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Article(id=1322912279179698605, tenantId=1146029695717560320, journalId=1255847919539208197, issueId=1322912162913596032, articleNumber=null, orderNo=null, doi=10.13193/j.issn.1673-7717.2025.01.018, pmid=null, cstr=null, oa=null, hot=null, price=null, onlineType=0, articleFormat=0, articleType=null, articleTypeStr=null, receivedDate=null, receivedDateStr=null, revisedDate=null, revisedDateStr=null, acceptedDate=null, acceptedDateStr=null, onlineDate=1793336465877, onlineDateStr=2026-10-30, pubDate=1736438400000, pubDateStr=2025-01-10, doiRegisterDate=null, doiRegisterDateStr=null, onlineIssueDate=1793336465877, onlineIssueDateStr=2026-10-30, onlineJustAcceptDate=null, onlineJustAcceptDateStr=null, onlineFirstDate=null, onlineFirstDateStr=null, sourceXml=null, magXml=null, createTime=1793336465877, creator=13701087609, updateTime=1793336465877, updator=13701087609, issue=Issue{id=1322912162913596032, tenantId=1146029695717560320, journalId=1255847919539208197, year='2025', volume='43', issue='1', pageStart='1', pageEnd='258', issueExtLink='null', onlineDate='null', pubDate='1736438400000', pubDateStr='2025-01-10', beforeIssueId=null, nextIssueId=null, price=null, status=1, issueComplete=1, articleOrder=1, issueType=-1, specialIssue=0, createTime=1793336438157, creator='13701087609', updateTime=1793340633627, updator='13701087609', preIssue=null, nextIssue=null, articleTotal=null, ext={EN=IssueExt(id=1322929760048906989, tenantId=1146029695717560320, journalId=1255847919539208197, issueId=1322912162913596032, language=EN, specialIssueTitle=, coverIllustrator=null, specialIssueEditor=, specialIssueAbout=), CN=IssueExt(id=1322929760048906990, tenantId=1146029695717560320, journalId=1255847919539208197, issueId=1322912162913596032, language=CN, specialIssueTitle=, coverIllustrator=null, specialIssueEditor=, specialIssueAbout=)}, issueFiles=null, downloadFileDto=null}, startPage=97, endPage=101, ext={EN=ArticleExt(id=1322912279401996718, articleId=1322912279179698605, tenantId=1146029695717560320, journalId=1255847919539208197, language=EN, title=Effect of Berberine on Energy Metabolism in EC9706 Cells Based on AMPK/mTOR Pathway, columnId=1256183361521967297, journalTitle=Chinese Archives of Traditional Chinese Medicine, columnName=Target on National Project, runingTitle=null, highlight=null, articleAbstract=
Objective

To investigate the mechanism of berberine on energy metabolism and related pathways in EC9706 cells.

Method

The cellswere routinely cultured，MTT screened，and two mass concentrations of 15 μg/mL and 30 μg/mL were selected. The cell cycle and apoptosis were detected by flow cytometry，the glycolytic potential and mitochondrial respiratory capacity were detected by energy metabolism analysis system，and the changes in the expression of phosphorylated adenylate activated protein kinase（p-AMPK）/adenylate activated protein kinase（AMPK）and the downstream phosphor ylated mammalian target of rapamyc in（p-mTOR）/mammalian target of rapamycin（mTOR）proteins were explored by Western Blotting. The expression levels of AMPK and downstream mTOR were verified at the gene level by quantitative real-time PCR（qPCR）.

Results

Berberine significantly inhibited the proliferation of EC9706 cells（P<0.01）and promoted the apoptosis of EC9706 cells（P<0.05）. Compared with the control group，berberine and drug group showed a significant decrease in the G0/G1 phase（P<0.05），and a significant increase in the proportion of Sphase（P<0.01）. Berberine inhibited the glycolytic potentia and mitochondrial respiration of EC9706 cells（P<0.01）in a concentration-dependent manner，and berberine promoted p-AMPK/AMPK（P<0.01）and inhibited the expression of p-mTOR/mTOR protein（P<0.05）. At the gene level，berberine promoted AMPK expression（P<0.05）as well asmTOR expression（P<0.01）.

Conclusion

Berberine can inhibit the proliferation of oesophageal cancer EC9706 cells through energy metabolic pathway，promote apoptosis of oesophageal cancer cells and hinder their division.

