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Article(id=1195009884086317453, tenantId=1146029695717560320, journalId=1190317699101192196, issueId=1195009883369091469, articleNumber=1001-2494(2025)09-0907-08, orderNo=null, doi=10.11669/cpj.2025.09.002, pmid=null, cstr=null, oa=null, hot=null, price=null, onlineType=0, articleFormat=0, articleType=null, articleTypeStr=research-article, receivedDate=1721750400000, receivedDateStr=2024-07-24, revisedDate=null, revisedDateStr=null, acceptedDate=null, acceptedDateStr=null, onlineDate=1762842158576, onlineDateStr=2025-11-11, pubDate=1746028800000, pubDateStr=2025-05-01, doiRegisterDate=null, doiRegisterDateStr=null, onlineIssueDate=1762842158576, onlineIssueDateStr=2025-11-11, onlineJustAcceptDate=null, onlineJustAcceptDateStr=null, onlineFirstDate=null, onlineFirstDateStr=null, sourceXml=null, magXml=null, createTime=1762842158576, creator=13701087609, updateTime=1762842158576, updator=13701087609, issue=Issue{id=1195009883369091469, tenantId=1146029695717560320, journalId=1190317699101192196, year='2025', volume='60', issue='9', pageStart='893', pageEnd='1004', issueExtLink='null', onlineDate='null', pubDate='null', beforeIssueId=null, nextIssueId=null, price=null, status=1, issueComplete=1, articleOrder=1, issueType=-1, specialIssue=0, createTime=1762842158405, creator=13701087609, updateTime=1762846632399, updator=13701087609, preIssue=null, nextIssue=null, ext={EN=IssueExt(id=1195028649066893312, tenantId=1146029695717560320, journalId=1190317699101192196, issueId=1195009883369091469, language=EN, specialIssueTitle=, coverIllustrator=null, specialIssueEditor=, specialIssueAbout=), CN=IssueExt(id=1195028649071087617, tenantId=1146029695717560320, journalId=1190317699101192196, issueId=1195009883369091469, language=CN, specialIssueTitle=, coverIllustrator=null, specialIssueEditor=, specialIssueAbout=)}, issueFiles=null}, startPage=907, endPage=914, ext={EN=ArticleExt(id=1195009884337975697, articleId=1195009884086317453, tenantId=1146029695717560320, journalId=1190317699101192196, language=EN, title=Reproductive Toxicity Mechanism of Tripterygium wilfordii Tablet Based on Gut Microbiota and Metabolomics, columnId=null, journalTitle=Chinese Pharmaceutical Journal, columnName=null, runingTitle=null, highlight=null, articleAbstract=

OBJECTIVE To investigate the toxic mechanisms of Tripterygium wilfordii tablet(TWT) causing male mice reproductive damage and to identify detoxification targets. METHODS TWT was used to induce reproductive injury in mice. Metagenomic and metabolomics analysis were employed to perform differential analysis and functional analysis of gut microbiota and metabolites, aiming to identify the causative strains and metabolic pathways for reproductive injury, and to elucidate the mechanisms by which the microbiota and metabolites affect reproductive injury. RESULTS TWT significantly reduced the testicular index and sperm count in mice, leading to oxidative stress in testicular tissues. And TWT disrupted the gut microbiota and testicular metabolism. Supplementation with exogenous indole-3-lactic acid and Lactobacillus reuteri could regulate oxidative stress and improve testicular damage induced by TWT. CONCLUSION TWT cause reproductive damage by disrupting the gut microbiota and testicular metabolism. Lactobacillus reuteri and its metabolite, indole-3-lactic acid, improve male mice reproductive damage induced by TWHF tablets by regulating oxidative stress in testicular tissues.

, correspAuthors=Fei LI, 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=Liqiong CHEN, Jiahui CHEN, Bin LI, Dongmei YAN, Yan CHENG, Ting ZHANG, Fei LI), CN=ArticleExt(id=1195010372915671972, articleId=1195009884086317453, tenantId=1146029695717560320, journalId=1190317699101192196, language=CN, title=肠道菌群改善雷公藤片致雄性小鼠生殖毒性的研究, columnId=1195009884417667474, journalTitle=中国药学杂志, columnName=肠道菌药学研究专栏, runingTitle=null, highlight=null, articleAbstract=

目的 研究雷公藤片致雄性生殖功能损伤的机制,寻找作用靶点。方法 利用雷公藤片诱导雄性小鼠生殖功能损伤,采用宏基因组学及代谢组学对肠道菌群及代谢物进行差异分析及功能分析,寻找致生殖损伤差异菌株及代谢通路,阐释菌群和代谢物影响生殖毒性的机制。结果 雷公藤片引起雄性小鼠睾丸氧化应激损伤,模型组小鼠的睾丸指数降低、精子数量减少;扰乱小鼠肠道菌群及睾丸代谢;补充外源性的吲哚-3-乳酸及罗伊乳杆菌能够调节氧化应激相关基因表达,改善雷公藤片诱导的睾丸损伤。结论 雷公藤片通过扰乱肠道菌群及睾丸代谢引起雄性小鼠生殖功能损伤,罗伊乳杆菌及其代谢产物吲哚-3-乳酸通过调节睾丸组织的氧化应激相关基因,改善雷公藤片诱导的雄性生殖功能损伤。

, correspAuthors=李飞, authorNote=null, correspAuthorsNote=
*李飞,男,博士,研究员 研究方向:肝损伤的代谢调控与药物干预 Tel:(0791)86362367
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陈丽琼,女,硕士研究生 研究方向:中药药理

