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Article(id=1241065987840209866, tenantId=1146029695717560320, journalId=1227665162245664772, issueId=1241065978004557893, articleNumber=null, orderNo=null, doi=10.20043/j.cnki.MPM.202409198, pmid=null, cstr=null, oa=null, hot=null, price=null, onlineType=0, articleFormat=0, articleType=null, articleTypeStr=null, receivedDate=1725897600000, receivedDateStr=2024-09-10, revisedDate=null, revisedDateStr=null, acceptedDate=null, acceptedDateStr=null, onlineDate=1773822789392, onlineDateStr=2026-03-18, pubDate=1740412800000, pubDateStr=2025-02-25, doiRegisterDate=null, doiRegisterDateStr=null, onlineIssueDate=1773822789392, onlineIssueDateStr=2026-03-18, onlineJustAcceptDate=null, onlineJustAcceptDateStr=null, onlineFirstDate=null, onlineFirstDateStr=null, sourceXml=null, magXml=null, createTime=1773822789392, creator=13701087609, updateTime=1773822789392, updator=13701087609, issue=Issue{id=1241065978004557893, tenantId=1146029695717560320, journalId=1227665162245664772, year='2025', volume='52', issue='4', pageStart='577', pageEnd='768', issueExtLink='null', onlineDate='null', pubDate='null', beforeIssueId=null, nextIssueId=null, price=null, status=1, issueComplete=1, articleOrder=1, issueType=-1, specialIssue=null, createTime=1773822787047, creator=13701087609, updateTime=1773823194927, updator=13701087609, preIssue=null, nextIssue=null, ext={EN=IssueExt(id=1241067688831808347, tenantId=1146029695717560320, journalId=1227665162245664772, issueId=1241065978004557893, language=EN, specialIssueTitle=, coverIllustrator=null, specialIssueEditor=, specialIssueAbout=), CN=IssueExt(id=1241067688831808348, tenantId=1146029695717560320, journalId=1227665162245664772, issueId=1241065978004557893, language=CN, specialIssueTitle=, coverIllustrator=null, specialIssueEditor=, specialIssueAbout=)}, issueFiles=null}, startPage=629, endPage=635, ext={EN=ArticleExt(id=1241065988289000431, articleId=1241065987840209866, tenantId=1146029695717560320, journalId=1227665162245664772, language=EN, title=Expression of matrix metalloproteinase 14 in silicosis and its regulation of epithelial-mesenchymal transition, columnId=1228016570660745413, journalTitle=Modern Preventive Medicine, columnName=Environmental and Occupational Health, runingTitle=null, highlight=null, articleAbstract=
Objective

To investigate the role of the potential pathogenic molecule MMP14 in silicosis.

Methods

18 SPF male C57 mice were randomly divided into control and silicosis group, and 16 human specimens from the pneumoconiosis cohort of the Fourth Hospital of West China, Sichuan University. Single-cell sequencing analysis was used to identify differentially expressed genes. A silicosis mouse model was induced by silica dioxide using a non-exposure tracheal instillation method. Hematoxylin-eosin staining and Masson staining were employed to assess the degree of inflammation and fibrosis in mouse lung tissues. Real-time quantitative polymerase chain reaction, western blot, and immunohistochemistry were used to verify the expression of MMP14 and N-cadherin in the lung tissues. Knockdown of MMP14 in epithelial cells (16HBE) was achieved by small interfering RNA, to further verify the expression of N-cadherin. Cell wound healing assays were used to assess the cell migration after MMP14 knockdown.

Results

MMP14 being selected as a potential pathogenic molecule by single-cell sequencing analysis. Compared with the normal control group, the expression of MMP14 and N-cadherin in silicosis lung tissues was significantly increased 3.78 and 2.42 times, respectively (P<0.001). Knockdown of MMP14 in 16HBE cells stimulated by SiO2 led to the downregulation of N-cadherin by about 30% (P<0.001) and inhibition of cell migration, which area was reduced by 50% (P<0.001).

Conclusion

MMP14 activates the expression of N-cadherin, regulates the epithelial-mesenchymal transition (EMT) process, and promotes silica-induced pulmonary fibrosis.

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目的

通过建立小鼠矽肺模型，探讨潜在致病分子MMP14在二氧化硅致肺损伤中的作用。

方法

SPF级雄性C57小鼠18只随机分为对照组和矽肺模型组组；人体标本数量16例，来自四川大学华西第四医院尘肺队列；采用单细胞测序技术分析差异表达基因，筛选潜在致病分子，采用非暴露式气管滴注法构建小鼠矽肺模型，通过苏木精-伊红染色和Masson染色评估小鼠肺组织炎症和纤维化程度。采用实时荧光定量聚合酶链式反应、蛋白免疫印迹和免疫组织化学等技术验证小鼠矽肺模型肺组织及正常对照肺组织中MMP14及N-cadherin的表达。通过小干扰RNA敲减上皮细胞16HBE中的MMP14，验证N-cadherin表达，并采用细胞划痕实验验证敲减MMP14对细胞迁移的调控。

