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Article(id=1322928337181606241, tenantId=1146029695717560320, journalId=1255847919539208197, issueId=1322926985957221241, articleNumber=null, orderNo=null, doi=10.13193/j.issn.1673-7717.2025.11.001, 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=1793340294404, onlineDateStr=2026-10-30, pubDate=1762704000000, pubDateStr=2025-11-10, doiRegisterDate=null, doiRegisterDateStr=null, onlineIssueDate=1793340294404, onlineIssueDateStr=2026-10-30, onlineJustAcceptDate=null, onlineJustAcceptDateStr=null, onlineFirstDate=null, onlineFirstDateStr=null, sourceXml=null, magXml=null, createTime=1793340294404, creator=13701087609, updateTime=1793340294404, updator=13701087609, issue=Issue{id=1322926985957221241, tenantId=1146029695717560320, journalId=1255847919539208197, year='2025', volume='43', issue='11', pageStart='1', pageEnd='258', issueExtLink='null', onlineDate='null', pubDate='1762704000000', pubDateStr='2025-11-10', beforeIssueId=null, nextIssueId=null, price=null, status=1, issueComplete=1, articleOrder=1, issueType=-1, specialIssue=0, createTime=1793339972247, creator='13701087609', updateTime=1793340743335, updator='13701087609', preIssue=null, nextIssue=null, articleTotal=null, ext={EN=IssueExt(id=1322930220201804556, tenantId=1146029695717560320, journalId=1255847919539208197, issueId=1322926985957221241, language=EN, specialIssueTitle=, coverIllustrator=null, specialIssueEditor=, specialIssueAbout=), CN=IssueExt(id=1322930220201804557, tenantId=1146029695717560320, journalId=1255847919539208197, issueId=1322926985957221241, language=CN, specialIssueTitle=, coverIllustrator=null, specialIssueEditor=, specialIssueAbout=)}, issueFiles=null, downloadFileDto=null}, startPage=1, endPage=7, ext={EN=ArticleExt(id=1322928337378738530, articleId=1322928337181606241, tenantId=1146029695717560320, journalId=1255847919539208197, language=EN, title=Reversal Effect and Mechanism of Chonglou（Rhizoma Paridis）on Multidrug Resistance of Leukemia CEM/VCR Cells, columnId=1256183423710970242, journalTitle=Chinese Archives of Traditional Chinese Medicine, columnName=New Opinion of Ph.D. Supervisor, runingTitle=null, highlight=null, articleAbstract=
Objective

To explore whether Chonglou（Rhizoma paridis）has a reversal effect on multidrug resistance of leukemia CEM/VCR and its reversal mechanism.

Methods

CEM/VCR cells were treated with different concentrations of Chonglou（Rhizoma paridis）for 72 hours，and the mortality rate was calculated，and the appropriate concentration of Chonglou（Rhizoma paridis）reversal agent was selected. MTT colorimetric experiment was used to calculate the inhibitory rate and half inhibitory concentration（IC50）of low，medium and high concentrations（0.1，0.5 and 2.5μg/mL）of vincristine（VCR）acting on Chonglou（Rhizoma paridis）treated cells（hereinafter referred to as the treated group）and unweighted Chonglou（Rhizoma paridis）treated cells（hereinafter referred to as the untreated group）for 24，48 and 72 hours respectively，and to calculate the reversal index（RI）and reversal multiple（IC50）between the two groups. Flow cytometry（FCM）was used to detect the apoptosis rate after VCR was applied to the two groups of cells. RT-qPCR and Western blot were used to detect the mRNA and protein expression levels of Bax，Bcl-2，Cyt-c，P-gp and MRP1 after VCR acted on the two groups of cells.

Results

The concentration of Chonglou（Rhizoma paridis）reversal agent was 0.008μg/mL. The inhibition rate of VCR in the treatment group was significantly higher than that in the untreated group（P<0.05 or P<0.01）. The IC50 value of VCR in the treatment group after 24，48 and 72 hours was reduced from 17.32，13.85 and 6.21μg/mL to 15.37，2.25 and 0.62μg/mL，and the reversal multiples were 1.12 respectively. The results of flow cytometry showed that the apoptosis rate of VCR group increased gradually with the increase of drug concentration，and the apoptosis rate of treated group was higher than that of untreated group under the same conditions. The results of RT-qPCR and Western blot showed that the expressions of Bcl-2，P-gp，MRP1-1 and Bax，Cyt-c genes and proteins were down-regulated and up-regulated by VCR with different concentrations at the same time compared with those of the control group（P<0.05），and this change was more significant in the treatment group.

Conclusion

Chonglou（Rhizoma paridis）can reverse the multidrug resistance of CEM/VCR cells，which may be related to down-regulating the expressions of P-gp and MRP1，reducing the efflux of chemotherapeutic drugs and increasing the intracellular concentration of VCR，down-regulating the expression of Bcl-2 and up-regulating the expressions of Bax and Cyt-c，inducing cell apoptosis.

