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Article(id=1210148026027471650, tenantId=1146029695717560320, journalId=1189982191388893191, issueId=1210148010437243088, articleNumber=null, orderNo=null, doi=10.16438/j.0513-4870.2022-0377, pmid=null, cstr=null, oa=null, hot=null, price=null, onlineType=0, articleFormat=0, articleType=null, articleTypeStr=research-article, receivedDate=1648569600000, receivedDateStr=2022-03-30, revisedDate=1656518400000, revisedDateStr=2022-06-30, acceptedDate=null, acceptedDateStr=null, onlineDate=1766451372867, onlineDateStr=2025-12-23, pubDate=1660233600000, pubDateStr=2022-08-12, doiRegisterDate=null, doiRegisterDateStr=null, onlineIssueDate=1766451372867, onlineIssueDateStr=2025-12-23, onlineJustAcceptDate=null, onlineJustAcceptDateStr=null, onlineFirstDate=null, onlineFirstDateStr=null, sourceXml=null, magXml=null, createTime=1766451372867, creator=13701087609, updateTime=1766451372867, updator=13701087609, issue=Issue{id=1210148010437243088, tenantId=1146029695717560320, journalId=1189982191388893191, year='2022', volume='57', issue='8', pageStart='2245', pageEnd='2556', issueExtLink='null', onlineDate='null', pubDate='null', beforeIssueId=null, nextIssueId=null, price=null, status=1, issueComplete=1, articleOrder=1, issueType=-1, specialIssue=null, createTime=1766451369151, creator=13701087609, updateTime=1766451533022, updator=13701087609, preIssue=null, nextIssue=null, ext={EN=IssueExt(id=1210148697808179705, tenantId=1146029695717560320, journalId=1189982191388893191, issueId=1210148010437243088, language=EN, specialIssueTitle=, coverIllustrator=null, specialIssueEditor=, specialIssueAbout=), CN=IssueExt(id=1210148697808179706, tenantId=1146029695717560320, journalId=1189982191388893191, issueId=1210148010437243088, language=CN, specialIssueTitle=, coverIllustrator=null, specialIssueEditor=, specialIssueAbout=)}, issueFiles=null}, startPage=2494, endPage=2502, ext={EN=ArticleExt(id=1210148026488845126, articleId=1210148026027471650, tenantId=1146029695717560320, journalId=1189982191388893191, language=EN, title=Mechanism study of rhubarb-peach kernel regulation of feces metabolic profile in mice with adenomyosis, columnId=1190335348761793317, journalTitle=Acta Pharmaceutica Sinica, columnName=Original Articles, runingTitle=null, highlight=null, articleAbstract=

This paper aims to investigate the regulatory mechanism of blood-activating and stasis-dissipating drugs on fecal metabolic characteristics of rhubarb-peach kernel in mice with adenomyosis (AM) using fecal metabolome method. Adenomyosis was modeled by pituitary transplantation, and after the end of modeling administration, fecal samples were collected from mice. Non-targeted metabolomics studies were performed using liquid chromatography-mass spectrometry (LC-MS) to compare the metabolic characteristics of the feces of mice in each group and to find intestinal differential metabolites and potential differential metabolic pathways. The results showed that compared with the normal group, 5-hydroxy-L-tryptophan, histidine, L-acetylcarnitine, 16-hydroxy hexadecanoic acid, thromboxane B2, etc. were significantly up-regulated, L-urobilin and prostaglandin D3 were down-regulated in the feces of the model group, and were reversed after treatment with the rhubarb-peach kernel. The results of metabolic pathway enrichment analysis showed that tryptophan metabolism and histidine metabolism were the main intervention pathways of the rhubarb-peach kernel on AM intestinal metabolism. This study found that the underlying mechanism of the rhubarb-peach kernel in the treatment of AM is related to the intervention of intestinal metabolism of tryptophan, histidine, bile acid, choline and arachidonic acid, and the regulation of pro-inflammatory microenvironment and fatty acid metabolic homeostasis. This study has been approved by the Experimental Animal Ethics Committee of China Three Gorges University (No. 20190801).

