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Article(id=1220655221815038425, tenantId=1146029695717560320, journalId=1189982191388893191, issueId=1220655218681893290, articleNumber=null, orderNo=null, doi=10.16438/j.0513-4870.2019-0933, pmid=null, cstr=null, oa=null, hot=null, price=null, onlineType=0, articleFormat=0, articleType=null, articleTypeStr=research-article, receivedDate=1574352000000, receivedDateStr=2019-11-22, revisedDate=1577462400000, revisedDateStr=2019-12-28, acceptedDate=null, acceptedDateStr=null, onlineDate=1768956483558, onlineDateStr=2026-01-21, pubDate=1589212800000, pubDateStr=2020-05-12, doiRegisterDate=null, doiRegisterDateStr=null, onlineIssueDate=1768956483558, onlineIssueDateStr=2026-01-21, onlineJustAcceptDate=null, onlineJustAcceptDateStr=null, onlineFirstDate=null, onlineFirstDateStr=null, sourceXml=null, magXml=null, createTime=1768956483558, creator=13701087609, updateTime=1768956483558, updator=13701087609, issue=Issue{id=1220655218681893290, tenantId=1146029695717560320, journalId=1189982191388893191, year='2020', volume='55', issue='5', pageStart='773', pageEnd='1072', issueExtLink='null', onlineDate='null', pubDate='null', beforeIssueId=null, nextIssueId=null, price=null, status=1, issueComplete=1, articleOrder=1, issueType=-1, specialIssue=null, createTime=1768956482811, creator=13701087609, updateTime=1768986431570, updator=13701087609, preIssue=null, nextIssue=null, ext={EN=IssueExt(id=1220780832940278305, tenantId=1146029695717560320, journalId=1189982191388893191, issueId=1220655218681893290, language=EN, specialIssueTitle=, coverIllustrator=null, specialIssueEditor=, specialIssueAbout=), CN=IssueExt(id=1220780832940278306, tenantId=1146029695717560320, journalId=1189982191388893191, issueId=1220655218681893290, language=CN, specialIssueTitle=, coverIllustrator=null, specialIssueEditor=, specialIssueAbout=)}, issueFiles=null}, startPage=868, endPage=876, ext={EN=ArticleExt(id=1220655222624539131, articleId=1220655221815038425, tenantId=1146029695717560320, journalId=1189982191388893191, language=EN, title=The effect and mechanism of baicalein on regulating gut microbiota and improving chemotherapy-induced intestinal mucositis in mice, columnId=1190335348761793317, journalTitle=Acta Pharmaceutica Sinica, columnName=Original Articles, runingTitle=null, highlight=null, articleAbstract=

We evaluate the therapeutic effects of baicalein on chemotherapy-induced intestinal mucositis (CIM) in mice. The role of gut microflora regulation in the therapeutic effects of baicalein was investigated meanwhile. Male Balb/c mice were randomly divided into three groups including normal control group, model group and experimental group. Except for normal control group, mice were injected with 5-fluorouracil and irinotecan to induce CIM. Animal welfare and experimental procedures comply follow the rules of the Animal Ethics Committee of the Institute of Materia Medica, Chinese Academy of Medical Sciences. Baicalein significantly reduced disease activity index (DAI) of CIM mice and decreased the content of interleukin 6 (IL-6) and tumor necrosis factor α (TNF-α) in serum. There were significant differences in the composition of the gut microbiota among groups according to the analysis of α diversity, β diversity, and the species differences. Compared with the normal control group, the Ruminococcaceae_UCG_014 and unclassified_f_Lachnospiraceae in mice of model group were significantly decreased while Bacteroides, Escherichia_Shigella, Enterococcus, Parabacteroides, Clostridium_sensu_stricto_1, and Lactococcus were significantly increased. Baicalein significantly decreased the abundance of Bacteroides, Escherichia_Shigella, Parabacteroides, Enterococcus, Clostridium_sensu_stricto_1, and Lactococcus. Meantime, norank_f_Muribaculaceae was notably increased by baicalein. The content of IL-6 and TNF-α in the serum of the three groups were positively correlated with the abundance of Clostridium_sensu_stricto_1, Lactococcus, Bacteroides, and Enterococcus according to correlation analysis. This study suggested the potential therapeutic effect of baicalein on CIM in mice. Regulation of gut microbiota probably plays a critical role in the therapeutic effects of baicalein.