, authors=Dacheng ZHU, Jiaxu WEI, Xiaoming XU, Yan LIU, Linzhi KANG, Jiahuan HE, authorsList=Dacheng ZHU, Jiaxu WEI, Xiaoming XU, Yan LIU, Linzhi KANG, Jiahuan HE, authorCompany=null, correspAuthors=null, 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=1322928342005055877, articleId=1322928337181606241, tenantId=1146029695717560320, journalId=1255847919539208197, language=CN, title=重楼对白血病CEM/VCR细胞多药耐药的逆转作用及机制研究, columnId=1256183426563096985, journalTitle=中华中医药学刊, columnName=博士导师新论, runingTitle=null, highlight=null, articleAbstract=
目的

探究重楼对白血病CEM/VCR细胞多药耐药是否具有逆转作用及其逆转耐药性的机制。

方法

不同浓度重楼作用CEM/VCR细胞72 h并计算死亡率，选择适宜的重楼逆转剂浓度；MTT比色实验计算低、中、高浓度（0.1、0.5、2.5μg/mL）长春新碱（Vincristine，VCR）分别作用于重楼处理细胞（以下统称处理组）及未加重楼处理细胞（以下统称未处理组）24、48、72 h后的抑制率及其半数抑制浓度（IC50），并计算两组间耐药的逆转倍数（Reversal index，RI）；流式细胞术（Flow cytometry，FCM）检测VCR作用于两组细胞后的凋亡率；RT-qPCR、Western blot检测VCR作用于两组细胞后Bax、Bcl-2、Cyt-c、P-gp、MRP1的mRNA和蛋白表达水平。

结果

重楼逆转剂浓度为0.008μg/mL；VCR作用于处理组的抑制率明显大于未处理组（P<0.05或P<0.01），处理组将VCR作用于细胞24、48、72 h的IC50值由17.32、13.85、6.21μg/mL降至15.37、2.25、0.62μg/mL，其逆转倍数分别为1.13、6.16、10.02；流式结果显示，VCR组细胞凋亡率随着药物浓度增加逐渐增大，且相同条件下处理组细胞凋亡率大于未处理组；RT-qPCR、Western blot结果显示，同一时间不同浓度VCR作用下，两组细胞的加药组与对照组比较，均能下调Bcl-2、P-gp、MRP1和上调Bax、Cyt-c基因及蛋白表达（P<0.05），且这种变化处理组更为显著。

结论

重楼可以逆转CEM/VCR细胞的多药耐药性，其可能机制是：①通过下调P-gp、MRP1的表达，降低VCR外排，增加细胞内VCR浓度；②通过下调Bcl-2和上调Bax、Cyt-c的表达，诱导细胞凋亡。

, authors=朱大诚, 魏佳旭, 徐笑明, 刘燕, 康林之, 何家寰, authorsList=朱大诚, 魏佳旭, 徐笑明, 刘燕, 康林之, 何家寰, authorCompany=null, correspAuthors=null, authorNote=

朱大诚（1964-），男，江西永新人，教授，博士研究生导师，学士，研究方向：中医药抗肿瘤。

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朱大诚（1964-），男，江西永新人，教授，博士研究生导师，学士，研究方向：中医药抗肿瘤。

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朱大诚（1964-），男，江西永新人，教授，博士研究生导师，学士，研究方向：中医药抗肿瘤。

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基因名称基因序列
GAPDHForward：5′-ACCCAGAAGACTGTGGATGG-3′
Reverse：5′-TCAGCTCAGGGATGACCTTG-3′
P-gpForward：5′-GGAGCCTACTTGGTGGCACATAA-3′
Reverse：5′-TGGCATAGTCAGGAGCAAATGAAC-3′
MRP1Forward：5′-CATTCAGCTCGTCTTGTCCTG-3′
Reverse：5′-GGATTAGGGTCGTGGATGGTT-3′
BaxForward：5′-CATGGGCTGGACATTGGACT-3′
Reverse：5′-AAAGTAGGAGAGGAGGCCGT-3′
Cyt-CForward：5′-CTTTGGGCGGAAGACAGGTC-3′
Reverse：5′-TTATTGGCGGCTGTGTAAGAG-3′
Bcl-2Forward：5′-CGCCAACATTCTCTCCACAG-3′
Reverse：5′-CTGGGCCAGAGCTACATCTT-3′
), ArticleFig(id=1322928350406246864, tenantId=1146029695717560320, journalId=1255847919539208197, articleId=1322928337181606241, language=CN, label=表1, caption=