, correspAuthors=Pei-pei CHEN, Zhao QU, authorNote=null, correspAuthorsNote=null, copyrightStatement=Copyright ©2022 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=Xian-yun FU, Ping MAO, Yong-li YI, Pei-pei CHEN, Zhao QU), CN=ArticleExt(id=1210148028703437812, articleId=1210148026027471650, tenantId=1146029695717560320, journalId=1189982191388893191, language=CN, title=大黄-桃仁调控子宫腺肌病小鼠粪便代谢谱的机制研究, columnId=1190335348896011050, journalTitle=药学学报, columnName=研究论文, runingTitle=null, highlight=null, articleAbstract=

采用粪便代谢组方法探究活血化瘀药对大黄-桃仁对子宫腺肌病(adenomyosis, AM) 小鼠粪便代谢特征的调控机制。子宫腺肌病造模采用垂体移植法, 造模给药结束后, 收集小鼠粪便样本。使用液质联用(LC-MS) 技术进行非靶向代谢组学研究, 比较各组小鼠粪便的代谢特征, 寻找肠道差异代谢物及潜在的差异代谢通路。结果显示, 与正常组相比, 5-羟基-L-色氨酸、组氨酸、L-乙酰肉碱、16-羟基十六烷酸、血栓素B2等显著上调, L-尿胆素和前列腺素D3在模型组粪便中发生下调, 经大黄-桃仁治疗后均发生回调。代谢通路富集分析结果显示, 色氨酸代谢及组氨酸代谢是大黄-桃仁对AM肠道代谢主要干预通路。本研究发现, 大黄-桃仁治疗AM的潜在机制与干预AM肠道色氨酸、组氨酸、胆汁酸、胆碱及花生四烯酸的代谢、调控促炎微环境及脂肪酸代谢稳态有关。本研究已获得三峡大学实验动物伦理委员会批准(批准号: 20190801)。

, correspAuthors=陈佩佩, 屈赵, authorNote=null, correspAuthorsNote=
*陈佩佩，E-mail: ;
屈赵，E-mail:
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A: Venn diagram analysis of C <i>vs</i> M and M <i>vs</i> D; B: Differential metabolites in fecal samples between groups C, M and D; C: Metabolic pathway changes in stool samples between groups C, M and D. a: Histidine metabolism; b: Tryptophan metabolism; c: Primary bile acid biosynthesis. , figureFileSmall=OSv2NQQf6SyhjUN8e3ZB+Q==, figureFileBig=o4KjFLxbeAP6eReE7G3IJg==, tableContent=null), ArticleFig(id=1210148034810343650, tenantId=1146029695717560320, journalId=1189982191388893191, articleId=1210148026027471650, language=EN, label=null, caption=null, figureFileSmall=null, figureFileBig=null, tableContent=
GroupBefore medication/gAfter medication/g
Normal group (n = 9)27.08 ± 1.7829.80 ± 2.19
Model group (n = 6)29.73 ± 1.1731.13 ± 2.13
Rhubarb-peach kernel group (n = 7)29.13 ± 1.2626.24 ± 3.49
), ArticleFig(id=1210148034902618344, tenantId=1146029695717560320, journalId=1189982191388893191, articleId=1210148026027471650, language=CN, label=Table 1, caption=

Changes in the weight of mice

, figureFileSmall=null, figureFileBig=null, tableContent=
GroupBefore medication/gAfter medication/g
Normal group (n = 9)27.08 ± 1.7829.80 ± 2.19
Model group (n = 6)29.73 ± 1.1731.13 ± 2.13
Rhubarb-peach kernel group (n = 7)29.13 ± 1.2626.24 ± 3.49
), ArticleFig(id=1210148035032641774, tenantId=1146029695717560320, journalId=1189982191388893191, articleId=1210148026027471650, language=EN, label=null, caption=null, figureFileSmall=null, figureFileBig=null, tableContent=
MetaboliteFormulam/zM/CD/M
FCPVIPFCPVIP
AlanyltryptophanC14H17N3O3275.131.9820.0431.2430.4580.0291.401
16-Hydroxy hexadecanoic acidC16H32O3254.232.5500.0021.4650.4550.0101.217
Prostaglandin D3C20H30O5350.210.4300.0031.4212.4300.0061.418
Cysteine-S-sulfateC3H7NO5S2200.982.4500.0031.5710.4900.0171.308
L-HistidineC6H9N3O2155.072.5890.0181.6440.2050.0032.153
L-AcetylcarnitineC9H18NO4203.123.4240.0181.4420.2750.0221.481
Glycyl-tyrosineC11H14N2O4238.101.8650.0231.3480.5280.0211.341
L-UrobilinC33H42N4O6594.340.1510.0032.3244.7360.0192.013
LeucylprolineC11H20N2O3228.152.3290.0041.4940.4950.0351.362
Thromboxane B2C20H34O6196.112.5410.0071.6410.5050.0341.343
N-Acetyl-5-aminosalicylic acidC9H9NO4195.051.9790.0101.3940.6090.0441.059
2-PhenylacetamideC8H9NO135.072.3780.0001.6310.4710.0011.500
Taurochenodesoxycholic acidC26H45NO6S499.306.7120.0002.1090.1990.0091.964
D-TryptophanC11H12N2O2204.092.3240.0001.6060.5660.0211.280
5-Hydroxy-L-tryptophanC11H12N2O3220.082.0820.0021.4680.5680.0181.231
), ArticleFig(id=1210148035112333556, tenantId=1146029695717560320, journalId=1189982191388893191, articleId=1210148026027471650, language=CN, label=Table 2, caption=

Identification results of potential biomarkers of rhubarb-peach kernel in the treatment of mice with adenomyosis. M/C: Model group vs normal group; D/M: Rhubarb-peach kernel group vs model group; FC: Fold change; P: P-value; VIP: Variable importance in the projection

, figureFileSmall=null, figureFileBig=null, tableContent=
MetaboliteFormulam/zM/CD/M
