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Article(id=1234106413480464612, tenantId=1146029695717560320, journalId=1234093305789726721, issueId=1234106384963400440, articleNumber=null, orderNo=null, doi=null, pmid=null, cstr=null, oa=null, hot=null, price=null, onlineType=0, articleFormat=0, articleType=null, articleTypeStr=null, receivedDate=1730995200000, receivedDateStr=2024-11-08, revisedDate=null, revisedDateStr=null, acceptedDate=null, acceptedDateStr=null, onlineDate=1772163497562, onlineDateStr=2026-02-27, pubDate=1750348800000, pubDateStr=2025-06-20, doiRegisterDate=null, doiRegisterDateStr=null, onlineIssueDate=1772163497562, onlineIssueDateStr=2026-02-27, onlineJustAcceptDate=null, onlineJustAcceptDateStr=null, onlineFirstDate=null, onlineFirstDateStr=null, sourceXml=null, magXml=null, createTime=1772163497562, creator=13701087609, updateTime=1772163497562, updator=13701087609, issue=Issue{id=1234106384963400440, tenantId=1146029695717560320, journalId=1234093305789726721, year='2025', volume='45', issue='6', pageStart='2961', pageEnd='3552', issueExtLink='null', onlineDate='null', pubDate='null', beforeIssueId=null, nextIssueId=null, price=null, status=1, issueComplete=1, articleOrder=1, issueType=1, specialIssue=null, createTime=1772163490763, creator=13701087609, updateTime=1772163969484, updator=13701087609, preIssue=null, nextIssue=null, ext={EN=IssueExt(id=1234108392948682946, tenantId=1146029695717560320, journalId=1234093305789726721, issueId=1234106384963400440, language=EN, specialIssueTitle=, coverIllustrator=null, specialIssueEditor=, specialIssueAbout=), CN=IssueExt(id=1234108392948682947, tenantId=1146029695717560320, journalId=1234093305789726721, issueId=1234106384963400440, language=CN, specialIssueTitle=, coverIllustrator=null, specialIssueEditor=, specialIssueAbout=)}, issueFiles=null}, startPage=3451, endPage=3459, ext={EN=ArticleExt(id=1234106415464370459, articleId=1234106413480464612, tenantId=1146029695717560320, journalId=1234093305789726721, language=EN, title=Study on the toxic effect and mechanism of organophosphorus flame retardants on the human lung cancer A549cell, columnId=1234106388687934088, journalTitle=China Environmental Science, columnName=Environmental Toxicology and Environmental Health, runingTitle=null, highlight=null, articleAbstract=

Human lung cancer cell A549were used as the test cell. Three kinds of organophosphorus flame retardants, i.e., tris(2-butoxyethyl) phosphate (TBOEP), tris(1-chloro-2-propyl)phosphate (TCIPP), and tri(4-isopropylphenyl)phosphate (IPPP), were selected as representative compounds, which are frequently detected in the environment. The toxic effects of the three compounds on A549cell were studied through multiple toxicity test endpoints. Results showed that the three OPFRs could inhibit cell viability, stimulate the production of excessive reactive oxygen species and reduce the mitochondrial membrane potential in cell, induce cell inflammation and cause DNA damage. All the cytotoxicity indicators were dose-dependent. OPFRs with low concentrations had less effect, and the toxic effect enhanced with the increase of OPFRs concentrations. Compared with the three OPFRs, their toxic effects on A549cells ranked as TBOEP > TCIPP ≈ IPPP. Especially, when the cells were exposed to TBOEP with a high concentration of 500 μmol/L, the cell viability was less than 5%, the amount of reactive oxygen species in cell increased by three times, the mitochondrial membrane potential decreased by 46.5%, the secretion of inflammatory factors IL-6 and TNF-α increased by 124.4% and 262.7%, and the content of DNA damage markers increased significantly.

, correspAuthors=Hui-hui LIU, authorNote=null, correspAuthorsNote=null, copyrightStatement=null, copyrightOwner=null, extLink=null, articleAbsUrl=null, sourceXml=null, magXml=null, pdfUrl=null, pdf=null, pdfFileSize=null, pdfExtLink=null, richHtmlUrl=null, mobilePdfUrl=null, reviewReport=null, pdfFirstPage=null, abstractGraph=null, abstractGraphContent=null, abstractVideo=null, citation=null, cebUrl=null, magXmlContent=null, mapNumber=null, authorCompany=null, fund=null, authors=null, authorsList=Cheng-cheng SHEN, Xian-hai YANG, Hui-hui LIU), CN=ArticleExt(id=1234106419797086734, articleId=1234106413480464612, tenantId=1146029695717560320, journalId=1234093305789726721, language=CN, title=有机磷阻燃剂对人肺癌A549细胞的毒性效应及机制, columnId=1234106394006311784, journalTitle=中国环境科学, columnName=环境毒理与健康, runingTitle=null, highlight=null, articleAbstract=

以A549人肺癌细胞作为体外模型，选取环境中检出频率较高的3种有机磷阻燃剂：磷酸三(2-丁氧基)乙酯(TBOEP)、磷酸三(2-氯丙基)酯(TCIPP)和磷酸三异丙基苯酯(IPPP)作为代表性物质，通过多种毒性测试终点，研究它们对人肺癌A549细胞的毒性效应.结果表明，3种OPFRs均能抑制细胞活力、刺激其产生过量的活性氧、降低细胞内线粒体膜电位、诱导细胞产生炎症、引起DNA损伤.每个细胞毒性指标都呈现出剂量依赖性.低浓度的OPFRs影响较小，随着OPFRs浓度升高，毒性效应越来越大.对比3种OPFRs，A549细胞毒性作用顺序为TBOEP > TCIPP ≈ IPPP.特别是在高浓度500 μmol/L的TBOEP暴露下，细胞活力不到5%，细胞内活性氧水平上升3倍，线粒体膜电位降低了46.5%，炎症因子IL-6和TNF-α的分泌量上升了124.4%和262.7%，DNA损伤标记物含量显著增加.本文研究结果为揭示不同OPFRs的毒性差异提供了新的实验数据和思路，为评估环境中OPFRs对人体健康风险提供了新的见解.