基因引物设计序列

, figureFileSmall=null, figureFileBig=null, tableContent=
基因名称基因序列
GAPDHForward：5′-ACCCAGAAGACTGTGGATGG-3′
Reverse：5′-TCAGCTCAGGGATGACCTTG-3′
P-gpForward：5′-GGAGCCTACTTGGTGGCACATAA-3′
Reverse：5′-TGGCATAGTCAGGAGCAAATGAAC-3′
MRP1Forward：5′-CATTCAGCTCGTCTTGTCCTG-3′
Reverse：5′-GGATTAGGGTCGTGGATGGTT-3′
BaxForward：5′-CATGGGCTGGACATTGGACT-3′
Reverse：5′-AAAGTAGGAGAGGAGGCCGT-3′
Cyt-CForward：5′-CTTTGGGCGGAAGACAGGTC-3′
Reverse：5′-TTATTGGCGGCTGTGTAAGAG-3′
Bcl-2Forward：5′-CGCCAACATTCTCTCCACAG-3′
Reverse：5′-CTGGGCCAGAGCTACATCTT-3′
), ArticleFig(id=1322928350473355729, tenantId=1146029695717560320, journalId=1255847919539208197, articleId=1322928337181606241, language=EN, label=null, caption=null, figureFileSmall=null, figureFileBig=null, tableContent=
组别nOD值（±s）抑制率/（%）
24 h48 h72 h24 h48 h72 h
空白组50.03±0.000.03±0.000.03±0.00---
对照组5（0.95±0.01）（1.42±0.09）（1.67±0.08）---
1.02±0.091.49±0.121.74±0.18---
VCR0.1 μg/mL5（0.91±0.08）*（1.28±0.03）*（1.19±0.04）**（4.10）（10.40）（28.94）
0.91±0.03▲△1.17±0.21▲▲△△1.14±0.15▲▲△10.1521.3534.28
VCR0.5 μg/mL5（0.85±0.05）**（1.16±0.04）**（1.00±0.07）**（10.89）（18.66）（40.23）
0.81±0.02▲△△0.98±0.10▲▲△△0.96±0.10▲▲△19.9434.3644.84
VCR2.5 μg/mL5（0.80±0.06）**（0.99±0.19）**（0.80±0.03）**（15.89）（30.42）（52.37）
0.75±0.12▲▲△0.88±0.03▲▲△0.57±0.04▲▲△△25.9840.8767.25
), ArticleFig(id=1322928350540464594, tenantId=1146029695717560320, journalId=1255847919539208197, articleId=1322928337181606241, language=CN, label=表2, caption=

VCR对细胞生长的影响

, figureFileSmall=null, figureFileBig=null, tableContent=
组别nOD值（±s）抑制率/（%）
24 h48 h72 h24 h48 h72 h
空白组50.03±0.000.03±0.000.03±0.00---
对照组5（0.95±0.01）（1.42±0.09）（1.67±0.08）---
1.02±0.091.49±0.121.74±0.18---
VCR0.1 μg/mL5（0.91±0.08）*（1.28±0.03）*（1.19±0.04）**（4.10）（10.40）（28.94）
0.91±0.03▲△1.17±0.21▲▲△△1.14±0.15▲▲△10.1521.3534.28
VCR0.5 μg/mL5（0.85±0.05）**（1.16±0.04）**（1.00±0.07）**（10.89）（18.66）（40.23）
0.81±0.02▲△△0.98±0.10▲▲△△0.96±0.10▲▲△19.9434.3644.84
VCR2.5 μg/mL5（0.80±0.06）**（0.99±0.19）**（0.80±0.03）**（15.89）（30.42）（52.37）
0.75±0.12▲▲△0.88±0.03▲▲△0.57±0.04▲▲△△25.9840.8767.25
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重楼对白血病CEM/VCR细胞多药耐药的逆转作用及机制研究
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朱大诚 , 魏佳旭 , 徐笑明 , 刘燕 , 康林之 , 何家寰
中华中医药学刊 | 博士导师新论 2025,43(11): 1-7
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中华中医药学刊 |博士导师新论 2025 , 43 (11) : 1 -7
重楼对白血病CEM/VCR细胞多药耐药的逆转作用及机制研究
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朱大诚（1964-），男，江西永新人，教授，博士研究生导师，学士，研究方向：中医药抗肿瘤。

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朱大诚（1964-），男，江西永新人，教授，博士研究生导师，学士，研究方向：中医药抗肿瘤。

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朱大诚, 魏佳旭, 徐笑明, 刘燕, 康林之, 何家寰
作者信息
  • 江西中医药大学，江西 南昌 330004
作者简介:

朱大诚（1964-），男，江西永新人，教授，博士研究生导师，学士，研究方向：中医药抗肿瘤。

Reversal Effect and Mechanism of Chonglou（Rhizoma Paridis）on Multidrug Resistance of Leukemia CEM/VCR Cells
Dacheng ZHU, Jiaxu WEI, Xiaoming XU, Yan LIU, Linzhi KANG, Jiahuan HE
Affiliations
  • Jiangxi University of Chinese Medicine，Nanchang 330004，Jiangxi，China
出版时间: 2025-11-10 doi: 10.13193/j.issn.1673-7717.2025.11.001
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摘要
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目的