结果

单细胞测序结果显示MMP14为潜在致病分子，与正常对照组相比，小鼠矽肺模型组肺组织中MMP14及N-cadherin表达分别增高3.78和2.42倍（P<0.001）。在SiO2刺激的16HBE细胞中敲减MMP14，可下调N-cadherin的表达约30%（P<0.001），同时抑制16HBE细胞迁移，细胞迁移面积降低50%（P<0.001）。

结论

MMP14激活N-cadherin表达，调控上皮细胞EMT过程，促进二氧化硅诱导的肺纤维化发生。

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许云屹，E-mail：
, copyrightStatement=本刊刊出的所有文章不代表中华预防医学会和本刊编委会的观点，除非特别声明。, copyrightOwner=中华预防医学会和四川大学华西公共卫生学院, extLink=null, articleAbsUrl=null, sourceXml=O4rsCWXiw1dxOK1Ulogi6w==, magXml=eJkxgtj9nOUa0dtNHzHOtA==, pdfUrl=null, pdf=tz+GiYYiIvjEcQV0vZ4k4Q==, pdfFileSize=1906034, pdfExtLink=null, richHtmlUrl=null, mobilePdfUrl=null, reviewReport=null, pdfFirstPage=null, abstractGraph=mAok41IbnL+efMGXoeHlpw==, abstractGraphContent=null, abstractVideo=null, citation=null, cebUrl=null, magXmlContent=mngT1LTPSU8wdlbvr55sCw==, mapNumber=null, authorCompany=null, fund=null, authors=

丁琼桦（1999—），女，硕士在读，研究方向：卫生毒理学

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丁琼桦（1999—），女，硕士在读，研究方向：卫生毒理学

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丁琼桦（1999—），女，硕士在读，研究方向：卫生毒理学

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Oncotarget, 2017, 8(41): 71024-71037., articleTitle=NOGO-B promotes EMT in lung fibrosis via MMP14 mediates free TGF-beta1 formation, refAbstract=null)], funds=[Fund(id=1241066000804803130, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1241065987840209866, awardId=82373548; U22A20359; U23A20495, language=CN, fundingSource=国家自然科学基金(82373548; U22A20359; U23A20495), fundOrder=null, country=null), Fund(id=1241066000926437950, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1241065987840209866, awardId=2023NSFSC1731; 2024NSFSC1258, language=CN, fundingSource=四川省科学技术厅基金(2023NSFSC1731; 2024NSFSC1258), fundOrder=null, country=null), Fund(id=1241066001014518338, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1241065987840209866, awardId=2022CDDZ-14, language=CN, fundingSource=四川大学与达州市战略合作项目(2022CDDZ-14), fundOrder=null, country=null)], companyList=[AuthorCompany(id=1241065991820603567, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1241065987840209866, xref=null, ext=[AuthorCompanyExt(id=1241065991828992180, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1241065987840209866, companyId=1241065991820603567, language=EN, country=null, province=null, city=null, postcode=null, companyName=null, departmentName=null, remark=Sichuan Provincial Key Laboratory of Molecular Toxicology, West China School of Public Health /West China Fourth Hospital, Sichuan University, Chengdu, Sichuan 610041, China), AuthorCompanyExt(id=1241065991837380787, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1241065987840209866, companyId=1241065991820603567, language=CN, country=null, province=null, city=null, postcode=null, companyName=null, departmentName=null, remark=四川大学华西公共卫生学院/华西第四医院，分子毒理四川省教育厅重点实验室，四川 成都 610041)])], figs=[ArticleFig(id=1241065997810069992, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1241065987840209866, language=EN, label=Fig.1, caption=Elevated MMP14 expression in silicosis, figureFileSmall=yvitI4Jsz5NKZhjaMXdpjg==, figureFileBig=mAok41IbnL+efMGXoeHlpw==, tableContent=null), ArticleFig(id=1241065997906538991, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1241065987840209866, language=CN, label=图1, caption=MMP14在矽肺组织中表达增高

注：A，单细胞测序结果显示，在尘肺患者肺组织穿刺样本中MMP14表达增高。B，单细胞测序结果显示在小鼠矽肺模型组中MMP14表达增高。基因表达范围面积越大，代表相对表达范围越大。基因表达强度颜色越深，代表相对表达强度越高。

, figureFileSmall=yvitI4Jsz5NKZhjaMXdpjg==, figureFileBig=mAok41IbnL+efMGXoeHlpw==, tableContent=null), ArticleFig(id=1241065999580066299, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1241065987840209866, language=EN, label=Fig.2, caption=Histopathological staining of the silicosis mouse lungs, figureFileSmall=15sm4QsPaD+r9IWw2bWEow==, figureFileBig=oKk+Kd2Ga+ip44zhkGNpow==, tableContent=null), ArticleFig(id=1241065999705895428, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1241065987840209866, language=CN, label=图2, caption=小鼠矽肺模型肺组织病理染色

