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Article(id=1322923362036625462, tenantId=1146029695717560320, journalId=1255847919539208197, issueId=1322923268038078806, articleNumber=null, orderNo=null, doi=10.13193/j.issn.1673-7717.2025.04.021, 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=1793339108237, onlineDateStr=2026-10-30, pubDate=1744214400000, pubDateStr=2025-04-10, doiRegisterDate=null, doiRegisterDateStr=null, onlineIssueDate=1793339108237, onlineIssueDateStr=2026-10-30, onlineJustAcceptDate=null, onlineJustAcceptDateStr=null, onlineFirstDate=null, onlineFirstDateStr=null, sourceXml=null, magXml=null, createTime=1793339108237, creator=13701087609, updateTime=1793339108237, updator=13701087609, issue=Issue{id=1322923268038078806, tenantId=1146029695717560320, journalId=1255847919539208197, year='2025', volume='43', issue='4', pageStart='1', pageEnd='258', issueExtLink='null', onlineDate='null', pubDate='1744214400000', pubDateStr='2025-04-10', beforeIssueId=null, nextIssueId=null, price=null, status=1, issueComplete=1, articleOrder=1, issueType=-1, specialIssue=0, createTime=1793339085826, creator='13701087609', updateTime=1793340586453, updator='13701087609', preIssue=null, nextIssue=null, articleTotal=null, ext={EN=IssueExt(id=1322929562572686061, tenantId=1146029695717560320, journalId=1255847919539208197, issueId=1322923268038078806, language=EN, specialIssueTitle=, coverIllustrator=null, specialIssueEditor=, specialIssueAbout=), CN=IssueExt(id=1322929562572686062, tenantId=1146029695717560320, journalId=1255847919539208197, issueId=1322923268038078806, language=CN, specialIssueTitle=, coverIllustrator=null, specialIssueEditor=, specialIssueAbout=)}, issueFiles=null, downloadFileDto=null}, startPage=133, endPage=139, ext={EN=ArticleExt(id=1322923362263117879, articleId=1322923362036625462, tenantId=1146029695717560320, journalId=1255847919539208197, language=EN, title=Mechanism of Ethyl Acetate Extract of Liujunzi Decoction（六君子汤）Regulating Energy Metabolism in Esophageal Cancer TE-1 Cells Based on miR-1/HIF-1α Axis, columnId=1256183361521967297, journalTitle=Chinese Archives of Traditional Chinese Medicine, columnName=Target on National Project, runingTitle=null, highlight=null, articleAbstract=
Objective

To explore whether ethyl acetate extract of Liujunzi Decoction（EAELD）can regulate the energy metabolism of TE-1 of esophageal cancer cells via the microRNA-1（miR-1）/hypoxia inducible factor-1α（HIF-1α）axis.

Methods

Stable transfection blocking miR-1 expression cell lines（miR-1 inhibitor，IN）and blank controls（miR-1 NC，NC）have been established in the preliminary experiments. The half maximal inhibitory concentration（IC50）and 30% inhibitory concentration（IC30）of EAELD on NC were obtained using MTT assay，and were used as the Liujunzi Decoction high and low concentrations to compare their effects on IN and NC，respectively. The effect of EAELD on miR-1 and HIF-1αmRNA in TE-1 cells was measured by quantitative real-time PCR（RT-qPCR）. Dual-luciferase gene reporter assay was used to validate the targeting relationship of miR-1 and HIF-1α. Then the experiments were divided into NC，Liujunzi Decoction low concentration，Liujunzi Decoction high concentration，IN＋Liujunzi Decoction low concentration and IN＋Liujunzi Decoction high concentration groups. Seahorse energy metabolism analysis system detected the mitochondrial pressure and glycolysis rate，and the protein expression level was detected by Western Blot.

Results

MTT results showed that EAELD could significantly inhibit the proliferation of NCin a concentration gradient dependent manner. The low and high concentration groups were 20 μg/mL（IC30）and 40 μg/mL（IC50），respectively. The RT-qPCR results showed that the EAELD high concentration group significantly promoted the gene expression of miR-1（P<0.05）and HIF-1αshowed a downward trend，without statistically significant difference. Dual-luciferase gene reporter assay showed that the fluorescence intensity of wild type（WT）＋mimics group was significantly lower than that of WT＋negative control（mimics NC）group（P<0.05），and there was no significant difference in the fluorescence intensity of mutant（MUT）＋mimics group compared with that of MUT＋mimics NCgroup. When high and low concentrations of EAELD were applied to IN，the MTT results showed that compared with that of NCgroup，the inhibitory effect of EAELD on IN group was significantly reduced（P<0.05）. Seahorse energy metabolism results showed that compared with those of NC group，the ratio of mitochondrial oxygen consumption to glycolysis（P<0.01，P<0.05），glycolytic potential（P<0.01），basal respiration value，proton leakage oxygen consumption（P<0.01，P<0.05），proton leakage oxygen consumption（P<0.01，P<0.05），mitochondrial maximum oxygen consumption capacity and spare respiratory capacity（P<0.01）were inhibited in the high and low concentration groups of Liujunzi Decoction. The high concentration group could inhibit basal glycolysis，compensate glycolysis，non-mitochondrial oxygen consumption and ATPsynthesis oxygen consumption（P<0.01）. Compared with those of NC＋Liujunzi Decoction low concentration group，basal glycolysis，mitochondrial to basal glycolysis ratio，glycolytic potential（P<0.05）and oxygen consumption for ATPsynthesis（P<0.01）were significantly increased in IN＋Liujunzi Decoction low concentration group. Compared with those of NC＋Liujunzi Decoction high concentration group，basal glycolysis，compensatory glycolysis（P<0.05），basal respiratory capacity，proton leakage oxygen consumption，maximum mitochondrial oxygen consumption and non-mitochondrial oxygen consumption（P<0.01）were significantly increased in IN＋Liujunzi Decoction high concentration group. WB results showed that compared with NCgroup，EAELD high and low concentration groups significantly decreased the protein relative expression levels of HK2（P<0.01），GLUT1（P<0.05，P<0.01）and MCT1（P<0.01，P<0.05）. The relative protein expressions of PKM2（P<0.05），MCT2 and MCT4（P<0.01）in the high concentration of EAELD group were significantly decreased. Compared with those of NC＋Liujunzi Decoction low concentration group，the expressions of HK2，GLUT1，PKM2（P<0.01），p-PKM2，MCT1 and MCT2（P<0.05）in IN＋Liujunzi Decoction low concentration group were significantly increased. Compared with those of NC＋Liujunzi Decoction high concentration group，the expressions of HK2，GLUT1，PKM2（P<0.01），p-PKM2，MCT1 and MCT2（P<0.05）in IN＋Liujunzi Decoction low concentration group were significantly increased. IN＋Liujunzi Decoction high concentration group could significantly promote the expressions of HK2，GLUT1，PKM2 and MCT4（P<0.05）.

Conclusion

EAELD can inhibit the energy metabolism of esophageal cancer cell line TE-1 by down-regulating the expressions of GLUT1，PKM2，p-PKM2，HK2，MCT1，MCT2 and MCT4，and the mechanism is partly related to miR-1/HIF-1αaxis.