探究重楼对白血病CEM/VCR细胞多药耐药是否具有逆转作用及其逆转耐药性的机制。

方法

不同浓度重楼作用CEM/VCR细胞72 h并计算死亡率，选择适宜的重楼逆转剂浓度；MTT比色实验计算低、中、高浓度（0.1、0.5、2.5μg/mL）长春新碱（Vincristine，VCR）分别作用于重楼处理细胞（以下统称处理组）及未加重楼处理细胞（以下统称未处理组）24、48、72 h后的抑制率及其半数抑制浓度（IC50），并计算两组间耐药的逆转倍数（Reversal index，RI）；流式细胞术（Flow cytometry，FCM）检测VCR作用于两组细胞后的凋亡率；RT-qPCR、Western blot检测VCR作用于两组细胞后Bax、Bcl-2、Cyt-c、P-gp、MRP1的mRNA和蛋白表达水平。

结果

重楼逆转剂浓度为0.008μg/mL；VCR作用于处理组的抑制率明显大于未处理组（P<0.05或P<0.01），处理组将VCR作用于细胞24、48、72 h的IC50值由17.32、13.85、6.21μg/mL降至15.37、2.25、0.62μg/mL，其逆转倍数分别为1.13、6.16、10.02；流式结果显示，VCR组细胞凋亡率随着药物浓度增加逐渐增大，且相同条件下处理组细胞凋亡率大于未处理组；RT-qPCR、Western blot结果显示，同一时间不同浓度VCR作用下，两组细胞的加药组与对照组比较，均能下调Bcl-2、P-gp、MRP1和上调Bax、Cyt-c基因及蛋白表达（P<0.05），且这种变化处理组更为显著。

结论

重楼可以逆转CEM/VCR细胞的多药耐药性，其可能机制是：①通过下调P-gp、MRP1的表达，降低VCR外排，增加细胞内VCR浓度；②通过下调Bcl-2和上调Bax、Cyt-c的表达，诱导细胞凋亡。

重楼  /  CEM/VCR细胞  /  白血病  /  逆转  /  多药耐药
Objective

To explore whether Chonglou（Rhizoma paridis）has a reversal effect on multidrug resistance of leukemia CEM/VCR and its reversal mechanism.

Methods

CEM/VCR cells were treated with different concentrations of Chonglou（Rhizoma paridis）for 72 hours，and the mortality rate was calculated，and the appropriate concentration of Chonglou（Rhizoma paridis）reversal agent was selected. MTT colorimetric experiment was used to calculate the inhibitory rate and half inhibitory concentration（IC50）of low，medium and high concentrations（0.1，0.5 and 2.5μg/mL）of vincristine（VCR）acting on Chonglou（Rhizoma paridis）treated cells（hereinafter referred to as the treated group）and unweighted Chonglou（Rhizoma paridis）treated cells（hereinafter referred to as the untreated group）for 24，48 and 72 hours respectively，and to calculate the reversal index（RI）and reversal multiple（IC50）between the two groups. Flow cytometry（FCM）was used to detect the apoptosis rate after VCR was applied to the two groups of cells. RT-qPCR and Western blot were used to detect the mRNA and protein expression levels of Bax，Bcl-2，Cyt-c，P-gp and MRP1 after VCR acted on the two groups of cells.

Results

The concentration of Chonglou（Rhizoma paridis）reversal agent was 0.008μg/mL. The inhibition rate of VCR in the treatment group was significantly higher than that in the untreated group（P<0.05 or P<0.01）. The IC50 value of VCR in the treatment group after 24，48 and 72 hours was reduced from 17.32，13.85 and 6.21μg/mL to 15.37，2.25 and 0.62μg/mL，and the reversal multiples were 1.12 respectively. The results of flow cytometry showed that the apoptosis rate of VCR group increased gradually with the increase of drug concentration，and the apoptosis rate of treated group was higher than that of untreated group under the same conditions. The results of RT-qPCR and Western blot showed that the expressions of Bcl-2，P-gp，MRP1-1 and Bax，Cyt-c genes and proteins were down-regulated and up-regulated by VCR with different concentrations at the same time compared with those of the control group（P<0.05），and this change was more significant in the treatment group.

Conclusion

Chonglou（Rhizoma paridis）can reverse the multidrug resistance of CEM/VCR cells，which may be related to down-regulating the expressions of P-gp and MRP1，reducing the efflux of chemotherapeutic drugs and increasing the intracellular concentration of VCR，down-regulating the expression of Bcl-2 and up-regulating the expressions of Bax and Cyt-c，inducing cell apoptosis.