FCPVIPFCPVIP
AlanyltryptophanC14H17N3O3275.131.9820.0431.2430.4580.0291.401
16-Hydroxy hexadecanoic acidC16H32O3254.232.5500.0021.4650.4550.0101.217
Prostaglandin D3C20H30O5350.210.4300.0031.4212.4300.0061.418
Cysteine-S-sulfateC3H7NO5S2200.982.4500.0031.5710.4900.0171.308
L-HistidineC6H9N3O2155.072.5890.0181.6440.2050.0032.153
L-AcetylcarnitineC9H18NO4203.123.4240.0181.4420.2750.0221.481
Glycyl-tyrosineC11H14N2O4238.101.8650.0231.3480.5280.0211.341
L-UrobilinC33H42N4O6594.340.1510.0032.3244.7360.0192.013
LeucylprolineC11H20N2O3228.152.3290.0041.4940.4950.0351.362
Thromboxane B2C20H34O6196.112.5410.0071.6410.5050.0341.343
N-Acetyl-5-aminosalicylic acidC9H9NO4195.051.9790.0101.3940.6090.0441.059
2-PhenylacetamideC8H9NO135.072.3780.0001.6310.4710.0011.500
Taurochenodesoxycholic acidC26H45NO6S499.306.7120.0002.1090.1990.0091.964
D-TryptophanC11H12N2O2204.092.3240.0001.6060.5660.0211.280
5-Hydroxy-L-tryptophanC11H12N2O3220.082.0820.0021.4680.5680.0181.231
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大黄-桃仁调控子宫腺肌病小鼠粪便代谢谱的机制研究
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付先芸 , 毛萍 , 易永丽 , 陈佩佩 * , 屈赵 *
药学学报 | 研究论文 2022,57(8): 2494-2502
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药学学报 | 研究论文 2022, 57(8): 2494-2502
大黄-桃仁调控子宫腺肌病小鼠粪便代谢谱的机制研究
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付先芸, 毛萍, 易永丽, 陈佩佩* , 屈赵*
作者信息
  • 三峡大学医学院, 三峡大学国家中医药管理局中药药理科研三级实验室, 湖北 宜昌 443000

通讯作者:

*陈佩佩，E-mail: ;
屈赵，E-mail:
Mechanism study of rhubarb-peach kernel regulation of feces metabolic profile in mice with adenomyosis
Xian-yun FU, Ping MAO, Yong-li YI, Pei-pei CHEN* , Zhao QU*
Affiliations
  • Third-Grade Pharmacological Laboratory on Traditional Chinese Medicine, State Administration of Traditional Chinese Medicine, China Three Gorges University, Medical College, China Three Gorges University, Yichang 443000, China
出版时间: 2022-08-12 doi: 10.16438/j.0513-4870.2022-0377
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摘要
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采用粪便代谢组方法探究活血化瘀药对大黄-桃仁对子宫腺肌病(adenomyosis, AM) 小鼠粪便代谢特征的调控机制。子宫腺肌病造模采用垂体移植法, 造模给药结束后, 收集小鼠粪便样本。使用液质联用(LC-MS) 技术进行非靶向代谢组学研究, 比较各组小鼠粪便的代谢特征, 寻找肠道差异代谢物及潜在的差异代谢通路。结果显示, 与正常组相比, 5-羟基-L-色氨酸、组氨酸、L-乙酰肉碱、16-羟基十六烷酸、血栓素B2等显著上调, L-尿胆素和前列腺素D3在模型组粪便中发生下调, 经大黄-桃仁治疗后均发生回调。代谢通路富集分析结果显示, 色氨酸代谢及组氨酸代谢是大黄-桃仁对AM肠道代谢主要干预通路。本研究发现, 大黄-桃仁治疗AM的潜在机制与干预AM肠道色氨酸、组氨酸、胆汁酸、胆碱及花生四烯酸的代谢、调控促炎微环境及脂肪酸代谢稳态有关。本研究已获得三峡大学实验动物伦理委员会批准(批准号: 20190801)。

子宫腺肌病  /  粪便代谢组  /  氨基酸代谢

This paper aims to investigate the regulatory mechanism of blood-activating and stasis-dissipating drugs on fecal metabolic characteristics of rhubarb-peach kernel in mice with adenomyosis (AM) using fecal metabolome method. Adenomyosis was modeled by pituitary transplantation, and after the end of modeling administration, fecal samples were collected from mice. Non-targeted metabolomics studies were performed using liquid chromatography-mass spectrometry (LC-MS) to compare the metabolic characteristics of the feces of mice in each group and to find intestinal differential metabolites and potential differential metabolic pathways. The results showed that compared with the normal group, 5-hydroxy-L-tryptophan, histidine, L-acetylcarnitine, 16-hydroxy hexadecanoic acid, thromboxane B2, etc. were significantly up-regulated, L-urobilin and prostaglandin D3 were down-regulated in the feces of the model group, and were reversed after treatment with the rhubarb-peach kernel. The results of metabolic pathway enrichment analysis showed that tryptophan metabolism and histidine metabolism were the main intervention pathways of the rhubarb-peach kernel on AM intestinal metabolism. This study found that the underlying mechanism of the rhubarb-peach kernel in the treatment of AM is related to the intervention of intestinal metabolism of tryptophan, histidine, bile acid, choline and arachidonic acid, and the regulation of pro-inflammatory microenvironment and fatty acid metabolic homeostasis. This study has been approved by the Experimental Animal Ethics Committee of China Three Gorges University (No. 20190801).