, correspAuthors=Guan-hua DU, authorNote=null, correspAuthorsNote=null, copyrightStatement=Copyright ©2020 Acta Pharmaceutica Sinica. All rights reserved., 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=Rui WANG, Lin WANG, Guang-yi WEI, Nan-nan LIU, Li ZHANG, Shu-mei WANG, Guan-hua DU), CN=ArticleExt(id=1220655225422140119, articleId=1220655221815038425, tenantId=1146029695717560320, journalId=1189982191388893191, language=CN, title=黄芩素调节肠道菌群并改善小鼠化疗诱导性肠黏膜炎的作用及其机制, columnId=1190335348896011050, journalTitle=药学学报, columnName=研究论文, runingTitle=null, highlight=null, articleAbstract=

研究黄芩素（baicalein，Bai）对化疗性肠黏膜炎（chemotherapy-induced intestinal mucositis，CIM）小鼠的治疗作用及对肠道菌群的调节作用，探讨黄芩素对CIM的治疗作用与肠道菌群调控的关系。选取雄性Balb/c小鼠随机分为正常对照组、模型组和黄芩素给药组，联合5-氟尿嘧啶（5-fluorouracil，5-FU）及伊利替康（irinotecan，IRI）制备CIM小鼠模型。动物福利和实验过程均遵循中国医学科学院药物研究所动物伦理委员会的规定。研究发现：黄芩素可显著抑制CIM小鼠体重下降、降低疾病活动指数及血清中白介素6（interleukin 6，IL-6）和肿瘤坏死因子α（tumor necrosis factor α，TNF-α）含量。菌群多样性分析和物种差异分析显示，模型组小鼠肠道菌群组成与对照组存在明显差异，黄芩素对CIM小鼠粪便菌群具有调节作用，可降低拟杆菌属、大肠杆菌属、志贺氏菌属、副杆菌属、肠球菌属、梭状芽孢杆菌属和乳球菌属丰度，而显著升高穆氏杆菌属丰度。关联性分析显示，CIM小鼠血清的IL-6和TNF-α含量与梭状芽孢杆菌属、乳球菌属、拟杆菌属等丰度相关性显著。本研究表明黄芩素可有效改善小鼠化疗性肠黏膜炎，这一作用与其对肠道菌群的调节密切相关。

, correspAuthors=杜冠华, authorNote=null, correspAuthorsNote=
*杜冠华, Tel/Fax:86-10-63165184, E-mail:
, copyrightStatement=版权所有©《药学学报》编辑部2020, copyrightOwner=null, extLink=null, articleAbsUrl=null, sourceXml=glplhw8VOaje1++ZzRJbWw==, magXml=k/7RksAkilzzSqciHXXY7Q==, pdfUrl=null, pdf=Ipx6sQq2JJXN9gUmkLC6Lw==, pdfFileSize=1157067, pdfExtLink=null, richHtmlUrl=null, mobilePdfUrl=null, reviewReport=null, pdfFirstPage=null, abstractGraph=IhDew2LIzhTRz/MJo4/TfQ==, abstractGraphContent=null, abstractVideo=null, citation=null, cebUrl=null, magXmlContent=HAoUStdA4026VpZBEpk7Ug==, mapNumber=null, authorCompany=null, fund=null, authors=null, authorsList=王睿, 王霖, 魏广义, 刘楠楠, 张莉, 王淑美, 杜冠华)}, authors=[Author(id=1220655225992565527, tenantId=1146029695717560320, journalId=1189982191388893191, articleId=1220655221815038425, orderNo=0, firstName=null, middleName=null, lastName=null, nameCn=null, orcid=null, stid=null, country=null, authorPic=null, dead=0, email=null, emailSecond=null, emailThird=null, correspondingAuthor=0, authorType=1, ext={EN=AuthorExt(id=1220655226101617446, tenantId=1146029695717560320, journalId=1189982191388893191, articleId=1220655221815038425, authorId=1220655225992565527, language=EN, stringName=Rui WANG, firstName=Rui, middleName=null, lastName=WANG, prefix=null, suffix=null, authorComment=null, nameInitials=null, affiliation=null, department=null, xref=1, 2, address=1. Guangdong Pharmaceutical University, Guangzhou 510006, China
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Guangdong Pharmaceutical University, Guangzhou 510006, China
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Food Funct, 2017, 8: 3383-3393., articleTitle=Dietary fucoidan of Acaudina molpadioides alters gut microbiota and mitigates intestinal mucosal injury induced by cyclophosphamide, refAbstract=null)], funds=[Fund(id=1220655232049140148, tenantId=1146029695717560320, journalId=1189982191388893191, articleId=1220655221815038425, awardId=2018YFC0311005, language=CN, fundingSource=国家重点研发计划资助项目(2018YFC0311005), fundOrder=null, country=null), Fund(id=1220655232162386366, tenantId=1146029695717560320, journalId=1189982191388893191, articleId=1220655221815038425, awardId=2017-I2M-1-010, language=CN, fundingSource=中国医学科学院医学与健康科技创新工程(2017-I2M-1-010), fundOrder=null, country=null)], companyList=[AuthorCompany(id=1220655225766073081, tenantId=1146029695717560320, journalId=1189982191388893191, articleId=1220655221815038425, xref=null, ext=[AuthorCompanyExt(id=1220655225782850300, tenantId=1146029695717560320, journalId=1189982191388893191, articleId=1220655221815038425, companyId=1220655225766073081, language=EN, country=null, province=null, city=null, postcode=null, companyName=null, departmentName=null, remark=1. 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A: Effect of Bai on fecal excretion in 3 hours; B: Effect of Bai on disease activity index (DAI); C: Effect of Bai on fecal storage. <i>n</i> = 8, <span class="mag-xml-inline-formula">$\bar x$</span> ± standard error of mean (SEM). <sup>*</sup><i>P</i> < 0.05, <sup>***</sup><i>P</i> < 0.001 <i>vs</i> model group, <sup>##</sup><i>P</i> < 0.01 <i>vs</i> control group , figureFileSmall=RDUJsCJNtAXH00lu7FnIVg==, figureFileBig=IhDew2LIzhTRz/MJo4/TfQ==, tableContent=null), ArticleFig(id=1220655230363029793, tenantId=1146029695717560320, journalId=1189982191388893191, articleId=1220655221815038425, language=EN, label=null, caption=null, figureFileSmall=Jiqn95yp0rE9v4NKaXCxsA==, figureFileBig=VLNTRCQJaBiiqIS04XJi4Q==, tableContent=null), ArticleFig(id=1220655230484664620, tenantId=1146029695717560320, journalId=1189982191388893191, articleId=1220655221815038425, language=CN, label=Figure 2, caption= The improved role of Bai against CIM in mice. A: Pathology score in each group; B: The content of interleukin 6 (IL-6) and tumor necrosis factor <i>α</i> (TNF-<i>α</i>) in serum of mice; C: Representative H & E-stained observation of colonic sections (eyepiece × objective magnification) in three groups. <i>n</i> = 8, <span class="mag-xml-inline-formula">$\bar