, authors=Yang LIU, Xing CHEN, Zhexu ZHOU, Yaru LIU, Xiaobo HU, Yulong CHEN, authorsList=Yang LIU, Xing CHEN, Zhexu ZHOU, Yaru LIU, Xiaobo HU, Yulong CHEN, authorCompany=null, correspAuthors=Yulong CHEN, 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, fund=null), CN=ArticleExt(id=1322912283533386185, articleId=1322912279179698605, tenantId=1146029695717560320, journalId=1255847919539208197, language=CN, title=小檗碱基于AMPK/mTOR通路对EC9706细胞能量代谢的影响, columnId=1256183362172142382, journalTitle=中华中医药学刊, columnName=国家项目点击, runingTitle=null, highlight=null, articleAbstract=
目的

通过观察小檗碱对EC9706细胞能量代谢及相关通路的影响从而探究其机制。

方法

常规培养细胞，MTT法筛药，选择15、30 μg/mL两个质量浓度，通过流式细胞术检测细胞周期、凋亡水平，能量代谢分析系统检测细胞糖酵解潜能及线粒体呼吸能力，蛋白质印迹实验探究细胞中p-AMPK/AMPK及下游p-mTOR/mTOR蛋白表达水平变化，通过荧光实时定量PCR（quantitative real-time PCR，qPCR）在基因水平上验证AMPK及下游mTOR的表达水平。

结果

小檗碱能够明显抑制EC9706细胞增殖（P<0.01），促进EC9706细胞凋亡（P<0.05），与对照组相比，小檗碱加药组G0/G1期明显降低（P<0.05），S期占比明显升高（P<0.01）。小檗碱能够抑制EC9706细胞的糖酵解潜能及线粒体呼吸能力（P<0.01）且具有浓度依赖性。小檗碱能够促进p-AMPK/AMPK（P<0.01）并抑制p-mTOR/mTOR蛋白表达（P<0.05）。在基因水平上，小檗碱促进了AMPK表达（P<0.05），同时促进了mTOR的表达（P<0.01）。

结论

小檗碱可以通过能量代谢途径抑制食管癌EC9706细胞的增殖，促进食管癌细胞凋亡并阻碍其分裂。

, authors=刘洋, 陈星, 周哲旭, 刘娅茹, 胡啸博, 陈玉龙, authorsList=刘洋, 陈星, 周哲旭, 刘娅茹, 胡啸博, 陈玉龙, authorCompany=null, correspAuthors=陈玉龙, authorNote=

刘洋（1993-），女，河南洛阳人，博士在读，研究方向：肿瘤中医方证。

, correspAuthorsNote=
陈玉龙（1973-），男，河南平舆人，教授，博士研究生导师，博士，研究方向：肿瘤中医方证。E-mail：。
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刘洋（1993-），女，河南洛阳人，博士在读，研究方向：肿瘤中医方证。

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刘洋（1993-），女，河南洛阳人，博士在读，研究方向：肿瘤中医方证。

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注：A对照组；B小檗碱低浓度组；C小檗碱高浓度组。

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注：A对照组；B小檗碱低浓度组；C小檗碱高浓度组。

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注：A对照组；B小檗碱低浓度组；C小檗碱高浓度组。

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引物序列（5'-3'）长度/（bp）
AMPKF：TTGAAACCTGAAAATGTCCTGCT113
R：GGTGAGCCACAACTTGTTCTT
mTORF：TCCGAGAGATGAGTCAAGAGG141
R：CACCTTCCACTCCTATGAGGC
β-actinF：ATTGCCGACAGGATGCAGAA150
R：GCTGATCCACATCTGCTGGAA
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引物序列

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引物序列（5'-3'）长度/（bp）
AMPKF：TTGAAACCTGAAAATGTCCTGCT113
R：GGTGAGCCACAACTTGTTCTT
mTORF：TCCGAGAGATGAGTCAAGAGG141
R：CACCTTCCACTCCTATGAGGC
β-actinF：ATTGCCGACAGGATGCAGAA150
R：GCTGATCCACATCTGCTGGAA
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组别n浓度/（μg·mL-1）抑制率/（%）
对照组300
小檗碱加药组312.527.70±6.76**
32550.25±9.02**
35061.98±2.40**
37569.87±0.84**
310076.85±2.14**
315095.47±4.21**
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小檗碱对EC9706细胞活性的影响（±s）

, figureFileSmall=null, figureFileBig=null, tableContent=
组别n浓度/（μg·mL-1）抑制率/（%）
对照组300
小檗碱加药组312.527.70±6.76**
32550.25±9.02**
35061.98±2.40**
37569.87±0.84**
310076.85±2.14**
315095.47±4.21**
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组别n浓度/（μg·mL-1）凋亡率/（%）
对照组3-4.46±0.57
小檗碱低浓度组31511.91±1.95*
小檗碱高浓度组33018.38±2.76*△
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小檗碱对EC9706细胞凋亡的影响（±s）

, figureFileSmall=null, figureFileBig=null, tableContent=
组别n浓度/（μg·mL-1）凋亡率/（%）
对照组3-4.46±0.57
小檗碱低浓度组31511.91±1.95*
小檗碱高浓度组33018.38±2.76*△
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组别n占比/（%）
G0/G1期S期G2/M期
对照组365.26±4.5818.93±0.3315.81±4.69
小檗碱低浓度组358.86±1.6630.84±3.66**10.30±3.12
小檗碱高浓度组354.57±4.34*28.27±2.59*17.16±6.87
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小檗碱对EC9706细胞周期的影响（±s）