adenomyosis  /  fecal metabolome  /  amino acid metabolism
付先芸, 毛萍, 易永丽, 陈佩佩, 屈赵. 大黄-桃仁调控子宫腺肌病小鼠粪便代谢谱的机制研究. 药学学报, 2022 , 57 (8) : 2494 -2502 . DOI: 10.16438/j.0513-4870.2022-0377
Xian-yun FU, Ping MAO, Yong-li YI, Pei-pei CHEN, Zhao QU. Mechanism study of rhubarb-peach kernel regulation of feces metabolic profile in mice with adenomyosis[J]. Acta Pharmaceutica Sinica, 2022 , 57 (8) : 2494 -2502 . DOI: 10.16438/j.0513-4870.2022-0377
正文
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代谢是细胞功能的基础。作为非肿瘤性疾病, 子宫腺肌病(adenomyosis, AM) 恶性增殖能力的发生可能更多取决于细胞代谢重塑导致的微环境的改变而非细胞本身的基因突变。因此, 富含大量信息的代谢谱日益引起研究者们的关注。随着高灵敏度和特异性的质谱分析技术的发展, 越来越多的研究者通过分析代谢组学的变化探索此类妇科良性疾病的潜在机制[1]。通过血清代谢谱的分析, 有研究者发现AM患者的差异性代谢产物参与免疫激活以及细胞增殖和细胞迁移[2]。另有研究者证实子宫肌层的代谢组学图谱差异表达与AM炎症反应、氧化应激、细胞增殖和凋亡以及能量代谢过程有关[3]。肠道内存在机体最庞大的微生态系统, 通过发酵和降解参与糖代谢、氨基酸代谢、胆汁酸代谢、胆碱代谢等, 粪便代谢组学变化可一定程度表征疾病及治疗的表型变化。然而, 目前尚缺乏AM肠道代谢组的研究。
AM的现有保守治疗方法伴随临床疗效不佳、复发率高、肝肾功能损伤及干扰生殖内分泌等问题[4], 严重影响患者生活和工作质量[5]。传统中医药治疗AM有悠久的历史, 具有显著改善AM病理浸润程度、且不干扰正常内分泌的显著优势[6]。中医学认为, “瘀血致癥”是AM病机核心, 化瘀法是治疗AM的核心大法, 化瘀类药物在AM治疗中获得高频次选用[7]。大黄-桃仁药对来源于中医活血化瘀经典方, 张仲景的22个活血化瘀经典方中, 6个[桃核承气汤、下淤血汤、大黄䗪虫丸、抵挡丸(汤)、鳖甲煎丸、大黄牡丹汤] 均含有该药对。本课题组已围绕该药对进行了大量的体内外研究, 证实其有调节免疫、抑制增殖、促进凋亡、改善氧化应激等多靶点作用。大黄、桃仁两药兼入胃或大肠经, 除下瘀血、破癥瘕积聚外, 同时具有荡涤肠胃、推陈致新、通利水谷的功效。大黄-桃仁药对是否对肠道代谢有一定的干预作用尚待进一步的研究。
因此, 本课题拟采用质谱分析方法, 探索AM肠道代谢谱的差异变化及大黄-桃仁对其潜在的干预机制。
材料与方法
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仪器与试剂  Q ExactiveTM HF质谱仪、Vanquish UHPLC色谱仪及Hypesil Gold column色谱柱(美国Thermo Fisher Scientific公司); D3024R低温离心机(美国Scilogex公司)。酒大黄免煎剂(批号19004961)、桃仁免煎剂(批号19006412) 购自于北京康仁堂制药有限公司。丙泊酚(批号21803281) 购自于西安立邦制药有限公司。色谱纯超纯水购自于德国Merck公司; 色谱纯甲醇、色谱纯甲酸及色谱纯醋酸铵均购自于美国Thermo Fisher Scientific公司。
实验动物  实验用ICR小鼠购于北京市维通利华实验动物技术有限公司, 许可证号: CXK (京) 2016-0006。整个实验过程均按照《三峡大学实验动物护理和使用指南》进行。实验期间动物自由饮食和进水, 昼夜节律正常。本研究已获得三峡大学实验动物伦理委员会批准(批准号: 20190801)。
分组、造模与给药  22只7周龄ICR雌性小鼠随机分为正常组(n = 9)、模型组(n = 6) 及大黄-桃仁组(n = 7)。本实验子宫腺肌病造模采用垂体移植法[8], 具体操作方法: 除正常组外, 其余两组小鼠, 腹腔注射丙泊酚100 mg·kg-1全麻, 下腹部消毒, 下腹正中偏右纵向切口2 cm, 分离出右侧子宫, 取同周龄ICR雄鼠, 引颈处死, 开颅取出脑垂体, 混合少量生理盐水, 吸入部分垂体生理盐水悬浊液于50 mL套管针头内, 缓慢推入宫腔, 腹腔内滴入庆大霉素溶液0.25 mL, 常规关腹。正常组和模型组均予以每天生理盐水灌胃, 大黄-桃仁组按照人与小鼠剂量换算[9], 予以大黄、桃仁免煎颗粒4.25 g·kg-1·d-1灌胃给药, 每日1次。检测小鼠给药前后体重变化。