Chonglou（Rhizoma paridis）  /  CEM/VCR cells  /  leukemia  /  reverse  /  multidrug resistance
朱大诚, 魏佳旭, 徐笑明, 刘燕, 康林之, 何家寰. 重楼对白血病CEM/VCR细胞多药耐药的逆转作用及机制研究. 中华中医药学刊, 2025 , 43 (11) : 1 -7 . DOI: 10.13193/j.issn.1673-7717.2025.11.001
Dacheng ZHU, Jiaxu WEI, Xiaoming XU, Yan LIU, Linzhi KANG, Jiahuan HE. Reversal Effect and Mechanism of Chonglou（Rhizoma Paridis）on Multidrug Resistance of Leukemia CEM/VCR Cells[J]. Chinese Archives of Traditional Chinese Medicine, 2025 , 43 (11) : 1 -7 . DOI: 10.13193/j.issn.1673-7717.2025.11.001
正文
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人急性T淋巴细胞白血病（Acute T-lymphocytic leukemia，T-ALL）的治疗主要以化疗为主[1]，但目前白血病化疗失败及复发的主要原因是多药耐药（Multidrug resistance，MDR）所导致的[2]。MDR的发生存在多种机制，主要包括：外排泵异常，如P-糖蛋白（P-glycoprotein，P-gp）及多药耐药相关蛋白（Recombinant multidrug resistance associated protein 1，MRP1）过表达，导致细胞内的有效药物泵出细胞增多，细胞内有效药物浓度降低；控制细胞凋亡相关基因，如Bcl-2、Bax、Cyt-c的异常表达，导致凋亡进程受阻而产生耐药等。
重楼（Rhizoma Paridis）为百合科重楼属植物，入药成分是干燥的根茎，有小毒，功效为清热解毒、凉肝定惊、消肿止痛等[3-4]，研究表明，重楼及其有效成分对抗肿瘤的作用不但范围广而且毒性较小，在体外实验中对多种肿瘤细胞具有细胞毒性作用[5-6]，如卵巢癌[7]、非小细胞癌[8]、结直肠癌[9]、胃癌[10]等，其可能是通过诱导肿瘤细胞的凋亡、逆转肿瘤细胞多药耐药发挥作用。在临床上常将重楼应用于白血病的相关治疗[11]，但目前重楼在抗白血病多药耐药方面的研究相对较少，因此本实验研究重楼是否可以逆转CEM/VCR细胞的多药耐药，并通过体外分子生物学技术等方法研究其机制，为重楼在临床治疗白血病基础上提供理论根据。
1　材料与仪器
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1.1　细胞株
白血病CEM/VCR多药耐药细胞株由本研究室建立[12]，并用0.01μg/mL VCR保持细胞耐药性，实验前1周脱药。
1.2　药品与主要试剂
重楼购自安徽省惠丰国药（产地：云南，批号：190601）；VCR由南京尚书生物有限公司生产（产地：深圳，批号：20190121）；含双抗的RPMI 1640培养基由凯基生物科技公司提供；新生牛血清由Dobio生物有限公司提供；瑞氏-Giemsa染色液由安徽Leagene公司提供；Bcl-2、Bax、Cyt-c、P-gp、MRP1、GAPDH引物由深圳BGI公司提供；Bcl-2、Bax、Cytc、P-gp、MRP1抗体由武汉ABclonal Technology公司提供；Anti-beta Actin antinbody由美国abcam公司提供；化学发光ECL检测试剂盒和BCA蛋白浓度测定试剂盒由康为世纪生物科技公司提供。
1.3　仪器与设备
CO2培养箱（美国Thermo Forma）；酶标仪（Thermo Fisher）；流式细胞分选系统（贝克曼库尔特MoFloXDP）；垂直电泳槽、转移电泳槽、PowerPac TW通用Bio-Rad电泳仪（上海伯乐生命医学有限公司）；凝胶成像系统（美国Protein Simple）；实时荧光定量PCR仪（Thermo Fisher，QuantStudio 5）。
2　方法
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2.1　重楼提取物制备
精密称取重楼50 g，干燥粉碎，350 mL三蒸水混匀浸泡24 h，80℃煎煮3 h，多层纱布粗过滤并收集滤液，滤渣中加入250 mL三蒸水，80℃复煎2次，每次2 h，定性滤纸过滤，合并滤液，80℃旋转蒸发浓缩并干燥，得到重楼水提物粉末。称取0.5 g重楼水提物粉末，加入5 mL三蒸水，溶解后滤过除菌，配制为100 mg/mL母液，于4℃冰箱密封保存。
2.2　VCR溶液配置
称取VCR 1 mg，加入三蒸水4 mL，溶解后滤过除菌，配制成浓度为0.25 mg/mL母液，加入一定比例灭菌三蒸水配制成低、中、高浓度的VCR溶液（2、10、50μg/mL），于4℃冰箱密封保存。