x$</span> ± SEM. <sup>*</sup><i>P</i> < 0.05, <sup>**</sup><i>P</i> < 0.01, <sup>***</sup><i>P</i> < 0.001 <i>vs</i> model group; <sup>#</sup><i>P</i> < 0.05, <sup>###</sup><i>P</i> < 0.001 <i>vs</i> control group. H & E: hematoxylin-eosin staining , figureFileSmall=Jiqn95yp0rE9v4NKaXCxsA==, figureFileBig=VLNTRCQJaBiiqIS04XJi4Q==, tableContent=null), ArticleFig(id=1220655230589522227, tenantId=1146029695717560320, journalId=1189982191388893191, articleId=1220655221815038425, language=EN, label=null, caption=null, figureFileSmall=HCAIx0Qi2orHG7jjjV6CgA==, figureFileBig=uyjP+GN9CsxkNTS8/w3erg==, tableContent=null), ArticleFig(id=1220655230690185529, tenantId=1146029695717560320, journalId=1189982191388893191, articleId=1220655221815038425, language=CN, label=Figure 3, caption= Diversity analysis of gut microbiota in mice. A: Rarefaction curves of samples; B: Venn diagram of OTU in the three groups; C: Multiple sample PCoA analysis; D: Multiple sample PCA analysis; E: Multiple sample NMDS analysis. Samples of the control group indicated by a, samples of the model group indicated by b, and samples of the Bai group indicated by c. OTU: Operational taxonomic units; PCoA: Principle coordination analysis; PCA: Principal components analysis; NMDS: Nonmetric multidimensional scaling , figureFileSmall=HCAIx0Qi2orHG7jjjV6CgA==, figureFileBig=uyjP+GN9CsxkNTS8/w3erg==, tableContent=null), ArticleFig(id=1220655230824403273, tenantId=1146029695717560320, journalId=1189982191388893191, articleId=1220655221815038425, language=EN, label=null, caption=null, figureFileSmall=X7EbKxMSO3SV2CKHtcdieg==, figureFileBig=mYFK1XJwlaR+PWYmc9N9BA==, tableContent=null), ArticleFig(id=1220655230954426709, tenantId=1146029695717560320, journalId=1189982191388893191, articleId=1220655221815038425, language=CN, label=Figure 4, caption= Effect of Bai on gut microbiota abundance in CIM mice. A: Distribution histogram based on LDA; B: Bar plot analysis of community abundance on genus level. Samples of the control group indicated by a, samples of the model group indicated by b, and samples of the Bai group indicated by c. LEfSe: linear discriminate analysis size effect; LDA: Linear discriminant analysis , figureFileSmall=X7EbKxMSO3SV2CKHtcdieg==, figureFileBig=mYFK1XJwlaR+PWYmc9N9BA==, tableContent=null), ArticleFig(id=1220655231076061537, tenantId=1146029695717560320, journalId=1189982191388893191, articleId=1220655221815038425, language=EN, label=null, caption=null, figureFileSmall=3yWenvesV0N7oObEHyHrBQ==, figureFileBig=4U8iNLPP0xoiAiP8zdm55w==, tableContent=null), ArticleFig(id=1220655231197696365, tenantId=1146029695717560320, journalId=1189982191388893191, articleId=1220655221815038425, language=CN, label=Figure 5, caption= The effect of Bai on gut microbial relative abundance in CIM mice at phylum and genus level. A: Imbalance of gut microbial between control group and model group at phylum level; B: Imbalance of gut microbial between control group and model group at genus level; C: Imbalance of gut microbial between Bai group and model group at phylum level; D: Imbalance of gut microbial between Bai group and model group at genus level. Control group (a); Model group (b); Bai group (c); <i>n</i> = 5, <span class="mag-xml-inline-formula">$\bar x$</span>± SEM. <sup>*</sup><i>P</i> < 0.05, <sup>**</sup><i>P</i> < 0.01 <i>vs</i> model group , figureFileSmall=3yWenvesV0N7oObEHyHrBQ==, figureFileBig=4U8iNLPP0xoiAiP8zdm55w==, tableContent=null), ArticleFig(id=1220655231310942580, tenantId=1146029695717560320, journalId=1189982191388893191, articleId=1220655221815038425, language=EN, label=null, caption=null, figureFileSmall=QaXbjOGeAB5jYCrlRUsC2g==, figureFileBig=zumMOsWwO0KVMXHqZ20G3A==, tableContent=null), ArticleFig(id=1220655231445160318, tenantId=1146029695717560320, journalId=1189982191388893191, articleId=1220655221815038425, language=CN, label=Figure 6, caption= The relativity analysis between inflammatory factors and gut microbiota. A: RDA analysis of correlation on genus level; B: db-RDA analysis of correlation on genus level; C: Spearman correlation heatmap. Samples of the control group indicated by a, samples of the model group indicated by b, and samples of the Bai group indicated by c , figureFileSmall=QaXbjOGeAB5jYCrlRUsC2g==, figureFileBig=zumMOsWwO0KVMXHqZ20G3A==, tableContent=null), ArticleFig(id=1220655231533240712, tenantId=1146029695717560320, journalId=1189982191388893191, articleId=1220655221815038425, language=EN, label=null, caption=null, figureFileSmall=null, figureFileBig=null, tableContent=
Group Day 3 Day 4 Day 5 Day 6 Day 7 Day 8
Control 0 0 0 0 0 0
Model 0.500 ± 0.189 0.500 ± 0.189 1.130 ± 0.125### 1.500 ± 0.267### 2.750 ± 0.164### 2.880 ± 0.125###
Bai 0.375 ± 0.183 0.500 ± 0.267 1.375 ± 0.183 1.250 ± 0.164 2.125 ± 0.227* 2.500 ± 0.189***
), ArticleFig(id=1220655231629709712, tenantId=1146029695717560320, journalId=1189982191388893191, articleId=1220655221815038425, language=CN, label=Table 1, caption=

Protective effect of Bai on diarrhea index in CIM mice. n = 8, $\bar x$ ± SEM. *P < 0.05, ***P < 0.001 vs model group; ###P < 0.001vs control group

, figureFileSmall=null, figureFileBig=null, tableContent=