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陈丽琼,女,硕士研究生 研究方向:中药药理

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陈丽琼,女,硕士研究生 研究方向:中药药理

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DOI: 10.1016/j.nut.2022.111673., articleTitle=Lactobacillus reuteri improves function of the intestinal barrier in rats with acute liver failure through Nrf-2/HO-1 pathway, refAbstract=null), Reference(id=1195061666313413038, tenantId=1146029695717560320, journalId=1190317699101192196, articleId=1195009884086317453, doi=null, pmid=null, pmcid=null, year=2023, volume=15, issue=5, pageStart=19, pageEnd=24, url=null, language=null, rfNumber=[25], rfOrder=24, authorNames=GE L Y, LIN S Y, CHEN H X, journalName=Chin J Front Med Sci Electrom Vers(中国医学前沿杂志电子版), refType=null, unstructuredReference=GE L Y, LIN S Y, CHEN H X. Application of systemic and topical drugs in the treatment of psoriasis[J]. Chin J Front Med Sci Electrom Vers(中国医学前沿杂志电子版), 2023, 15(5): 19-24., articleTitle=Application of systemic and topical drugs in the treatment of psoriasis, refAbstract=null)], funds=[Fund(id=1195061664585359765, tenantId=1146029695717560320, journalId=1190317699101192196, articleId=1195009884086317453, awardId=ZYYC21003, language=CN, fundingSource=四川大学华西医院“1·#3·#5工程”项目资助(ZYYC21003), fundOrder=null, country=null)], companyList=[AuthorCompany(id=1195061661221527888, tenantId=1146029695717560320, journalId=1190317699101192196, articleId=1195009884086317453, xref=1, ext=[AuthorCompanyExt(id=1195061661229916497, tenantId=1146029695717560320, journalId=1190317699101192196, articleId=1195009884086317453, companyId=1195061661221527888, language=EN, country=null, province=null, city=null, postcode=null, companyName=null, departmentName=null, remark=1 Academician Workstation, Jiangxi University of Chinese Medicine, Nanchang 330004, China), AuthorCompanyExt(id=1195061661234110802, tenantId=1146029695717560320, journalId=1190317699101192196, articleId=1195009884086317453, companyId=1195061661221527888, language=CN, country=null, province=null, city=null, postcode=null, companyName=null, departmentName=null, remark=1 江西中医药大学院士工作站, 南昌 330004)]), AuthorCompany(id=1195061661305413971, tenantId=1146029695717560320, journalId=1190317699101192196, articleId=1195009884086317453, xref=2, ext=[AuthorCompanyExt(id=1195061661313802580, tenantId=1146029695717560320, journalId=1190317699101192196, articleId=1195009884086317453, companyId=1195061661305413971, language=EN, country=null, province=null, city=null, postcode=null, companyName=null, departmentName=null, remark=2 Laboratory of Hepatointestinal Diseases and Metabolism, Frontiers Science Center for Disease-related Molecular Network, West China Hospital, Sichuan University, Chengdu 610041, China), AuthorCompanyExt(id=1195061661317996885, tenantId=1146029695717560320, journalId=1190317699101192196, articleId=1195009884086317453, companyId=1195061661305413971, language=CN, country=null, province=null, city=null, postcode=null, companyName=null, departmentName=null, remark=2 四川大学华西医院疾病分子网络前沿科学中心肝肠疾病与代谢研究室, 成都 610041)]), AuthorCompany(id=1195061661376717142, tenantId=1146029695717560320, journalId=1190317699101192196, articleId=1195009884086317453, xref=3, ext=[AuthorCompanyExt(id=1195061661385105751, tenantId=1146029695717560320, journalId=1190317699101192196, articleId=1195009884086317453, companyId=1195061661376717142, language=EN, country=null, province=null, city=null, postcode=null, companyName=null, departmentName=null, remark=3 Innovative Institute of Chinese Medicine and Pharmacy, Chengdu University of Traditional Chinese Medicine, Chengdu 611100, China), AuthorCompanyExt(id=1195061661389300056, tenantId=1146029695717560320, journalId=1190317699101192196, articleId=1195009884086317453, companyId=1195061661376717142, language=CN, country=null, province=null, city=null, postcode=null, companyName=null, departmentName=null, remark=3 成都中医药大学中医药创新研究所, 成都 611100)])], figs=[ArticleFig(id=1195061663532589447, tenantId=1146029695717560320, journalId=1190317699101192196, articleId=1195009884086317453, language=EN, label=Fig.1, caption=The reproductive injury was triggered by Tripterygium wilfordii tablet(TWT). n=6, $\overline{x}$±s

A-testis index of mice (testis mass/body mass×100%) and sperm count in the mouse epididymis; B-HE staining of testis, the arrow indicates the damaged area; C-mRNA level involved in spermatogenesis in the testis; D-mRNA level related to oxidative stress;1)P<0.001, vs control group.

, figureFileSmall=k8Zy2YLgq7IrB9rX21fAQA==, figureFileBig=PSlJys0sJwqCNHru6qcwPQ==, tableContent=null), ArticleFig(id=1195061663595504008, tenantId=1146029695717560320, journalId=1190317699101192196, articleId=1195009884086317453, language=CN, label=图1, caption=雷公藤片(TWT)诱导雄性生殖损伤。n=6, $\overline{x}$±s

A-小鼠的睾丸指数(睾丸质量/体质量×100%)及精子数量;B-睾丸组织苏木精-伊红(HE)染色,箭头所示为损伤部位;C-睾丸中与精子生成相关的基因mRNA水平;D-睾丸中氧化应激相关基因表达水平;与对照组相比,1)P<0.001。

, figureFileSmall=k8Zy2YLgq7IrB9rX21fAQA==, figureFileBig=PSlJys0sJwqCNHru6qcwPQ==, tableContent=null), ArticleFig(id=1195061663671001481, tenantId=1146029695717560320, journalId=1190317699101192196, articleId=1195009884086317453, language=EN, label=Fig.2, caption=The loss of gut microbiota exacerbated the reproductive toxicity induced by TWT. n=5, $\overline{x}$±s

A-testis index of mice(testis mass/body mass×100%); B-sperm count in the mouse epididymis; C-mRNA level involved in spermatogenesis in the testis; D-HE staining of testis, the arrow indicates the damaged area; 1)P<0.05, 2)P<0.01,3)P<0.001, vs control group; 4)P<0.001, vs TWT group.