注：A，为HE染色（放大倍数分别为5×和20×），结果显示，与对照组相比，模型组出现炎性细胞浸润、肺泡正常生理结构破坏。B，为 Szapiel炎性评分。C，为Masson染色（放大倍数分别为5×和20×），模型组可见胶原纤维沉积。D，为胶原纤维面积占比。 ***与对照组相比，P<0.001。

, figureFileSmall=15sm4QsPaD+r9IWw2bWEow==, figureFileBig=oKk+Kd2Ga+ip44zhkGNpow==, tableContent=null), ArticleFig(id=1241065999814947338, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1241065987840209866, language=EN, label=Fig.3, caption=MMP14 overexpression in lung of the 12-week mouse silicosis, figureFileSmall=FW5gebs/NgZ9jgVTH+3aUw==, figureFileBig=IvB50Kt1poqeofHCQUZ9SQ==, tableContent=null), ArticleFig(id=1241065999940776466, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1241065987840209866, language=CN, label=图3, caption=MMP14在12周小鼠矽肺模型肺组织中高表达

注：A-B，12周小鼠矽肺模型肺组织中MMP14、N-cadherin mRNA表达增高。C，WB显示，MMP14蛋白表达在矽肺模型组显著增高。D，WB蛋白半定量分析。E，免疫组织化学染色显示（放大倍数为10x和40x），MMP14在小鼠矽肺模型组肺组织纤维结节区域呈阳性表达。F，MMP14阳性表达强度和面积半定量分析。 ***与对照组相比，P<0.001 。

, figureFileSmall=FW5gebs/NgZ9jgVTH+3aUw==, figureFileBig=IvB50Kt1poqeofHCQUZ9SQ==, tableContent=null), ArticleFig(id=1241066000049828375, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1241065987840209866, language=EN, label=Fig.4, caption=MMP14 enhances the expression of N-cadherin, figureFileSmall=MjJ8O43wgw/sgbEbx4+CTQ==, figureFileBig=/eMRRBclfiGEn6JYmeoMoA==, tableContent=null), ArticleFig(id=1241066000179851804, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1241065987840209866, language=CN, label=图4, caption=MMP14促进N-cadherin表达

注：A，WB图示si-MMP14可同时抑制MMP14和N-cadherin蛋白表达。B，为WB蛋白半定量分析。*与si-NC组相比，P<0.05；***与si-NC组相比，P<0.001。

, figureFileSmall=MjJ8O43wgw/sgbEbx4+CTQ==, figureFileBig=/eMRRBclfiGEn6JYmeoMoA==, tableContent=null), ArticleFig(id=1241066000280515108, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1241065987840209866, language=EN, label=Fig.5, caption=Knockdown of MMP14 in 16HBE inhibits SiO2-induced cell migration, figureFileSmall=KK2cQyrtqKyTRTsik3ffGg==, figureFileBig=LUgdr2Vxz+6AYl9zGkCNjQ==, tableContent=null), ArticleFig(id=1241066000397955625, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1241065987840209866, language=CN, label=图5, caption=敲减MMP14抑制SiO2诱导的上皮细胞迁移

注：A，在上皮细胞16HBE中，si-MMP14可显著抑制SiO2诱导的MMP14表达。B，细胞划痕实验显示，敲低MMP14可抑制SiO2诱导的16HBE细胞迁移。C，上皮细胞迁移面积量化结果。*两组相比，P<0.05；**两组相比，P<0.01；***两组相比，P<0.001。

, figureFileSmall=KK2cQyrtqKyTRTsik3ffGg==, figureFileBig=LUgdr2Vxz+6AYl9zGkCNjQ==, tableContent=null), ArticleFig(id=1241066000498618927, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1241065987840209866, language=EN, label=Table 1, caption=

Sequences of primers used for RT-qPCR

, figureFileSmall=null, figureFileBig=null, tableContent=
基因名称引物序列(5’- 3’)（上游F，下游R ）
β-actin(鼠)F：GTGACGTTGACATCCGTAAAGA
R：GCCGGACTCATCGTACTCC
Mmp14(鼠)F：CTCCCCCTGCTCACGCTT
R：TCCCCTGGAGGTAGGTAGCC
N-cadherin(鼠)F：AGCCAACCTTAACTGAGGAGT
R：GGCAAGTTGATTGGAGGGATG
β-actin(人)F：CTGGCACCACACCTTCTACAATG
R：CCTCGTAGATGGGCACAGTGTG
Mmp14(人)F：TAAACCCAAAAACCCCACCTA
R：TTGCCATCCTTCCTCTCGTAG
N-cadherin(人)F：AGCCAACCTTAACTGAGGAGT
R：GGCAAGTTGATTGGAGGGATG
), ArticleFig(id=1241066000637030967, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1241065987840209866, language=CN, label=表1, caption=