, figureFileSmall=null, figureFileBig=null, tableContent=
组别n占比/（%）
G0/G1期S期G2/M期
对照组365.26±4.5818.93±0.3315.81±4.69
小檗碱低浓度组358.86±1.6630.84±3.66**10.30±3.12
小檗碱高浓度组354.57±4.34*28.27±2.59*17.16±6.87
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组别n浓度/（μg·mL-1）基础糖酵解/（pmol·min-1）代偿性糖酵解/（pmol·min-1）线粒体代谢率与基础糖酵解比值/（%）糖酵解潜能/（pmol·min-1）
对照组3-1 045.67±73.141 342.08±77.530.080±0.010209.65±7.87
小檗碱低浓度组315977.79±31.131 041.05±40.68**0.010±0.002**51.21±11.54**
小檗碱高浓度组330496.30±70.79**△△511.39±78.99**△△0.006±0.002**△△11.90±8.54**△△
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小檗碱对EC9706细胞糖酵解的影响（±s）

, figureFileSmall=null, figureFileBig=null, tableContent=
组别n浓度/（μg·mL-1）基础糖酵解/（pmol·min-1）代偿性糖酵解/（pmol·min-1）线粒体代谢率与基础糖酵解比值/（%）糖酵解潜能/（pmol·min-1）
对照组3-1 045.67±73.141 342.08±77.530.080±0.010209.65±7.87
小檗碱低浓度组315977.79±31.131 041.05±40.68**0.010±0.002**51.21±11.54**
小檗碱高浓度组330496.30±70.79**△△511.39±78.99**△△0.006±0.002**△△11.90±8.54**△△
), ArticleFig(id=1322912523980243067, tenantId=1146029695717560320, journalId=1255847919539208197, articleId=1322912279179698605, language=EN, label=null, caption=null, figureFileSmall=null, figureFileBig=null, tableContent=
组别n浓度/（μg·mL-1）非线粒体耗氧基础呼吸备用呼吸能力最大耗氧量ATP合成耗氧量
对照组3-315.29±10.68137.08±10.9432.25±6.05169.33±14.3618.31±3.39
小檗碱低浓度组315130.27±1.15**21.58±4.24**13.43±1.95**35.00±6.12**0.74±0.68**
小檗碱高浓度组33037.83±19.07**△4.79±2.09**△0.70±0.39**△5.49±2.21**△1.30±0.72**△
), ArticleFig(id=1322912524055740540, tenantId=1146029695717560320, journalId=1255847919539208197, articleId=1322912279179698605, language=CN, label=表6, caption=

小檗碱对EC9706细胞线粒体压力的影响（±s）

, figureFileSmall=null, figureFileBig=null, tableContent=
组别n浓度/（μg·mL-1）非线粒体耗氧基础呼吸备用呼吸能力最大耗氧量ATP合成耗氧量
对照组3-315.29±10.68137.08±10.9432.25±6.05169.33±14.3618.31±3.39
小檗碱低浓度组315130.27±1.15**21.58±4.24**13.43±1.95**35.00±6.12**0.74±0.68**
小檗碱高浓度组33037.83±19.07**△4.79±2.09**△0.70±0.39**△5.49±2.21**△1.30±0.72**△
), ArticleFig(id=1322912524148015229, tenantId=1146029695717560320, journalId=1255847919539208197, articleId=1322912279179698605, language=EN, label=null, caption=null, figureFileSmall=null, figureFileBig=null, tableContent=
组别n浓度/（μg·mL-1）p-AMPKAMPKp-mTORmTOR
对照组3-1111
小檗碱低浓度组3152.37±0.60**2.33±0.65**0.640±0.13*0.85±0.08
小檗碱高浓度组3302.34±0.40**2.35±0.39**0.666±0.18*0.44±0.22**
), ArticleFig(id=1322912524248678526, tenantId=1146029695717560320, journalId=1255847919539208197, articleId=1322912279179698605, language=CN, label=表7, caption=

小檗碱对EC9706细胞p-AMPK、AMPK、p-mTOR、mTOR蛋白表达的影响（±s）

, figureFileSmall=null, figureFileBig=null, tableContent=
组别n浓度/（μg·mL-1）p-AMPKAMPKp-mTORmTOR
对照组3-1111
小檗碱低浓度组3152.37±0.60**2.33±0.65**0.640±0.13*0.85±0.08
小檗碱高浓度组3302.34±0.40**2.35±0.39**0.666±0.18*0.44±0.22**
), ArticleFig(id=1322912524353536127, tenantId=1146029695717560320, journalId=1255847919539208197, articleId=1322912279179698605, language=EN, label=null, caption=null, figureFileSmall=null, figureFileBig=null, tableContent=
组别n浓度/（μg·mL-1）AMPKmTOR
对照组3-11
小檗碱低浓度组3151.19±0.085.48±0.89*
小檗碱高浓度组3301.76±0.14*7.61±1.43**
), ArticleFig(id=1322912524445810816, tenantId=1146029695717560320, journalId=1255847919539208197, articleId=1322912279179698605, language=CN, label=表8, caption=