样本收集与贮存  连续灌胃给药6周后于增生期颈椎脱臼处死小鼠。剖腹取出小鼠右侧子宫样本和结肠新鲜粪便, 其中子宫放置于4%的多聚甲醇中保存, 用于组织病理学评价, 粪便样本冻于-80 ℃冰箱用于代谢组学分析。
HE染色组织学评价  小鼠子宫组织用4%的多聚甲醛固定24 h后, 脱水、石蜡包埋、切片、二甲苯脱蜡、水化、苏木精染色、分化、伊红染色、脱水、封片。封片后在光学显微镜下观察子宫内膜浸润深度。
代谢组学样本制备  实验前取出-80 ℃保存的粪便组织, 称取100 mg样本并加适当液氮进行研磨后, 置于EP管中, 加入500 μL含0.1%甲酸的80%甲醇水溶液, 涡旋震荡, 冰浴静置5 min, 15 000 g、4 ℃离心10 min, 取上清液300 μL, 加150 μL质谱水稀释至甲醇含量为53%, 并置于离心管中15 000 g、4 ℃离心10 min, 集上清液, 采用LC-MS方法进行分析。量控制样品(quality control, QC) 为等比混合所有实验样品组成, 与实验样本按照同样的方法处理, 在实验样本LC-MS/MS进样前、进样中和进样后上机检测, 以评价整体实验过程系统稳定性, 并进行后续数据质控分析。
色谱条件  样品测定采用Vanquish UHPLC系统(Thermo Fisher, 德国), 选取Hypesil Gold column色谱柱(100 mm × 2.1 mm, 1.9 μm), 柱温为40 ℃, 流速为0.2 mL·min-1; 正、负离子模式: 正离子模式流动相由0.1%甲酸水(A) 和甲醇(B) 构成; 负离子模式下流动相由5 mmol·L-1醋酸铵(pH 9.0, A) 和甲醇(B) 构成; 梯度洗脱条件: 0~1.5 min, 2% B; 1.5~12 min, 2%~100% B; 12~14 min, 100% B; 14~14.1 min, 100%~2% B; 14.1~17 min, 2% B。
质谱条件  采用Q ExactiveTM HF质谱仪(Thermo Fisher, 德国), 正负离子扫描模式; 数据采集范围m/z 70~1 050; 诱导碰撞解离能量20、40、60 eV; 喷雾电压3.2 kV; 毛细管温度320 ℃; 鞘气流速40 arb; 辅助气流速10 arb。
代谢组学数据处理与分析  原始数据文件通过Compound Discoverer 3.1 (Thermo Fisher, 美国) 软件, 进行峰识别、对齐、降噪、峰面积归一化等数据预处理, 得到含有代谢物保留时间(tR)、质荷比等信息的数据矩阵文件[10]。将得到的数据矩阵文件导入SMICA 14.0软件中, 进行无监督的主成分分析(principal component analysis, PCA) 和有监督的正交偏最小二乘判别分析(partial least squares discriminant analysis, OPLS-DA)。根据OPLS-DA分析中的变量投影重要性(variable importance in the projection, VIP) > 1.0以及t检验(P < 0.05) 筛选出组间具有显著性差异的代谢物。通过HMDB (Human Metabolome Database, http://www.hmdb.ca/) 数据库对筛选得到的差异代谢物进行检索, 得到差异代谢物的HMDB ID, 然后将得到的HMDB ID导入到Metaboanalyst 5.0 (https://www.metaboanalyst.ca/) 网站进行代谢通路分析。
统计学分析  数据均用$ \stackrel{-}{x} $ ± s表示, 采用SPSS 17.0进行统计分析, 多组间差异比较采用单因素方差分析, P < 0.05认为差异有统计学意义。
结果
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1 各组小鼠体重变化及粪便性状
用药前后的小鼠体重对照, 模型组小鼠体重显著增加, 正常组有增加趋势, 大黄桃仁组有减小趋势, 但均无显著统计学差异, 见表 1。对小鼠新鲜粪便观察, 除模型组1只小鼠粪便稀溏不成型外, 余各组小鼠粪便均为成形软便, 无明显异常, 证实酒大黄与桃仁无明显泻下作用, 不干扰正常大便性状。
2 小鼠子宫病理变化
HE染色下, 增生期子宫内膜间质组织致密度高, 螺旋动脉呈现主弯曲增长趋势, 内膜腺体数量较多, 生长形态为弯曲[11]。HE染色结果表明, 正常组小鼠子宫内膜层结构完整, 与子宫肌层有明显的分界线, 肌层内未见腺体和间质细胞; 模型组子宫内膜层与肌层无明显分界线, 腺体浸润到子宫内肌层、外肌层, 形成腺肌瘤(黑色箭头); 与模型组相比, 大黄-桃仁组的腺体和间质细胞浸润子宫肌层程度有明显改善, 见图 1。