引物序列

, figureFileSmall=null, figureFileBig=null, tableContent=
基因名称引物序列(5’- 3’)（上游F，下游R ）
β-actin(鼠)F：GTGACGTTGACATCCGTAAAGA
R：GCCGGACTCATCGTACTCC
Mmp14(鼠)F：CTCCCCCTGCTCACGCTT
R：TCCCCTGGAGGTAGGTAGCC
N-cadherin(鼠)F：AGCCAACCTTAACTGAGGAGT
R：GGCAAGTTGATTGGAGGGATG
β-actin(人)F：CTGGCACCACACCTTCTACAATG
R：CCTCGTAGATGGGCACAGTGTG
Mmp14(人)F：TAAACCCAAAAACCCCACCTA
R：TTGCCATCCTTCCTCTCGTAG
N-cadherin(人)F：AGCCAACCTTAACTGAGGAGT
R：GGCAAGTTGATTGGAGGGATG
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基质金属蛋白酶14在矽肺中的表达及其对上皮间充质转化的调控作用
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丁琼桦 , 马子怡 , 钱蕊 , 陈叙汐 , 王礼群 , 陈晴 , 肖月 , 姚于勤 , 许云屹
现代预防医学 | 环境与职业卫生 2025,52(4): 629-635
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现代预防医学 | 环境与职业卫生 2025, 52(4): 629-635
基质金属蛋白酶14在矽肺中的表达及其对上皮间充质转化的调控作用
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丁琼桦, 马子怡, 钱蕊, 陈叙汐, 王礼群, 陈晴, 肖月, 姚于勤, 许云屹
作者信息
  • 四川大学华西公共卫生学院/华西第四医院，分子毒理四川省教育厅重点实验室，四川 成都 610041

    • 丁琼桦（1999—），女，硕士在读，研究方向：卫生毒理学

通讯作者:

许云屹，E-mail：
Expression of matrix metalloproteinase 14 in silicosis and its regulation of epithelial-mesenchymal transition
Qiong-hua DING, Zi-yi MA, Rui QIAN, Xu-xi CHEN, Li-qun WANG, Qing CHEN, Yue XIAO, Yu-qin YAO, Yun-yi XU
Affiliations
  • Sichuan Provincial Key Laboratory of Molecular Toxicology, West China School of Public Health /West China Fourth Hospital, Sichuan University, Chengdu, Sichuan 610041, China
出版时间: 2025-02-25 doi: 10.20043/j.cnki.MPM.202409198
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摘要
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目的

通过建立小鼠矽肺模型，探讨潜在致病分子MMP14在二氧化硅致肺损伤中的作用。

方法

SPF级雄性C57小鼠18只随机分为对照组和矽肺模型组组；人体标本数量16例，来自四川大学华西第四医院尘肺队列；采用单细胞测序技术分析差异表达基因，筛选潜在致病分子，采用非暴露式气管滴注法构建小鼠矽肺模型，通过苏木精-伊红染色和Masson染色评估小鼠肺组织炎症和纤维化程度。采用实时荧光定量聚合酶链式反应、蛋白免疫印迹和免疫组织化学等技术验证小鼠矽肺模型肺组织及正常对照肺组织中MMP14及N-cadherin的表达。通过小干扰RNA敲减上皮细胞16HBE中的MMP14，验证N-cadherin表达，并采用细胞划痕实验验证敲减MMP14对细胞迁移的调控。

结果

单细胞测序结果显示MMP14为潜在致病分子，与正常对照组相比，小鼠矽肺模型组肺组织中MMP14及N-cadherin表达分别增高3.78和2.42倍（P<0.001）。在SiO2刺激的16HBE细胞中敲减MMP14，可下调N-cadherin的表达约30%（P<0.001），同时抑制16HBE细胞迁移，细胞迁移面积降低50%（P<0.001）。

结论

MMP14激活N-cadherin表达，调控上皮细胞EMT过程，促进二氧化硅诱导的肺纤维化发生。

矽肺  /  肺纤维化  /  基质金属蛋白酶14  /  上皮间充质转化  /  神经钙黏蛋白
Objective

To investigate the role of the potential pathogenic molecule MMP14 in silicosis.

Methods

18 SPF male C57 mice were randomly divided into control and silicosis group, and 16 human specimens from the pneumoconiosis cohort of the Fourth Hospital of West China, Sichuan University. Single-cell sequencing analysis was used to identify differentially expressed genes. A silicosis mouse model was induced by silica dioxide using a non-exposure tracheal instillation method. Hematoxylin-eosin staining and Masson staining were employed to assess the degree of inflammation and fibrosis in mouse lung tissues. Real-time quantitative polymerase chain reaction, western blot, and immunohistochemistry were used to verify the expression of MMP14 and N-cadherin in the lung tissues. Knockdown of MMP14 in epithelial cells (16HBE) was achieved by small interfering RNA, to further verify the expression of N-cadherin. Cell wound healing assays were used to assess the cell migration after MMP14 knockdown.