, figureFileSmall=V0J6y1yKQYkKRDU+NyT+dQ==, figureFileBig=xOTzPNCrWv0zwLZqiThSdg==, tableContent=null), ArticleFig(id=1195061663738110346, tenantId=1146029695717560320, journalId=1190317699101192196, articleId=1195009884086317453, language=CN, label=图2, caption=菌群缺失加重TWT生殖毒性。n=5, $\overline{x}$±s

A-小鼠的睾丸指数(睾丸质量/体质量×100%);B-小鼠附睾精子数量;C-睾丸中与精子生成相关的基因mRNA水平;D-睾丸组织HE染色, 箭头所示为损伤部位;与对照组相比,1)P<0.05,2)P<0.01,3)P<0.001;与TWT组比较,4)P<0.001。

, figureFileSmall=V0J6y1yKQYkKRDU+NyT+dQ==, figureFileBig=xOTzPNCrWv0zwLZqiThSdg==, tableContent=null), ArticleFig(id=1195061663796830603, tenantId=1146029695717560320, journalId=1190317699101192196, articleId=1195009884086317453, language=EN, label=Fig.3, caption=Gut microbiota dysbiosis of TWT treated mice. n=4, $\stackrel{-}{x}$±s

A-α diversity; B-the PCA graph of gut microbiota; C-species distribution maps; D-the cladogram of LEfSe; E-analysis of functional differences in gut microbiota; F-the level of Lactobacillus and Lactobacillus reuteri; 1)P<0.05,2)P<0.01, vs control group.

, figureFileSmall=ax5R9EmvMGmUeJMX22kPGw==, figureFileBig=0ZgAUcihJjbiQsYrOpzbOg==, tableContent=null), ArticleFig(id=1195061663851356556, tenantId=1146029695717560320, journalId=1190317699101192196, articleId=1195009884086317453, language=CN, label=图3, caption=TWT致小鼠肠道菌群失调。n=4, $\stackrel{-}{x}$±s

A-α多样性;B-主成分分析(PCA)评分图;C-物种分布图;D-线性判别分析(LEfSe)环形进化分支图;E-肠道菌群功能差异分析;F-乳杆菌属及罗伊乳杆菌水平;与对照组相比,1)P<0.05,2)P<0.01。

, figureFileSmall=ax5R9EmvMGmUeJMX22kPGw==, figureFileBig=0ZgAUcihJjbiQsYrOpzbOg==, tableContent=null), ArticleFig(id=1195061663914271117, tenantId=1146029695717560320, journalId=1190317699101192196, articleId=1195009884086317453, language=EN, label=Fig.4, caption=Labtobacillus reuteri ameliorated TWT-induced reproductive injury. n=6, $\overline{x}$±s

A-mRNA level involved in spermatogenesis in the testis; B-mRNA level related to oxidative stress; C-HE staining of testis, the arrow indicates the location of the difference in damage;1)P<0.001, vs control group; 2)P<0.05,3)P<0.001, vs TWT group.

, figureFileSmall=4KFaGo7M4wYDMFraE4mJKQ==, figureFileBig=DGbK9Crn7NbKGeFacTw7Dw==, tableContent=null), ArticleFig(id=1195061663985574286, tenantId=1146029695717560320, journalId=1190317699101192196, articleId=1195009884086317453, language=CN, label=图4, caption=罗伊乳杆菌改善TWT诱导的生殖损伤。n=6, $\overline{x}$±s

A-睾丸中与精子生成相关的基因mRNA水平;B-睾丸中氧化应激相关基因表达水平;C-HE染色,箭头所示为损伤差异部位;与对照组相比,1)P<0.001;与TWT组相比,2)P<0.05,3)P<0.001。

, figureFileSmall=4KFaGo7M4wYDMFraE4mJKQ==, figureFileBig=DGbK9Crn7NbKGeFacTw7Dw==, tableContent=null), ArticleFig(id=1195061664044294543, tenantId=1146029695717560320, journalId=1190317699101192196, articleId=1195009884086317453, language=EN, label=Fig.5, caption=Non-targeted metabolomics analysis of testis. n=5, $\stackrel{-}{x}$±s

A-the PCA graph and S-plot graph of testis ions; B-the heatmap of changed metabolites in testis; C-the level of ILA and IPA;1)P<0.001, vs control group.

, figureFileSmall=1sEhsEl2jznFBNgtfLmJUQ==, figureFileBig=gzRdoC64YFrcwAlNT2BRQg==, tableContent=null), ArticleFig(id=1195061664107209104, tenantId=1146029695717560320, journalId=1190317699101192196, articleId=1195009884086317453, language=CN, label=图5, caption=睾丸代谢物非靶向代谢组学分析。n=5, $\stackrel{-}{x}$±s

A-睾丸离子PCA图及S-plot图;B-睾丸代谢物热图;C-吲哚-3-乳酸(ILA)和吲哚-3-丙酸水平(IPA);与对照组相比,1)P<0.001。

, figureFileSmall=1sEhsEl2jznFBNgtfLmJUQ==, figureFileBig=gzRdoC64YFrcwAlNT2BRQg==, tableContent=null), ArticleFig(id=1195061664170123665, tenantId=1146029695717560320, journalId=1190317699101192196, articleId=1195009884086317453, language=EN, label=Fig.6, caption=ILA ameliorated TWT-induced reproductive injury. n=6, $\overline{x}$±s

A-mRNA level involved in spermatogenesis in the testis;B-mRNA level related to oxidative stress; C-HE staining of testis, the arrow indicates the location of the difference in damage;1)P<0.001, vs control group;2)P<0.05, 3)P<0.01, vs TWT group.