小檗碱对EC9706细胞AMPK、mTOR基因表达的影响（±s）

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组别n浓度/（μg·mL-1）AMPKmTOR
对照组3-11
小檗碱低浓度组3151.19±0.085.48±0.89*
小檗碱高浓度组3301.76±0.14*7.61±1.43**
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小檗碱基于AMPK/mTOR通路对EC9706细胞能量代谢的影响
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刘洋 , 陈星 , 周哲旭 , 刘娅茹 , 胡啸博 , 陈玉龙
中华中医药学刊 | 国家项目点击 2025,43(1): 97-101
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中华中医药学刊 |国家项目点击 2025 , 43 (1) : 97 -101
小檗碱基于AMPK/mTOR通路对EC9706细胞能量代谢的影响
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刘洋, 陈星, 周哲旭, 刘娅茹, 胡啸博, 陈玉龙
作者信息
  • 河南中医药大学河南省方证信号传导重点实验室，河南　郑州　450046
通讯作者:
陈玉龙（1973-），男，河南平舆人，教授，博士研究生导师，博士，研究方向：肿瘤中医方证。E-mail：。
作者简介:

刘洋（1993-），女，河南洛阳人，博士在读，研究方向：肿瘤中医方证。

Effect of Berberine on Energy Metabolism in EC9706 Cells Based on AMPK/mTOR Pathway
Yang LIU, Xing CHEN, Zhexu ZHOU, Yaru LIU, Xiaobo HU, Yulong CHEN
Affiliations
  • Henan Key Laboratory of Signal Transduction, Henan University of Chinese Medicine, Zhengzhou 450046, Henan, China
出版时间: 2025-01-10 doi: 10.13193/j.issn.1673-7717.2025.01.018
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摘要
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目的

通过观察小檗碱对EC9706细胞能量代谢及相关通路的影响从而探究其机制。

方法

常规培养细胞，MTT法筛药，选择15、30 μg/mL两个质量浓度，通过流式细胞术检测细胞周期、凋亡水平，能量代谢分析系统检测细胞糖酵解潜能及线粒体呼吸能力，蛋白质印迹实验探究细胞中p-AMPK/AMPK及下游p-mTOR/mTOR蛋白表达水平变化，通过荧光实时定量PCR（quantitative real-time PCR，qPCR）在基因水平上验证AMPK及下游mTOR的表达水平。

结果

小檗碱能够明显抑制EC9706细胞增殖（P<0.01），促进EC9706细胞凋亡（P<0.05），与对照组相比，小檗碱加药组G0/G1期明显降低（P<0.05），S期占比明显升高（P<0.01）。小檗碱能够抑制EC9706细胞的糖酵解潜能及线粒体呼吸能力（P<0.01）且具有浓度依赖性。小檗碱能够促进p-AMPK/AMPK（P<0.01）并抑制p-mTOR/mTOR蛋白表达（P<0.05）。在基因水平上，小檗碱促进了AMPK表达（P<0.05），同时促进了mTOR的表达（P<0.01）。

结论

小檗碱可以通过能量代谢途径抑制食管癌EC9706细胞的增殖，促进食管癌细胞凋亡并阻碍其分裂。

小檗碱  /  能量代谢  /  AMPK/mTOR通路  /  增殖  /  周期  /  凋亡
Objective

To investigate the mechanism of berberine on energy metabolism and related pathways in EC9706 cells.

Method

The cellswere routinely cultured，MTT screened，and two mass concentrations of 15 μg/mL and 30 μg/mL were selected. The cell cycle and apoptosis were detected by flow cytometry，the glycolytic potential and mitochondrial respiratory capacity were detected by energy metabolism analysis system，and the changes in the expression of phosphorylated adenylate activated protein kinase（p-AMPK）/adenylate activated protein kinase（AMPK）and the downstream phosphor ylated mammalian target of rapamyc in（p-mTOR）/mammalian target of rapamycin（mTOR）proteins were explored by Western Blotting. The expression levels of AMPK and downstream mTOR were verified at the gene level by quantitative real-time PCR（qPCR）.

Results

Berberine significantly inhibited the proliferation of EC9706 cells（P<0.01）and promoted the apoptosis of EC9706 cells（P<0.05）. Compared with the control group，berberine and drug group showed a significant decrease in the G0/G1 phase（P<0.05），and a significant increase in the proportion of Sphase（P<0.01）. Berberine inhibited the glycolytic potentia and mitochondrial respiration of EC9706 cells（P<0.01）in a concentration-dependent manner，and berberine promoted p-AMPK/AMPK（P<0.01）and inhibited the expression of p-mTOR/mTOR protein（P<0.05）. At the gene level，berberine promoted AMPK expression（P<0.05）as well asmTOR expression（P<0.01）.