Results

MMP14 being selected as a potential pathogenic molecule by single-cell sequencing analysis. Compared with the normal control group, the expression of MMP14 and N-cadherin in silicosis lung tissues was significantly increased 3.78 and 2.42 times, respectively (P<0.001). Knockdown of MMP14 in 16HBE cells stimulated by SiO2 led to the downregulation of N-cadherin by about 30% (P<0.001) and inhibition of cell migration, which area was reduced by 50% (P<0.001).

Conclusion

MMP14 activates the expression of N-cadherin, regulates the epithelial-mesenchymal transition (EMT) process, and promotes silica-induced pulmonary fibrosis.

Pneumoconiosis  /  Pulmonary fibrosis  /  Matrix metalloproteinase 14  /  Epithelial-mesenchymal transition  /  N-cadherin
丁琼桦, 马子怡, 钱蕊, 陈叙汐, 王礼群, 陈晴, 肖月, 姚于勤, 许云屹. 基质金属蛋白酶14在矽肺中的表达及其对上皮间充质转化的调控作用. 现代预防医学, 2025 , 52 (4) : 629 -635 . DOI: 10.20043/j.cnki.MPM.202409198
Qiong-hua DING, Zi-yi MA, Rui QIAN, Xu-xi CHEN, Li-qun WANG, Qing CHEN, Yue XIAO, Yu-qin YAO, Yun-yi XU. Expression of matrix metalloproteinase 14 in silicosis and its regulation of epithelial-mesenchymal transition[J]. Modern Preventive Medicine, 2025 , 52 (4) : 629 -635 . DOI: 10.20043/j.cnki.MPM.202409198
正文
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尘肺病是在世界范围内普遍发生的职业病，我国是受尘肺病影响最严重的国家之一，其中矽肺是最常见且危害最严重的类型[1]。矽肺是由长期吸入大量游离二氧化硅（Silicon dioxide，SiO2）粉尘引起的，以肺部持续性炎症和不可逆纤维化为特征的发展性肺部疾病[2]。在形态学上，可观察到吞噬SiO2颗粒的巨噬细胞聚集，SiO2对气道上皮细胞的持续损伤，肺泡腔正常生理结构的破坏及细支气管周围纤维化[3]。
基质金属蛋白酶(Matrix metalloproteinases，MMPs )参与维持细胞外基质( Extracellular matrix，ECM )和组织修复，可分为6类：包括胶原酶、明胶酶、基质酶、基质溶解素、金属弹性蛋白酶和膜型MMPs[4]。基质金属蛋白酶14（Matrix metalloproteinase 14，MMP14），又称MT1-MMP，是最早被发现的基质金属蛋白酶之一，是一类跨膜蛋白，与细胞运动密切相关[5]。MMP14影响细胞迁移和侵袭，可下调E-cadherin，上调N-cadherin，促进上皮间充质转化（Epithelial-Mesenchymal Transition，EMT）发生，在骨骼发育、伤口愈合、炎症反应等多种生理功能中具有重要作用[6]。矽肺疾病进展中，上皮细胞出现EMT现象[3]，即失去上皮表型（E-cadherin），间充质细胞标志物表达增加（N-cadherin、Vimentin、α-SMA等），分泌胶原蛋白和ECM促进矽肺纤维化的形成[7]。多项研究表明，抑制上皮细胞EMT，可有效减缓肺纤维化发生[8-10]。上皮细胞EMT与矽肺纤维化发生密切相关，而MMP14高表达则促使上皮细胞发生EMT，因此MMP14与上皮细胞作用机制的发现为今后缓解矽肺治疗进展提供了新的途径。本研究旨在探索MMP14在矽肺中的表达及其发挥作用的潜在分子调控机制。
1　材料与方法
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1.1　动物与实验样本
雄性C57/BL小鼠，6~8周龄，体重23±2 g，购自上海维通利华有限公司，饲养于四川大学华西公共卫生学院SPF级实验动物中心。16例人肺组织穿刺样本自四川大学华西第四医院尘肺队列样本采集获得，-80 ℃保存。动物及人肺组织穿刺样本采集均通过四川大学医学伦理委员会批准（伦理号：GwII2024103）。