, figureFileSmall=rxYqYWVO13X0edTjaBz1Lg==, figureFileBig=iCI1w/AZ/ipxq7SEhphP1w==, tableContent=null), ArticleFig(id=1195061664241426834, tenantId=1146029695717560320, journalId=1190317699101192196, articleId=1195009884086317453, language=CN, label=图6, caption=ILA改善TWT诱导的生殖功能损伤。n=6, $\overline{x}$±s

A-睾丸中与精子生成相关的基因mRNA水平;B-睾丸中氧化应激基因表达水平; C-HE染色,箭头所示为损伤差异部位;与对照组相比,1)P<0.001;与TWT组相比,2)P<0.05, 3)P<0.01。

, figureFileSmall=rxYqYWVO13X0edTjaBz1Lg==, figureFileBig=iCI1w/AZ/ipxq7SEhphP1w==, tableContent=null), ArticleFig(id=1195061664329507219, tenantId=1146029695717560320, journalId=1190317699101192196, articleId=1195009884086317453, language=EN, label=Tab.1, caption=

Primers for RT-qPCR

, figureFileSmall=null, figureFileBig=null, tableContent=
Gene F primer R primer
Gapdh TTGTATGTGCAACAATCTCCAC CGTCCCGTAGACAAAATGTGT
Id4 CGGTGGCTTGTTTCTCTTAATTTC TGAACAAGCAGGGTGACAG
Bmi1 TCTTCTTCTCTTCATCTCATTTTTGA AAACCAGACCACTCCTGAACA
Tdrd7 CTAAGGGCTGTCCTGCAGTC TGAGAGTTGCCTTTGGCTTT
Adam3 GGTAACGACAGCCAGCAGTAAT GCTTCTTGGTTGTGGTCTTCTT
Brdt AGGGAAGCCAGTGAAAGCAT TCCTTCGCATTATGCTCCAG
Sod1 AAGCGGTGAACCAGTTGTGTT AGCCTTGTGTATTGTCCCCATACT
Sod2 AGGAGAGTTGCTGGAGGCTA TCTGTAAGCGACCTTGCTCC
Ho-1 GAGCCTGAATCGAGCAGAAC AGCCTTCTCTGGACACCTGA
Cat CGACCAGGGCATCAAAAACTT AACGTCCAGGACGGGTAATTG
Gpx4 GATGGAGCCCATTCCTGAACC CCCTGTACTTATCCAGGCAGA
), ArticleFig(id=1195061664392421780, tenantId=1146029695717560320, journalId=1190317699101192196, articleId=1195009884086317453, language=CN, label=表1, caption=

实时荧光定量反转录聚合酶链式反应(RT-qPCR)引物序列

, figureFileSmall=null, figureFileBig=null, tableContent=
Gene F primer R primer
Gapdh TTGTATGTGCAACAATCTCCAC CGTCCCGTAGACAAAATGTGT
Id4 CGGTGGCTTGTTTCTCTTAATTTC TGAACAAGCAGGGTGACAG
Bmi1 TCTTCTTCTCTTCATCTCATTTTTGA AAACCAGACCACTCCTGAACA
Tdrd7 CTAAGGGCTGTCCTGCAGTC TGAGAGTTGCCTTTGGCTTT
Adam3 GGTAACGACAGCCAGCAGTAAT GCTTCTTGGTTGTGGTCTTCTT
Brdt AGGGAAGCCAGTGAAAGCAT TCCTTCGCATTATGCTCCAG
Sod1 AAGCGGTGAACCAGTTGTGTT AGCCTTGTGTATTGTCCCCATACT
Sod2 AGGAGAGTTGCTGGAGGCTA TCTGTAAGCGACCTTGCTCC
Ho-1 GAGCCTGAATCGAGCAGAAC AGCCTTCTCTGGACACCTGA
Cat CGACCAGGGCATCAAAAACTT AACGTCCAGGACGGGTAATTG
Gpx4 GATGGAGCCCATTCCTGAACC CCCTGTACTTATCCAGGCAGA
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肠道菌群改善雷公藤片致雄性小鼠生殖毒性的研究
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陈丽琼 1, 2 , 陈家辉 1, 2 , 李斌 1 , 颜冬梅 1 , 程燕 1 , 张婷 2, 3 , 李飞 2, *
中国药学杂志 | 肠道菌药学研究专栏 2025,60(9): 907-914
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中国药学杂志 | 肠道菌药学研究专栏 2025, 60(9): 907-914
肠道菌群改善雷公藤片致雄性小鼠生殖毒性的研究
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陈丽琼1, 2, 陈家辉1, 2, 李斌1, 颜冬梅1, 程燕1, 张婷2, 3, 李飞2, *
作者信息
  • 1 江西中医药大学院士工作站, 南昌 330004
  • 2 四川大学华西医院疾病分子网络前沿科学中心肝肠疾病与代谢研究室, 成都 610041
  • 3 成都中医药大学中医药创新研究所, 成都 611100

    • 陈丽琼,女,硕士研究生 研究方向:中药药理

通讯作者:

*李飞,男,博士,研究员 研究方向:肝损伤的代谢调控与药物干预 Tel:(0791)86362367
Reproductive Toxicity Mechanism of Tripterygium wilfordii Tablet Based on Gut Microbiota and Metabolomics
Liqiong CHEN1, 2, Jiahui CHEN1, 2, Bin LI1, Dongmei YAN1, Yan CHENG1, Ting ZHANG2, 3, Fei LI2, *
Affiliations
  • 1 Academician Workstation, Jiangxi University of Chinese Medicine, Nanchang 330004, China
  • 2 Laboratory of Hepatointestinal Diseases and Metabolism, Frontiers Science Center for Disease-related Molecular Network, West China Hospital, Sichuan University, Chengdu 610041, China
  • 3 Innovative Institute of Chinese Medicine and Pharmacy, Chengdu University of Traditional Chinese Medicine, Chengdu 611100, China
出版时间: 2025-05-01 doi: 10.11669/cpj.2025.09.002
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摘要
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目的 研究雷公藤片致雄性生殖功能损伤的机制,寻找作用靶点。方法 利用雷公藤片诱导雄性小鼠生殖功能损伤,采用宏基因组学及代谢组学对肠道菌群及代谢物进行差异分析及功能分析,寻找致生殖损伤差异菌株及代谢通路,阐释菌群和代谢物影响生殖毒性的机制。结果 雷公藤片引起雄性小鼠睾丸氧化应激损伤,模型组小鼠的睾丸指数降低、精子数量减少;扰乱小鼠肠道菌群及睾丸代谢;补充外源性的吲哚-3-乳酸及罗伊乳杆菌能够调节氧化应激相关基因表达,改善雷公藤片诱导的睾丸损伤。结论 雷公藤片通过扰乱肠道菌群及睾丸代谢引起雄性小鼠生殖功能损伤,罗伊乳杆菌及其代谢产物吲哚-3-乳酸通过调节睾丸组织的氧化应激相关基因,改善雷公藤片诱导的雄性生殖功能损伤。

雷公藤片  /  生殖损伤  /  肠道菌群  /  代谢组学

OBJECTIVE To investigate the toxic mechanisms of Tripterygium wilfordii tablet(TWT) causing male mice reproductive damage and to identify detoxification targets. METHODS TWT was used to induce reproductive injury in mice. Metagenomic and metabolomics analysis were employed to perform differential analysis and functional analysis of gut microbiota and metabolites, aiming to identify the causative strains and metabolic pathways for reproductive injury, and to elucidate the mechanisms by which the microbiota and metabolites affect reproductive injury. RESULTS TWT significantly reduced the testicular index and sperm count in mice, leading to oxidative stress in testicular tissues. And TWT disrupted the gut microbiota and testicular metabolism. Supplementation with exogenous indole-3-lactic acid and Lactobacillus reuteri could regulate oxidative stress and improve testicular damage induced by TWT. CONCLUSION TWT cause reproductive damage by disrupting the gut microbiota and testicular metabolism. Lactobacillus reuteri and its metabolite, indole-3-lactic acid, improve male mice reproductive damage induced by TWHF tablets by regulating oxidative stress in testicular tissues.