, authors=Xing CHEN, Zhexu ZHOU, Yiwan SHANG, Yang LIU, Yaru LIU, Xiaobo HU, Jianing JIAN, Xiaoqiao XIAO, Yulong CHEN, authorsList=Xing CHEN, Zhexu ZHOU, Yiwan SHANG, Yang LIU, Yaru LIU, Xiaobo HU, Jianing JIAN, Xiaoqiao XIAO, 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=1322923367694741597, articleId=1322923362036625462, tenantId=1146029695717560320, journalId=1255847919539208197, language=CN, title=基于miR-1/HIF-1α轴研究六君子汤乙酸乙酯提取物调控食管癌细胞TE-1能量代谢的作用机制, columnId=1256183362172142382, journalTitle=中华中医药学刊, columnName=国家项目点击, runingTitle=null, highlight=null, articleAbstract=
目的

探索六君子汤乙酸乙酯提取物（EAELD）能否通过miR-1/HIF-1α轴调控食管癌细胞TE-1的能量代谢及其分子机制。

方法

前期实验已建立稳定转染阻滞miR-1表达细胞株（IN）及空白对照（NC），采用MTT法得到EAELD对NC的半数抑制浓度（IC50）及30%抑制浓度（IC30），将其作为六高、六低浓度分别作用于IN与NC进行对比。实时荧光定量PCR（RT-qPCR）法检测EAELD对于TE-1细胞miR-1、HIF-1αmRNA的影响。双荧光素酶基因报告实验验证miR-1、HIF-1α靶向关系。然后将实验分组为NC组、六低组、六高组、IN＋六低组、IN＋六高组，Seahorse能量代谢分析系统检测线粒体压力与糖酵解速率，蛋白免疫印迹法（WB）检测能量代谢相关分子蛋白表达水平变化。

结果

MTT结果显示EAELD能够显著抑制NC增殖能力，呈浓度梯度依赖，选取20 μg/mL（IC30）、40 μg/mL（IC50）为低、高浓度组。RT-qPCR结果显示EAELD高浓度组显著促进miR-1的基因表达（P<0.05），HIF-1α有下降趋势，差异无统计学意义。双荧光素酶基因报告实验显示与野生型（WT）＋阴性对照（mimics NC）组相比，WT＋mimics荧光强度明显下降（P<0.05），与突变型（MUT）＋阴性对照（mimics NC）组相比，MUT＋mimics荧光强度无明显差别。将高、低浓度EAELD作用于IN时，MTT结果显示与NC相比，EAELD对于IN的抑制作用显著降低（P<0.05）。Seahorse能量代谢结果显示与NC组相比，EAELD高、低浓度组均可以抑制线粒体耗氧与糖酵解的比值（P<0.01，P<0.05）、糖酵解潜能（P<0.01）、基础呼吸值、质子漏耗氧（P<0.01，P<0.05）、线粒体最大耗氧能力、备用呼吸能力（P<0.01），高浓度组可以抑制基础糖酵解、补偿糖酵解、非线粒体耗氧、ATP合成耗氧（P<0.01）。与NC＋六低组相比，IN＋六低组的基础糖酵解、线粒体与基础糖酵解的比值、糖酵解潜能（P<0.05）、ATP合成耗氧（P<0.01）显著升高；与NC＋六高组相比，IN＋六高基础糖酵解、补偿糖酵解（P<0.05）、基础呼吸能力、质子漏耗氧、线粒体最大耗氧量、非线粒体耗氧显著升高（P<0.01）。WB结果显示与NC相比，EAELD高、低浓度组可以显著降低HK2（P<0.01）、GLUT1（P<0.05、P<0.01）、MCT1（P<0.01、P<0.05）蛋白相对表达量，高浓度组可以显著抑制PKM2（P<0.05）、MCT2、MCT4（P<0.01）的蛋白相对表达量；与NC＋六低组相比，IN＋六低组HK2、GLUT1、PKM2（P<0.01）、p-PKM2、MCT1、MCT2（P<0.05）的表达明显升高，与NC＋六高组相比，IN＋六高组可以显著促进HK2、GLUT1、PKM2、MCT4的表达（P<0.05）。

结论

六君子汤乙酸乙酯提取物可以通过下调能量代谢相关分子GLUT1、PKM2、p-PKM2、HK2、MCT1、MCT2、MCT4的蛋白表达抑制食管癌细胞TE-1的能量代谢，其部分机制与miR-1/HIF-1α轴有关。

, authors=陈星, 周哲旭, 尚艺婉, 刘洋, 刘娅茹, 胡啸博, 菅佳宁, 肖小乔, 陈玉龙, authorsList=陈星, 周哲旭, 尚艺婉, 刘洋, 刘娅茹, 胡啸博, 菅佳宁, 肖小乔, 陈玉龙, authorCompany=null, correspAuthors=陈玉龙, authorNote=

陈星（1996-），女，河南新乡人，硕士在读，研究方向：肿瘤的病机与防治。

, correspAuthorsNote=
陈玉龙（1972-），男，河南平舆人，教授，博士研究生导师，博士，研究方向：中医药防治肿瘤。E-mail：。
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陈星（1996-），女，河南新乡人，硕士在读，研究方向：肿瘤的病机与防治。

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陈星（1996-），女，河南新乡人，硕士在读，研究方向：肿瘤的病机与防治。

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ArticleFig(id=1322923383419187373, tenantId=1146029695717560320, journalId=1255847919539208197, articleId=1322923362036625462, language=EN, label=null, caption=null, figureFileSmall=null, figureFileBig=null, tableContent=
基因序列5＇-3＇
miR-1-RTGTCGTATCCAGTGCAGGGTCCGAGGTATTCGCACTGGATACGACATACAT
miR-1-FAAGCGCCTTGGAATGTAAAGAA
miR-1-RGTCGTATCCAGTGCAGGGT
HIF-1α-FGAACGTCGAAAAGAAAAGTCTCG
HIF-1α-RCCTTATCAAGATGCGAACTCACA
β-actin-FATTGCCGACAGGATGCAGAA
β-actin-RGCTGATCCACATCTGCTGGAA
U6-FCTCGCTTCGGCAGCACA
U6-RAACGCTTCACGAATTTGCGT
), ArticleFig(id=1322923383486296238, tenantId=1146029695717560320, journalId=1255847919539208197, articleId=1322923362036625462, language=CN, label=表1, caption=

引物序列

, figureFileSmall=null, figureFileBig=null, tableContent=
基因序列5＇-3＇
miR-1-RTGTCGTATCCAGTGCAGGGTCCGAGGTATTCGCACTGGATACGACATACAT
miR-1-FAAGCGCCTTGGAATGTAAAGAA
miR-1-RGTCGTATCCAGTGCAGGGT
HIF-1α-FGAACGTCGAAAAGAAAAGTCTCG
HIF-1α-RCCTTATCAAGATGCGAACTCACA
β-actin-FATTGCCGACAGGATGCAGAA
β-actin-RGCTGATCCACATCTGCTGGAA
U6-FCTCGCTTCGGCAGCACA
U6-RAACGCTTCACGAATTTGCGT
), ArticleFig(id=1322923383557599407, tenantId=1146029695717560320, journalId=1255847919539208197, articleId=1322923362036625462, language=EN, label=null, caption=null, figureFileSmall=null, figureFileBig=null, tableContent=
名称序列5＇-3＇
miR-1-3p正义UGGAAUGUAAAGAAGUAUGUAU
反义ACAUACUUCUUUACAUUCCAUU
Negative Control正义UUCUCCGAACGUGUCACGUTT
反义ACGUGACACGUUCGGAGAATT
), ArticleFig(id=1322923383616319664, tenantId=1146029695717560320, journalId=1255847919539208197, articleId=1322923362036625462, language=CN, label=表2, caption=