3 代谢组学数据质控
代谢组具有易受外界因素干扰且变化迅速的特点, 大量样本上机检测需要一定的时间, 高通量数据批次内和批次间存在的非生物误差对分析结果有不可忽视的影响。因此, 监控检测过程中样品及仪器的稳定性、信号响应的强度对于结果的质量控制尤为重要。本研究在样本检测前、中、后分别插入5个QC样本, 基于代谢物的相对定量值来计算5个QC样本之间Pearson相关性。QC样本在正、负离子模式下Pearson相关系数r均 > 0.99, P < 0.001, 说明QC样本间显著正相关(图 2A、B); r2接近于1, 拟合程度好, 证实数据稳定性好, 质量较高(图 2C、D)。
4 代谢轮廓分析
正、负离子模式下, 各组小鼠粪便样品总离子流图(total ion chromatogram, TIC) 基本相似, 但各组峰型、峰高和峰面积具有一定的差异, 表明各组小鼠体内代谢物存在差异, 见图 3。
5 多元统计分析
本研究旨在寻找与子宫腺肌病有关的潜在生物标志物, 探讨大黄-桃仁对子宫腺肌病的治疗作用及可能的作用机制。将正常组(C)、模型组(M)、大黄-桃仁组(D) 及质控样本组(QC) 正负离子模式下得到的数据导入到SMICA 14.0软件中进行无监督的PCA分析。在正负离子模式下, QC样本聚集良好, 说明该检测系统稳定可靠, 重复性好, 所得差异物可以反映样本间的生物学差异。各样本正、负离子模式下PCA图显示, 正常组、模型组和大黄-桃仁组之间分离趋势显著, 说明不同生理或病理状态下的小鼠其内源性代谢物存在明显差异。大黄-桃仁组位于正常组和模型组之间, 表明大黄-桃仁能够使模型组小鼠代谢紊乱趋向正常, 见图 4A、B。
6 潜在生物标志物的筛选
为了进一步确定给药后小鼠粪便内源性代谢物的变化, 分别对正常组与模型组、模型组与大黄桃仁组进行了OPLS-DA分析。OPLS-DA分析能够进一步使组间区别最大化, 有利于发现差异代谢物。OPLS-DA分析结果显示, 正常组与模型组、模型组与大黄-桃仁组之间均能明显分开, 证实AM小鼠粪便样本与健康小鼠相比代谢产物有明显差异(图 4C), 大黄-桃仁对模型组小鼠肠道代谢具有一定的调控作用(图 4D)。所得模型参数正离子模式下为R2X = 0.461, R2Y = 1, Q2 = 0.760; 负离子模式下为R2X = 0.382, R2Y = 0.998, Q2 = 0.643, 说明该模型具有较好的解释力以及预测力。200次模型验证结果表明, Q2点的回归线与纵轴相交于原点以下, 表明未产生过拟合, 模型可靠, 见图 4E、F。
以VIP > 1和t检验中P < 0.05作为显著变化的差异变量, 然后将所得的变量差异借助韦恩图进行分析, 见图 5A。造模成功后可引起113个变量发生显著变化, 而经过大黄-桃仁治疗后, 可以显著改善80个变量, 其中, 有22个为共有的差异变量。然后将共有的22个差异变量进行数据库鉴定, 最后鉴定得到L-组氨酸、5-羟基-L-色氨酸、丙氨酰色氨酸等共15个共同的差异代谢物, 差异代谢物详细信息见表 2。
选择倍数变化(fold change, FC) 值作为反映模型组与正常组、大黄-桃仁组与模型组粪便代谢物含量变化的指标。当FC > 1时, 表明粪便中该代谢物含量上升; 当FC < 1时, 表明粪便中该代谢物含量下降。模型组小鼠粪便中5-羟基-L-色氨酸、亮氨酰脯氨酸、D-色氨酸等13个代谢物含量增加, 前列腺素D3 (prostaglandin D3, PGD3)、L-尿胆素2个代谢物含量下降, 给予大黄-桃仁后, 对15个差异代谢物均有所回调, 见表 2。进一步采用MetaboAlalyst 5.0网站将组间的差异代谢物进行聚类分析, 得到可视化热图(图 5B)。水平轴代表样本, 垂直轴代表差异代谢物, 颜色深浅反映变量值大小; 图中红色代表含量高; 蓝色代表含量低。
7 代谢通路分析
将筛选出的15个差异代谢物导入到MetaboAnalyst 5.0网站中进行代谢通路分析。代谢通路分析发现, 大黄-桃仁影响子宫腺肌病小鼠的代谢途径主要为组氨酸代谢、色氨酸代谢和初级胆汁酸生物合成等, 见图 5C。
讨论
