CircEZH2调节miR-340-5p/PUM1轴对结肠癌细胞奥沙利铂耐药性的影响

doi:10.3877/cma.j.issn.2095-1221.2025.04.002

目的

研究环状Zeste同源蛋白2增强子（CircEZH2）调节miR-340-5p/ Pumilio RNA结合家族成员1 （PUM1）轴对结肠癌细胞奥沙利铂（OXA）耐药性的影响。

方法

体外培养人结肠癌细胞系HCT116并采用浓度梯度法构建OXA耐药细胞株HCT116/OXA，通过RT-qPCR和Western blot检测人结肠癌细胞系HCT116和其OXA耐药细胞系HCT116/OXA中CircEZH2、miR-340-5p、PUM1表达。体外培养HCT116/OXA细胞并分为对照组、OXA组、OXA + CircEZH2阴性对照组、OXA + miR- 340-5p阴性对照组、OXA + CircEZH2敲低组、OXA + CircEZH2敲低+ miR- 340- 5p inhibitor组，分组转染后通过RT-qPCR和Western blot检测细胞CircEZH2、miR-340-5p、PUM1表达；通过CCK-8和流式细胞实验检测细胞增殖凋亡；通过Western blot检测细胞凋亡蛋白（cleaved caspase-3、Bax）与耐药蛋白[乳腺癌耐药蛋白（BCRP）、P-糖蛋白（P-gp）]表达。体外培养HCT116/OXA细胞并分为对照组、CircEZH2敲低组、阴性对照组、CircEZH2敲低+ miR- 340-5p inhibitor组，分组转染后通过CCK-8法检测细胞存活率并计算耐药指数。通过双荧光素酶报告基因实验检测HCT116/OXA细胞CircEZH2对miR- 340- 5p及miR-340- 5p对PUM1的靶向调节。多组间比较行单因素方差分析，进一步两两比较采用SNK-q检验。

结果

与对照组比较，OXA + CircEZH2敲低组细胞活力[（45.84 ± 7.63）%比（100.00 ± 0.00）%]、P-gp蛋白表达（0.31 ± 0.05比0.92 ± 0.20）降低，凋亡率[（57.92 ± 9.84）%比（1.60 ± 0.53）%]升高，差异具有统计学意义（P均< 0.05）。与OXA组比较，OXA + CircEZH2敲低组细胞活力[（45.84 ± 7.63）%比（93.46 ± 16.75）%]、P-gp蛋白表达（0.31 ± 0.05比0.78 ± 0.18）降低，凋亡率[（57.92 ± 9.84）%比（2.74 ± 0.81）%]升高，差异具有统计学意义（P均< 0.05）。与OXA + CircEZH2敲低组比较，OXA + CircEZH2敲低+ miR- 340-5p inhibitor组细胞活力[（85.79 ± 18.93）%比（45.84 ±7.63）%]、P-gp蛋白表达（0.73 ± 0.11比0.31 ± 0.05）升高，凋亡率[（3.93 ± 1.22）%比（57.92 ± 9.84）%]降低，差异具有统计学意义（P均< 0.05）。与对照组比较，CircEZH2敲低组细胞耐药指数（1.08 ± 0.15比3.19 ± 0.30）降低，差异具有统计学意义（P < 0.05）；与CircEZH2敲低组比较，CircEZH2敲低+ miR-340- 5p inhibitor组细胞耐药指数（3.06 ± 0.19比1.08 ± 0.15）升高，差异具有统计学意义（P < 0.05）。CircEZH2可靶向下调HCT116/OXA细胞miR-340-5p表达，且miR-340-5p可靶向下调其PUM1表达。

结论

敲低CircEZH2可通过上调miR-340-5p而下调PUM1表达，从而减轻结肠癌细胞OXA耐药性，增强OXA对结肠癌细胞的杀伤力并诱导OXA处理下的HCT116/OXA细胞凋亡。

关键词: CircEZH2, miR-340-5p, PUM1, 结肠癌, 奥沙利铂, 耐药性

Objective

To study the effect of circular enhancer of zeste homolog 2 (CircEZH2) on oxaliplatin (OXA) resistance in colon cancer cells by regulating the miR-340-5p/Pumilio RNA binding family member 1 (PUM1) axis.