转染质粒序列

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名称序列5＇-3＇
miR-1-3p正义UGGAAUGUAAAGAAGUAUGUAU
反义ACAUACUUCUUUACAUUCCAUU
Negative Control正义UUCUCCGAACGUGUCACGUTT
反义ACGUGACACGUUCGGAGAATT
), ArticleFig(id=1322923383670845617, tenantId=1146029695717560320, journalId=1255847919539208197, articleId=1322923362036625462, language=EN, label=null, caption=null, figureFileSmall=null, figureFileBig=null, tableContent=
组别nmiR-1HIF-1α
NC组311
六低组31.63±0.451.14±0.25
六高组32.81±0.41）0.85±0.06
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EAELD对TE-1细胞miR-1、HIF-1α mRNA的影响（±s）

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组别nmiR-1HIF-1α
NC组311
六低组31.63±0.451.14±0.25
六高组32.81±0.41）0.85±0.06
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浓度/（μg/mL）n抑制率/（%）
NCIN
20440.44±3.8123.46±5.221）
40443.45±5.4933.60±4.761）
), ArticleFig(id=1322923383905726644, tenantId=1146029695717560320, journalId=1255847919539208197, articleId=1322923362036625462, language=CN, label=表4, caption=

EAELD对于NC、IN细胞增殖的影响（±s）

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浓度/（μg/mL）n抑制率/（%）
NCIN
20440.44±3.8123.46±5.221）
40443.45±5.4933.60±4.761）
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组别n基础糖酵解/（pmol/min）线粒体耗氧与基础糖酵解比值补偿糖酵解/（pmol/min）糖酵解潜能/（pmol/min）
NC组4466.35±155.770.12±0.03684.48±140.7154.42±5.92
六低组4372.18±101.250.07±0.011）476.58±131.6527.27±9.572）
六高组4180.78±109.322）0.05±0.032）195.13±126.982）7.90±5.282）
), ArticleFig(id=1322923384044138678, tenantId=1146029695717560320, journalId=1255847919539208197, articleId=1322923362036625462, language=CN, label=表5, caption=

EAELD对食管癌TE-1细胞糖酵解速率的影响（±s）

, figureFileSmall=null, figureFileBig=null, tableContent=
组别n基础糖酵解/（pmol/min）线粒体耗氧与基础糖酵解比值补偿糖酵解/（pmol/min）糖酵解潜能/（pmol/min）
NC组4466.35±155.770.12±0.03684.48±140.7154.42±5.92
六低组4372.18±101.250.07±0.011）476.58±131.6527.27±9.572）
六高组4180.78±109.322）0.05±0.032）195.13±126.982）7.90±5.282）
), ArticleFig(id=1322923384128024759, tenantId=1146029695717560320, journalId=1255847919539208197, articleId=1322923362036625462, language=EN, label=null, caption=null, figureFileSmall=null, figureFileBig=null, tableContent=
组别n基础呼吸值质子漏耗氧线粒体最大耗氧能力备用呼吸能力非线粒体耗氧ATP合成耗氧
NC组469.16±13.7965.51±13.1089.70±16.6820.53±3.728.33±3.593.65±0.69
六低组439.33±16.841）37.72±16.211）49.93±20.642）10.60±4.302）16.41±3.381.60±0.65
六高组46.23±6.842）6.41±5.592）11.52±9.822）5.28±3.092）2.28±3.832）0.44±0.882）
), ArticleFig(id=1322923384199327928, tenantId=1146029695717560320, journalId=1255847919539208197, articleId=1322923362036625462, language=CN, label=表6, caption=

EAELD对食管癌TE-1细胞线粒体功能的影响（±s）

, figureFileSmall=null, figureFileBig=null, tableContent=
组别n基础呼吸值质子漏耗氧线粒体最大耗氧能力备用呼吸能力非线粒体耗氧ATP合成耗氧
NC组469.16±13.7965.51±13.1089.70±16.6820.53±3.728.33±3.593.65±0.69
六低组439.33±16.841）37.72±16.211）49.93±20.642）10.60±4.302）16.41±3.381.60±0.65
六高组46.23±6.842）6.41±5.592）11.52±9.822）5.28±3.092）2.28±3.832）0.44±0.882）
), ArticleFig(id=1322923384279019705, tenantId=1146029695717560320, journalId=1255847919539208197, articleId=1322923362036625462, language=EN, label=null, caption=null, figureFileSmall=null, figureFileBig=null, tableContent=
组别nHK2GLUT1PKM2p-PKM2MCT1MCT2MCT4
NC组30.93±0.100.54±0.030.96±0.050.57±0.050.68±0.070.63±0.020.39±0.03
六低组30.38±0.182）0.33±0.052）0.98±0.150.41±0.220.45±0.091）0.30±0.150.10±0.14
六高组30.13±0.052）0.38±0.101）0.75±0.081）0.47±0.020.21±0.122）0.32±0.022）0.14±0.032）
), ArticleFig(id=1322923384396460218, tenantId=1146029695717560320, journalId=1255847919539208197, articleId=1322923362036625462, language=CN, label=表7, caption=

EAELD对食管癌TE-1细胞能量代谢相关分子蛋白的影响（±s）

, figureFileSmall=null, figureFileBig=null, tableContent=
组别nHK2GLUT1PKM2p-PKM2MCT1MCT2MCT4
NC组30.93±0.100.54±0.030.96±0.050.57±0.050.68±0.070.63±0.020.39±0.03
六低组30.38±0.182）0.33±0.052）0.98±0.150.41±0.220.45±0.091）0.30±0.150.10±0.14
六高组30.13±0.052）0.38±0.101）0.75±0.081）0.47±0.020.21±0.122）0.32±0.022）0.14±0.032）
), ArticleFig(id=1322923384480346299, tenantId=1146029695717560320, journalId=1255847919539208197, articleId=1322923362036625462, language=EN, label=null, caption=null, figureFileSmall=null, figureFileBig=null, tableContent=
组别n基础糖酵解/（pmol/min）线粒体耗氧与基础糖酵解比值补偿糖酵解/（pmol/min）糖酵解潜能/（pmol/min）
NC+六低组4372.18±101.250.07±0.01476.58±131.6577.13±34.01
IN+六低组4565.70±120.833）0.09±0.033）783.70±145.56169.07±52.133）
NC+六高组4180.78±109.320.05±0.03195.13±126.986.45±14.02
IN+六高组4363.63±54.995）0.04±0.02398.93±82.965）20.45±23.85
), ArticleFig(id=1322923384555843772, tenantId=1146029695717560320, journalId=1255847919539208197, articleId=1322923362036625462, language=CN, label=表8, caption=