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* 责任作者，副教授，
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沈铖澄(1999-)，男，浙江绍兴人，南京理工大学硕士研究生，主要从事环境毒理学.发表论文1篇..

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沈铖澄(1999-)，男，浙江绍兴人，南京理工大学硕士研究生，主要从事环境毒理学.发表论文1篇..

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沈铖澄(1999-)，男，浙江绍兴人，南京理工大学硕士研究生，主要从事环境毒理学.发表论文1篇..

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Chemical Research in Toxicology，2018，31(11):1164-1171., articleTitle=Polybrominated diphenyl ethers quinone induced parthanatos-like cell death through a reactive oxygen species-associated poly(ADP-ribose) polymerase 1signaling, refAbstract=null)], funds=[Fund(id=1234106426084348779, tenantId=1146029695717560320, journalId=1234093305789726721, articleId=1234106413480464612, awardId=22176097, language=CN, fundingSource=国家自然科学基金资助项目(22176097), fundOrder=null, country=null)], companyList=[AuthorCompany(id=1234106420170379824, tenantId=1146029695717560320, journalId=1234093305789726721, articleId=1234106413480464612, xref=null, ext=[AuthorCompanyExt(id=1234106420174574130, tenantId=1146029695717560320, journalId=1234093305789726721, articleId=1234106413480464612, companyId=1234106420170379824, language=EN, country=null, province=null, city=null, postcode=null, companyName=null, departmentName=null, remark=School of Environmental and Biological Engineering, Nanjing University of Science and Technology, Nanjing 210000, China), AuthorCompanyExt(id=1234106420187157043, tenantId=1146029695717560320, journalId=1234093305789726721, articleId=1234106413480464612, companyId=1234106420170379824, language=CN, country=null, province=null, city=null, postcode=null, companyName=null, departmentName=null, remark=南京理工大学环境与生物工程学院，江苏 南京 210000)])], figs=[ArticleFig(id=1234106424452764422, tenantId=1146029695717560320, journalId=1234093305789726721, articleId=1234106413480464612, language=EN, label=Fig.1, caption=Effects of TBOEP, TCIPP and IPPP on the viability of A549 cells under different concentrations, figureFileSmall=uEgDM8XAgl4eigjdGHfc+g==, figureFileBig=c9wY+eIgMXwsn5naC4yFPg==, tableContent=null), ArticleFig(id=1234106424582787857, tenantId=1146029695717560320, journalId=1234093305789726721, articleId=1234106413480464612, language=CN, label=图1, caption=不同浓度TBOEP、TCIPP和IPPP对A549细胞活力的影响

字母相同表示组间无显著性差异(P>0.05)，字母不同表示组间有显著性差异(P<0.05)

, figureFileSmall=uEgDM8XAgl4eigjdGHfc+g==, figureFileBig=c9wY+eIgMXwsn5naC4yFPg==, tableContent=null), ArticleFig(id=1234106424821863200, tenantId=1146029695717560320, journalId=1234093305789726721, articleId=1234106413480464612, language=EN, label=Fig.2, caption=Effects of TBOEP, TCIPP and IPPP on the ROS of A549 cells under different concentrations, figureFileSmall=jVE55DRNv5NoLRCiYdE82A==, figureFileBig=KCsw1ChqkzCI/62iOAxcJg==, tableContent=null), ArticleFig(id=1234106424909943593, tenantId=1146029695717560320, journalId=1234093305789726721, articleId=1234106413480464612, language=CN, label=图2, caption=不同浓度TBOEP、TCIPP和IPPP对A549内活性氧水平的影响

字母相同表示组间无显著性差异(P>0.05)，字母不同表示组间有显著性差异(P<0.05)

, figureFileSmall=jVE55DRNv5NoLRCiYdE82A==, figureFileBig=KCsw1ChqkzCI/62iOAxcJg==, tableContent=null), ArticleFig(id=1234106425018995504, tenantId=1146029695717560320, journalId=1234093305789726721, articleId=1234106413480464612, language=EN, label=Fig.3, caption=Effects of TBOEP, TCIPP and IPPP on the MMP of A549 cells under different concentrations, figureFileSmall=KJShtMrM5eNKTMeMxewUSA==, figureFileBig=wE0K7SyMlWp5cCNLmaZzgg==, tableContent=null), ArticleFig(id=1234106425128047415, tenantId=1146029695717560320, journalId=1234093305789726721, articleId=1234106413480464612, language=CN, label=图3, caption=不同浓度TBOEP、TCIPP和IPPP对A549线粒体膜电位的影响

字母相同表示组间无显著性差异(P>0.05)，字母不同表示组间有显著性差异(P<0.05)

, figureFileSmall=KJShtMrM5eNKTMeMxewUSA==, figureFileBig=wE0K7SyMlWp5cCNLmaZzgg==, tableContent=null), ArticleFig(id=1234106425237099329, tenantId=1146029695717560320, journalId=1234093305789726721, articleId=1234106413480464612, language=EN, label=Fig.4, caption=Effects of TBOEP, TCIPP and IPPP on the inflammatory factor (a)IL-6, (b)TNF-α of A549 cells under different concentrations, figureFileSmall=zBDBQvlLO2dZQG9Xu36q5w==, figureFileBig=AVgqETvKaCTmOE1diW2dzA==, tableContent=null), ArticleFig(id=1234106425341956932, tenantId=1146029695717560320, journalId=1234093305789726721, articleId=1234106413480464612, language=CN, label=图4, caption=不同浓度TBOEP、TCIPP和IPPP暴露24h后对A549炎症因子(a)IL-6,(b)TNF-α的影响