Methods

Human colon cancer cell line HCT116 was cultured in vitro and its OXA resistant cell line HCT116/OXA was constructed using concentration gradient method. RT-qPCR and Western blot were applied to detect the expression of CircEZH2, miR-340-5p, and PUM1 in human colon cancer cell line HCT116 and its OXA resistant cell line HCT116/OXA. HCT116/OXA cells were cultured in vitro and randomly grouped into control group, OXA group, OXA+CircEZH2 negative control group, OXA+miR-340-5p negative control group, OXA+CircEZH2 knockdown group, and OXA+ CircEZH2 knockdown + miR-340- 5p inhibitor group. RT-qPCR and Western blot were applied to detect the expression of CircEZH2, miR- 340-5p, and PUM1 of cells in each group. CCK-8 assay and flow cytometry were applied to detect cell proliferation and apoptosis in each group. Western blot was applied to detect the expression of apoptotic proteins (Cleaved Caspase-3, Bax) and drug resistant proteins [breast cancer resistance protein (BCRP), P-glycoprotein (P-gp) ] in each group. HCT116/OXA cells were cultured in vitro and randomlydivided into control group, CircEZH2 knockdown group, negative control group, and CircEZH2 knockdown+miR-340-5p inhibitor group, CCK-8 assay was applied to detect the survival rate of cells in each group and calculating their drug resistance index. The double luciferase reporter gene experiment was applied to detect the targeted regulation of CircEZH2 on miR-340-5p and miR-340-5p on PUM1 in HCT116/OXA cells. One-way ANOVA was used for comparison between multiple groups, and SNK-q test was used for comparison between pairwise groups.

Results

Compared with control group, cell viability[ (45.84 ± 7.63) % vs (100.00 ± 0.00) %] and the expression of P-gp protein (0.31 ± 0.05 vs 0.92 ± 0.20) in the OXA+CircEZH2 knockdown group were decreased, while the apoptosis rate [ (57.92 ± 9.84) % vs (1.60 ± 0.53) %] was increased (all P < 0.05). Compared with the OXA group, cell viability [ (45.84 ± 7.63) % vs (93.46 ± 16.75) %] and the expression of P-gp protein (0.31 ± 0.05 vs 0.78 ± 0.18) in the OXA+CircEZH2 knockdown group were decreased, while the apoptosis rate [ (57.92 ± 9.84) % vs (2.74 ± 0.81) %] was increased (all P < 0.05). Compared with the OXA+CircEZH2 knockdown group, cell viability [ (85.79 ± 18.93 ) % vs (45.84 ± 7.63) %] and the expression of P-gp protein (0.73 ± 0.11 vs 0.31 ± 0.05) in the the OXA+CircEZH2 knockdown+miR-340-5p inhibitor group were increased, while the apoptosis rate [ (3.93 ± 1.22) % vs (57.92 ± 9.84) %] was decreaseds (all P < 0.05). Compared with the control group, the drug resistance index (1.08 ± 0.15 vs 3.19 ± 0.30) of the CircEZH2 knockdown group was decreased significantly (P < 0.05). Compared with the CircEZH2 knockdown group, the drug resistance index (3.06 ± 0.19 vs 1.08 ± 0.15) of the CircEZH2 knockdown+miR-340-5p inhibitor group was increased signiticantly (P < 0.05). CircEZH2 was able to target and down-regulation the expression of miR-340-5p in HCT116/OXA cells, and miR-340- 5p could target and down-regulation the expression of PUM1.

Conclusion

Knocking down CircEZH2 can down-regulate PUM1 expression by up-regulating miR-340-5p, reducing OXA resistance in colon cancer cells, enhancing the killing power of OXA on colon cancer cells, and inducing apoptosis of HCT116/OXA cells under OXA treatment.

Key words: CircEZH2, miR-340-5p, PUM1, Colon cancer, Oxaliplatin, Resistance

表1 基因引物序列

基因	序列（5'→3'）	预期扩增产物长度（bp）
CircEZH2	上游AACCAAGAATGGAAACAGCGAAGG	132
	下游AGTCGCATGTACTCTGATTTT
PUM1	上游TGAGTTTATTCCTTCAGACCAGCAG	137
	下游GCAAATACCTGTCCCTTAAACGCA
GAPDH	上游AATGGATTTGGACGCATTGGT	120
	下游TTTGCACTGGTACGTGTTGAT
miR-340-5p	上游GCGGTTATAAAGCAATGAGA	181
	下游GTGCGTGTCGTGGAGTCG
U6	上游GCTTCGGCAGCACATATACTAAAAT	140
	下游GGAAGAAGCAGGAGATTTGG

表1 基因引物序列

基因	序列（5'→3'）	预期扩增产物长度（bp）
CircEZH2	上游AACCAAGAATGGAAACAGCGAAGG	132
	下游AGTCGCATGTACTCTGATTTT
PUM1	上游TGAGTTTATTCCTTCAGACCAGCAG	137
	下游GCAAATACCTGTCCCTTAAACGCA
GAPDH	上游AATGGATTTGGACGCATTGGT	120
	下游TTTGCACTGGTACGTGTTGAT
miR-340-5p	上游GCGGTTATAAAGCAATGAGA	181
	下游GTGCGTGTCGTGGAGTCG
U6	上游GCTTCGGCAGCACATATACTAAAAT	140
	下游GGAAGAAGCAGGAGATTTGG