1.2　试剂
SiO2粉尘购自德国默克生物科技公司（4808-60-7）；兔抗MMP14单抗（A0067）购自武汉爱博泰克生物科技有限公司，鼠抗GAPDH单抗（60004-1-Ig）购自武汉三鹰生物技术有限公司；兔抗N-cadherin单抗（ET1607-37）、山羊抗兔HRP标记二抗（HA1001）、山羊抗鼠HRP标记二抗（HA1006）购自杭州华安生物有限公司；通用型快速封闭液（10133-2）购自陕西普罗安蒂生物科技发展有限公司；试剂Trizol购自宝日医生物技术有限公司；RNA逆转录试剂（RK20429）购自武汉爱博泰克生物科技有限公司；实时荧光定量PCR试剂盒（Q712-01）购自南京诺唯赞生物科技股份有限公司；双敏化学发光试剂（KF8005）购自江苏亲科生物研究中心有限公司；胶原蛋白酶（10103578001）购自德国Sigma Aldrich®公司；弹性蛋白酶（LS002292）、中性蛋白酶（LS02100）购自美国Worthington Biochemical公司。
1.3　仪器
倒置显微镜（奥林巴斯CKX51）、iBrightTMCL1500成像系统（Thermo A44114）、PCR仪（BIO-RAD C1000）、全切片扫描系统 Pannoramic MIDI、实时定量PCR仪（Thermo Fisher QuantStudio 3）。
1.4　方法
1.4.1　单细胞测序
将组织样本约10 mg放入含有胶原蛋白酶：弹性蛋白酶：中性蛋白酶：CaCl2：DNA酶：DPBS为60：100：100：5：5：730的1 ml混合酶液中进行冰上解离，每3 min用1 ml移液枪将其研磨10次。每2 min摇动3~5次以重新悬浮。培养45 min后，将上清液用无菌30 μm滤膜过滤，用15 ml预冷的PBS/BSA 0.04%冲洗滤膜。将流出液置于4 ℃，650 g离心5 min后将上清液取出，并将其与回收的细胞混合。将细胞颗粒重新悬浮在14 ml预冷的PBS/BSA 0.04%的锥形瓶中。将剩余组织重复上述步骤。将细胞重新悬浮在250 μl预冷的PBS/BSA 0.04%中。用台盼蓝血球计数仪分析细胞活率和细胞含量。
1.4.2　小鼠矽肺模型构建
将18只小鼠随机分为两组，模型组采用非暴露式气管滴注160 mg/kg无菌二氧化硅悬浊液（50 mg/ml），对照组给予同等体积无菌生理盐水[11]。自造模日开始计算，在12周结束时处死。收集小鼠肺组织用于后续实验。小鼠肺组织及人肺组织单细胞测序由杭州联川生物技术股份有限公司完成。
1.4.3　组织病理学
收集的小鼠肺组织用4%多聚甲醛固定，进行石蜡包埋并切成5 μm的切片。使用苏木精-伊红（HE）染色评估小鼠炎性状况，采用Szapiel标准[12]进行炎性评分。Masson三色染色技术评价肺组织纤维化情况，采用Image J对胶原纤维区域进行识别，评价胶原纤维蓝色区域占全肺染色比重。采用免疫组化（Immunohistochemistry，IHC）技术评价MMP14蛋白在小鼠矽肺模型肺组织中的表达情况，MMP14抗体浓度为1：3 000，采用Image J对阳性面积及强度进行分析，计算阳性率。采用病理组织切片扫描系统（Pannoramic MIDI，3DHISTECH）对切片进行扫描。
1.4.4　细胞培养及转染
人支气管上皮细胞16HBE在含有10%胎牛血清的DMEM培养基中培养，当细胞密度达到约90%时胰酶消化，取4×105个细胞接种于6孔板。12 h贴壁后更换无血清DMEM培养基饥饿6 h，将Lipo3000与无血清培养基DMEM混合并加入相应siRNA，转染后6 h换液，在24 h时收集细胞。将细胞分为对照组（si-NC）、敲减组（si-MMP14）、SiO2对照组200 mg/ml（SiO2 + si-NC）组以及SiO2 200 mg/ml敲减组（SiO2 + si-MMP14）。siRNA购自广州市锐博生物科技有限公司，100 nM转染（si-MMP14-1：5’-GGTCTCAAATGGCAACATA-3’ ；si-MMP14-2：5’-GCAAATTCGTCTTCTTCAA-3’ ；si-MMP14-3：5’-GGCCTTCTGTTCCTGATAA-3’ ；si-NC：5’-ATTATCTGGCTTAAATTGCCA-3’ ）。
1.4.5　细胞划痕实验
在16HBE细胞转染6 h后，用200 μl枪尖在细胞单层进行划痕。使用数码相机系统和显微镜拍摄划痕照片(× 4放大)。将细胞培养12 h~24 h，在相应时间拍摄照片。数据量化：细胞迁移百分比=（T0划痕区域-Tt划痕区域）/ T0划痕区域。
1.4.6　SYBR Green染料法实时定量聚合酶链式反应（SYBR Green Quantitative Real-time PCR，SYBR Green qPCR）