字母相同表示组间无显著性差异(P>0.05)，字母不同表示组间有显著性差异(P<0.05)

, figureFileSmall=zBDBQvlLO2dZQG9Xu36q5w==, figureFileBig=AVgqETvKaCTmOE1diW2dzA==, tableContent=null), ArticleFig(id=1234106425438425932, tenantId=1146029695717560320, journalId=1234093305789726721, articleId=1234106413480464612, language=EN, label=Fig.5, caption=Effects of TBOEP, TCIPP and IPPP on the viability of A549 cells under different concentrations, figureFileSmall=sCttWLedrXeWTp9U+z8lbQ==, figureFileBig=ahPAwTJc0ITnhdmRY1L8fQ==, tableContent=null), ArticleFig(id=1234106425539089233, tenantId=1146029695717560320, journalId=1234093305789726721, articleId=1234106413480464612, language=CN, label=图5, caption=不同浓度TBOEP、TCIPP和IPPP对A549的DNA损伤情况

第1列表示γ-H2AX，第2列表示DAPI染色细胞核.比例尺=100μm

, figureFileSmall=sCttWLedrXeWTp9U+z8lbQ==, figureFileBig=ahPAwTJc0ITnhdmRY1L8fQ==, tableContent=null), ArticleFig(id=1234106425631363927, tenantId=1146029695717560320, journalId=1234093305789726721, articleId=1234106413480464612, language=EN, label=Fig.6, caption=Comparison of the cytotoxicity of A549 cells under different concentrations of OPFRs, figureFileSmall=Lv/jFCssdFOCtmlnJfQ3tQ==, figureFileBig=bWPS7w7BYeF0Ixpfb+7Rkw==, tableContent=null), ArticleFig(id=1234106425723638616, tenantId=1146029695717560320, journalId=1234093305789726721, articleId=1234106413480464612, language=CN, label=图6, caption=不同浓度的OPFRs对A549细胞毒性的差异性比较

(a)、(b)、(c)分别表示3种OPFRs在浓度为500,125,15.63μmol/L下的指标差异

, figureFileSmall=Lv/jFCssdFOCtmlnJfQ3tQ==, figureFileBig=bWPS7w7BYeF0Ixpfb+7Rkw==, tableContent=null), ArticleFig(id=1234106425845273437, tenantId=1146029695717560320, journalId=1234093305789726721, articleId=1234106413480464612, language=EN, label=Table 1, caption=

Correlation coefficients between cell viability, oxidative stress, apoptosis and inflammation

, figureFileSmall=null, figureFileBig=null, tableContent=
OPFRs指标细胞活力ROSMMPIL-6TNF-α
TBOEP细胞活力1-0.993**0.879**-0.909**-0.981**
ROS1-0.830**0.865**0.964**
MMP1-0.991**-0.943**
IL-610.960**
TNF-α1
TCIPP细胞活力1-0.952**0.981**-0.866**-0.943**
ROS1-0.965**0.914**0.982**
MMP1-0.889**-0.953**
IL-610.875**
TNF-α1
IPPP细胞活力1-0.894**0.935**-0.882**-0.922**
ROS1-0.962**0.897**0.966**
MMP1-0.917**-0.981**
IL-610.920**
TNF-α1
), ArticleFig(id=1234106425962713957, tenantId=1146029695717560320, journalId=1234093305789726721, articleId=1234106413480464612, language=CN, label=表1, caption=

OPFRs的细胞活力、氧化应激、细胞凋亡和炎症反应之间的相关性

, figureFileSmall=null, figureFileBig=null, tableContent=
OPFRs指标细胞活力ROSMMPIL-6TNF-α
TBOEP细胞活力1-0.993**0.879**-0.909**-0.981**
ROS1-0.830**0.865**0.964**
MMP1-0.991**-0.943**
IL-610.960**
TNF-α1
TCIPP细胞活力1-0.952**0.981**-0.866**-0.943**
ROS1-0.965**0.914**0.982**
MMP1-0.889**-0.953**
IL-610.875**
TNF-α1
IPPP细胞活力1-0.894**0.935**-0.882**-0.922**
ROS1-0.962**0.897**0.966**
MMP1-0.917**-0.981**
IL-610.920**
TNF-α1
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有机磷阻燃剂对人肺癌A549细胞的毒性效应及机制
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沈铖澄 , 杨先海 , 刘会会 *
中国环境科学 | 环境毒理与健康 2025,45(6): 3451-3459
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中国环境科学 | 环境毒理与健康 2025, 45(6): 3451-3459
有机磷阻燃剂对人肺癌A549细胞的毒性效应及机制
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沈铖澄 , 杨先海, 刘会会*
作者信息
  • 南京理工大学环境与生物工程学院，江苏 南京 210000

    • 沈铖澄(1999-)，男，浙江绍兴人，南京理工大学硕士研究生，主要从事环境毒理学.发表论文1篇..