Group Day 3 Day 4 Day 5 Day 6 Day 7 Day 8
Control 0 0 0 0 0 0
Model 0.500 ± 0.189 0.500 ± 0.189 1.130 ± 0.125### 1.500 ± 0.267### 2.750 ± 0.164### 2.880 ± 0.125###
Bai 0.375 ± 0.183 0.500 ± 0.267 1.375 ± 0.183 1.250 ± 0.164 2.125 ± 0.227* 2.500 ± 0.189***
), ArticleFig(id=1220655231780704670, tenantId=1146029695717560320, journalId=1189982191388893191, articleId=1220655221815038425, language=EN, label=null, caption=null, figureFileSmall=null, figureFileBig=null, tableContent=
Group Sobs Shannon Simpson Ace Chao Coverage
Control 257.8 ± 6.21 3.206 ± 0.115 0.124 ± 0.026 293.2 ± 7.80 296.9 ± 8.33 0.9 ± 0.000 06
Model 173.4 ± 28.77* 3.089 ± 0.099 0.098 ± 0.017 203.0 ± 30.60* 213.5 ± 33.46* 0.9 ± 0.000 22
Bai 245.8 ± 33.11 3.351 ± 0.295 0.084 ± 0.022 280.7 ± 34.51 285.1 ± 41.41 0.9 ± 0.000 14
), ArticleFig(id=1220655231910728104, tenantId=1146029695717560320, journalId=1189982191388893191, articleId=1220655221815038425, language=CN, label=Table 2, caption=

Gut microbiota diversity indexes in three groups. n = 5, $\bar x$ ± SEM. *P < 0.05vs control group

, figureFileSmall=null, figureFileBig=null, tableContent=
Group Sobs Shannon Simpson Ace Chao Coverage
Control 257.8 ± 6.21 3.206 ± 0.115 0.124 ± 0.026 293.2 ± 7.80 296.9 ± 8.33 0.9 ± 0.000 06
Model 173.4 ± 28.77* 3.089 ± 0.099 0.098 ± 0.017 203.0 ± 30.60* 213.5 ± 33.46* 0.9 ± 0.000 22
Bai 245.8 ± 33.11 3.351 ± 0.295 0.084 ± 0.022 280.7 ± 34.51 285.1 ± 41.41 0.9 ± 0.000 14
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黄芩素调节肠道菌群并改善小鼠化疗诱导性肠黏膜炎的作用及其机制
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王睿 1, 2 , 王霖 2 , 魏广义 1, 2 , 刘楠楠 1, 2 , 张莉 2 , 王淑美 1 , 杜冠华 1, 2, *
药学学报 | 研究论文 2020,55(5): 868-876
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药学学报 | 研究论文 2020, 55(5): 868-876
黄芩素调节肠道菌群并改善小鼠化疗诱导性肠黏膜炎的作用及其机制
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王睿1, 2, 王霖2, 魏广义1, 2, 刘楠楠1, 2, 张莉2, 王淑美1, 杜冠华1, 2, *
作者信息
  • 1.广东药科大学, 广东 广州 510006
  • 2.中国医学科学院、北京协和医学院药物研究所, 药物靶点研究与新药筛选北京市重点实验室, 北京 100050

通讯作者:

*杜冠华, Tel/Fax:86-10-63165184, E-mail:
The effect and mechanism of baicalein on regulating gut microbiota and improving chemotherapy-induced intestinal mucositis in mice
Rui WANG1, 2, Lin WANG2, Guang-yi WEI1, 2, Nan-nan LIU1, 2, Li ZHANG2, Shu-mei WANG1, Guan-hua DU1, 2, *
Affiliations
  • 1. Guangdong Pharmaceutical University, Guangzhou 510006, China
  • 2. Beijing Key Laboratory of Drug Target and Screening Research, Institute of Materia Medica, Chinese Academy of Medical Sciences and Peking Union Medical College, Beijing 100050, China
出版时间: 2020-05-12 doi: 10.16438/j.0513-4870.2019-0933
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摘要
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研究黄芩素（baicalein，Bai）对化疗性肠黏膜炎（chemotherapy-induced intestinal mucositis，CIM）小鼠的治疗作用及对肠道菌群的调节作用，探讨黄芩素对CIM的治疗作用与肠道菌群调控的关系。选取雄性Balb/c小鼠随机分为正常对照组、模型组和黄芩素给药组，联合5-氟尿嘧啶（5-fluorouracil，5-FU）及伊利替康（irinotecan，IRI）制备CIM小鼠模型。动物福利和实验过程均遵循中国医学科学院药物研究所动物伦理委员会的规定。研究发现：黄芩素可显著抑制CIM小鼠体重下降、降低疾病活动指数及血清中白介素6（interleukin 6，IL-6）和肿瘤坏死因子α（tumor necrosis factor α，TNF-α）含量。菌群多样性分析和物种差异分析显示，模型组小鼠肠道菌群组成与对照组存在明显差异，黄芩素对CIM小鼠粪便菌群具有调节作用，可降低拟杆菌属、大肠杆菌属、志贺氏菌属、副杆菌属、肠球菌属、梭状芽孢杆菌属和乳球菌属丰度，而显著升高穆氏杆菌属丰度。关联性分析显示，CIM小鼠血清的IL-6和TNF-α含量与梭状芽孢杆菌属、乳球菌属、拟杆菌属等丰度相关性显著。本研究表明黄芩素可有效改善小鼠化疗性肠黏膜炎，这一作用与其对肠道菌群的调节密切相关。

黄芩素  /  化疗性肠黏膜炎  /  肠道菌群  /  高通量测序  /  白介素6  /  肿瘤坏死因子α

We evaluate the therapeutic effects of baicalein on chemotherapy-induced intestinal mucositis (CIM) in mice. The role of gut microflora regulation in the therapeutic effects of baicalein was investigated meanwhile. Male Balb/c mice were randomly divided into three groups including normal control group, model group and experimental group. Except for normal control group, mice were injected with 5-fluorouracil and irinotecan to induce CIM. Animal welfare and experimental procedures comply follow the rules of the Animal Ethics Committee of the Institute of Materia Medica, Chinese Academy of Medical Sciences. Baicalein significantly reduced disease activity index (DAI) of CIM mice and decreased the content of interleukin 6 (IL-6) and tumor necrosis factor α (TNF-α) in serum. There were significant differences in the composition of the gut microbiota among groups according to the analysis of α diversity, β diversity, and the species differences. Compared with the normal control group, the Ruminococcaceae_UCG_014 and unclassified_f_Lachnospiraceae in mice of model group were significantly decreased while Bacteroides, Escherichia_Shigella, Enterococcus, Parabacteroides, Clostridium_sensu_stricto_1, and Lactococcus were significantly increased. Baicalein significantly decreased the abundance of Bacteroides, Escherichia_Shigella, Parabacteroides, Enterococcus, Clostridium_sensu_stricto_1, and Lactococcus. Meantime, norank_f_Muribaculaceae was notably increased by baicalein. The content of IL-6 and TNF-α in the serum of the three groups were positively correlated with the abundance of Clostridium_sensu_stricto_1, Lactococcus, Bacteroides, and Enterococcus according to correlation analysis. This study suggested the potential therapeutic effect of baicalein on CIM in mice. Regulation of gut microbiota probably plays a critical role in the therapeutic effects of baicalein.