将约15 mg肺组织放入组织研磨管中，加入1 ml Trizol进行研磨，采用Trizol法提取RNA。NanoDrop 2000分光光度计测定RNA浓度和纯度。取1 μg总RNA逆转录，反应条件为37 ℃、2 min ，50 ℃、15 min，85 ℃、5 min。对cDNA进行RT-qPCR，反应条件为95 ℃、5min，95 ℃、10 s，60 ℃、10 s，72 ℃、10 s，共40个循环；溶解曲线95 ℃、10 s，60 ℃、60 s，95 ℃、10 s。小鼠肺组织Mmp14、N-cadherin以β-actin（鼠）为内参，16HBE细胞Mmp14、N-cadherin以β-actin（人）为内参，采用2-ΔΔCt法定量分析。引物序列详见表1，均购自上海生物工程有限公司。
1.4.7　蛋白免疫印迹（Western blot，WB）
将组织或细胞样本在含有RIPA：磷酸酶抑制剂I：磷酸酶抑制剂II：PMSP为97：1：1：1的蛋白裂解液中冰上裂解30 min以上，4 ℃条件13 500 r/min离心15 min，收集上清液蛋白，进行蛋白定量与变性处理。蛋白通过十二烷基硫酸钠聚丙烯酰胺凝胶电泳（SDS-PAGE）分离，并转移到聚偏二氟乙烯膜（PVDF）膜上。在室温下使用快速封闭液封闭30 min后，加入GAPDH（1：10 000）、MMP14 （1：1 000）以及N-cadherin（1：1 000）一抗在4 ℃下孵育过夜，在室温下孵育鼠抗（1：20 000）、兔抗（1：20 000）二抗1 h。采用电化学发光法（ECL）显色，以GAPDH作为内参，使用Image J对蛋白表达强度进行分析。
1.4.8　统计学分析
采用GraphPad Prism 8.0软件处理，变量以表示。样本多组间比较采用单因素方差分析，组间比较为Dunnett-t检验。两组间比较若正态分布且方差齐性，则采用t检验，若不符合标准则采用Mann-Whitney U检验。检验水准α=0.05。
2　结果
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2.1　MMP14为矽肺中高表达分子
用尘肺患者肺组织穿刺标本及SiO2小鼠矽肺模型肺组织样本行单细胞测序。结果显示，与对照组样本相比，MMP14表达水平在人尘肺组织及小鼠不同时间点矽肺模型组肺组织中均表达增高（图1A-B）。在小鼠矽肺模型组中，SiO2作用12周时MMP14表达增高最为显著（图1B）。
2.2　小鼠矽肺模型建立
根据单细胞测序结果，建立12周小鼠矽肺模型。HE染色结果显示，模型组炎性细胞浸润、肺泡间隔显著增厚及肺组织结构破坏（图2A），且其炎症评分显著高于对照组（图2B）。Masson染色结果显示，模型组中小鼠肺组织肌成纤维细胞数量及胶原纤维沉积均显著增多（图2C）。定量结果表明，模型组纤维化程度比对照组高约9倍（图2D）。
2.3　小鼠矽肺模型中MMP14表达增高
采用12周小鼠矽肺模型肺组织进行验证，RT-qPCR结果显示MMP14 mRNA表达较对照组上调约3.78倍（图3A），且EMT关键分子间充质细胞标志物N-cadherin mRNA上调约2.42倍（图3B）。WB结果显示，与对照组相比，模型组MMP14和N-cadherin蛋白表达水平亦显著上调（图3C-D）。IHC结果显示，MMP14在模型组纤维结节区域呈强阳性表达，阳性信号为黄棕色，定位于细胞浆（图3E-F）。
2.4　敲低MMP14抑制N-cadherin表达
为验证MMP14通过调控N-cadherin促进上皮细胞EMT发生，本课题采用siRNA敲减上皮细胞16BHE中MMP14，WB结果显示si-MMP14可显著下调MMP14表达，同时抑制N-cadherin蛋白表达（图4A-B）。其中以si-MMP14-3敲减效果最为显著，后续采用si-MMP14-3（后文均简称si-MMP14）进行实验验证。
2.5　敲减MMP14抑制SiO2诱导的上皮细胞迁移
RT-qPCR结果显示，在200 μg/ml SiO2暴露下，上皮细胞16HBE中MMP14表达水平上升，转染si-MMP14后，可抑制MMP14表达（图5A）。采用细胞划痕实验评估16HBE细胞迁移能力，结果显示，SiO2刺激16HBE细胞迁移能力增强，而采用si-MMP14抑制MMP14则而可逆转该效应，细胞迁移面积降低约0.56倍。提示，敲减MMP14可能通过抑制上皮细胞EMT过程，减缓矽肺进展。
3　讨论
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矽肺是一种在职业环境中长期吸入二氧化硅粉尘所引起的、以进行性肺功能损害为特征的职业性疾病[13]。肺纤维化是矽肺晚期的关键病理表现，目前尚无有效疗法能够逆转。目前研究认为，部分成纤维细胞可能起源于肺内上皮细胞的EMT过程，肺成纤维细胞被促纤维化因子刺激后，分化为肌成纤维细胞促进纤维化发展[5]。本研究成功建立12周小鼠矽肺模型，发现MMP14在矽肺模型组中表达显著增高，且集中定位于纤维结节区域，提示MMP14在矽肺纤维化发生中发挥重要调控作用。