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AM的病理表现为内膜细胞向肌层的癌样浸润, 其发病率高[12], 90%的患者伴有月经过多或子宫异常出血、痛经、性交困难、不孕等临床症状[13], 其发病与性激素失调、低级别炎症、慢性氧化应激、增殖与凋亡紊乱等多种机制有关。子宫腺肌病属于中医学中“癥瘕”、“痛经”的范畴。中医理论认为, 情志内伤、外邪入侵、体质因素或手术损伤导致气血失和、冲任损伤, 瘀血恶血壅于肌肉, 内结成块而致癥。因此, “瘀血致癥”是AM的核心病机环节。活血化瘀为基本治疗大法[14], 化瘀类药物在AM治疗中获得高频次选用[7]。本课题组前期研究证实, 活血化瘀中药可抑制子宫内膜异位细胞的侵袭能力, 显著改善AM病理浸润程度, 且不干扰正常内分泌, 具有多靶点作用[6]。代谢组的多元化综合分析与中医整体观相应, 可从整体上探索疾病过程中代谢物的变化及中药的多靶点干预机制。本课题首次采用动物模型方法, 以AM粪便代谢谱的变化为靶点, 探索了AM的可能发病机制及活血化瘀药对大黄-桃仁的潜在干预机制。
肠道存在机体最庞大的微生态系统, 肠道代谢产物与人体的生理及病理过程密切相关[3, 15]。本课题研究结果表明, 正常组和模型组粪便代谢组学之间分离趋势显著, 证实AM病理状态下的小鼠肠道内代谢物存在明显差异。
大黄-桃仁药对来源于中医经典活血化瘀方。其中, 酒大黄性寒味苦, 入脾、胃、肝、大肠、心包经; 桃仁性平味苦, 入心、肝、肺、大肠经。两者同有活血化瘀、润肠通便功效[16]。因两药均可兼入胃或大肠经, 推测其对胃肠道的功能有潜在的干预作用。研究首先观察了各组小鼠的体重差异。观察发现, 在体重的变化上, 模型组小鼠体重在6周后显著上升, 空白组有上升趋势, 而大黄桃仁组有下降趋势。大黄-桃仁药对未造成模型小鼠粪便性状的改变, 证实酒制大黄提取物配伍桃仁无明显泻下不良反应。对AM小鼠造模前后及中药治疗后肠道代谢组的差异分析结果显示, 大黄-桃仁组与模型组分离趋势显著, 且位于正常组和模型组之间。该结果证实, 大黄-桃仁可回调AM导致的肠道代谢组紊乱, 使AM小鼠肠道代谢趋向正常。
本研究对差异代谢物进行了代谢通路分析结果表明, 色氨酸代谢通路是AM发病及中药治疗的潜在机制。色氨酸为必需氨基酸, 肠道是其合成的主要场所, 食物蛋白质在小肠中被水解成寡肽和氨基酸, 经主动转运吸收。体内色氨酸除参与蛋白质合成外, 主要经过犬尿氨酸途径和5-羟色胺途径进行代谢生成生物活性物质。外周组织的5-羟色胺可以发挥强血管收缩剂和平滑肌收缩刺激剂的作用, 并呈浓度依赖性促进成纤维细胞增殖, 被认为与AM疾病进展有关[17]。绝大多数色氨酸通过犬尿氨酸途径代谢, 吲哚胺-2, 3-双加氧酶(indoleamine 2, 3-di-oxygenase, IDO) 是该代谢途径的关键限速酶, 可催化色氨酸降解生成N-甲酰犬尿氨酸, 最终转化为犬尿氨酸(kynurenine, KYN)。有研究表明, 子宫内膜异位症患者IDO的表达增加, 可上调色氨酸分解代谢[18], 雌激素/IDO1轴调控子宫内膜异位症免疫细胞的分化, 促进促炎微环境的形成[19]。KYN被证实可以作为芳基烃受体(aryl hydrocarbon receptor, AhR) 的内源性配体, 通过自分泌或旁分泌方式与AhR受体相互作用, 抑制抗肿瘤免疫反应, 促进肿瘤细胞存活。子宫内膜异位性疾病有类似肿瘤的恶性增殖能力, 有研究发现, 色氨酸过度分解代谢是允许子宫内膜异位植入的免疫耐受性产生的重要原因[20], 其作用与KYN激活AhR上调IL-17和活性氧(reactive oxygen species, ROS) 有关[21], 氧化应激、炎症和肠道代谢之间在子宫内膜异位性疾病中存在相关性[22]。因此, 子宫内膜肌层界面的ROS及促炎微环境的形成与肠道内大量色氨酸吸收入血、为局部色氨酸代谢的增加提供前体来源有关, 大黄-桃仁的干预可显著减少肠道色氨酸的合成从而下调色氨酸活性代谢产物及相关信号通路[16]。该结论尚需进一步的实验研究证实。
组氨酸代谢通路的激活是本研究聚焦的另一个潜在的机制。组氨酸同样也是必需氨基酸之一, 其合成已被证实发生于大肠杆菌[23]。中医学认为, “瘀血致癥”是AM的核心病机。研究表明, 组氨酸代谢与中医血瘀证型相关, 如寒凝血瘀证中组氨酸代谢呈现高度活跃状态[24], 寒凝血瘀模型大鼠粪便中组氨酸脱氨基分解产物尿刊酸升高[24]; 而痰瘀互结证型组氨酸含量较健康者显著升高[25]。组氨酸可经脱羧酶的作用转化为重要炎症活性物质组胺。有研究者认为, 人和小鼠粪便中检测到较高的组氨酸与潜在的炎症反应有关[26]。动物实验研究发现, 子宫内膜异位性疾病患者疼痛综合征的强度与外周血组胺水平存在直接关系[27]。作者研究证实, 与健康小鼠比较, 组氨酸在AM小鼠肠道内的合成显著增加, 推测其是“瘀血证”下疼痛发生的重要物质基础。进一步研究证实, 降低肥大细胞分泌的组氨水平可显著减轻内异症大鼠的痛觉过敏反应[28]。现有研究发现, 活血化瘀药物如大黄对血瘀证模型大鼠血浆代谢物有显著的调控作用[29], 作者的研究结果证实, 经大黄-桃仁干预后AM小鼠组氨酸合成显著下降。因此, 大黄-桃仁对组氨酸肠道合成及代谢的作用是改善AM痛经症状的潜在机制。