通讯作者:

* 责任作者，副教授，
Study on the toxic effect and mechanism of organophosphorus flame retardants on the human lung cancer A549cell
Cheng-cheng SHEN , Xian-hai YANG, Hui-hui LIU*
Affiliations
  • School of Environmental and Biological Engineering, Nanjing University of Science and Technology, Nanjing 210000, China
出版时间: 2025-06-20
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摘要
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以A549人肺癌细胞作为体外模型，选取环境中检出频率较高的3种有机磷阻燃剂：磷酸三(2-丁氧基)乙酯(TBOEP)、磷酸三(2-氯丙基)酯(TCIPP)和磷酸三异丙基苯酯(IPPP)作为代表性物质，通过多种毒性测试终点，研究它们对人肺癌A549细胞的毒性效应.结果表明，3种OPFRs均能抑制细胞活力、刺激其产生过量的活性氧、降低细胞内线粒体膜电位、诱导细胞产生炎症、引起DNA损伤.每个细胞毒性指标都呈现出剂量依赖性.低浓度的OPFRs影响较小，随着OPFRs浓度升高，毒性效应越来越大.对比3种OPFRs，A549细胞毒性作用顺序为TBOEP > TCIPP ≈ IPPP.特别是在高浓度500 μmol/L的TBOEP暴露下，细胞活力不到5%，细胞内活性氧水平上升3倍，线粒体膜电位降低了46.5%，炎症因子IL-6和TNF-α的分泌量上升了124.4%和262.7%，DNA损伤标记物含量显著增加.本文研究结果为揭示不同OPFRs的毒性差异提供了新的实验数据和思路，为评估环境中OPFRs对人体健康风险提供了新的见解.

有机磷阻燃剂  /  细胞毒性  /  氧化应激  /  DNA损伤  /  线粒体损伤

Human lung cancer cell A549were used as the test cell. Three kinds of organophosphorus flame retardants, i.e., tris(2-butoxyethyl) phosphate (TBOEP), tris(1-chloro-2-propyl)phosphate (TCIPP), and tri(4-isopropylphenyl)phosphate (IPPP), were selected as representative compounds, which are frequently detected in the environment. The toxic effects of the three compounds on A549cell were studied through multiple toxicity test endpoints. Results showed that the three OPFRs could inhibit cell viability, stimulate the production of excessive reactive oxygen species and reduce the mitochondrial membrane potential in cell, induce cell inflammation and cause DNA damage. All the cytotoxicity indicators were dose-dependent. OPFRs with low concentrations had less effect, and the toxic effect enhanced with the increase of OPFRs concentrations. Compared with the three OPFRs, their toxic effects on A549cells ranked as TBOEP > TCIPP ≈ IPPP. Especially, when the cells were exposed to TBOEP with a high concentration of 500 μmol/L, the cell viability was less than 5%, the amount of reactive oxygen species in cell increased by three times, the mitochondrial membrane potential decreased by 46.5%, the secretion of inflammatory factors IL-6 and TNF-α increased by 124.4% and 262.7%, and the content of DNA damage markers increased significantly.