2.3　重楼逆转剂浓度确定
取对数生长期的CEM/VCR细胞悬液，调细胞浓度为1×105/mL，接种于96孔培养板，分3个实验组，每组3个复孔，每孔95μL悬液，培养24 h后，每组加入不同浓度重楼溶液5 μL，使终浓度分别为0.003、0.008、0.01μg/mL，继续培养72 h后，分别进行台盼蓝染色计数，计算得出以上3个浓度重楼作用下细胞死亡率分别为1.64%、4.50%、5.43%，由此选择死亡率低于5%的最高浓度0.008μg/mL作为重楼逆转剂浓度。根据以上结果，取对数生长的CEM/VCR细胞分为两组，一组用0.008μg/mL重楼干预培养1周，中途换液1次，即为处理组；另一组在其他条件相同情况下，用灭菌三蒸水干预，即为未处理组。
2.4　MTT比色实验
将处理组和未处理组细胞的浓度调为1×105/mL，处理组和未处理组各分5组，分别为空白组、对照组、药物组（0.1、0.5、2.5μg/mL VCR），每组5个平行孔，除空白组（加190μL RPMI 1640）外，其余各组用移液枪加对应190μL细胞悬液于96孔板。培养24 h后，空白组每孔加10μL RPMI 1640，对照组加10μL三蒸水，给药组依次加入10μL不同浓度VCR，使终浓度分别为0.1、0.5、2.5μg/mL。继续培养24、48、72 h后，除空白组外，每孔加入20μL MTT，培养箱避光4 h后离心，吸去上清，每孔加150μL二甲基亚砜，使用酶标仪在490 nm波长处检测各孔OD值（吸光度值）。计算抑制率（%）＝（1-实验组OD值/对照组OD值）×100%。采用GraphPad Prism 8.3软件分析，计算24、48、72 h的IC50，RI＝未处理组IC50/处理组IC50。
2.5　流式细胞术
因为细胞凋亡主要发生在细胞死亡进程的早期，所以后续流式细胞术、RT-qPCR、Western blot实验选择24 h和48 h两个时间段进行检测。将两组细胞的密度调为1×105/mL，处理组和未处理组各分4组，分别为对照组、药物组（0.1、0.5、2.5 μg/mL VCR），每组用移液枪加对应950μL细胞悬于24孔板，培养24 h后，对照组加50μL三蒸水，给药组加入不同浓度VCR 50μL，使终浓度为0.1、0.5、2.5μg/mL，继续培养24、48 h后离心收集细胞，PBS（预冷）洗涤，用500μL 1×Binding buffer重悬各组细胞。按照之前调整好的细胞参数，每组加10μL PI和5μL Annexin V-FITC轻柔混匀，25℃避光孵育5 min。流式细胞分选系统检测药物作用于细胞24、48 h后的凋亡率。
2.6　RT-qPCR实验
引物由北京六合生物公司设计与合成，见表1。
将两组细胞的密度调为1×105/mL，用移液枪加对应9.5 mL细胞悬液于6孔板，培养24 h后，对照组加500μL三蒸水，给药组加入不同浓度VCR各500μL，使终浓度为0.1、0.5、2.5μg/mL，继续培养24、48 h后离心收集细胞，按试剂盒操作步骤提取各组RNA；根据cDNA反应体系42℃、15 min，85℃、5 min，温度降至4℃，逆转录得cDNA；按照说明书的扩增条件在PCR仪上完成扩增，使用LightCycler®96软件采集扩增数据，采用2-ΔΔCt法进行定量分析。
2.7　Western blot实验
细胞培养条件和实验分组同实验2.6，加药培养24、48 h后，按试剂盒操作步骤提取各组蛋白后进行蛋白定量分析。制胶后准备好各组蛋白在仪器上电泳，在80 V分离蛋白，恒定电流200 mA转膜1～2 h，1×TBST洗膜，每次10 min，重复3次；用脱脂奶粉（5%）封闭2 h，1×TBST洗膜10 min，重复3次；将已经配好的一抗（1∶800）和内参（1∶2000）加到相对应孵育盒内的PVDF膜上，摇床（4℃）过夜，结束后洗膜10 min，重复3次。转移至二抗（1∶2000）溶液中孵育1 h，孵育后1×TBST洗膜10 min，重复3次。对PVDF膜进行曝光显影，采集并使用Image J读取条带的灰度值，β-actin作为内参，目的蛋白的半定量表达＝目的蛋白灰度值/β-actin灰度值。
2.8　统计学方法
使用SPSS23.0软件统计分析，数据采用单因素方差进行分析，采用均数±标准差（）表示，P<0.05为差异有统计学意义，P<0.01为差异有显著统计学意义。
3　结果
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3.1　VCR对两组细胞生长的影响
MTT实验结果显示，低、中、高浓度VCR作用于两组细胞24、48、72 h的OD值见表2。随着VCR浓度的增加和时间的延长，OD值逐渐降低，抑制率逐渐增大。当药物浓度为0.5 μg/mL，作用48、72 h后，两组细胞与对照组相比差异均有统计学意义（P<0.01），药物浓度达到2.5μg/mL时，抑制作用更为明显。72 h处理组及未处理组抑制率分别高达67.25%、52.37%。相同条件下，处理组细胞抑制率均大于未处理组细胞抑制率。通过GraphPad Prism 8.3软件分析计算出未处理组24、48、72 h IC50值分别为17.32、13.85、6.21μg/mL；处理组分别为15.37、2.25、0.62μg/mL；逆转倍数分别为1.13、6.16、10.02倍。