除两个主要代谢通路外, 本研究还初步发现AM小鼠肠道中存在棕榈酰肉碱及牛磺鹅去氧胆酸钠的代谢异常, 两种代谢物的变化与AM的脂肪酸代谢紊乱有关。脂肪酸β-氧化的速率由辅酶A和肉碱穿梭细胞控制线粒体对脂肪酸的摄取来调节, 高表达的棕榈酰肉碱导致人体内脂肪氧化代谢稳态失调。有研究证实子宫腺肌病患者血液中、子宫平滑肌层棕榈酰肉碱含量均显著增高[2, 3, 17], 与子宫肌层干细胞异常分化、能量需求增高、子宫肌层纤维化、子宫异常增大有关[17]。酰基肉碱可作为AM的标志物之一, 酰基肉碱的增高程度可用于预测子宫内膜异位性疾病的分期[30]。胆汁酸的合成发生在肝脏细胞, 合成了初级胆汁酸, 即胆酸和鹅去氧胆酸。肝脏中的胆汁酸会共轭结合牛磺酸和甘氨酸。二级胆汁酸被分泌进肠道, 并被细菌修饰脱羟基, 转化成脱氧胆酸、石胆酸。80%~90%的胆汁酸可以通过门静脉血运的肝肠循环回到肝脏中, 再次通过肝脏合成胆汁, 进入到胆道, 帮助脂肪食物乳化、吸收, 促进脂质代谢[25]。肠道内的生态失调导致胆汁酸水解酶活性的降低, 是导致初级胆汁酸增加和次级胆汁酸池减少的重要原因[31], 本研究结果发现次级胆汁酸盐牛磺鹅去氧胆酸钠在AM小鼠肠道中显著下调。经大黄-桃仁治疗后棕榈酰肉碱和胆酸盐在肠道内均发生显著回调, 证实该药对的治疗作用与改善脂肪代谢的稳态有关。
PGD3与血栓素B2 (thromboxane B2, TXB2) 均来源于花生四烯酸代谢。PGD3是二十碳五烯酸(eicosapentaenoic acid, EPA) 代谢产物, 内源性和外源性的EPA均可通过其抗炎作用来保护子宫内膜异位性疾病的发生[32]。研究发现EPA摄入量较高的妇女子宫内膜异位症发生率较低[33], 血清EPA含量与子宫内膜异位症的患病可能性负相关[33], 这可以部分解释本研究发现的AM小鼠中肠道代谢PGD3的减少。本研究中, 大黄-桃仁的治疗可增加肠道内二十碳五烯酸代谢物PGD3含量。另一个花生四烯酸代谢产物TXB2在AM模型小鼠中增高, 血栓素B2是血栓素A2 (thromboxane A2, TXA2) 的代谢产物, TXA2可直接诱导子宫内膜细胞神经突生长, 导致痛经症状的发生[34]; 研究也发现, 抑制TXB2的形成可通过抑制炎症改善小鼠子宫内膜异位的发生[35]。本研究发现, 大黄-桃仁的治疗可显著下调肠道内TXB2的含量, 可能与其改善AM的痛经症状及促炎微环境有关。
综上, 本研究的结果证实, 大黄桃仁的治疗作用可能与干预AM肠道色氨酸、组氨酸合成以及胆汁酸、胆碱及花生四烯酸的代谢、调控促炎微环境及脂肪酸代谢稳态有关, 该结果可为中医药治疗子宫内膜异位性疾病的机制研究提供新的思路和方向。
作者贡献: 屈赵、付先芸负责整体实验思路设计及文章修改; 付先芸、陈佩佩负责完成实验数据处理和文章的撰写; 毛萍、易永丽负责完成主要的实验部分; 所有作者均对本文有所贡献。
利益冲突: 本文研究内容无任何利益冲突。
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  • 国家自然科学基金面上项目(81973897)
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2022年第57卷第8期
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doi: 10.16438/j.0513-4870.2022-0377
  • 接收时间：2022-03-30
  • 首发时间：2025-12-23
  • 出版时间：2022-08-12
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  • 收稿日期：2022-03-30
  • 修回日期：2022-06-30
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国家自然科学基金面上项目(81973897)
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    三峡大学医学院, 三峡大学国家中医药管理局中药药理科研三级实验室, 湖北 宜昌 443000

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2种不同金属材料的力学参数
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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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