MMP14可通过多种机制调控纤维化发生。在心脏特异性过表达CD147的转基因小鼠中，MMP2和MMP14的表达增高促进心脏纤维化和病理性左室重构发生[14]。在以慢性炎症和纤维化为主要特征的Duchenne型肌营养不良疾病中，MMP14敲低可减少成纤维细胞的胶原分泌，缓解纤维化进程[15]。MMP14在皮肤纤维化发生中也发挥重要作用[16]。在纤维化超敏反应性肺炎中，高表达MMP14的巨噬细胞亚群具有M2型表型特征，将过表达MMP14的巨噬细胞转移到小鼠体内可加重肺部炎症和纤维化程度，且过表达MMP14的巨噬细胞源外泌体能促进成纤维细胞向肌成纤维细胞转化[17]。在小鼠矽肺模型中，肝素结合性表皮生长因子（Heparin-Binding EGF-Like Growth Factor, HBEGF）-CD44轴和集落刺激因子1及其受体CSF1-CSF1R轴可促进高表达趋化因子配体10（C-X-C motif chemokine ligand 10，Cxcl10+）/ MMP14+的单核细胞与趋化因子配体3+（chemokine (C-C motif) ligand 3, Ccl3+）中性粒细胞的募集和活化，进而导致肺纤维化发生[18]。
肺泡上皮细胞在维持肺泡稳态中发挥关键作用，包括产生肺表面活性物质和自我更新，当其发生功能障碍时可导致异常的细胞信号传导、ECM异常沉积且发生EMT获得间质细胞表型，从而促进纤维化过程[19]。当上皮细胞发生EMT时，侵袭能力增强，间质细胞标记物表达增加，上皮细胞标记物表达和细胞黏附能力减弱[20]。在SiO2诱导人支气管上皮细胞16HBE使NLRP3炎症小体活化促进IL-1β分泌，激活转化生长因子激酶-β激活激酶1（Transforming growth factor-β-activated kinase 1, TAK1）和丝裂原活化蛋白激酶（Mitogen-activated protein kinase，MAPK），促进EMT信号分子Snail表达，诱导矽肺肺纤维化形成[21]。在小鼠矽肺模型及SiO2刺激的小鼠II型肺泡上皮细胞MLE 12中，采用天然多肽化合物Ac-SDKP进行分子干预，可抑制胶原蛋白Collagen I、Collagen III 以及波形蛋白Vimentin表达，并促进E-cadherin表达，抑制上皮细胞EMT，减缓肺纤维化发生[10]。上述研究表明上皮细胞EMT，促进矽肺肺纤维化发生，我们聚焦于MMP14，研究其对上皮细胞EMT的调控。在上皮细胞中敲低MMP14，N-cadherin表达降低，且抑制上皮细胞迁移，提示MMP14可能通过调控N-cadherin，促进上皮细胞发生EMT，影响矽肺纤维化发生。
MMP14参与调控EMT的发生，例如在膀胱尿路上皮细胞癌中，活化诱导性胞嘧啶核苷脱氨酶（Activation-induced cytidine deaminase, AID）通过DNA去甲基化修饰促进MMP14表达，同时影响E-cadherin和N-cadherin表达，促进EMT进程[22]。在肾细胞癌中，环状RNA circPTCH1作为miR-489-5p的海绵，解除miR-489-5p对MMP14的转录后抑制作用，促进MMP14表达，使EMT信号分子E-cadherin下调、N-cadherin及Vimentin上调，促进肾癌细胞A498和 OS-RC-2的迁移和侵袭[23]。在博来霉素诱导的小鼠和A549细胞模型中，内质网蛋白Nogo-B通过增强MMP14的表达促进TGF-β1的活化，使EMT 标志物Vimentin、α-SMA表达上调和E-cadherin的表达下调，促进肺纤维化发生[24]。
综上所述，本研究发现MMP14在小鼠矽肺模型中显著高表达，并通过体外实验证实了MMP14通过调控N-cadherin促进上皮细胞迁移。这些结果与上述相关研究报道共同表明，MMP14可能通过促进上皮细胞EMT，在矽肺发生和发展中起重要调控作用，为矽肺机制研究及治疗提供了新视角和潜在靶点。
基金
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  • 国家自然科学基金(82373548; U22A20359; U23A20495)
  • 四川省科学技术厅基金(2023NSFSC1731; 2024NSFSC1258)
  • 四川大学与达州市战略合作项目(2022CDDZ-14)
文献
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2025年第52卷第4期
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doi: 10.20043/j.cnki.MPM.202409198
  • 接收时间：2024-09-10
  • 首发时间：2026-03-18
  • 出版时间：2025-02-25
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  • 收稿日期：2024-09-10
基金
国家自然科学基金(82373548; U22A20359; U23A20495)
四川省科学技术厅基金(2023NSFSC1731; 2024NSFSC1258)
四川大学与达州市战略合作项目(2022CDDZ-14)
作者信息
    四川大学华西公共卫生学院/华西第四医院，分子毒理四川省教育厅重点实验室，四川 成都 610041

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鹅膏菌科Amanitaceae 2 11 5.26 鹅膏菌属 Amanita 10 4.78
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