baicalein  /  chemotherapy-induced intestinal mucositis  /  gut microbiota  /  high-throughput sequencing  /  interleukin 6  /  tumor necrosis factor α
王睿, 王霖, 魏广义, 刘楠楠, 张莉, 王淑美, 杜冠华. 黄芩素调节肠道菌群并改善小鼠化疗诱导性肠黏膜炎的作用及其机制. 药学学报, 2020 , 55 (5) : 868 -876 . DOI: 10.16438/j.0513-4870.2019-0933
Rui WANG, Lin WANG, Guang-yi WEI, Nan-nan LIU, Li ZHANG, Shu-mei WANG, Guan-hua DU. The effect and mechanism of baicalein on regulating gut microbiota and improving chemotherapy-induced intestinal mucositis in mice[J]. Acta Pharmaceutica Sinica, 2020 , 55 (5) : 868 -876 . DOI: 10.16438/j.0513-4870.2019-0933
正文
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随着肿瘤发病率的逐年上升, 化疗引起的毒副作用受到人们普遍关注。据统计, 使用抗肿瘤化疗药的患者10%以上会出现化疗诱导性肠黏膜炎, 而在接受5-氟尿嘧啶或伊立替康治疗的癌症患者中, 其发生率更可分别高达90%和40%[1]。化疗性肠黏膜炎(chemotherapy-induced intestinal mucositis, CIM)的主要发病机制是化疗药物破坏了消化道黏膜的完整性, 导致黏膜屏障功能失调和免疫功能损伤, 从而导致胃肠黏膜炎、肠出血性坏死以及细菌易位, 伴或不伴败血症[2]。临床表现为腹痛、腹泻、便秘、麻痹性肠梗阻、消化道溃疡、甚至胃肠出血等[3]。CIM不仅限制了抗肿瘤药物的临床应用, 也严重影响患者的生活和生存质量, 导致病情恶化、危及生命。研究表明, 肠道菌群紊乱破坏肠黏膜屏障, 其中肠球菌、肠杆菌、乳球菌、变形杆菌等致病菌的增加与炎症性肠病的发生具有密切的关联性[4-7], 失衡的肠道菌群与化疗性结肠炎的严重程度成正比。因此, 通过调节肠道菌群的平衡来改善化疗后肠黏膜炎症状是预防与治疗CIM的重要研究方向。
黄芩素(baicalein, Bai)是从唇形科植物黄芩干燥根中分离得到的黄酮类化合物[8], 其药理作用众多, 具有抗菌、保肝、抗炎、修复脑损伤、改善糖尿病以及抗肿瘤活性[9-11]。然而黄芩素对CIM是否具有改善作用, 以及这一作用与肠道菌群的关系尚未有报道。本研究考察了黄芩素对CIM小鼠肠黏膜炎的治疗作用, 采用16S rRNA高通量测序方法检测黄芩素对CIM小鼠粪便菌群的调控作用, 并探讨了黄芩素对肠道菌群的调控与其抗CIM作用的相关性。
材料与方法
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实验动物
雄性Balb/c小鼠, 6~8周龄, 体重20~22 g, SPF级, 购于北京维通利华实验动物技术有限公司, 许可证号SCXK (京) 2016-0006。饲养环境:温度22~27 ℃, 相对湿度60%~65%, 光照12 h, 自由进食、饮水。动物福利和实验过程均遵循中国医学科学院药物研究所动物伦理委员会的规定。
药材、试剂及实验仪器
黄芩素(由中国医学科学院药物研究所吕扬教授再纯化制备成β晶型, 专利申请号200710177330.8, 高效液相色谱检测纯度 > 98%); 5-氟尿嘧啶(5-fluorouracil, 5-FU, MCE公司, CAS: 51-21-8);伊利替康(irinotecan, IRI, MCE公司, CAS: 100286-90-6);羧甲基纤维素钠(国药集团化学试剂有限公司, CAS: 9004-32-4); IL-6检测试剂盒和TNF-α检测试剂盒(武汉伊莱瑞特生物科技股份有限公司); 移液器(Eppendorf公司); 干式恒温器(杭州奥盛仪器有限公司); 电子天平(Mettler toledeo XS105, Mettler公司); 高速冷冻离心机(AllegraTMX-22R Centrifuge, 美国Beckman Coulter公司); SpectraMax M5酶标仪(美国MD公司)。
造模方法
参考Tan等[12]报道的CIM小鼠造模方法并加以改进, 采取腹腔注射(ip) 5-氟尿嘧啶(25 mg·kg-1), 间隔1 h后, 腹腔注射伊利替康(20 mg·kg-1)的方式联合造模, 以小鼠出现嗜睡疲倦、畏寒扎堆、毛色枯槁、粪便稀软、肛周着色等症状提示CIM模型造模成功。
实验分组及样品采集
选取雄性Balb/c小鼠24只, 按体重随机分为对照组、模型组和黄芩素给药组, 每组8只, 实验共计8天。对照组:灌胃(ig) 0.9%生理盐水, 每日1次, 连续8天; 模型组: Day 1~2灌胃0.9%生理盐水, Day 3~6连续造模4天, Day 7~8灌胃0.9%生理盐水; 黄芩素给药组:灌胃Bai (100 mg·kg-1), 每日1次, 连续8天, 在Day 3~6连续造模4天。末次给药后, 将各组小鼠放进干净的铺有消毒滤网的笼子里, 采用悬尾刺激法促进小鼠排便, 收集4~5粒粪便样本至灭菌eppendorf (EP)管, 液氮速冻后于-80 ℃保存, 进行肠道菌群检测。各组小鼠眼眶后静脉丛取血0.5 mL, 4 ℃、5 000 r·min-1离心15 min, 取上清液血清样品, 置于-80 ℃保存待测。脱颈处死小鼠, 剖开腹腔观察结肠外观, 取肛门至回盲部的结肠, 记录肠道内粪便存储量。用生理盐水冲洗肠道内容物后, 沿肠系膜边缘纵行剪开, 取靠近肛门处的结肠近端肠段1 cm大小, 放入4%多聚甲醛固定(4 ℃)固定, 脱水、包埋、浸蜡, 按照标准实验流程进行苏木素-伊红染色法(hematoxylin-eosin staining, H & E)染色, 于光学显微镜下观察病理组织学改变。