阻滞miR-1后EAELD对食管癌TE-1细胞糖酵解速率的影响（±s）

, figureFileSmall=null, figureFileBig=null, tableContent=
组别n基础糖酵解/（pmol/min）线粒体耗氧与基础糖酵解比值补偿糖酵解/（pmol/min）糖酵解潜能/（pmol/min）
NC+六低组4372.18±101.250.07±0.01476.58±131.6577.13±34.01
IN+六低组4565.70±120.833）0.09±0.033）783.70±145.56169.07±52.133）
NC+六高组4180.78±109.320.05±0.03195.13±126.986.45±14.02
IN+六高组4363.63±54.995）0.04±0.02398.93±82.965）20.45±23.85
), ArticleFig(id=1322923384631341245, tenantId=1146029695717560320, journalId=1255847919539208197, articleId=1322923362036625462, language=EN, label=null, caption=null, figureFileSmall=null, figureFileBig=null, tableContent=
组别n基础呼吸值质子漏耗氧线粒体最大耗氧能力备用呼吸能力非线粒体耗氧ATP合成耗氧
NC+六低组439.33±16.8437.72±16.2149.93±20.6410.60±4.3016.41±3.381.60±0.65
IN+六低组461.48±15.4358.34±14.4276.60±19.9115.11±4.6123.43±5.873.14±1.063）
NC+六高组46.23±6.846.41±5.5911.52±9.825.28±3.092.28±3.830.44±0.88
IN+六高组422.27±9.545）22.15±8.145）34.38±12.525）12.10±4.8310.41±4.595）0.72±1.04
), ArticleFig(id=1322923384706838718, tenantId=1146029695717560320, journalId=1255847919539208197, articleId=1322923362036625462, language=CN, label=表9, caption=

阻滞miR-1后EAELD对食管癌TE-1细胞线粒体功能的影响（±s）

, figureFileSmall=null, figureFileBig=null, tableContent=
组别n基础呼吸值质子漏耗氧线粒体最大耗氧能力备用呼吸能力非线粒体耗氧ATP合成耗氧
NC+六低组439.33±16.8437.72±16.2149.93±20.6410.60±4.3016.41±3.381.60±0.65
IN+六低组461.48±15.4358.34±14.4276.60±19.9115.11±4.6123.43±5.873.14±1.063）
NC+六高组46.23±6.846.41±5.5911.52±9.825.28±3.092.28±3.830.44±0.88
IN+六高组422.27±9.545）22.15±8.145）34.38±12.525）12.10±4.8310.41±4.595）0.72±1.04
), ArticleFig(id=1322923384773947583, tenantId=1146029695717560320, journalId=1255847919539208197, articleId=1322923362036625462, language=EN, label=null, caption=null, figureFileSmall=null, figureFileBig=null, tableContent=
组别nHK2GLUT1PKM2p-PKM2MCT1MCT2MCT4
NC+六低组30.47±0.180.37±0.080.78±0.120.11±0.050.25±0.040.21±0.130.19±0.33
IN+六低组31.09±0.14）1.30±0.164）1.49±0.184）0.30±0.103）1.00±0.413）0.58±0.143）0.39±0.02
NC+六高组30.32±0.090.53±0.140.87±0.130.40±0.070.77±0.140.27±0.070.48±0.18
IN+六高组30.60±0.075）1.12±0.235）1.27±0.175）0.57±0.121.19±0.160.89±0.410.82±0.105）
), ArticleFig(id=1322923384866222272, tenantId=1146029695717560320, journalId=1255847919539208197, articleId=1322923362036625462, language=CN, label=表10, caption=

阻滞miR-1后EAELD对食管癌TE-1细胞能量代谢相关分子蛋白的影响（±s）

, figureFileSmall=null, figureFileBig=null, tableContent=
组别nHK2GLUT1PKM2p-PKM2MCT1MCT2MCT4
NC+六低组30.47±0.180.37±0.080.78±0.120.11±0.050.25±0.040.21±0.130.19±0.33
IN+六低组31.09±0.14）1.30±0.164）1.49±0.184）0.30±0.103）1.00±0.413）0.58±0.143）0.39±0.02
NC+六高组30.32±0.090.53±0.140.87±0.130.40±0.070.77±0.140.27±0.070.48±0.18
IN+六高组30.60±0.075）1.12±0.235）1.27±0.175）0.57±0.121.19±0.160.89±0.410.82±0.105）
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基于miR-1/HIF-1α轴研究六君子汤乙酸乙酯提取物调控食管癌细胞TE-1能量代谢的作用机制
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陈星 , 周哲旭 , 尚艺婉 , 刘洋 , 刘娅茹 , 胡啸博 , 菅佳宁 , 肖小乔 , 陈玉龙
中华中医药学刊 | 国家项目点击 2025,43(4): 133-139
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中华中医药学刊 |国家项目点击 2025 , 43 (4) : 133 -139
基于miR-1/HIF-1α轴研究六君子汤乙酸乙酯提取物调控食管癌细胞TE-1能量代谢的作用机制
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陈星, 周哲旭, 尚艺婉, 刘洋, 刘娅茹, 胡啸博, 菅佳宁, 肖小乔, 陈玉龙
作者信息
  • 河南中医药大学，河南省中医方证信号传导重点实验室，河南　郑州　450046
通讯作者:
陈玉龙（1972-），男，河南平舆人，教授，博士研究生导师，博士，研究方向：中医药防治肿瘤。E-mail：。
作者简介:

陈星（1996-），女，河南新乡人，硕士在读，研究方向：肿瘤的病机与防治。

Mechanism of Ethyl Acetate Extract of Liujunzi Decoction（六君子汤）Regulating Energy Metabolism in Esophageal Cancer TE-1 Cells Based on miR-1/HIF-1α Axis
Xing CHEN, Zhexu ZHOU, Yiwan SHANG, Yang LIU, Yaru LIU, Xiaobo HU, Jianing JIAN, Xiaoqiao XIAO, Yulong CHEN
Affiliations
  • Henan University of Chinese Medicine, Henan Provincial Key Laboratory of Prescription and Syndrome Signal Transduction, Zhengzhou 450046, Henan, China
出版时间: 2025-04-10 doi: 10.13193/j.issn.1673-7717.2025.04.021
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摘要
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目的

探索六君子汤乙酸乙酯提取物（EAELD）能否通过miR-1/HIF-1α轴调控食管癌细胞TE-1的能量代谢及其分子机制。

方法

前期实验已建立稳定转染阻滞miR-1表达细胞株（IN）及空白对照（NC），采用MTT法得到EAELD对NC的半数抑制浓度（IC50）及30%抑制浓度（IC30），将其作为六高、六低浓度分别作用于IN与NC进行对比。实时荧光定量PCR（RT-qPCR）法检测EAELD对于TE-1细胞miR-1、HIF-1αmRNA的影响。双荧光素酶基因报告实验验证miR-1、HIF-1α靶向关系。然后将实验分组为NC组、六低组、六高组、IN＋六低组、IN＋六高组，Seahorse能量代谢分析系统检测线粒体压力与糖酵解速率，蛋白免疫印迹法（WB）检测能量代谢相关分子蛋白表达水平变化。