Conclusion

Berberine can inhibit the proliferation of oesophageal cancer EC9706 cells through energy metabolic pathway，promote apoptosis of oesophageal cancer cells and hinder their division.

berberine  /  energy metabolism  /  AMPK/mTOR pathway  /  proliferation  /  cycle  /  apoptosis
刘洋, 陈星, 周哲旭, 刘娅茹, 胡啸博, 陈玉龙. 小檗碱基于AMPK/mTOR通路对EC9706细胞能量代谢的影响. 中华中医药学刊, 2025 , 43 (1) : 97 -101 . DOI: 10.13193/j.issn.1673-7717.2025.01.018
Yang LIU, Xing CHEN, Zhexu ZHOU, Yaru LIU, Xiaobo HU, Yulong CHEN. Effect of Berberine on Energy Metabolism in EC9706 Cells Based on AMPK/mTOR Pathway[J]. Chinese Archives of Traditional Chinese Medicine, 2025 , 43 (1) : 97 -101 . DOI: 10.13193/j.issn.1673-7717.2025.01.018
正文
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食管癌世界范围内居癌症发病第8位，是中国地区高发肿瘤之一，2020年中国新增食管癌死亡病例人数占全球死亡病例的50%以上，在中国发病率存在明显地区差异及性别差异[1]。发病主要以鳞癌为主[2]，中国中北部为世界范围内食管鳞癌高发地区之一[3]，近年来中国对食管鳞癌的研究进展产生了较大影响[4-5]。
食管癌中医的病因病机与痰、气、瘀、热相关[6]，从经典验方到单味中药再到有效成分的研究都有一定的理论临床基础，亟待长足发展。
小檗碱作为一种广泛使用的生物活性剂已证实了对肿瘤的抑制作用[7]，在微观水平对肿瘤细胞的研究有了明确进展。已证实小檗碱能够诱导肿瘤细胞凋亡、促进细胞周期停滞、触发或者抑制细胞自噬[8]。能量代谢作为肿瘤相关热点方向被广泛研究[9]，与食管癌患者生存预后及临床疗效具有显著相关性，有良好的临床应用前景[10]。本实验从细胞水平证明了小檗碱对食管癌EC9706细胞周期、凋亡、能量代谢及相关通路的影响。
1　材料
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1.1　细胞
人食管鳞癌EC9706细胞由河南中医药大学分子生物实验中心提供。
1.2　药品与试剂
小檗碱购于成都乐天美医药有限公司，批号：DSTDY002801；二甲双胍，Sigma，批号：STBB0847V；兔单克隆抗体P-AMPK，CST，货号：D4D6D；兔单克隆抗体AMPK，CST，货号：D63G4；兔单克隆抗体P-mTOR，CST，货号：D9C2；兔单克隆抗体mTOR，CST，货号：7C10；兔单克隆抗体β-Actin，CST，货号：13E5；XF糖酵解测定试剂盒，Seahorse，批号：16671064；XF线粒体压力测试试剂盒，Seahorse，批号：16814026；水化液，Agilent，货号：100840-100；基础检测培养基，批号：23217002；葡萄糖，批号：SLBW5196；L-谷氨酰胺，批号：1917006；丙酮酸钠，批号：SL-BX1167；Annexin V FITC/PIApoptosis凋亡试剂盒，联科生物，批号：A20455；Cell Cycle Staining Kit细胞周期检测试剂盒，联科生物，批号：A21132，反转录试剂盒，日本TOYOBO，批号：FSQ-101，2×Universal SYBR green，ABclonal，批号962103G1433，TRIZOL，Ambion，批号：257407。
1.3　仪器
CO2培养箱，德国Eppendorf；超净工作台，苏净集团安泰；荧光倒置显微镜，德国Laica；低速离心机，美国Thermo；高速台式离心机，德国Eppendorf；酶标仪，美国BIO-TE；FACS Vantage SE型流式细胞仪，美国BD；XFe96能量代谢分析系统，美国安捷伦；垂直电泳槽、垂直湿转膜槽、凝胶成像扫描仪，美国Bio-Rad；QuantStudio 6型实时荧光定量PCR仪，美国ThermoFisher。
2　方法
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2.1　细胞培养