体重及排便量检测
每日记录各组小鼠体重, 观察各组小鼠的生理状态和粪便的颜色、性状等, 称重统计白天给药后3 h内各组小鼠的排便量。
疾病活动指数(disease activity index, DAI)评分
参考Xu等[13]的评分方法并加以改进, 取小鼠体重下降分数(无, 0分; 1%~5%, 1分; 6%~10%, 2分; 11%~15%, 3分; > 15%, 4分)、小鼠腹泻等级分数(正常, 0分; 软便, 1分; 大便稀湿不成形且轻度肛周着色, 2分; 重度肛周着色, 3分)和小鼠白天3 h排便量(> 0.6 g, 0分; 0.4~0.6 g, 1分; 0.2~0.4 g, 2分; 0~0.2 g, 3分)三者的平均值。在实验的第3~8天分别对各组小鼠进行疾病活动指数评分。
病理学评价
结肠组织按常规方法进行包埋和切片, 厚度为5 μm, 进行H & E染色, 镜下观察结肠组织形态。在高倍镜下选取视野观察是否出现以下病理学表现, 包括黏膜层不同数量的单个核细胞及嗜中性粒细胞浸润、粘膜厚度变薄、腺体扩张并伴有杯状细胞减少、隐窝及腺体远离基底膜、基底浆细胞增多或淋巴细胞聚集等, 进行病理学评分(伴有以上1种病理学表现的, 1分; 2种, 2分; 3种, 3分; > 3种, 4分)。
DNA提取及测序
测序引物为16S rRNA基因的V3~V4高变区的特异引物338 F (5'-CCTAYGGGRBGCASCAG-3')和806 R (5'-GGACTACNNGGGTATCTAAT-3')。每个样本扩增实验均进行3次重复, 使用2%琼脂糖凝胶回收PCR产物, 应用AxyPrep DNA Gel Extraction Kit (Axygen Biosciences公司)进行纯化, 并进行Tris-HCl洗脱和2%琼脂糖电泳检测。应用Quanti FluorTM-ST (Promega公司)蓝色荧光定量系统进行定量检测。根据Illumina MiSeq平台标准操作规程将纯化后的扩增片段构建为双端测序(paired-end, PE)文库。通过数据分析Miseq测序得到的PE reads测序序列, 首先根据overlap关系进行拼接, 同时对序列质量进行质控和过滤, 区分样本后将操作分类单元(operational taxonomic units, OTU)聚类分析和物种分类学分析, 并基于OTU进行多种多样性指数分析, 包括α多样性分析、β多样性分析和多级物种差异判别分析(linear discriminate analysis size effect, LEfSe); 使用spearman correlation分析进行环境因子相关性分析。
统计学方法
实验结果以$\bar x$ ± standard error of mean (SEM)表示, 应用GraphPad软件对数据进行处理, 各组间差异采用单因素方差分析(one-way ANOVA)及Tukey's post hoc test计算, P < 0.05代表组间差异具有统计学意义。
结果
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1 黄芩素对CIM小鼠表观症状及疾病活动指数评分的影响
对照组小鼠在实验过程中饮食及活动正常, 体重逐渐增加。模型组和黄芩素给药组小鼠在造模后第1~2天出现不同程度的毛色枯槁、精神萎靡、胃寒扎堆、竖毛拱背等症状, 粪便湿软不成形。在造模后第3~4天, 模型组小鼠出现腹泻、粪便色黑不成形、聚结于肛门并附有重度的肛门着色, 个别小鼠出现便血, 且在第5~6天症状未恢复。黄芩素给药组小鼠在给药第7天后出现不同程度表观症状的恢复, 肛周着色程度降低。各组小鼠3 h粪便排泄量见图 1A, DAI评分见图 1B, 腹泻指数评分见表 1, 肠道内粪便存储量见图 1C。DAI评分显示, 模型组和黄芩素给药组与对照组相比有显著差异(P < 0.01)。从第7天起, 与模型组相比, 黄芩素给药组DAI评分显著降低(P < 0.01)。
2 黄芩素对CIM小鼠结肠组织病理形态的影响
结肠组织病理学评分和H & E染色结果如图 2所示。对照组小鼠结肠黏膜结构完整, 组织排列紧密整齐, 未见异常。模型组小鼠肠黏膜萎缩/变性, 隐窝腺体远离基底膜、甚至消失, 杯状细胞减少, 基底浆细胞增多, 黏膜层嗜中性粒细胞浸润。而黄芩素给药组的结肠黏膜及炎性细胞浸润与模型组相比均有显著改善(P < 0.05)。
3 黄芩素对CIM小鼠血清中IL-6及TNF-α含量的影响
如图 2B所示, 正常对照组血清IL-6含量为(122.900 ± 8.336) pg·mL-1, 模型组为(154.800 ± 2.484) pg·mL-1, 两组之间差异显著(P < 0.05);正常对照组血清TNF-α含量为(35.630 ± 1.076) pg·mL-1, 模型组为(58.480 ± 4.117) pg·mL-1, 两组之间差异显著(P < 0.001)。黄芩素可显著降低小鼠血清中IL-6及TNF-α含量。
4 黄芩素对菌群多样性的影响
