家重点研发计划(2022YFC2601200)
作者信息
    1 安徽医科大学 基础医学院，安徽 合肥
    2 军事医学研究院，病原微生物与生物安全全国重点实验室，北京
    3 北京大学肿瘤医院 胸部肿瘤内一科，北京
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2种不同金属材料的力学参数
科
Family		 属数
Number of
genus		 种数
Number of
species		 占总种数比例
Percentage of
total species (%)		 属
Genus		 种数
Number of
species		 占总种数比例
Percentage of total
species (%)
鹅膏菌科Amanitaceae 2 11 5.26 鹅膏菌属 Amanita 10 4.78
小菇科 Mycenaceae 2 12 5.74 丝盖伞属 Inocybe 5 2.39
多孔菌科 Polyporaceae 8 14 6.70 蜡蘑属 Laccaria 5 2.39
红菇科 Russulaceae 3 23 11.00 小皮伞属 Marasmius 6 2.87
小菇属 Mycena 11 5.26
光柄菇属 Pluteus 5 2.39
红菇属 Russula 17 8.13
栓菌属 Trametes 5 2.39
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