用含10%胎牛血清的DMEM高糖培养基培养EC9706细胞，置于5% CO2、37℃饱和湿度的培养箱中常规培养，48 h换液，2～3 d传代1次。
2.2　药物制备
用二甲基亚砜（dimethyl sulfoxide，DMSO）将小檗碱单体配制成质量浓度为40 mg·mL-1的药物悬液。用DMEM将二甲双胍配置成1 mol·L-1母液。
2.3　MTT法检测小檗碱对EC9706细胞增殖的影响
取对数生长期EC9706细胞，在96孔板中加入每孔200 μL、1×104个细胞的细胞悬液。24 h后分别加入200 μL一定浓度（0、12.5、25、50、75、100、150 μg·mL-1）的小檗碱溶液，于CO2培养箱中37℃孵育48 h后MTT法，酶标仪检测490 nm吸收光值（OD值），计算各组细胞抑制率进行统计学分析。
抑制率：抑制率（%）＝（对照组OD值-给药组OD值）/对照组OD值×100%。
2.4　流式细胞术检测小檗碱对EC9706细胞凋亡的影响
取对数生长期EC9706细胞以每孔3×105的密度接种于6孔板中，于CO2培养箱中培养24 h后弃上清，分别加入含浓度为15、30 μg·mL-1小檗碱的完培，继续培养48 h，使用不含EDTA的胰酶消化收集细胞，200 μL血清终止消化，预冷的PBS洗涤2次。使用500 μL 1×Binding Buffer重悬细胞，加入5 μL An-nexin V-FITC及10 μL PI染色，混匀后避光室温孵育10 min后流式细胞仪检测细胞凋亡。
2.5　流式细胞术检测小檗碱对EC9706细胞周期的影响
细胞培养同2.4，收集上清，使用不含EDTA的胰酶消化收集细胞，200 μL血清终止消化，常规离心细胞，预冷的PBS洗2次。加入1 mL DNA Staining Solution和10 μL Permeabilization Solution，涡旋振荡5～10 s混匀。室温避光孵育30 min后流式细胞仪检测细胞周期。
2.6　XFe 96能量代谢分析系统检测小檗碱及二甲双胍对EC9706细胞糖酵解和线粒体呼吸能力的影响
取对数生长期EC9706细胞以每孔80 μL，8×104个细胞的密度接种于SeahorseXF96细胞培养板中，于CO2培养箱中培养24 h后分别加入含有浓度为15 μg·mL-1和30 μg·mL-1小檗碱的完培，于37℃CO2培养箱中培养48 h后在能量代谢分析系统检测细胞糖酵解能力和线粒体呼吸能力。上机前一天水化探针，放入37℃恒温培养箱中，上机前2 h，换水化液入探针板中，放入37℃恒温培养箱备用，上机前1 h将细胞培养板用检测培养基清洗两次，分别配置检测糖酵解速率和线粒体压力试剂盒中包含的药品，按次序加入探针板微孔中，上机检测细胞糖酵解潜能以及备用呼吸能力。
2.7　蛋白免疫印迹法检测小檗碱对EC9706细胞P-AMPK、AMPK、P-mTOR、mTOR表达的影响
取对数生长期EC9706细胞以每孔3×105的密度接种于6孔板中，于CO2培养箱中培养24 h后，加入含浓度为15、30 μg·mL-1小檗碱、20 mmol·L-1二甲双胍的完培，48 h后置于冰上加入RIPA裂解液提取细胞总蛋白，将样本进行十二烷基硫酸钠-聚丙烯酰胺凝胶电泳（SDS-PAGE），转模，封闭，分别加入一抗，P-AMPK（1∶1000）、AMPK（1∶1000）、P-mTOR（1∶1000）、mTOR（1∶1000）、β-actin（1∶1000）洗膜后加入对应二抗稀释液（1∶10 000），凝胶成像系统显影，应用Image J软件分析图像灰度值。
2.8　实时荧光定量PCR（quantitative real-time PCR，qRT-PCR）法检测小檗碱对EC9706细胞AMPK、mTOR表达水平的影响
细胞培养同2.4，TRIzol法提取各组样本总RNA，根据反转录试剂盒操作步骤将RNA反转录为cDNA，每组样本每个待测基因设3个附孔，按照universal SYBR green fast qPCR Mix试剂说明书，设定95℃ 3 min，95℃ 5 s，60℃ 30 s，为1个循环，共40个循环，通过2-ΔΔCt分析相对表达定量对各基因进行检测，引物序列见表1，由苏州金唯智生物科技有限公司合成。
2.9　统计学方法
采用SPSS 24.0进行数据分析，若数据符合正态分布及方差齐性，采用单因素方差分析，组间比较用LSD检验，结果以±s进行描述统计。若符合正态分布但方差不齐，用Dunnett T3检验。若不符合正态分布，用非参数检验。P<0.05表示数据有统计学意义。
3　结果
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3.1　小檗碱对EC9706细胞活性的影响
MTT法检测，通过SPSS 24.0对数据进行统计学分析，与对照组相比，小檗碱加药组对EC9706增殖有明显的抑制作用（P<0.01），且随浓度增高抑制率上升。取IC30 15 μg·mL-1、IC50 30 μg·mL-1进行后续试验。见表2。