表2 miR-340-5p、CircEZH2、PUM1 mRNA与蛋白相对表达水平（

± s，n = 6）

分组	CircEZH2	miR-340-5p	PUM1 mRNA	PUM1蛋白
NCM460细胞	0.98±0.20	1.01±0.12	1.00±0.15	0.34±0.05
HCT116细胞	1.87±0.16^a	0.47±0.07^a	1.83±0.20^a	0.75±0.06^a
HCT116/OXA细胞	2.54±0.23^b	0.16±0.04^b	2.59±0.22^b	1.17±0.11^b
F值	93.028	159.359	102.649	170.341
P值	< 0.001	< 0.001	< 0.001	< 0.001

表2 miR-340-5p、CircEZH2、PUM1 mRNA与蛋白相对表达水平（

± s，n = 6）

分组	CircEZH2	miR-340-5p	PUM1 mRNA	PUM1蛋白
NCM460细胞	0.98±0.20	1.01±0.12	1.00±0.15	0.34±0.05
HCT116细胞	1.87±0.16^a	0.47±0.07^a	1.83±0.20^a	0.75±0.06^a
HCT116/OXA细胞	2.54±0.23^b	0.16±0.04^b	2.59±0.22^b	1.17±0.11^b
F值	93.028	159.359	102.649	170.341
P值	< 0.001	< 0.001	< 0.001	< 0.001

图1 Western blot检测HCT116和HCT116/OXA细胞PUM1表达

表3 HCT116/OXA细胞的miR-340-5p、CircEZH2、PUM1 mRNA与蛋白相对表达水平（

± s，n = 6）

分组	CircEZH2	miR-340-5p	PUM1 mRNA	PUM1蛋白
对照组	0.97 ± 0.24	1.01 ± 0.17	1.02 ± 0.20	0.79 ± 0.10
OXA组	1.05 ± 0.19	0.93 ± 0.15	1.10 ± 0.17	0.82 ± 0.13
OXA+ CircEZH2阴性对照组	1.04 ± 0.25	0.94 ± 0.21	1.12 ± 0.20	0.81 ± 0.15
OXA+ CircEZH2敲低组	0.27 ± 0.04	2.10 ± 0.26^ab	0.36 ± 0.06^ab	0.22 ± 0.03^ab
OXA+ CircEZH2敲低+ miR-340-5p阴性对照组	0.23 ± 0.06	2.12 ± 0.20	0.38 ± 0.07	0.23 ± 0.04
OXA+ CircEZH2敲低+ miR-340-5p inhibitor组	0.28 ± 0.05	0.97 ± 0.18^cd	1.05 ± 0.15^cd	0.77 ± 0.14^cd
F值	38.289	53.801	34.198	44.160
P值	< 0.001	< 0.001	< 0.001	< 0.001

表3 HCT116/OXA细胞的miR-340-5p、CircEZH2、PUM1 mRNA与蛋白相对表达水平（

± s，n = 6）

分组	CircEZH2	miR-340-5p	PUM1 mRNA	PUM1蛋白
对照组	0.97 ± 0.24	1.01 ± 0.17	1.02 ± 0.20	0.79 ± 0.10
OXA组	1.05 ± 0.19	0.93 ± 0.15	1.10 ± 0.17	0.82 ± 0.13
OXA+ CircEZH2阴性对照组	1.04 ± 0.25	0.94 ± 0.21	1.12 ± 0.20	0.81 ± 0.15
OXA+ CircEZH2敲低组	0.27 ± 0.04	2.10 ± 0.26^ab	0.36 ± 0.06^ab	0.22 ± 0.03^ab
OXA+ CircEZH2敲低+ miR-340-5p阴性对照组	0.23 ± 0.06	2.12 ± 0.20	0.38 ± 0.07	0.23 ± 0.04
OXA+ CircEZH2敲低+ miR-340-5p inhibitor组	0.28 ± 0.05	0.97 ± 0.18^cd	1.05 ± 0.15^cd	0.77 ± 0.14^cd
F值	38.289	53.801	34.198	44.160
P值	< 0.001	< 0.001	< 0.001	< 0.001