3.2　流式细胞术检测细胞凋亡率
低、中、高浓度VCR作用于两组细胞后，结果显示：24 h未处理组与处理组相比，对照组凋亡率平均值分别为1.86%、2.02%，VCR低、中、高剂量组凋亡率平均值分别3.98%、4.91%、10.51%；6.32%、15.06%、25.33%，见插页Ⅰ图1；而随着药物作用时间延长至48 h，两组细胞的凋亡率也随之不断增大，未处理组与处理组相比，对照组凋亡率平均值分别为2.59%、2.93%，VCR低、中、高剂量组凋亡率平均值分别6.8%、11.49%、25.55%；21.11%、30.65%、34.74%，见插页Ⅱ图2。相同条件下处理组凋亡率明显大于未处理组，且两组与各自对照组相比差异均具有统计学意义（P<0.05或P<0.01），见图3。
3.3　Bax、Bcl-2、Cyt-c、P-gp、MRP1基因转录情况
3.3.1　Bax、Cyt-c基因转录情况
低、中、高浓度VCR作用于两组细胞24 h后，Bax、Cyt-c基因转录水平随着VCR浓度增大逐渐升高，呈上升趋势，且在0.5、2.5μg/mL浓度时，差异逐渐明显（P<0.05或P<0.01），见图4。当给药时间延长至48 h，Bax、Cyt-c基因转录水平上调更为明显，且差异呈现更加显著的统计学意义（P<0.05或P<0.01）。同等条件下，处理组较未处理组Bax、Cyt-c基因转录水平更高，差异有统计学意义（P<0.05或P<0.01），见图5。
3.3.2　Bcl-2、P-gp、MRP1基因转录情况
低、中、高VCR作用于两组细胞24 h后，Bcl-2、P-gp、MRP1基因转录水平与对照组相比有所降低，呈下降趋势，且在0.5、2.5μg/mL浓度时，与对照组相比，差异逐渐明显（P<0.05或P<0.01），见图6；当给药时间延长至48 h，Bcl-2、P-gp、MRP1基因转录水平下调更为明显，且呈现更加显著的统计学差异（P<0.05或P<0.01），见图7。同等条件下，处理组较未处理组Bcl-2、P-gp、MRP1基因转录水平更低，差异有统计学意义（P<0.05或P<0.01）。
3.4　Bax、Bcl-2、Cyt-c、P-gp、MRP1蛋白表达情况
3.4.1　Bax、Cyt-c蛋白表达情况
Bax、Cyt-c蛋白表达情况见图8、图9，低、中、高浓度VCR作用于两组细胞24 h后，Bax、Cyt-c蛋白的表达随VCR浓度增加逐渐增强，且在0.5、2.5 μg/mL时差异逐渐明显（P<0.05或P<0.01），见图10；当给药时间到达48 h，两组细胞Bax、Cyt-c蛋白表达增强更为明显，在给药浓度到达2.5μg/mL时，差异有统计学意义（P<0.01），见图11，同等条件下，Cyt-c蛋白在低、中、高浓度、Bax蛋白在高浓度时，处理组较未加处理组表达更强，且差异有统计学意义（P<0.05或P<0.01）。
3.4.2　Bcl-2、P-gp、MRP1蛋白的表达情况
Bcl-2、Pgp、MRP1蛋白表达情况见图12、图13，低、中、高浓度VCR作用于两组细胞24 h后，Bcl-2、P-gp、MRP1蛋白的表达随VCR浓度增加逐渐减弱，呈下降趋势，处理组在0.5、2.5μg/mL时差异有统计学意义（P<0.05或P<0.01），而未处理组在2.5μg/mL时差异逐渐明显（P<0.05）（图14）；当给药时间到达48 h，未处理组细胞在0.5、2.5μg/mL时，Bcl-2、Pgp、MRP1蛋白表达减弱更为显著（P<0.05或P<0.01），而处理组在低、中、高浓度下，Bcl-2、P-gp、MRP1蛋白表达均明显减弱（P<0.05或P<0.01）见图15。同等条件下，Bcl-2、Pgp、MRP1蛋白在0.5、2.5μg/mL浓度时，处理组较未处理组表达更弱，且差异有统计学意义（P<0.05或P<0.01）。
4　讨论
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白血病细胞产生MDR是指在治疗白血病过程当中，抗肿瘤药物长时间作用于白血病细胞后，药物对细胞产生的疗效降低，甚至细胞对那些未接触的其他抗肿瘤药物也会产生耐药[13-14]。白血病多药耐药的产生具有异常复杂的分子作用机制，是由多种因素共同参与所致，包括P-gp、MRP1等错误表达介导的药物外排；细胞凋亡水平的异常即Bcl-2等凋亡相关基因的过表达等[15]。