organophosphate flame retardants  /  cytotoxicity  /  oxidative stress  /  DNA damage  /  mitochondrial damage
沈铖澄, 杨先海, 刘会会. 有机磷阻燃剂对人肺癌A549细胞的毒性效应及机制. 中国环境科学, 2025 , 45 (6) : 3451 -3459 .
Cheng-cheng SHEN, Xian-hai YANG, Hui-hui LIU. Study on the toxic effect and mechanism of organophosphorus flame retardants on the human lung cancer A549cell[J]. China Environmental Science, 2025 , 45 (6) : 3451 -3459 .
正文
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有机磷阻燃剂(OPFRs)可以长时间存在于不同的环境介质中，例如土壤、空气、灰尘、水和食品等[1].环境中常检出的OPFRs，按取代基结构可以分为烷基-OPFRs，卤代-OPFRs和芳基-OPFRs，不同种类的OPFRs理化性质和毒性差异较大[2].越来越多的证据表明OPFRs会对人类健康和生态环境产生负面影响.人的一生大约有80%~90%的时间处于室内环境中，特别是老人和儿童停留在室内环境时间可能更长，这意味着室内环境中的OPFRs污染可能有更高的环境风险[3].
近年来，OPFRs在世界各地室内环境中高频检出率和高浓度引起人们担忧.室内粉尘和污染空气吸入是人体摄入室内环境中OPFRs最主要的方式[3]，目前已在人体尿液、血液、血清、指甲、母乳和头发等检出了多种OPFRs[4-6].Wong等[7]研究的72份空气样品中都检测到OPFRs.类似的，在土耳其收集的空气样本中也都检测到OPFRs[8].在东京和瑞士室内中，磷酸三(2-氯丙基)酯(TCIPP)浓度分别高达1260和1179ng/m3，高于同期溴代阻燃剂的浓度[9-10].另外，在日托中心中OPFRs最高浓度达2080ng/m3，其中磷酸三(2-正丁氧乙基)酯(TBOEP)是最主要的污染物[11].
据统计，成人每日在室内环境中吸入OPFRs量约为14000pg/(kg-bwd)[3]，而直接暴露于OPFRs污染的呼吸道、消化道可能遭受更大的损伤.毒理学研究表明，OPFRs可以在动植物体内积累并造成多种不良反应，包括脏器毒性、神经毒性、生殖毒性、呼吸道疾病、内分泌干扰效应和基因毒性[12].体外细胞实验证明，OPFRs对细胞生长普遍存在抑制作用，高剂量或是长时间暴露更容易造成严重的细胞损伤，引起细胞功能障碍，甚至导致细胞死亡.例如，OPFRs会引起的人肝癌细胞脂质代谢破坏，产生过量的活性氧自由基(ROS)，并且导致线粒体功能障碍[13];氯代-OPFRs引起人体肠道菌群细胞毒性，诱导ROS产生和降低线粒体膜电位(MMP)[14].然而，当前关于OPFRs的毒理学研究报道集中于消化道和内分泌系统，而有关呼吸系统的毒理学数据很少.现有相关报道指出，磷酸三(2-正丁氧乙基)酯、磷酸三(2-氯丙基)酯、磷酸三(1,3-二氯-2-丙基)酯可以降低人正常支气管上皮细胞BEAS-2B细胞活力[15].多种OPFRs会导致人肺腺癌细胞NCI-H1975细胞活性降低，氧化应激和细胞凋亡[16].磷酸三(2-氯乙基)酯、磷酸三甲苯酯和磷酸三苯酯可降低肺癌人类肺泡基底上皮细胞A549细胞活力，促进ROS产生并导致细胞凋亡[17].
人肺癌A549细胞是一种被广泛应用于呼吸系统毒理学研究的体外模型，对多种刺激因素敏感，故适用于研究大气污染物对人体呼吸道的影响[18].本文选择了环境中典型的OPFRs：烷基-OPFRs(磷酸三(2-丁氧基)乙酯，TBOEP)、卤代-OPFRs(磷酸三(2-氯丙基)酯，TCIPP)和芳基-OPFRs(磷酸三异丙基苯酯，IPPP)作为代表性物质，通过人肺癌A549细胞毒性测试，考察OPFRs对肺细胞的细胞毒性及其作用机制.本文旨在：通过研究不同OPFRs的细胞毒性(包括细胞活性，氧化应激，线粒体膜损伤和DNA损伤等)影响，探究OPFRs对细胞的致毒机理，以期为室内环境中OPFRs的风险和健康评估提供参考.
1　材料与方法
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1.1　主要化学试剂
磷酸三(2-正丁氧乙基)酯[TBOEP；CAS:78-51-3]、磷酸三(2-氯丙基)酯[TCIPP；CAS:13674-84-5]、三异丙苯基磷酸酯[IPPP；CAS:26967-76-0]购自阿拉丁公司，纯度均高于98%.二甲基亚砜(DMSO)购自兰杰柯科技有限公司，胎牛血清(FBS)购自浙江天杭生物科技股份有限公司.DMEM高糖培养基、PBS缓冲液、0.25%胰蛋白酶-EDTA溶液和青霉素/链霉素混合溶液购自美国Gibco公司，CCK-8细胞活力检测试剂盒、活性氧检测试剂盒、线粒体膜电位检测试剂盒和DNA损伤检测试剂盒购自上海碧云天生物科技有限公司，人白细胞介素6(IL-6)和人肿瘤坏死因子α(TNF-α)ELISA试剂盒购自江苏菲亚生物科技有限公司.人非小细胞肺癌细胞A549细胞购自上海信裕生物科技有限公司.
1.2　细胞培养
复苏冻存细胞并接种在含6mL完全培养基(体积分数为89%DMEM、10%FBS和1%青霉素/链霉素混合溶液)的细胞培养瓶，于CO2恒温培养箱(37℃、体积分数5%CO2)培养细胞.细胞培养基每2d进行一次更换并在细胞生长至80%进行1:3传代.实验过程中选择3至15代的细胞进行实验.
1.3　细胞染毒
1.3.1　OPFRs母液配制
TBOEP、TCIPP、IPPP在常温下均为液态，纯度均高于98%.各取一定体积的OPFRs溶液置于DMSO中，配制浓度为500mol/L的OPFRs母液，再分别用DMSO稀释母液，获得不同浓度的OPFRs溶液，经0.22μm有机相滤膜过滤后置于-20℃冰箱保存.