通过α和β多样性分析, 采用一系列统计学分析指数来估计和反映微生物群落的丰度和多样性。Sobs、Ace和Chao指数用来评估菌群物种的OTU数量; Shannon和Simpson指数用来评估菌群的多样性, 菌群的多样性越高, Shannon值越大, Simpson值越小; Coverage指样品文库的覆盖率, 反映测序的深度。该指数越接近于1, 说明样本序列未被检测的概率越低。如表 2所示, Sobs、Chao和Ace指数在3组中均有显著性差异, 模型组群落的物种丰富度较正常对照组显著降低(P < 0.05), 黄芩素给药组较模型组明显升高。物种丰富度α指数稀释曲线图中, 各样本稀释性曲线趋于平坦且分布较集中, 说明测序数据量合理, 可反映样本中绝大多数的微生物多样性信息(图 3A)。韦恩图(Venn diagram, Venn)显示, 3组共有270个OTU, 正常对照组和模型组共有283个OTU, 模型组和黄芩素给药组共有292个OTU, 正常对照组、模型组和黄芩素给药组独有的OTU数量分别为43、22和39个(图 3B)。主坐标分析(principle coordination analysis, PCoA)和主成分分析(principal components analysis, PCA)中, 横纵坐标的百分比表示主成分轴和主坐标轴对样本组成差异的解释度值, X轴和Y轴的刻度是相对距离, 无实际意义。结果显示, 模型组和正常对照组相比, 菌群结构差异明显。黄芩素给药组与对照组的样本点接近, 表明两组样本物种组成相似(图 3C、D)。非度量多维尺度(nonmetric multidimensional scaling, NMDS)其基本特征是将对象间的相似性或相异性数据看成点间距离的单调函数, 在保持原始数据次序关系的基础上, 用新的相同次序的数据替换原始数据进行度量型多维尺度分析。Stress值检验了NMDS分析结果的优劣, stress < 0.1可认为NMDS的二维点图中的样本点具有很好的代表性。分析结果显示对照组和模型组组间样本未重叠, 说明两组菌群的构成存在明显差异, 而黄芩素给药组与对照组的样本点接近, 表明黄芩素使菌群构成基本恢复至正常水平(图 3E)。
5 CIM小鼠和黄芩素治疗后菌群物种的变化
多级物种差异判别分析(linear discriminate analysis size effect, LEfSe)及线性判别分析(linear discriminant analysis, LDA)结果显示(图 4), 对照组中f_Ruminococcacea (瘤胃球菌科)、g_norank_f_Lachnospiracea (毛螺旋菌科)、f_Acidaminococcaceae (氨基酸球菌科)、g_Phascolarctobacterium (考拉杆菌属)、g_Muribaculum丰度较高; 模型组中g_Bacteroides (拟杆菌属)、c_Gammaproteobacteri (变形菌纲)、f_Enterobacteriaceae (肠杆菌科)丰度较高; 黄芩素治疗组中g_ norank_f_Muribaculaceae、g_GCA_900066225、g_Harryflintia、g_unclassified_o_Clostridiales (梭菌目)、g_ norank_f_Ruminococcaceae (瘤胃球菌属)、g_norank_ o_Rhodospirillales (红螺菌目)丰度较高。
6 黄芩素对肠道菌群的调控作用
黄芩素对菌群的调节作用如图 5所示。在门水平(phymlum level):与对照组相比, 模型组变形菌门丰度增多, 拟杆菌门和厚壁菌门的丰度有减少的趋势(图 5A)。具体到属水平(genus level):模型组拟杆菌门的Bacteroides (拟杆菌属)、变形菌门的Escherichia_ Shigella (志贺氏菌属)、厚壁菌门的Parabacteroides (副杆菌属)及Lactococcus (乳球菌属)丰度增多; Clostridium_sensu_stricto_1 (梭状芽孢杆菌属)丰度显著增多; 厚壁菌门的Ruminococcaceae_UCG-014 (瘤胃球菌属), 变形菌门的unclassified_f_Lachnospiraceae (毛螺旋菌科)丰度显著降低(图 5B)。
与模型组相比, 在门水平:黄芩素给药组变形菌门、蓝藻门丰度显著降低, 厚壁菌门的丰度有降低的趋势, 拟杆菌门的丰度有升高的趋势(图 5C)。具体到属水平:黄芩素给药组norank_f_Muribaculaceae的丰度增多, Ruminococcaceae_UCG_014 (瘤胃球菌属)、Lachnospiraceae (毛螺科菌属)的丰度有增高的趋势; 拟杆菌门的Bacteroides (拟杆菌属)、变形菌门的Escherichia_Shigella (志贺氏菌属)、厚壁菌门的Parabacteroides (副杆菌属)、Enterococcus (肠球菌属)和Lactococcus (乳球菌属)丰度显著减少; Clostridium_sensu_ stricto_1 (梭状芽孢杆菌属)丰度显著减少(图 5D)。
7 菌群的环境因子关联性分析
通过进行冗余分析(redundancy analysis, RDA)及基于距离的冗余分析(distance-based redundancy analysis, db-RDA), 分析小鼠血清中IL-6和TNF-α的含量等环境因子与菌群的关联性。横纵坐标的百分比表示对样本组成差异的解释权重。结果显示, 肠道菌群的分布与IL-6和TNF-α含量的相关性具有显著性差异。在门水平上: Firmicutes (厚壁菌门)、Proteobacteria (变形菌门)、Actinobacteria (放线菌门)与IL-6和TNF-α的含量等环境因子呈正相关; Bacteroidetes (拟杆菌门)、Verrucomicrobia (疣微菌门)与IL-6、TNF-α的含量等环境因子呈负相关。具体到属水平: Bacteroides (拟杆菌属)、Lactobacillus (乳杆菌属)、Escherichia_Shigella (志贺氏菌属)、Streptococcus (链球菌属)、Enterococcus (肠球菌属)、Parabacteroides (副杆菌属)、Clostridium_ sensu_stricto_1 (梭状芽孢杆菌属)、Lactococcus (乳球菌属)与IL-6和TNF-α的含量等环境因子呈正相关; norank_f_Muribaculaceae、Prevotellaceae_UCG_001 (普雷沃氏菌属)、Alloprevotella (拟普雷沃菌属)、Ruminococcaceae_UCG_014 (瘤胃菌属)、Unclassified_f_Lachnospiraceae (毛螺菌属)、Lachnospiraceae_NK4A136_ group (毛螺菌属)、AKKermansia (艾克曼菌属)和Rikenellaceae_RC9_gut_group (理研菌属)与IL-6和TNF-α的含量等环境因子呈负相关。