3.2　流式细胞仪检测小檗碱对EC9706细胞凋亡的影响
与对照组比较，小檗碱加药组明显诱导了细胞凋亡（P<0.05），15 μg·mL-1与30 μg·mL-1浓度的小檗碱对细胞凋亡的影响差异有统计学意义（P<0.05）。见表3、插页Ⅻ图1。
3.3　流式细胞仪检测小檗碱对EC9706细胞周期的影响
与对照组比较，小檗碱加药组G0/G1（P<0.05）以及S期细胞明显增加（P<0.01），小檗碱不同浓度之间差异无统计学意义（P>0.05）。见表4、插页Ⅻ图2。
3.4　小檗碱对EC9706细胞能量代谢的影响
3.4.1　小檗碱对EC9706细胞糖酵解速率的影响
与对照组相比，小檗碱15 μg·mL-1与30 μg·mL-1浓度组的基础糖酵解、代偿糖酵解、线粒体代谢率与基础糖酵解比值、糖酵解潜能均降低（P<0.01），小檗碱不同浓度给药组在代偿糖酵解能力上差异存在显著统计学意义（P<0.01）。见表5、插页Ⅻ图3。
3.4.2　小檗碱对EC9706细胞线粒体压力的影响
与对照组相比，小檗碱15 μg·mL-1与30 μg·mL-1浓度组的非线粒体耗氧、基础呼吸、备用呼吸能力、最大耗氧量、ATP合成耗氧量均降低（P<0.01），且小檗碱不同浓度给药组之间差异存在统计学意义（P<0.05）。见表6、插页ⅩⅢ图4。
3.5　小檗碱对EC9706细胞mTOR、p-mTOR、AMPK、p-AMPK蛋白表达的影响
与对照组比较，小檗碱低、高浓度组AMPK、p-AMPK蛋白表达水平显著升高，mTOR、p-mTOR、表达水平降低。见表7、图5。
3.6　小檗碱对EC9706细胞AMPK、mTOR基因表达的影响
与对照组比较，小檗碱加药组AMPK及mTOR基因表达均显著增高。见表8。
4　讨论
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噎膈为“风、痨、鼓、膈”四大顽疾之一，最早见于《素问·至真要大论篇》曰：“食饮不下，鬲咽不通”，《素问·评热病论篇》，描述其症状表现为“食不下”，其辨证分型不乏阴津液亏虚，夹燥夹火，阴阳失调之象[11]。对噎膈的认识从病因病机到理法方药发展出了完整的辨证治疗体系。小檗碱为黄连主要成分，黄连是泻心汤重要药物组成，为历代医家治疗噎膈的常用方剂[12-14]，常为半夏黄连合用，寒热并用，共奏辛开苦降之功，多见于痰热、热痞等证型，与行气药同用可恢复脾胃气机升降。
小檗碱作为抗肿瘤有效生物成分，在动物模型以及细胞实验中得到了充分证实[15]。有研究表明小檗碱可能通过调节细胞周期和细胞自噬，促进细胞凋亡来抑制细胞增殖[16]。通过抑制上皮细胞-间充质转化（epithelial-mesenchymal transition，EMT），影响细胞迁移通路相关蛋白的表达来抑制肿瘤细胞的迁移和侵袭。此外，随着miRNA的研究不断深入，发现小檗碱通过与其相互作用能够抑制肿瘤细胞端粒酶活性从而抑制肿瘤细胞增殖[17]。
本实验选取EC9706细胞探究小檗碱对食管癌的影响，通过MTT法发现小檗碱对EC9706细胞增殖有抑制作用，设置浓度梯度证实了其有明确的剂量依赖性，其差异存在统计学意义，说明小檗碱是EC9706细胞生长的有效抑制剂。与对照组相比，小檗碱15、30 μg·mL浓度细胞凋亡率明显高于对照组，表明小檗碱可促进细胞凋亡，且随着药物浓度增加，细胞凋亡率增高，凋亡是肿瘤细胞死亡的主要机制，与对照组比较，小檗碱能够促进食管癌EC9706细胞凋亡，效果呈浓度依赖性，差异具有统计学意义。
癌症是一组细胞持续过度分裂的疾病[18]。传统认为癌细胞的周期相关位点发生了突变使得其不受细胞周期进程的控制，通过干扰细胞周期控制的癌症相关突变，使其持续在细胞周期中循环，模拟了癌细胞的旺盛分裂。然而近期研究发现，癌细胞退出周期进程的相关基因损害导致了其持续不断地分裂。深入研究肿瘤细胞周期具有广泛的临床前景。有研究表明细胞周期调节与细胞的合成代谢和分解代谢相关，对CDK相关的周期蛋白及抑制蛋白的研究证实了细胞周期调节因子可以控制维持细胞存活所需的代谢修饰，参与细胞周期相关分子和糖酵解、氧化磷酸化、线粒体调控之间的多重联系[19-20]。与常规培养的EC9706相比，小檗碱加药组S期细胞比例增高，G0/G1期细胞比例降低，且差异具有统计学意义，说明细胞分裂阻滞在S期，小檗碱通过抑制EC9706细胞周期从而抑制细胞增殖。通过流式细胞术检测细胞凋亡，发现小檗碱能够通过诱导细胞凋亡抑制细胞增殖，且具有浓度依赖性，证实小檗碱能够抑制食管癌EC9706细胞分裂、促进其凋亡。