通过污染空气吸入和吸入粉尘估计OPFRs的肺摄入量，计算方法如下：
式中：C空气表示空气中OPFRs的浓度，ng/m3;RR为呼吸速率，成人为20m3/d，儿童为4.5m3/d[3].C灰尘表示灰尘中OPFRs的浓度，μg/g；DIG表示为估计的摄尘量(成人为2.5mg/d，儿童为41mg/d)[19];1000用于单位间的转换.
研究发现，TBOEP是污染空气和室内粉尘中最主要的OPFRs，污染空气和粉尘中TBOEP最高浓度分别为130ng/m3和1900μg/g[7-8,11,19-20]，其相对分子质量为398.47g/mol，那么成人和儿童肺摄入量分别为7.3和78.49μg.人肺液体积为10~15mL，可估计成人肺中TBOEP浓度范围为1.2~1.8μmol/L，儿童为13.14~19.71μmol/L.可知儿童的OPFRs暴露风险更高，更应关注OPFRs对儿童肺损伤情况，故本文设置的低浓度(15.63μmol/L)具有儿童在污染环境中短期暴露的实际意义.考虑到OPFRs在人体肺部的累积效应，中浓度(125μmol/L)和高浓度(500μmol/L)分别以一周和一个月作为累积时间，以评估OPFRs长期累积后对人肺的影响.TCIPP和IPPP的浓度选取方法与TBOEP相同，经综合评估后，选择统一的实验浓度.
1.3.2　细胞染毒
用DMEM培养液以1000:1的倍数稀释不同种类、不同浓度的OPFRs母液至工作浓度.随后，用0.25%胰蛋白酶-EDTA溶液消化细胞至离心管，离心去除上清液后加入完全培养基，分别以1.0×104或5.0×105个细胞/孔的初始密度接种于96孔或12孔细胞培养板.孵育24h，待细胞完全贴壁后，去除原有培养基，加入OPFRs工作液暴露24h后进行相关指标的测试.
1.4　细胞活力测试
利用CCK-8细胞活力检测试剂盒测试OPFRs对A549细胞活力的影响.主要步骤如下：96孔板中的细胞暴露在100μL的OPFRs工作液24h后，每孔加入10μLCCK-8试剂，37℃孵育2h后，使用多功能酶标仪在450nm处测定每孔对应的吸光度(OD).细胞活力计算公式如下：
1.5　细胞内ROS变化水平的检测
采用2,7-二氯荧光素二乙酸酯(DCFH-DA)荧光探针检测A549细胞内ROS水平，DCFA-DA荧光强度与细胞内ROS水平正相关.A549细胞暴露OPFRs工作液24h后，胰酶消化收集细胞，并用PBS冲洗2次.之后，将细胞重悬在含DCFH-DA(10μmol/L)的DMEM培养基中，37℃避光孵育30min，再用PBS洗去多余的DCFH-DA探针.然后，加入适量的缓冲液重悬细胞，使用荧光分光光度计在激发波长为488nm，发射波长为525nm的条件下测定荧光强度.
1.6　细胞内线粒体膜电位变化的测定
荧光探针JC-1常用于评估线粒体膜电位(MMP)变化，被广泛用于表征线粒体早期凋亡和去极化水平.本文通过测量JC-1聚集体(红色)与JC-1单体(绿色)的比例来定量MMP去极化率.A549细胞染毒24h后，胰酶消化收集细胞，并用PBS冲洗2次.根据试剂盒说明书配制JC-1染色工作液和JC-1染色缓冲液，将细胞重悬在含JC-1染色工作液，37 ℃避光孵育30min，然后用冷JC-1染色缓冲液洗涤2次，并加入适量的缓冲液重悬细胞.最后，使用荧光分光光度计测量JC-1的荧光强度来确定MMP的变化.
1.7　Elisa法检测细胞内炎症因子水平
炎症因子存在于细胞外泌体中，超速离心法是目前外泌体分离最常用的方法.待暴露结束后，收集细胞上清，在4℃下以300r/min的转速离心10min，去除活细胞和死细胞，并收集细胞上清液.然后以2000r/min的转速离心10min去除细胞凋亡碎片，并收集细胞上清.最后，以10000r/min的转速离心20min，去除大泡膜，收集细胞上清于-80℃冰箱保存.炎症因子IL-6(白细胞介素-6)和TNF-α(肿瘤坏死因子-α)是人体免疫系统中起关键作用的重要蛋白质分子.根据试剂盒说明书，采用双抗夹心法ELISA测定细胞外泌体中炎症因子IL-6和TNF-α的分泌情况.
1.8　γ-H2AX免疫荧光测定
H2AX磷酸化产生的γ-H2AX含量水平可以清楚地反映出DNA的损伤程度及修复情况，而被广泛应用于DNA损伤和细胞凋亡研究中，成为一种重要的DNA损伤标记物[21].预先在12孔细胞培养板中放置细胞爬片，然后将处于对数增长期的A549细胞接种于细胞爬片.待细胞生长密度80%时，加入不同的OPFRs溶液处理.暴露24h后，各孔用PBS洗涤2次，并加入适量的4%多聚甲醛进行固定15min.吸除固定液，PBS洗3次，加入免疫荧光染色封闭液(含0.3% Triton X-100)封闭15min.吸除封闭液，加入兔γ-H2AX单克隆抗体(1:500稀释)4℃孵育过夜.PBS洗3次，加入Alexa Fluor 488标记山羊抗兔抗体(1:500稀释)37℃避光孵育1h，PBS清洗3次后，加入DAPI室温染色5min.最后，将细胞爬片倒扣到载玻片，中性树脂封片后用荧光显微镜进行拍摄.
1.9　数据处理
采用GraphPad Prism 9.0软件进行统计分析和图片绘制.实验结果为3个独立重复实验的平均值±标准差.各暴露组与对照组之间的显著性水平采用方差分析检验.P<0.05被认为具有统计学意义.
1.10　质量控制与质量保证
细胞毒性试验在96孔板中进行，每个暴露组，设置5个平行样，并进行3个独立重复实验.每组数据的标准差控制在10%以内.OPFRs的助溶剂采用对生物毒性较小的DMSO，各暴露组中的DMSO浓度均低于0.1%(V/V)，以确保DMSO对A549细胞生长无影响.空白对照组是加入含有0.1%(V/V)DMSO的DMEM培养基，每个毒性效应指标均以空白对照组为参考，图表的绘制都包含对照组的数据.OPFRs的浓度采用液质联用仪(Triple TOF 5600+)进行检测，结果表明细胞暴露前后，OPFRs的浓度均保持恒定.
2　结果与讨论
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2.1　体外细胞毒性