其中, Clostridium_ sensu_stricto_1 (状芽孢杆菌属)、actococcus (乳酸菌属)、acteroides (拟杆菌属)、Enterococcus (肠球菌属)、Prevotellaceae_UCG_001 (普雷沃氏菌属)与IL-6和TNF-α的含量等环境因子相关性显著(图 6)。
讨论
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以5-氟尿嘧啶或伊立替康为代表的化疗药物在杀伤癌细胞的同时, 也破坏了人体免疫功能, 造成消化道黏膜损伤及肠道菌群失调, 产生炎症、溃疡及腹泻等消化道症状, 因此在化疗时保护肠黏膜屏障结构完整和功能正常是近年防治化疗不良反应的研究热点[14]。大量研究表明, 包括黄芩素在内的中药对肠道微生态系统的平衡有很好的保护作用, 能直接或间接地调节肠道菌群[15], 但黄芩素治疗化疗性药物肠黏膜炎的活性及其对黏膜炎小鼠肠道菌群的调节作用尚无报道。
如结果所示, 黄芩素可有效改善黏膜炎小鼠便血和肛门着色等症状, 同时减轻结肠组织上皮缺失、黏膜溃疡、肠道结构破坏、隐窝及杯状细胞丢失、炎症性细胞浸润等病理学改变。与正常对照组比较, 模型组中变形菌门的丰度显著增多, 黄芩素可显著降低其丰度。在属水平上, 黄芩素可显著降低模型组中丰度升高的志贺氏菌属、副杆菌属、梭状芽孢杆菌属、乳球菌属, 升高模型组中丰度降低的瘤胃球菌属、毛螺科菌属, 使治疗组小鼠肠道菌群的构成恢复至接近正常水平。
肠球菌属是条件致病菌的代表, 有研究表明, 持续感染这种微生物可能增加患肠道炎性疾病的风险; 梭状芽孢杆菌属是最常见的抗生素相关性腹泻致病菌, 据报道, 炎症性肠病患者拥有更高的难辨梭状芽孢杆菌感染发生率[16]。Ferrari等[17]研究发现, 志贺氏菌属可通过分泌特定的毒力因子, 抑制宿主细胞的分泌、回收及内吞3个胞内运输途径, 以促进肠道上皮生理变化及组织侵袭。这提示了上述菌群的增多与炎症性肠道疾病密切相关。黄芩素给药组减少了造模后增多的肠球菌属、梭状芽孢杆菌属和志贺氏菌属等有害菌, 表明黄芩素可有效抑制诸多致病菌的增殖。已有研究表明[18, 19], 瘤胃球菌属与超敏C反应蛋白和IL-6等炎症标志物呈负相关, 可能通过病原相关分子模式、菌群代谢物短链脂肪酸和衍生物氧化三甲胺、胆汁酸代谢、影响肠肽分泌和肠道通透性等机制, 调节炎症状态; 毛螺菌科与丁酸盐代谢有关, 且与抗炎症免疫细胞数量呈正相关, 该结果表明黄芩素可促进益生菌生长, 并抑制致病菌生长。IL-6和TNF-α被报道与肠黏膜炎的发现发展密切相关[20], 本研究发现黄芩素可显著降低CIM小鼠血清中IL-6、TNF-α的含量, 减缓了炎症反应的发生。已有研究报道[21-23], 肠道内链球菌属的色氨酸代谢产物吲哚丙烯酸可促进肠道上皮屏障功能, 抑制TNF-α并缓解炎症反应; Akk菌是潜在的益生菌, 具有抗慢性结肠炎的作用, 改善结肠炎症状, 降低结肠中TNF-α和γ-干扰素等促炎细胞因子的表达, 促进肠道菌群正常化。由菌群与环境因子的关联性分析看出, 链球菌属、肠球菌属、乳球菌属等与IL-6、TNF-α的含量等环境因子呈正相关; 瘤胃菌属、艾克曼菌属、理研菌属等与IL-6和TNF-α的含量等环境因子呈负相关。这一结果提示化疗诱导性肠黏膜炎小鼠中肠道菌群的变化参与炎性因子表达的调控, 二者的共同作用促进了炎症性肠病的发生发展和治疗。
综上所述, 本研究报道了黄芩素治疗化疗性肠黏膜炎的作用, 这一作用可能是通过调节肠道菌群、修复结肠黏膜及抑制炎症因子表达实现的。同时, 促炎因子与菌群环境关联性分析也反映了黄芩素对肠道菌群的调节与其抗炎活性密切相关。
基金
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  • 国家重点研发计划资助项目(2018YFC0311005)
  • 中国医学科学院医学与健康科技创新工程(2017-I2M-1-010)
文献
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2020年第55卷第5期
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doi: 10.16438/j.0513-4870.2019-0933
  • 接收时间：2019-11-22
  • 首发时间：2026-01-21
  • 出版时间：2020-05-12
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  • 收稿日期：2019-11-22
  • 修回日期：2019-12-28
基金
国家重点研发计划资助项目(2018YFC0311005)
中国医学科学院医学与健康科技创新工程(2017-I2M-1-010)
作者信息
    1.广东药科大学, 广东 广州 510006
    2.中国医学科学院、北京协和医学院药物研究所, 药物靶点研究与新药筛选北京市重点实验室, 北京 100050

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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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