Tripterygium wilfordii tablet  /  reproductive injury  /  gut microbiota  /  metabolomics
陈丽琼, 陈家辉, 李斌, 颜冬梅, 程燕, 张婷, 李飞. 肠道菌群改善雷公藤片致雄性小鼠生殖毒性的研究. 中国药学杂志, 2025 , 60 (9) : 907 -914 . DOI: 10.11669/cpj.2025.09.002
Liqiong CHEN, Jiahui CHEN, Bin LI, Dongmei YAN, Yan CHENG, Ting ZHANG, Fei LI. Reproductive Toxicity Mechanism of Tripterygium wilfordii Tablet Based on Gut Microbiota and Metabolomics[J]. Chinese Pharmaceutical Journal, 2025 , 60 (9) : 907 -914 . DOI: 10.11669/cpj.2025.09.002
正文
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雷公藤(Tripterygium wilfordii Hook. f.)为卫矛科雷公藤属藤本灌木植物,根或根的木质部入药,具有祛风、解毒、杀虫的功效,主要用于治疗风湿性关节炎、皮肤发痒等[1]。雷公藤片(Tripterygium wilfordii tablet,TWT)是临床常用的雷公藤制剂,活性成分有二萜、三萜和生物碱等[2],具有抗炎、抗肿瘤、免疫调节等作用,用于类风湿关节炎、肾小球肾炎红斑狼疮等自身免疫性疾病,但其生殖毒性限制了其临床应用[3]。动物模型研究表明,连续给予TWT会显著增加附睾精子畸形率、导致睾丸指数下降和曲精管疾病[4]。尽管目前TWT的毒性研究已有很多报道[5],但TWT致生殖毒性的机制尚不清楚。
肠道菌群是影响宿主生物学的关键“器官”,在人体的免疫和代谢中发挥着一些基本功能[6]。肠道菌群对维持男性生殖功能至关重要,菌群的紊乱可导致生殖功能障碍[7]。已有研究表明,雷公藤甲素可通过诱导肠道菌群紊乱致睾丸损伤,高能量饮食能够扰乱肠道菌群影响正常绵羊的精子发生[8-9]。此外,肠道微生物群可能在改善高脂肪饮食诱导的生殖功能障碍和邻苯二甲酸二(2-乙基己基)酯(DHEP)诱导的小鼠生殖毒性方面发挥重要作用[10]。
本实验拟通过TWT引起的生殖损伤模型来研究微生物群在生殖损伤中的作用,首先采用代谢组学分析比较TWT给药前后对睾丸内源性代谢物的影响,接着采用宏基因组学方法研究TWT对肠道菌群的影响,以探讨TWT的生殖毒性机制,为TWT致生殖毒性的机制研究提供科学依据。
1 材料与仪器
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1.1 动物
SPF级C57BL/6J雄鼠,8~10周龄[江苏集萃药康生物科技股份有限公司,动物生产许可证号:SCXK(苏)2023-0009,动物质量合格证号: 511214900035422],小鼠饲养于12 h昼夜交替环境中,饲养室温控制在(22±1)℃,相对湿度(50±2)%,自由饮食饮水。动物实验经四川大学华西医院动物伦理委员会批准(20231127003)。
1.2 药物与试剂
TWT[货号:Z42021534,华润三九(黄石)制药有限公司];吲哚-3-乳酸(indole-3-lactic acid, ILA)(货号:I157602-1G,上海阿拉丁生化技术有限公司);罗伊乳杆菌(Lactobacillus reuteri)(货号:22DB083,拜奥公司);粪便基因组DNA提取试剂盒(货号:DP328,天根生化科技有限公司);Trizol(货号:15596026,美国Invitrogen公司);HiScript Ⅲ RT SuperMix for qPCR、Taq Pro Universal SYBR qPCR Master Mix(南京诺唯赞生物科技股份有限公司);体积分数10%福尔马林、中性树脂、苏木素、伊红、MRS肉汤(北京索莱宝科技有限公司);甲醇、乙腈(色谱纯);甲醇、乙腈、甲酸(质谱级);甲硝唑、氨苄青霉素、硫酸新霉素(北京中生瑞泰科技有限公司);万古霉素(德国Merck公司)。
1.3 仪器
HPLC色谱柱(4.6 mm×150 mm,3.5 μm;2.1 mm×100 mm,1.8 μm,XDB-C18)(美国Agilent科技有限公司);聚合酶链式反应(PCR)仪(型号:SimpliAmp,美国Applied Biosystems公司);荧光定量PCR检测系统(型号:CFX ConnectTM,美国BioRad公司);氮吹仪(型号:Turbo Vap LV,瑞典Biotage公司);四极杆飞行时间液质联用系统(型号:6530 Q-TOF LC/MS,美国Agilent科技有限公司);E500厌氧工作站(型号:E500,上海塔正科技有限公司)。
2 方法
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2.1 动物实验
实验一:TWT诱导的雄性小鼠生殖功能损伤。取C57BL/6J小鼠12只,适应性喂养1周后随机分为2组,分别为对照组(Con)和TWT组,每组6只。TWT[每片含雷公藤甲素(triptolide, TP)12 μg]研磨后溶于质量分数0.5%羧甲基纤维素钠(CMC-Na)中,按1 760 mg·kg-1(TP 0.2 mg·kg-1)每日灌胃给药,灌胃体积为0.01 mL·g-1,连续灌胃14 d[11]。对照组在同等条件下灌胃等体积的0.5% CMC-Na。末次给予TWT间隔24 h后用CO2处死小鼠,采集血浆、睾丸、附睾及盲肠样本以便评估睾丸损伤、组织学观察、代谢组研究、菌群分析。
实验二:探究肠道菌群对TWT致雄性小鼠生殖毒性的影响。将C57BL/6J小鼠20只随机分为4组,分别为Con、TWT、抗生素(A)和A+TWT组,每组5只。抗生素由氨苄青霉素(0.25 mg·mL-1)、硫酸新霉素(0.25 mg·mL-1)、甲硝唑(0.25 mg·mL-1)和万古霉素(0.125 mg·mL-1)组成,溶于灭菌水后备用。A组及A+TWT组小鼠自由饮用含抗生素的水7 d[8]。第8天对TWT、A+TWT组小鼠灌胃883.3 mg·kg-1(TP 0.1 mg·kg-1)的TWT 14 d(溶于0.5%CMC-Na),其他组别在同样条件下灌胃等量的空白溶剂。第22天处死小鼠,采集血浆、睾丸、附睾及盲肠样本。