细胞活力是评价污染物对细胞毒性影响的关键指标，如图1显示，OPFRs均不同程度地降低了A549细胞活力，且具有剂量依赖性，与之前研究结果一致[22].24h暴露后，在低浓度下，OPFRs对A549细胞活力均无显著影响，细胞活力均高于90%;在较高浓度下，细胞活力均有所下降，TBOEP、TCIPP和IPPP暴露后的细胞活力分别为78.4%，84.31%和92.7%，TBOEP降低细胞活力效应略高于TCIPP和IPPP;在500 μmol/L高浓度暴露下，TBOEP使细胞活力不到5%，远低于TCIPP和IPPP暴露后的细胞活力.对比3种物质可以看出，TBOTP对细胞活力抑制作用最强，而TCIPP对细胞活力抑制作用略高于IPPP，毒性作用顺序为TBOEP>TCIPP>IPPP.OPFRs毒性强弱与Yu研究呼吸细胞结果一致，毒性作用顺序为TBOEP>TCIPP>芳基OPFRs[18].在另一项实验中，研究员使用含脂量高的HepG2肝癌细胞研究不同取代基的OPFRs的细胞毒性，毒性作用顺序为芳基OPFRs>TBOEP>TCIPP[23].这表明不同的取代基结构的OPFRs对细胞产生的毒性作用和毒性机制也不同.此外，由于构效关系不同，同分异构体的OPFRs毒性也并不完全相同，例如三(2-氯异丙基)磷酸(TCIPP)和三(2-氯乙基)磷酸(TCEP)，TCIPP对NCI-H1975的细胞活力损伤高于TCEP[16].
2.2　OPFRs对细胞内活性氧水平的影响
ROS(活性氧)在正常生理状态下参与细胞信号传导和调节，影响细胞增值与分化，但细胞在受到外界刺激后，ROS可能会过量产生，从而导致细胞损伤[24].故此，ROS的过量产生是评估细胞受到污染物毒性影响的重要指标之一.
作用24h后，根据图2所示，ROS水平与OPFRs呈剂量依赖关系，OPFRs浓度越高，细胞内ROS水平也越高.与对照组相比，低中高浓度的TBOEP使A549内活性氧水平分别上升了18.0%,40.8%,297.6%;低中高浓度的TCIPP使其分别了上升了17.3%,33.3%,69.0%;低中高浓度的IPPP使其分别上升了14.6%,30.6%,43.2%.在低浓度OPFRs暴露下，ROS有所上升，此时细胞未大量死亡.然而，在高浓度TBOEP暴露后，活性氧水平增加了3倍，结合上述细胞活力的抑制作用，可以推测出过量活性氧可能是导致A549细胞死亡的重要因素.类似的报道指出，TCEP和TPHP可以通过氧化应激方式降低大肠杆菌的细胞活力[25].An等[18]也发现，OPFRs可以在较高浓度下诱导各种细胞系产生过量ROS并降低细胞活性[18].溴化阻燃剂和部分OPFRs已被证实会诱导细胞产生过量的ROS，进而产生其他毒性损伤，例如细胞脂质过氧化、线粒体损伤与DNA损伤等[17].不同的OPFRs对细胞氧化应激的作用机制并不一致，一项使用大鼠肝细胞系细胞的研究表明，TBOEP增加谷胱甘肽过氧化物酶活性并降低谷胱甘肽还原酶活性，而TPHP则产生相反的效果[26].
2.3　OPFRs对A549线粒体膜电位的影响
线粒体是胞内细胞器负责细胞能量代谢，MMP(线粒体膜电位)是线粒体功能的重要指标，可以反映有害物质对细胞的毒性损伤程度[27].通过测量JC-1聚集体(红色)与JC-1单体(绿色)的比例来定量MMP去极化率，MMP下降通常是细胞凋亡和坏死的信号.图3显示，3个不同浓度的处理组与对照组相比，TBOEP暴露后的荧光比分别下降了6.6%，33.1%和46.5%，TCIPP暴露后的荧光比分别下降了5.0%，18.9%和29.9%，IPPP暴露后的荧光比分别下降了5.6%，17.5%和30.3%.研究结果可知，3种OPFRs对细胞膜均有损伤，TBOEP损伤程度高于TCIPP和IPPP，后两者对细胞膜损伤程度接近.此外，研究显示MMP降低与ROS上升存在一定关系.过量ROS可以改变线粒体通透性过渡孔(MPTP)的构象，从而触发MPTP的开放，并破坏离子平衡，导致呼吸链解耦联，进而释放细胞色素c进入细胞质，导致MMP减小[28].当细胞处于氧化应激状态时，线粒体内产生大量的ROS，从而导致线粒体膜电位降低.反过来，线粒体膜电位的降低又会进一步增加ROS的产生，形成一个恶性循环.另外有研究报道，线粒体凋亡的根本原因是Ca2+过载，当细胞内活性氧ROS含量升高时，可导致Ca2+-ATPase活性降低，从而致使线粒体Ca2+内流增加使线粒体凋亡[29].
2.4　OPFRs对A549细胞炎症因子水平的影响
炎症反应是机体对于细菌、病毒及其他有害刺激的保护性反应[30].当机体受到药物刺激时，细胞会释放生物活性细胞因子，例如炎症细胞因子、炎症介质和细胞粘附因子等，引起炎症反应，以缓解有害物质的毒性或是修复受损组织[31].过量的炎症因子会导致细胞发生程序性死亡.本研究表明(图4)，TBOEP、TCIPP和IPPP可诱导细胞分泌炎症因子IL-6和TNF-α.与对照组相比，3种OPFRs均会导致细胞内IL-6和TNF-α含量上升，且呈剂量依赖性关系. OPFRs浓度越高，IL-6和TNF-α表达水平也越高.3个不同浓度的TBOEP暴露后IL-6分别上升了18.8%，82.8%和124.4%，TNF-α含量分别上升了33.5%，103.9%和262.7%.TBOEP对炎症因子的刺激作用远高于TCIPP和IPPP.TCIPP导致A549细胞炎症因子水平上升程度略高于IPPP.氧化应激和炎症因子水平变化趋势相似，这表明两者可能存在某种联系.根据以往的研究，氧化应激可激活转录因子激活蛋白-1和NF-κB信号通路，导致NF-κB的磷酸化进而导致促炎症因子和趋化因子相关基因的表达，从而在免疫和炎症反应中发挥关键作用[32].另外有研究报道，OPFRs也可以增加细胞内NLRP3炎症小体水平，加重细胞炎症反应，促使半胱天冬酶激活和白细胞介素分泌[33].本研究表明炎症加重是OPFRs诱导细胞毒性的潜在机制.
2.5　OPFRs对A549细胞DNA的损伤