P-gp（多药耐药相关蛋白MDR1编码）在药物外排机制中发挥药物外输泵的作用，它是ABC转运蛋白超家族成员。P-gp表达过强，细胞膜对药物外排能力就会增强，细胞内抗肿瘤药物排出增多，胞内药物浓度降低，从而引起MDR。Pgp和MRP1既为膜转运蛋白，又是能与ATP结合的盒式蛋白的糖蛋白，高表达的MRP1与P-gp发挥相同作用诱发MDR[16]。目前研究发现，多种中药单体、中药复方等可以通过下调P-gp、MRP1表达，进一步逆转白血病多药耐药。王东萍等[17]发现秦巴硒菇提取物联合多柔比星可以上调BAD、下调P-gp、BCL-XL、p-PI3K、p-AKT、p-mTOR等蛋白表达，从而促进K562/ADR细胞凋亡、减少细胞内化疗药物外排而发挥作用。LOPES-RODRIGUESV等[18]研究表明，一种新的姜黄素衍生物可以通过抑制P-gp的表达，将细胞周期阻滞于G2/M期，并诱导MDR慢性髓性白血病细胞系的凋亡。LIN KN等[19]研究表明，葡萄籽原花青素提取物可以在HL-60/ADR细胞中诱导更高的细胞内ADR水平，它还可以抑制Akt磷酸化，导致MRP1、MDR1和LRP的下调，并诱导细胞凋亡。
细胞凋亡水平的异常同样也是肿瘤细胞产生MDR的主要机制之一，Bax、Cyt-c、Caspase家族等促凋亡因子的低表达，Bcl-2、IAP家族、NF-κB等抗凋亡因子高表达等，都可能引起白血病细胞的MDR发生[20]。在细胞对抗凋亡刺激时，Bcl-2发挥着抑制剂的作用。朱大诚等[21]研究发现，中药蟾酥能够下调Bcl-2、上调Bax的表达，诱导细胞凋亡；下调Pgp的表达，减少药物外泵，从而逆转CEM/VCR细胞的耐药性。MISRA R等[22]联合黄色素和阿霉素（Doxorubicin，DOX）并做成小微米粒，作用于K562细胞，发现在姜黄素的作用下，DOX在胞核中停留的时间延长，Bcl-2表达减弱，对K562细胞的毒性增强，逆转其耐药并协同促进细胞凋亡。林婷等[23]将复方君子汤和DOX联合作用于K562/VCR细胞，可下调Bcl-2、上调Bax蛋白的表达达到逆转K562/VCR细胞的多药耐药。
重楼具有良好的抗白血病药理作用，当中的多种化学成分已被鉴定，例如甾体皂苷类、植物甾醇类、胆甾烷醇类、黄酮类、三萜类、多糖等等[24]，活性物质经分析主要是甾体皂苷，其具有治疗肿瘤、抗菌消炎、免疫调节等作用[25]。现有研究发现，重楼皂苷Ⅵ可通过p38 MAPK通路，促进cleaved Caspase-3与Bax蛋白、抑制Bcl-2蛋白表达，诱导THP-1细胞凋亡[26]；陆芹等[27]发现，长柱重楼皂苷作用于白血病HL-60、K562、KG-1和HT-93细胞，通过活化内源性凋亡通路，促进Bax、P53、P27蛋白、抑制Bcl-2蛋白表达，有效抑制白血病细胞增殖。
本实验将低、中、高浓度VCR同时作用于处理组和未处理组细胞。MTT实验结果显示，相同条件下，处理组抑制率大于未处理组，逆转倍数最高达10.02；流式细胞术结果表明，相同条件下，处理组凋亡率明显大于未处理组。以上表明重楼能够使CEM/VCR细胞对VCR敏感性增强，并诱导细胞凋亡，其可能为一种有效的逆转多药耐药的药物。因此，为进一步探讨重楼作为耐药逆转剂逆转耐药的相关通路，采取RT-qPCR、Western blot检测不同浓度VCR作用于两组CEM/VCR细胞24 h、48 h后Bax、Bcl-2、Cyt-c、P-gp、MRP1基因转录及蛋白表达情况。结果显示，同一时间不同浓度，处理组和未处理组与各自对照组相比较，均能下调Bcl-2、P-gp、MRP1和上调Bax与Cyt-c基因与蛋白的表达（P<0.05），且相同作用条件下处理组较未处理组表现更为显著。本实验表明重楼水提物对逆转CEM/VCR细胞多药耐药性的作用明显，但其发挥作用的具体有效成分今后还需进一步深入探讨。
综上所述，本实验结果提示重楼作为耐药逆转剂可能是通过抑制细胞表面P-gp、MRP1作为药物外排泵的表达，降低化疗药物外排，增加CEM/VCR细胞内VCR药物浓度；通过下调Bcl-2，上调Bax表达，使Bcl-2/Bax的比值下降，促进Cyt-C的释放从而诱导细胞凋亡。
基金
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  • 国家自然科学基金项目(81260580)
  • 江西省大学生创新创业训练计划项目(S202010412043)
  • 江西中医药大学中西医结合一级学科（江西省双一流学科）项目(zxyylxk20220103)
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2025年第43卷第11期
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doi: 10.13193/j.issn.1673-7717.2025.11.001
  • 首发时间：2026-10-30
  • 出版时间：2025-11-10
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国家自然科学基金项目(81260580)
江西省大学生创新创业训练计划项目(S202010412043)
江西中医药大学中西医结合一级学科（江西省双一流学科）项目(zxyylxk20220103)
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    江西中医药大学，江西 南昌 330004
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