我们采用了Seahorse能量代谢分析仪器验证了小檗碱对EC9706细胞能量代谢的影响，加入相关试剂后检测细胞耗氧率（O2 consumption rate，OCR）和胞外酸化率（extracellular acidification rate，ECAR）来表征细胞能量代谢。OCR研究线粒体氧化磷酸化功能时先测定正常状态下的基础呼吸，通过加入寡霉素抑制ATP合成酶，OCR显著下降，仅余下质子渗漏造成的耗氧率。降低部分即为氧化磷酸化的耗氧率。加入解偶联剂线粒体氧化磷酸化特异性抑制剂羰基氰-对-三氟甲氧基苯腙（carbonyl cyanide-p-trifluoromethoxyphenylhydrazone，FCCP）后，电子传递失去质子梯度的约束，以最大速率进行。所以OCR急剧升高，达到最大耗氧量。此值与基础呼吸之差，称为呼吸潜力。最后加入电子传递抑制剂鱼藤酮和抗霉素A混合物完全抑制电子传递，耗氧率降至最低。细胞的糖酵解潜能是先通过细胞耗氧量计算二氧化碳产出，除去线粒体酸化对细胞pH值的影响，计算出细胞糖酵解速率。加入寡霉素后，线粒体呼吸被抑制，完全采用乳酸发酵供能，产酸增加，细胞达到糖酵解最大容量，与基础糖酵解以及线粒体氧化磷酸化之差代表了细胞的酵解能力。最后加入2-脱氧-D-葡萄糖（2-deoxy-D-glucose，2-DG），作为己糖激酶的竞争性抑制剂阻断糖酵解，曲线回归基础值。同时测定小檗碱给药组对于细胞的糖酵解潜能以及线粒体呼吸效率均有明显抑制作用，且具有明显的浓度依赖性。肿瘤细胞通过有氧糖酵解为其供能，促癌信号加速了细胞的糖酵解活动，肿瘤细胞的糖酵解能力一定程度上反映了细胞的恶性程度[21]。有研究表明，通过回顾生物信息线粒体相关研究的最新进展，发现线粒体核糖体控制的氧化磷酸化相关蛋白与癌症患者预后密切相关，或能作为潜在的肿瘤标志物[22]。
AMPK是细胞能量代谢相关的核心分子，当细胞的ATP水平下降、ADP以及AMP水平上升时，细胞内的AMPK被激活促进ATP的产生，同时抑制其消耗，维持了细胞内能量代谢的平衡。AMPK激活是通过它的α亚基上的T172位点发生磷酸化介导的。这种发生磷酸化的AMPK被称作p-AMPK。AMPK能够促进葡萄糖的摄取和利用，促进脂肪酸的氧化代谢，以及体内多种蛋白质的降解，当细胞内能量代谢水平下降时，被激活的AMPK通过上述途径促进能量的生成，抑制其降解从而维持能量平衡。除了AMPK的经典途径，最近研究中发现了包括AMPK感知葡萄糖、糖原或脂肪酸可用性的途径以及可以感知溶酶体和核DNA的损伤[23]。AMPK下游mTOR与AMPK同为细胞能量代谢的核心分子，mTOR信号转导异常与代谢紊乱有关[24]，mTOR参与了细胞增殖、代谢调节、生长、增殖、分化等多种过程，氨基酸、脂肪酸、脂质、核苷酸以及葡萄糖的代谢均受mTOR调节[25]。mTOR的活性主要由mTORC1和mTORC2两个复合物调节，其活性受到多种信号因子的影响，包括氧浓度、细胞营养状态以及细胞应激反应等。当细胞中ATP产生降低的时候，会激活能量响应调节子AMPK，AMPK可以磷酸化并激活复合物TSC从而间接抑制mTORC1。同时AMPK也可以直接磷酸化mTORC1的Raptor来直接抑制mTORC1，相反的是，mTORC1直接磷酸化AMPK的催化亚基a1或a2，减少AMPK活化环中的Thr172磷酸化，限制AMPK活性，AMPK和mTORC1是相互拮抗的[26]。小檗碱能够抑制细胞的能量代谢，使AMPK过表达且激活其磷酸化位点高表达p-AMPK，从而抑制下游mTOR分子及其磷酸化，减少细胞的能量消耗[27]。然而，PCR结果显示AMPK以及下游mTOR mRNA表达量均增高，或由于上游AMPK mRNA及蛋白过表达后导致下游mTOR蛋白及其磷酸化蛋白表达量降低，从而导致mTOR mRNA产生了负反馈调节。
综上所述，小檗碱能够抑制EC9706细胞的增殖，诱导细胞凋亡，将细胞周期阻滞于S期，并且抑制细胞的能量代谢，作用呈现浓度依赖性，小檗碱可以通过AMPK/mTOR途径抑制肿瘤细胞，具体分子机制有待进一步研究。
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2025年第43卷第1期
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doi: 10.13193/j.issn.1673-7717.2025.01.018
  • 首发时间：2026-10-30
  • 出版时间：2025-01-10
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国家自然科学基金面上项目(81873285; 82074313; 82274438)
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    河南中医药大学河南省方证信号传导重点实验室，河南　郑州　450046

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陈玉龙（1973-），男，河南平舆人，教授，博士研究生导师，博士，研究方向：肿瘤中医方证。E-mail：。
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