DNA损伤是氧化应激的常见后果，环境污染物可直接或间接引起活性氧攻击细胞核内的DNA，导致DNA断裂[21].如图5所示，根据免疫荧光染色显示，OPFRs暴露导致γ-H2AX的升高，这与氧化应激一致.此外，A549细胞内γ-H2AX含量呈浓度依赖性增加，OPFRs在高浓度下，会引发更严重的DNA损伤.值得注意的是，TBOEP对A549细胞DNA损伤高于TCIPP和IPPP，在高浓度下，γ-H2AX数量点数最多，这说明高浓度的TBOEP对细胞有明显的DNA损伤作用.Rendic等[34]均发现TBOEP可以特异性激活细胞色素P450酶导致人肝癌细胞内γ-H2AX表达上升.相同浓度暴露下，TBOEP对A549细胞DNA损伤高于TCIPP和IPPP，这表明TBOEP具有更高的毒性效应.TCIPP和IPPP对A549细胞损伤能力相近，这可能与TCIPP和IPPP的诱导A549产生氧化应激能力相近有关.在过去的研究中，氧化应激与DNA损伤之间的密切关系已被广泛研究[35]，氧化性DNA损伤是最常见的细胞遗传学损伤之一[36].故此，本文猜测OPFRs对A549细胞的DNA损伤很可能是氧化性损伤.
2.6　OPFRs对A549细胞毒性影响的综合评估
比较TBOEP、TCIPP和IPPP对A549细胞的综合影响，首先将细胞活力、ROS水平、MMP水平、IL-6和TNF-α做归一化处理，然后分别以雷达图形式表示在低浓度(15.63μmol/L)、中浓度(125μmol/L)和高浓度(500μmol/L)的不同指标间的差异.如图6所示，本实验中OPFRs导致细胞炎症因子水平变化水平最为显著，其次为ROS水平.在不同浓度下，TBOEP引起A549炎症水平变化(IL-6和TNF-α)均高于同浓度下的TCIPP和IPPP，并且随着剂量上升，TBOEP与TCIPP、IPPP变化差值增大.随着浓度的升高，TBEOP与TCIPP组的归一化后TNF-α差值从0.04上升至1.8，TBEOP与IPPP差值从0.17上升至1.99，这表明TBOEP更能引起A549细胞发生炎症反应.相同的，ROS变化也十分显著，TBEOP与TCIPP组的归一化后TNF-α差值从0.01上升至2.29，TBEOP与IPPP差值从0.04上升至2.55，这表明氧化应激是TBOEP主要的致毒机制.然而，在低浓度时，暴露在不同OPFRs中的A549细胞的细胞活力、ROS水平和MMP水平差异不显著;在中浓度时，TBOEP暴露下的A549细胞的细胞活力和MMP水平低于TCIPP和IPPP暴露组;在高浓度时，TBOEP暴露后的细胞活力和MMP水平显著低于其余组.总体来看，3种OPFRs对A549细胞毒性作用顺序为TBOEP > TCIPP ≈ IPPP.
2.7　OPFRs对A549细胞的致毒机制
通过研究细胞活力、氧化应激、凋亡指标和炎症反应的相关性，分析了OPFRs的细胞毒性机制.以TBOEP、TCIPP和IPPP浓度为自变量，以细胞毒性参数和4个参数(ROS、MMP、IL-6和TNF-α)为因变量，进行Pearson(双尾)相关性分析.由表1可知，OPFRs的细胞活力与MMP呈正相关，与ROS、IL-6、TNF-α水平呈负相关，差异有统计学意义(P<0.01).值得注意的是，与其他OPFRs相比，TBOEP暴露组中的细胞活力与ROS、TNF-α的相关性系数绝对值更高，分别为-0.993和-0.981，具有很强的负相关性.因此，烷基-OPFRs可能带来更强的氧化应激和炎症风险，这与Zhu等[37]研究结果一致.
通过表1中的数据发现，细胞内ROS与IL-6、TNF-α呈正相关，与MMP呈负相关.有研究表明，OPFRs可导致细胞内ROS水平超载，通过氧化应激方式诱导DNA损伤与细胞死亡，加剧细胞炎症反应[38].另外，线粒体已被证明在炎症水平的调节中起关键作用[39].OPFRs会破坏MMP的完整性，增加线粒体膜的通透性，导致MMP降低[28]，引发线粒体功能障碍，甚至诱导细胞凋亡[40].然而，线粒体功能障碍以及细胞凋亡都可能会促使细胞分泌炎症因子，加重细胞炎症损伤状况[39].在本研究中，ROS、炎症因子与细胞毒性的显著相关性可能是由于ROS增加引起氧化应激损伤，以及炎症因子水平升高引发炎症反应导致细胞活性降低.故此，OPFRs对A549细胞的毒性机制主要为ROS超载导致的氧化应激以及炎症损伤，氧化应激和炎症会损害个体的防御机制，诱导多种自身免疫性疾病.
3　结论
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3.1　所有OPFRs均可抑制细胞活力、促使过量ROS的产生、引起线粒体功能障碍、诱导细胞炎症反应和细胞DNA损伤.
3.2　TBOEP对A549细胞的细胞毒性最强，TCIPP和IPPP毒性效应相近.值得注意的是，在低浓度下三者毒性表现差异并不大，在中高浓度时，毒性表现差异较大.特别是在高浓度500μmol/L的TBOEP暴露下，细胞活力不到5%，细胞内活性氧水平上升3倍，线粒体膜电位降低了46.5%，炎症因子IL-6和TNF-α的分泌量上升了124.4%和262.7%.
基金
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  • 国家自然科学基金资助项目(22176097)
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参考文献 引证文献
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  • 接收时间：2024-11-08
  • 首发时间：2026-02-27
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  • 收稿日期：2024-11-08
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    南京理工大学环境与生物工程学院，江苏 南京 210000

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