结果

MTT结果显示EAELD能够显著抑制NC增殖能力，呈浓度梯度依赖，选取20 μg/mL（IC30）、40 μg/mL（IC50）为低、高浓度组。RT-qPCR结果显示EAELD高浓度组显著促进miR-1的基因表达（P<0.05），HIF-1α有下降趋势，差异无统计学意义。双荧光素酶基因报告实验显示与野生型（WT）＋阴性对照（mimics NC）组相比，WT＋mimics荧光强度明显下降（P<0.05），与突变型（MUT）＋阴性对照（mimics NC）组相比，MUT＋mimics荧光强度无明显差别。将高、低浓度EAELD作用于IN时，MTT结果显示与NC相比，EAELD对于IN的抑制作用显著降低（P<0.05）。Seahorse能量代谢结果显示与NC组相比，EAELD高、低浓度组均可以抑制线粒体耗氧与糖酵解的比值（P<0.01，P<0.05）、糖酵解潜能（P<0.01）、基础呼吸值、质子漏耗氧（P<0.01，P<0.05）、线粒体最大耗氧能力、备用呼吸能力（P<0.01），高浓度组可以抑制基础糖酵解、补偿糖酵解、非线粒体耗氧、ATP合成耗氧（P<0.01）。与NC＋六低组相比，IN＋六低组的基础糖酵解、线粒体与基础糖酵解的比值、糖酵解潜能（P<0.05）、ATP合成耗氧（P<0.01）显著升高；与NC＋六高组相比，IN＋六高基础糖酵解、补偿糖酵解（P<0.05）、基础呼吸能力、质子漏耗氧、线粒体最大耗氧量、非线粒体耗氧显著升高（P<0.01）。WB结果显示与NC相比，EAELD高、低浓度组可以显著降低HK2（P<0.01）、GLUT1（P<0.05、P<0.01）、MCT1（P<0.01、P<0.05）蛋白相对表达量，高浓度组可以显著抑制PKM2（P<0.05）、MCT2、MCT4（P<0.01）的蛋白相对表达量；与NC＋六低组相比，IN＋六低组HK2、GLUT1、PKM2（P<0.01）、p-PKM2、MCT1、MCT2（P<0.05）的表达明显升高，与NC＋六高组相比，IN＋六高组可以显著促进HK2、GLUT1、PKM2、MCT4的表达（P<0.05）。

结论

六君子汤乙酸乙酯提取物可以通过下调能量代谢相关分子GLUT1、PKM2、p-PKM2、HK2、MCT1、MCT2、MCT4的蛋白表达抑制食管癌细胞TE-1的能量代谢，其部分机制与miR-1/HIF-1α轴有关。

六君子汤乙酸乙酯提取物  /  食管癌  /  能量代谢  /  miR-1/HIF-1α轴  /  分子机制
Objective

To explore whether ethyl acetate extract of Liujunzi Decoction（EAELD）can regulate the energy metabolism of TE-1 of esophageal cancer cells via the microRNA-1（miR-1）/hypoxia inducible factor-1α（HIF-1α）axis.

Methods

Stable transfection blocking miR-1 expression cell lines（miR-1 inhibitor，IN）and blank controls（miR-1 NC，NC）have been established in the preliminary experiments. The half maximal inhibitory concentration（IC50）and 30% inhibitory concentration（IC30）of EAELD on NC were obtained using MTT assay，and were used as the Liujunzi Decoction high and low concentrations to compare their effects on IN and NC，respectively. The effect of EAELD on miR-1 and HIF-1αmRNA in TE-1 cells was measured by quantitative real-time PCR（RT-qPCR）. Dual-luciferase gene reporter assay was used to validate the targeting relationship of miR-1 and HIF-1α. Then the experiments were divided into NC，Liujunzi Decoction low concentration，Liujunzi Decoction high concentration，IN＋Liujunzi Decoction low concentration and IN＋Liujunzi Decoction high concentration groups. Seahorse energy metabolism analysis system detected the mitochondrial pressure and glycolysis rate，and the protein expression level was detected by Western Blot.

Results

MTT results showed that EAELD could significantly inhibit the proliferation of NCin a concentration gradient dependent manner. The low and high concentration groups were 20 μg/mL（IC30）and 40 μg/mL（IC50），respectively. The RT-qPCR results showed that the EAELD high concentration group significantly promoted the gene expression of miR-1（P<0.05）and HIF-1αshowed a downward trend，without statistically significant difference. Dual-luciferase gene reporter assay showed that the fluorescence intensity of wild type（WT）＋mimics group was significantly lower than that of WT＋negative control（mimics NC）group（P<0.05），and there was no significant difference in the fluorescence intensity of mutant（MUT）＋mimics group compared with that of MUT＋mimics NCgroup. When high and low concentrations of EAELD were applied to IN，the MTT results showed that compared with that of NCgroup，the inhibitory effect of EAELD on IN group was significantly reduced（P<0.05）. Seahorse energy metabolism results showed that compared with those of NC group，the ratio of mitochondrial oxygen consumption to glycolysis（P<0.01，P<0.05），glycolytic potential（P<0.01），basal respiration value，proton leakage oxygen consumption（P<0.01，P<0.05），proton leakage oxygen consumption（P<0.01，P<0.05），mitochondrial maximum oxygen consumption capacity and spare respiratory capacity（P<0.01）were inhibited in the high and low concentration groups of Liujunzi Decoction. The high concentration group could inhibit basal glycolysis，compensate glycolysis，non-mitochondrial oxygen consumption and ATPsynthesis oxygen consumption（P<0.01）. Compared with those of NC＋Liujunzi Decoction low concentration group，basal glycolysis，mitochondrial to basal glycolysis ratio，glycolytic potential（P<0.05）and oxygen consumption for ATPsynthesis（P<0.01）were significantly increased in IN＋Liujunzi Decoction low concentration group. Compared with those of NC＋Liujunzi Decoction high concentration group，basal glycolysis，compensatory glycolysis（P<0.05），basal respiratory capacity，proton leakage oxygen consumption，maximum mitochondrial oxygen consumption and non-mitochondrial oxygen consumption（P<0.01）were significantly increased in IN＋Liujunzi Decoction high concentration group. WB results showed that compared with NCgroup，EAELD high and low concentration groups significantly decreased the protein relative expression levels of HK2（P<0.01），GLUT1（P<0.05，P<0.01）and MCT1（P<0.01，P<0.05）. The relative protein expressions of PKM2（P<0.05），MCT2 and MCT4（P<0.01）in the high concentration of EAELD group were significantly decreased. Compared with those of NC＋Liujunzi Decoction low concentration group，the expressions of HK2，GLUT1，PKM2（P<0.01），p-PKM2，MCT1 and MCT2（P<0.05）in IN＋Liujunzi Decoction low concentration group were significantly increased. Compared with those of NC＋Liujunzi Decoction high concentration group，the expressions of HK2，GLUT1，PKM2（P<0.01），p-PKM2，MCT1 and MCT2（P<0.05）in IN＋Liujunzi Decoction low concentration group were significantly increased. IN＋Liujunzi Decoction high concentration group could significantly promote the expressions of HK2，GLUT1，PKM2 and MCT4（P<0.05）.