实验三:罗伊乳杆菌,在37 ℃的厌氧室中用MRS肉汤制备的培养基中培养10 h。在4 ℃、8 000×g(重力加速度)条件下离心罗伊乳杆菌培养基10 min。在无菌条件下用磷酸盐缓冲液(PBS)重悬后,将罗伊乳杆菌细胞以0.2 mL含有2×108CFU的量灌胃给小鼠。雄性小鼠随机分为4组(n=6):①空白组;②TWT组;③罗伊乳杆菌+TWT组(L.r+TWT);④罗伊乳杆菌组(L.r)。L.r+TWT组和L.r组给予罗伊乳杆菌移植14 d,每天在罗伊乳杆菌(0.2 mL含有2×108 CFU)给菌2 h后灌胃TWT(1 760 mg·kg-1)或0.5%CMC-Na 14 d[12]。末次给药间隔24 h后处死小鼠,采集血浆、睾丸、附睾及盲肠样本。
实验四:探究吲哚-3-乳酸对TWT诱导的雄性生殖损伤的保护作用。将小鼠随机分为4组:Con组(n=6)、TWT组(n=6)、ILA+TWT组(n=6)和ILA组(n=6)。ILA(10 mg·kg-1)灌胃3 d后[13],TWT组和ILA+TWT组每天灌胃TWT(1 760 mg·kg-1)14 d,在TWT给药期间,每隔1 d给予ILA(10 mg·kg-1),共7次[14]。在最后一剂TWT后24 h,通过CO2处死小鼠并采集血浆、睾丸、附睾及盲肠样本。
2.2 组织切片分析
睾丸组织在10%福尔马林中固定48 h,在不同浓度的乙醇中脱水,然后用二甲苯清除。石蜡包埋后,制备4 μm切片,并用苏木精和伊红染色,中性树胶封片,晾干后镜下观察。
2.3 代谢组学分析
用200 μL体积分数80%甲醇和5 μmol·L-1氯丙酰胺提取10 mg睾丸组织。采用四极杆飞行时间液质联用系统,反相XDB-C18色谱柱对样品进行分离。液体流速为0.3 mL·min-1。流动相A为体积分数0.01%甲酸水溶液,流动相B为0.01%甲酸乙腈溶液,原始数据由MS-DAIL处理以导出数据矩阵[15]。SIMCA-P+13.0(Umetrics,USA)用于主成分分析(principal component analysis,PCA)和正交偏最小二乘判别分析(orthogonal partial least squares discriminant analysis, OPLS-DA)。将变化后的代谢产物与人类代谢组数据库(HMDB)进行匹配。
2.4 宏基因组测序
天安粪便DNA试剂盒(中国天根)用于从盲肠内容物中提取微生物基因组DNA。宏基因组测序和生物信息学分析由华大基因完成。
2.5 实时荧光PCR(q-PCR)分析
使用Trizol试剂从冷冻睾丸组织中提取总RNA[11]。qPCR使用Taq Pro Universal SYBR qPCR Master Mix在CFX Connect实时系统(Bio-Rad Laboratories,USA)上进行。采用Gapdh作为内参,所用引物见表1。
2.6 统计分析
使用GraphPad Prism 8.0进行数据分析,双样本t检验用于评估两组之间的差异,单因素方差分析和Tukey事后检验用于多重比较。数据以 $\overline{x}$±s表示,P<0.05被认为具有统计学意义。
3 结果
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3.1 TWT诱导小鼠雄性生殖功能损伤
给药期间,TWT显著降低小鼠体质量,造模结束后对小鼠睾丸组织进行称重,计算器官指数(器官质量/体质量×100%)发现TWT显著降低睾丸指数(P<0.001),使用血球计数板对附睾精子数量计数,结果显示TWT组精子数量显著下降(P<0.001)。HE染色结果显示,空白组小鼠睾丸生精小管排列紧密,生精细胞及睾丸间质细胞数量丰富;与之相比TWT组小鼠睾丸的生精小管管径显著减小,生精上皮的厚度及生殖细胞的数量显著降低,组织出现大范围空泡化,表明TWT对小鼠的睾丸组织造成严重损伤。对睾丸组织mRNA水平变化进行检测发现,TWT显著降低了睾丸组织中与精子生成相关的基因(Id4、Bmi1、Brdt、Tdrd7和Adam3)表达水平(P<0.001),此外TWT影响了睾丸组织的氧化应激相关基因的表达水平,下调Sod1、Sod2、Gpx4的水平,上调Ho-1和Cat的水平,见图1。
3.2 菌群清除加重TWT诱导的雄性生殖功能损伤
分别对抗生素处理小鼠及正常饮水小鼠灌胃883.3 mg·kg-1(TP 0.1 mg·kg-1)TWT14 d,结果显示,A+TWT组睾丸指数显著降低,但对精子数量无明显影响。qPCR结果显示,与TWT组相比,抗生素显著降低了精子生成相关基因Bmi1、Tdrd7和Adam3的表达水平。HE染色结果显示,在883.3 mg·kg-1剂量下TWT组生精小管出现空泡化,小管排列较为松散,间质细胞密度降低;菌群耗尽后给予TWT显著缩小了生精小管直径,组织出现大面积空泡化,生精上皮变薄,生精细胞数量显著降低(图2)。本实验显示,肠道菌群对TWT生殖毒性有着重要影响,提示了肠道菌群对TWT诱导的雄性生殖毒性可能具有保护作用。
3.3 宏基因组学分析TWT给药后肠道菌群变化
宏基因组测序结果显示,Chao1、Shannon和Simpson指数评估的α-多样性在两组之间表现出显著差异。使用PCA,笔者发现对照组和TWT组之间肠道微生物群组成的β多样性明显不同(图3A和3B)。 LEfSe 分析显示TWT降低了小鼠微生物组中Bacterodales、Duncaniella、Muribaculaceae等细菌的水平,上调了Alistipes、Akkermansia、Acutalibacter等的水平。在物种水平上,对40种最丰富的细菌物种分析表明,TWT降低了Duncaniella sp B8、Duncaniella dubosii、Muribaculum intestinale和罗伊乳杆菌的水平,并上调了Akkermansia muscinifila和Lachnochlorostridium sp YL32等细菌的水平(图3C和3D)。
肠道菌群基因组KEGG功能差异分析显示,TWT降低了三羧酸循环(tricarboxylic acid cycle,TAC)、丙酮酸代谢、硫代谢、丁酸代谢和硝基甲苯降解,同时增加了酚类、酪氨酸和色氨酸的生物合成、生物素代谢,光合生物中的固碳作用以及叶酸的生物合成(图3E)。TWT影响了色氨酸的生物合成,下调了肠道中的罗伊乳杆菌(图3F),而罗伊乳杆菌能够产生ILA等色氨酸代谢物,这表明罗伊乳杆菌在雷公藤致雄性生殖损伤中发挥着关键作用。综上所述,这些数据表明,肠道微生物群的组成在对照组和TWT组之间是不同的,TWT显著改变了肠道菌群的组成结构,降低了某些有益菌的丰度,影响了部分肠道菌群功能途径。