Conclusion

EAELD can inhibit the energy metabolism of esophageal cancer cell line TE-1 by down-regulating the expressions of GLUT1，PKM2，p-PKM2，HK2，MCT1，MCT2 and MCT4，and the mechanism is partly related to miR-1/HIF-1αaxis.

ethyl acetate extract of Liujunzi Decoction（六君子汤）  /  esophageal cancer  /  energy metabolism  /  miR-1/HIF-1αaxis  /  molecular mechanism
陈星, 周哲旭, 尚艺婉, 刘洋, 刘娅茹, 胡啸博, 菅佳宁, 肖小乔, 陈玉龙. 基于miR-1/HIF-1α轴研究六君子汤乙酸乙酯提取物调控食管癌细胞TE-1能量代谢的作用机制. 中华中医药学刊, 2025 , 43 (4) : 133 -139 . DOI: 10.13193/j.issn.1673-7717.2025.04.021
Xing CHEN, Zhexu ZHOU, Yiwan SHANG, Yang LIU, Yaru LIU, Xiaobo HU, Jianing JIAN, Xiaoqiao XIAO, Yulong CHEN. Mechanism of Ethyl Acetate Extract of Liujunzi Decoction（六君子汤）Regulating Energy Metabolism in Esophageal Cancer TE-1 Cells Based on miR-1/HIF-1α Axis[J]. Chinese Archives of Traditional Chinese Medicine, 2025 , 43 (4) : 133 -139 . DOI: 10.13193/j.issn.1673-7717.2025.04.021
正文
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根据2020年全球最新癌症统计调查发现，2020年全球新发癌症病例达1900多万例，将近1000万人死于癌症，是全球最大死亡原因[1]。食管癌作为中国第四大与癌症有关的死亡原因，同时也是全球第六大癌症死亡原因[2]。由于早期食管癌患者并无任何特殊症状，导致其大多数发展较为迅速，直至晚期，此时治疗方案有限，治愈极低[3-4]。
通过对食管癌临床患者信息收集，发现食管癌临床常见证素主要有气虚、气郁、痰凝、血瘀等，证候以气虚证为主，与脾胃密切相关[5]。因此，在食管癌的治疗上应紧抓脾胃失调这一病机。六君子汤以补气健脾著称，主要用于治疗脾胃气虚夹痰湿证，这与食管癌的病机相契合。研究证明[6]加减六君子汤能够改善食管癌患者放化疗后的不良反应，提高生活质量，并且六君子汤可用于多种肿瘤，提高患者免疫力，提升临床治疗疗效[7-8]。不仅如此六君子汤乙酸乙酯提取物（EAELD）可抑制食管癌细胞的增殖、迁移与侵袭，抑制食管癌裸鼠移植瘤的生长[9-11]。前期实验也显示EAELD可以调控AMPK/mTOR信号通路影响食管癌细胞的能量代谢，增强顺铂的疗效，抑制食管癌细胞的生长[12]。
MicroRNA-1（miR-1）已经被证实在多种肿瘤中呈现低表达状态，包括食管癌[13]，可以直接通过多种途径抑制食管癌细胞的增殖、迁移、侵袭[14]。不仅如此，miR-1可通过失活Smad3和直接靶向HIF-1α，降低HK2和MCT4的表达，从而抑制肿瘤细胞有氧糖酵解和增殖[15]，直接参与肿瘤细胞的能量代谢，影响肿瘤进程。
因此，本实验在前期研究的基础上，首先验证miR-1、HIF-1α的靶向关系，以阻滞miR-1表达的TE-1细胞为研究对象，探究EAELD能否通过miR-1/HIF-1α轴影响食管癌细胞TE-1的能量代谢及其分子机制，以期为六君子汤治疗食管癌的临床应用提供部分实验依据。
1　材料
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1.1　细胞
人食管癌TE-1细胞感染慢病毒建立稳转miR-1 NC（NC）、miR-1 inhibitor（IN）细胞株，NC细胞作为IN细胞空白对照组，由课题组其他成员转染鉴定。人肾上皮细胞293T细胞，由本实验室冻存、培养。
1.2　药物
六君子汤饮片购于河南中医药大学第一附属医院。
1.3　主要试剂
DMEM高糖培养基（货号：12100）、胰蛋白酶-EDTA消化液（货号：T1300）、四甲基偶氮唑盐（MTT，货号：M8180）、RIPA（货号：R0010）、二甲基亚砜（货号：D8370，Solarbio公司）、胎牛血清（Lonsera公司，货号：A97E00G）、XF糖酵解速率测定试剂盒（货号：10334-100）、水化液（货号：08418001）、XF96孔细胞培养板（货号：101085-004）、基础检测培养基（货号：23217002）、XFp细胞线粒体压力测试试剂盒（货号：103101-100，Agilent公司）、兔抗人PKM2抗体（货号：4053s）、兔抗人p-PKM2抗体（货号：3827s）、兔抗人HK2抗体（货号：2867s）、兔抗人α-TUBULIN抗体（货号：2125S，CST公司）、兔抗人GLUT1抗体（货号：YN4056）、兔抗人MCT-1抗体（货号：ab179832）、兔抗人MCT-4抗体（货号：ab234728，Immunoway公司）、反转录试剂盒（Toyobo公司，货号：117000）、2×SYBR® Green（武汉ABclonal公司，货号：RM21203）、Lipofectamine 2000（美国Thermo公司，货号：2328448）、双荧光素酶检测试剂盒（Dual-Luciferase® Reporter Assay System，美国Promega公司，货号：E1910）、OPTI-MEM（美国Thermo公司，货号：2328448）。
1.4　主要仪器
酶标仪（BIO-TEK公司，型号：ELx-800），CO2培养箱（Thermo公司，型号：371），超净工作台（苏净集团安泰公司，型号37997），能量代谢分析系统（Agilent公司，型号：Seahorse XFe96），倒置显微镜（Laica公司，型号DFC450C），荧光定量PCR仪（美国ABI，型号QuantStudioTM 6 Flex），荧光分光光度计（Thermo公司，型号：NanoDrop One），电泳仪（BIO-RAD公司，型号：PowerPac Basic），凝胶成像系统（BIO-RAD公司，型号Universal Hood Ⅱ）。
2　实验方法
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2.1　细胞培养
NC、IN、293T细胞是由含10%的胎牛血清与90% DMEM含双抗高糖培养基培养，置于含CO2浓度5%、37℃恒温培养箱中培养，2 d换一次液，3～4 d，1∶3～1∶5传代。
2.2　六君子汤乙酸乙酯部位提取