3.4 罗伊乳杆菌改善TWT诱导的雄性生殖损伤
罗伊乳杆菌可产生多种色氨酸代谢产物,如ILA和吲哚-3-丙酸(indolyl-3-propionic acid, IPA)。考虑到TWT降低了罗伊乳杆菌的丰度,影响了色氨酸的生物合成,本研究假设补充罗伊乳杆菌可以改善TWT诱导的生殖毒性。实验结果表明,罗伊乳杆菌能显著上调精子生成相关基因包括Id4、Bmi1、Brdt、Tdrd7和Adam3的表达水平,恢复Sod2和Gpx4的表达水平,下调Ho-1和Cat的表达(图4A和4B)。睾丸组织切片HE染色结果显示,与TWT组相比,L.r+TWT组小鼠恢复了生精细胞数量,增加了生精上皮的厚度(图4C)。
3.5 TWT对睾丸代谢物的影响
为了探究TWT是否通过影响睾丸代谢物从而产生生殖毒性,本实验采用基于LC-MS的代谢组学对小鼠睾丸代谢物进行分析。睾丸正离子和负离子PCA图显示TWT组与对照组代谢物出现明显的聚类现象;S-plot图显示提供差异性的离子主要有牛磺酸、苹果酸、ILA、谷氨酸、D-天冬氨酸、腺苷-3'-磷酸、磷酰胆碱、甜菜碱、肌酸及次黄嘌呤等(图5A)。
对OPLS-DA分析的离子按|P(corr)|≥0.8、VIP值≥1.2筛选代谢物离子。在HMDB中对筛选出的离子进行比对筛选内源性代谢物。随后对筛选出的代谢物进行靶标抽提,结果显示TWT影响了睾丸中氨基酸及其衍生物的代谢,参与色氨酸代谢的ILA及IPA,其他的核苷类及溶血磷脂酰胆碱等的代谢(图5B和5C5C)。鉴于TWT扰乱了色氨酸代谢,增加了睾丸中ILA的水平,而ILA能够通过罗伊乳杆菌代谢产生,本研究认为ILA可能在睾丸功能中起重要作用。
3.6 ILA改善TWT诱导的雄性生殖功能损伤
为了验证ILA是否在TWT诱导的生殖毒性中起关键作用,本实验在给予小鼠TWT的同时补充ILA。实验结果显示,ILA能够显著恢复睾丸中与精子生成相关的基因表达水平(包括Id4、Brdt和Adam3),同时恢复了氧化应激相关的Sod1、Sod2和Gpx4表达水平。HE染色结果显示,与TWT组相比ILA+TWT组小鼠生精细胞数量增加,生精上皮的厚度增加,见图6。提示ILA改善了TWT诱导的雄性生殖功能损伤。
4 讨论
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本实验发现,肠道菌群的紊乱和ILA水平变化与TWT诱导的小鼠生殖功能障碍有关。TWT诱导了小鼠睾丸组织学损伤,降低了睾丸指数、精子数量以及与精子生成事件相关的Bmi1、Tdrd7、Brdt、Tdrd7和Adam3的表达水平。补充外源性ILA或移植能产生ILA的菌株能够通过调节氧化应激相关基因表达,改善TWT引起的睾丸组织学损伤和精子生成相关mRNA的减少。
氧化应激是精子功能缺陷的主要诱因之一,通过诱导细胞凋亡、自噬,破坏精子 DNA 的完整性,损伤精子质膜蛋白质和脂质,限制其受精潜能[16-17]。本实验发现TWT引起睾丸氧化应激损伤,补充外源性的罗伊乳杆菌及代谢物ILA能够抗睾丸氧化应激作用,改善睾丸损伤。
ILA是色氨酸代谢中通过ILA途径的吲哚-3-丙酮酸(IPyA)酶促还原产物,它可以代谢成吲哚丙烯酸和吲哚-3-丙酸[18]。色氨酸的代谢产物通常作为体内芳香烃受体(AHR)的配体,发挥免疫调节、细胞促进和调节氧化应激等生理功能[19-20]。在肠上皮细胞中,ILA被证实能够通过激活AHR和NRF2途径发挥抗炎作用[21-22]。本实验中ILA能够下调氧化应激损伤相关Sod1、Sod2、Gpx4的表达水平,改善雄性生殖功能损伤,推测通过NRF2-GPX4通路改善生殖损伤可能是ILA的潜在机制。
罗伊乳杆菌是一种已知的益生菌,可以调节免疫并将色氨酸代谢成多种衍生物,已有研究表明罗伊乳杆菌对老年小鼠的睾酮水平和睾丸指数有保护作用[23]。同时,罗伊乳杆菌也可以调控Nrf2/HO-1通路改善大鼠肠道屏障功能,调节胆汁酸改善肝损伤[12,24]。本实验发现在小鼠接受TWT干预后肠道中罗伊乳杆菌的水平下降,补充罗伊乳杆菌可以改善TWT引起的生殖功能损伤。
此外,本实验发现抗生素与TWT联合使用会加重生殖损伤,降低睾丸指数,通过睾丸病理切片可以看出TWT显著降低生精小管中的精子数量,损伤生精细胞,导致空泡化(图2D),联合抗生素给药后会加剧生精细胞损伤,降低生精细胞数量及睾丸指数,但精子数量未明显改变,推测可能由于给予TWT后精子数量已处于较低水平,所以在联合抗生素给药并未进一步影响精子数量。TWT临床上会与其他药物联合用于治疗银屑病,抗生素也可用于治疗某些银屑病[25]。因此,在临床使用中应避免将TWT与抗生素联合使用,以避免加重其不良反应。
本实验表明,TWT通过扰乱肠道菌群及睾丸代谢引起生殖功能损伤,罗伊乳杆菌及其代谢产物ILA对TWT诱导的雄性生殖功能损伤有保护作用,主要是通过抗睾丸组织的氧化应激发挥作用。本实验为减少TWT致雄性生殖功能损伤提供了新的策略。
基金
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  • 四川大学华西医院“1·#3·#5工程”项目资助(ZYYC21003)
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doi: 10.11669/cpj.2025.09.002
  • 接收时间：2024-07-24
  • 首发时间：2025-11-11
  • 出版时间：2025-05-01
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  • 收稿日期：2024-07-24
基金
四川大学华西医院“1·#3·#5工程”项目资助(ZYYC21003)
作者信息
    1 江西中医药大学院士工作站, 南昌 330004
    2 四川大学华西医院疾病分子网络前沿科学中心肝肠疾病与代谢研究室, 成都 610041
    3 成都中医药大学中医药创新研究所, 成都 611100

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*李飞,男,博士,研究员 研究方向:肝损伤的代谢调控与药物干预 Tel:(0791)86362367
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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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