将六君子汤按照人参∶白术∶茯苓∶甘草∶陈皮∶半夏＝1∶1.5∶1∶1∶1∶1.5饮片打粉、称重，按照药粉∶75%乙醇＝1∶8比例沸腾加热两次，分别为1.5 h和1 h，将两次药液8层纱布过滤，静置过夜。将药液浓缩与生药的体积一致，将2倍体积的乙酸乙酯加入，混匀，分液漏斗进行萃取，萃取8次，收集萃取液，旋转蒸发仪回收乙酸乙酯，低温真空干燥机进行冷冻干燥。经质谱分析鉴定其共有663种物质，主要成分以2-羟基肉桂酸、4-二羟基苯甲酸、5-羟基酸橙黄酮、草黄素-8-C-葡萄糖苷（金雀花素）、高车前素-8-C-葡萄糖苷等酚酸类、黄酮类为主。称取适量提取物，DMSO溶解为250 mg/mL，避光储存于-20℃，此为储存液。然后使用DMEM高糖培养基稀释为2.5 mg/mL，此为工作液，供后续使用。
2.3　MTT法检测不同浓度EAELD对NC、IN细胞增殖的影响
将对数生长期的TE-1细胞以1×104个/孔，200 μL体积种于96孔板，培养箱培养24 h后，弃去孔内旧的培养基，设置0、10、20、40、60、80 μg/mL的浓度使用DMEM高糖培养基进行加药处理，继续培养48 h，抽掉孔内药液，90% DMEM＋10% MTT溶液以每孔100 μL体积加入，放入培养箱4～6 h，弃去孔内旧的液体，每孔加入150 μL DMSO溶液，摇床混匀，酶标仪490 nm检测吸光值，按照抑制率＝1-用药组/空白对照组×100%公式进行计算，SPSS估测IC30、IC50应用于后续实验。
根据上述将六君子汤分为高、低浓度（六高、六低）两组，分别应用NC、IN。MTT法检测，IN与NC相比，药物的抑制作用有无显著变化。
2.4　实时荧光定量PCR法（RT-qPCR）检测EAELD对于TE-1细胞miR-1、HIF-1αmRNA的影响
TRIzol法提取各组总RNA，按照说明书进行逆转录，采用SYBR Green染料法以10 μL体系对c-DNA进行扩增，miR-1以U6为内参，HIF-1α以β-actin为内参，用2-△△Ct计算各个样品中目的mRNA相对表达量。引物序列由GENEWIZ公司设计合成。见表1。
2.5　双荧光素酶基因报告实验
首先通过TargetScan 4.2来预测hsa-miR-1-3p的靶基因HIF-1α及其结合位点，其靶点位置为HIF-1α的3＇UTR的3466～3472区。我们将HIF-1α的序列由TTCCA突变为AGATC，构建pMIR-REPORT荧光素酶载体，委托上海吉玛制药技术有限公司构建合成。转染质粒序列见表2。
将处于对数生长期的293T细胞按照8×103个/孔种于96孔板，每组3个复孔，置于含5% CO2，37℃恒温培养箱中培养24 h。吸去每孔内旧的培养基，沿孔壁加入100 μL/孔PBS清洗细胞1次，抽出，每孔加入50 μL减血清培养基OPTIMEM，培养箱培养1 h。分别转染野生型（WT）＋miR-1 mimics、突变型（MUT）＋miR-1 mimics、WT＋miR-1 NC、MUT＋miR-1 NC，其中mimics、NC孔内终浓度保证为50 nmol/L，WT、MUT每孔0.2 μL、Lipofectamine 2000每孔0.25 μL。培养6 h后，将转染液抽取出来，每孔加入100 μL完全培养基，继续培养42 h。按照双荧光素酶检测说明书，配置萤火虫与海肾检测试剂，上机检测。
2.6　Seahorse能量代谢分析系统检测线粒体压力与糖酵解速率
分组为NC组、NC＋六低组、NC＋六高组、IN＋六低组、IN＋六高组，接种于Seahorse 96孔板中，每孔细胞悬液80 μL，每孔8000个细胞，每组3个复孔。置于CO2培养箱中培养24 h后换液，根据2.3中MTT检测结果，选取IC30（20 μg/mL）作为低剂量组、IC50（40 μg/mL）作为高剂量组，用DMEM配制六君子汤工作液，分别处理细胞，继续培养48 h。按照说明书，检测各组细胞能量代谢情况。实验结果由Wave软件分析。
2.7　蛋白免疫印迹法（WB）检测能量代谢相关分子蛋白表达影响
分组同2.6，加药培养48 h后，以RIPA裂解液∶蛋白磷酸酶抑制剂∶PMSF＝100∶1∶1的比例，配制细胞裂解液混合物，每孔加入130 μL裂解细胞，BCA蛋白浓度测定法测定各组蛋白浓度，98℃变性8 min，取20 μg蛋白上样，用10%SDSPAGE凝胶电泳，200 mA转膜60 min，5%脱脂牛奶室温封闭4 h，一抗（1∶1000）4℃孵育过夜，TBST漂洗3次，二抗（1∶1000）室温孵育1 h，再次漂洗3次，配制ECL发光显影液，显影拍照。以α-微管蛋白（α-Tublin）为内参，使用“ImageLab”分析每组条带的光密度值，以目的条带光密度值/内参条带光密度值，计算各组蛋白相对表达量。
2.8　统计学分析
各实验组数据收集后采用IBM SPSS Statistics 21进行分析，每组实验至少重复3次。若数据符合正态分布并且方差齐，两组间对比采用独立样本t检验，若符合正态分布但是方差不齐，则采用Dunnett T3检验。若不符合正态分布，则采用非参数检验。柱状图使用GraphPad Prism 8绘制，当P<0.05时认为差异有统计学意义。
3　结果
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3.1　MTT法检测EAELD对食管癌TE-1细胞增殖的影响
MTT结果显示与NC组相比，不同浓度的EAELD对TE-1细胞的增殖均有抑制作用（P<0.01），抑制作用随EAELD的升高而升高，见图1。选取20 μg/mL（IC30）、40 μg/mL（IC50）分别为低浓度组、高浓度组。
3.2　qPCR法检测不同浓度EAELD对TE-1细胞miR-1、HIF-1α mRNA的影响
如表3所示，与NC组相比，EAELD高浓度组（六高）能够明显促进miR-1 mRNA的表达（P<0.05），低浓度组（六低）有升高趋势，差异无统计学意义。EAELD对HIF-1α的mRNA表达有抑制趋势，差异无统计学意义。后续选取阻滞miR-1进行反向验证，做能量代谢检测。
3.3　双荧光素酶基因报告实验验证miR-1与HIF-1α靶向关系
查阅文献及利用TargetScan 4.2来进行筛选发现，miR-1与HIF-1α存在靶向关系，如图2所示，双荧光素酶基因报告实验结果显示，与WT＋阴性对照（mimics NC）组相比，WT＋mimics荧光强度明显下降，差异具有统计学意义，与MUT＋阴性对照（mimics NC）组相比，MUT＋mimics荧光强度无明显差别。表明miR-1 mimics可以有效抑制HIF-1α野生型荧光素酶活性，对于突变型HIF-1α无明显影响，证实HIF-1α为miR-1的靶基因，且miR-1主要是通过与HIF-1α3＇UTR区域的结合来调控HIF-1α的表达。
3.4　MTT法检测不同浓度的EAELD对于NC、IN细胞增殖的影响
在阻滞miR-1的食管癌TE-1（IN）组加入相同浓度EAELD后，与空白对照组（NC）相比，EAELD对细胞增殖的抑制作用仍随着药物浓度的升高而升高，而IN在相同EAELD浓度作用下，对细胞增殖的抑制作用低于空白对照组（P<0.05）。表明在阻滞miR-1的表达后，EAELD对TE-1细胞生长的抑制作用明显下降。见表4。
3.5　EAELD对食管癌TE-1细胞的能量代谢的影响
3.5.1　不同浓度EAELD对食管癌TE-1细胞糖酵解速率的影响
与NC组相比，六高、六低组均可以抑制线粒体耗氧与糖酵解的比值（P<0.01，P<0.05）、糖酵解潜能（P<0.01），六高组同样可以有效抑制基础糖酵解、补偿糖酵解（P<0.01）。见表5、插页ⅩⅩⅨ图3。
3.5.2　不同浓度EAELD对食管癌TE-1细胞线粒体功能的影响
与NC组相比，六低、六高组的基础呼吸值、质子漏耗氧、线粒体最大耗氧能力、备用呼吸能力、非线粒体耗氧、ATP合成耗氧均随着用药浓度的增加而减少，除六低组非线粒体耗氧、ATP合成耗氧外，差异均具有统计学意义。见表6、插页ⅩⅩⅨ图4。
3.5.3　不同浓度EAELD对TE-1细胞能量代谢相关分子蛋白的影响
与NC组相比，六高、六低组的HK2（P<0.01）、GLUT1（P<0.05、P<0.01）、MCT1（P<0.01、P<0.05），六高组的PKM2（P<0.05）、MCT2、MCT4（P<0.01）的相对蛋白表达量显著降低。见表7、图5。
3.6　阻滞miR-1后EAELD对食管癌TE-1细胞能量代谢的影响
3.6.1　阻滞miR-1后EAELD对食管癌TE-1细胞糖酵解速率的影响
与NC＋六低组相比，IN＋六低组的基础糖酵解、线粒体与基础糖酵解的比值、糖酵解潜能显著升高（P<0.05），补偿糖酵解有升高趋势。与NC＋六高组相比，IN＋六高组基础糖酵解、补偿糖酵解明显升高（P<0.05），糖酵解潜能有升高趋势。见表8、插页ⅩⅩⅨ图6。
3.6.2　阻滞miR-1后EAELD对食管癌TE-1线粒体功能的影响
与NC＋六低组相比，IN＋六高组的ATP合成耗氧量明显升高（P<0.01），基础呼吸能力、质子漏耗氧、线粒体最大耗氧能力、备用呼吸能力有升高趋势。与NC＋六高组相比，IN＋六高组的基础呼吸能力、质子漏耗氧、线粒体最大耗氧量、非线粒体耗氧显著升高（P<0.01）。备用呼吸能力、ATP合成耗氧有升高趋势。见表9、插页ⅩⅩⅨ图7。
3.6.3　阻滞miR-1后EAELD对食管癌TE-1细胞能量代谢相关分子蛋白的影响
与NC＋六低组相比，IN＋六低组HK2、GLUT1、PKM2（P<0.01）、p-PKM2、MCT1、MCT2（P<0.05）的表达明显提高，MCT4有升高趋势。与NC＋六高组相比，IN＋六高组可以显著促进HK2、GLUT1、PKM2、MCT4的表达（P<0.05），p-PKM2、MCT1、MCT2有升高趋势。见表10、图8、图9。
4　讨论
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食管癌在中医上属于“噎嗝”，病名首见于《黄帝内经》，病因较为复杂，主要与七情内伤、酒食不节、久病年老有关，致使气、痰、瘀交阻，津气耗伤，胃失通降而成。病位主在食道，属胃。脾胃为后天之本、气血生化之源，因此临床上多针对脾胃来进行食管癌治疗与术后恢复。六君子汤方中共有人参、白术、茯苓、甘草、陈皮、半夏6味药组成，四君子汤益气健脾和胃，加以陈皮、半夏，燥湿化痰、理气降逆，治疗由脾胃气虚引起的痰湿、呃逆等证，临床与实验研究表明其对食管癌的治疗与术后恢复也有很好疗效。本研究从食管癌病因病机入手，研究EAELD治疗食管癌的部分机制。基于前期EAELD对于食管癌细胞EC9706的能量代谢具有显著抑制作用的发现，进一步研究EAELD抑制能量代谢的分子机制与miR-1/HIF-1α轴的关系。
miR-1、HIF-1α与肿瘤细胞的能量代谢关系密切。研究表明miR-1可通过直接靶向糖酵解和糖原形成的主要调节剂雌激素相关受体β（Errβ），来抑制心脏胎儿基因程序[16]，也可调控Smad3介导的有氧糖酵解，从而使得大肠癌细胞的增殖被抑制[17]。HIF-1α可通过调控GLUT1、MCT1来促进肿瘤细胞的糖酵解[18-19]。甚至miR-1可直接靶向HIF-1α表达促进肿瘤细胞的能量代谢[15]。MTT结果显示不同浓度EAELD对食管癌TE-1细胞的抑制作用呈剂量浓度依赖，并且可以促进miR-1、抑制HIF-1α的基因表达，而荧光素酶基因检测实验也证实了miR-1与HIF-1α的靶向关系，且miR-1主要是通过与HIF-1α3＇UTR区域的结合来调控HIF-1α的表达，因此后续选取了阻滞miR-1进行EAELD的反向验证。
Seahorse能量代谢分析系统可以根据培养基的pH值变化来判断细胞的代谢状态。当细胞进行糖酵解活动时，会产生大量乳酸，然后伴随着H＋流出，当细胞发生氧化磷酸化反应时，会产生大量的CO2，二者均可导致细胞所处的培养基pH值发生变化，其中重点关注糖酵解测试的糖酵解潜能，线粒体压力测试中的备用呼吸能力。当选取EAELD高、低浓度分别作用于NC时，结果表明EAELD可以显著抑制肿瘤细胞的糖酵解与氧化磷酸化能力，而阻滞miR-1时，EAELD的抑制作用有所下降。
GLUT1作为有氧糖酵解的主要开关，可以加速有氧糖酵解，为原发肿瘤细胞向远处移动提供能量[20-22]。PKM2可以将磷酸烯醇丙酮酸（PEP）转化为丙酮酸，是糖酵解的最后一步[23]。HK2通过抑制葡萄糖6-磷酸的负反馈来促进糖酵解，并通过增加ATP，来促进有氧糖酵解、抑制细胞凋亡[24-25]，是糖酵解的第一个限速酶。MCT1、MCT4可以促进肿瘤细胞中的糖酵解产物乳酸的转运[26-28]，MCT2则对丙酮酸有着较高亲和力，可以通过调节肿瘤微环境，促进肿瘤细胞的高糖酵解通量[29-30]，三者可以实现肿瘤细胞乳酸、丙酮酸的高效利用，促进肿瘤细胞的能量代谢[31]。WB结果显示EAELD能够显著降低能量代谢相关分子GLUT1、PKM2、p-PKM2、HK2、MCT1、MCT2、MCT4的蛋白表达，抑制食管癌细胞TE-1的能量代谢。当阻滞miR-1时，EAELD对于能量代谢相关蛋白的抑制作用明显减小，与能量代谢结果相一致，作用机制见插页ⅩⅩⅨ图10。
同时研究中发现HIF-1α的蛋白表达极低，经查阅相关资料，认为HIF-1α作为低氧因子，在常氧环境中几乎不表达，因此后续需要进一步在低氧环境下验证miR-1与HIF-1α的靶向关系及EAELD抑制食管癌细胞TE-1的能量代谢的分子机制。
综上所述，EAELD可以通过调控能量代谢相关分子GLUT1、PKM2、p-PKM2、HK2、MCT1、MCT2、MCT4的蛋白表达抑制食管癌细胞TE-1的能量代谢，其部分机制与miR-1/HIF-1α轴有关，但是EAELD影响能量代谢的其他途径及其作用机制还有待进一步研究。
基金
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  • 国家自然科学基金项目(82074313)
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2025年第43卷第4期
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doi: 10.13193/j.issn.1673-7717.2025.04.021
  • 首发时间：2026-10-30
  • 出版时间：2025-04-10
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国家自然科学基金项目(82074313)
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    河南中医药大学，河南省中医方证信号传导重点实验室，河南　郑州　450046

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陈玉龙（1972-），男，河南平舆人，教授，博士研究生导师，博士，研究方向：中医药防治肿瘤。E-mail：。
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