图2 Western blot检测HCT116/OXA细胞PUM1表达

表4 HCT116/OXA细胞的活力、凋亡率的比较（

± s，n = 6）

分组	细胞活力（%）	凋亡率（%）
对照组	100.00 ± 0.00	1.60 ± 0.53
OXA组	93.46 ± 16.75	2.74 ± 0.81
OXA+CircEZH2阴性对照组	95.62 ± 18.73	2.47 ± 0.69
OXA+CircEZH2敲低组	45.84 ± 7.63^ab	57.92 ± 9.84^ab
OXA+CircEZH2敲低+ miR-340-5p阴性对照组	47.05 ± 7.52	56.56 ± 8.75
OXA+CircEZH2敲低+ miR-340-5p inhibitor组	85.79 ± 18.93^cd	3.93 ± 1.22^cd
F值	20.119	162.225
P值	< 0.001	< 0.001

表4 HCT116/OXA细胞的活力、凋亡率的比较（

± s，n = 6）

分组	细胞活力（%）	凋亡率（%）
对照组	100.00 ± 0.00	1.60 ± 0.53
OXA组	93.46 ± 16.75	2.74 ± 0.81
OXA+CircEZH2阴性对照组	95.62 ± 18.73	2.47 ± 0.69
OXA+CircEZH2敲低组	45.84 ± 7.63^ab	57.92 ± 9.84^ab
OXA+CircEZH2敲低+ miR-340-5p阴性对照组	47.05 ± 7.52	56.56 ± 8.75
OXA+CircEZH2敲低+ miR-340-5p inhibitor组	85.79 ± 18.93^cd	3.93 ± 1.22^cd
F值	20.119	162.225
P值	< 0.001	< 0.001

图3 流式细胞实验检测HCT116/OXA细胞凋亡

表5 HCT116/OXA细胞的凋亡与耐药蛋白相对表达（

± s，n=6）

分组	cleaved caspase-3	Bax	BCRP	P-gp
对照组	0.37 ± 0.04	0.50 ± 0.08	0.85 ± 0.15	0.92 ± 0.20
OXA组	0.40 ± 0.06	0.53 ± 0.09	0.81 ± 0.16	0.78 ± 0.18
OXA+CircEZH2阴性对照组	0.39 ± 0.07	0.53 ± 0.11	0.83 ± 0.14	0.77 ± 0.16
OXA+CircEZH2敲低组	0.94 ± 0.16^ab	1.07 ± 0.19^ab	0.28 ± 0.04^ab	0.31 ± 0.05^ab
OXA+CircEZH2敲低+miR-340-5p阴性对照组	0.98 ± 0.15	1.04 ± 0.10	0.30 ± 0.03	0.33 ± 0.05
OXA+CircEZH2敲低+miR-340-5p inhibitor组	0.44 ± 0.07^cd	0.57 ± 0.11^cd	0.76 ± 0.17^cd	0.73 ± 0.11^cd
F值	48.099	31.155	26.786	20.518
P值	< 0.001	< 0.001	< 0.001	< 0.001

表5 HCT116/OXA细胞的凋亡与耐药蛋白相对表达（

± s，n=6）

分组	cleaved caspase-3	Bax	BCRP	P-gp
对照组	0.37 ± 0.04	0.50 ± 0.08	0.85 ± 0.15	0.92 ± 0.20
OXA组	0.40 ± 0.06	0.53 ± 0.09	0.81 ± 0.16	0.78 ± 0.18
OXA+CircEZH2阴性对照组	0.39 ± 0.07	0.53 ± 0.11	0.83 ± 0.14	0.77 ± 0.16
OXA+CircEZH2敲低组	0.94 ± 0.16^ab	1.07 ± 0.19^ab	0.28 ± 0.04^ab	0.31 ± 0.05^ab
OXA+CircEZH2敲低+miR-340-5p阴性对照组	0.98 ± 0.15	1.04 ± 0.10	0.30 ± 0.03	0.33 ± 0.05
OXA+CircEZH2敲低+miR-340-5p inhibitor组	0.44 ± 0.07^cd	0.57 ± 0.11^cd	0.76 ± 0.17^cd	0.73 ± 0.11^cd
F值	48.099	31.155	26.786	20.518
P值	< 0.001	< 0.001	< 0.001	< 0.001

图4 Western blot检测HCT116/OXA细胞的凋亡与耐药蛋白表达注：1为对照组，2为OXA组，3为OXA+CircEZH2阴性对照组，4为OXA+CircEZH2敲低组，5为OXA+CircEZH2敲低+miR-340-5p阴性对照组，6为OXA+CircEZH2敲低+miR-340-5p inhibitor组

图5 不同浓度OXA对HCT116细胞和各组HCT116/OXA细胞存活率的影响

表6 HCT116/OXA细胞相对荧光素酶活性值（n = 6，

± s）

分组	CircEZH2过表达	CircEZH2空载
miR-340-5p突变	1.00 ± 0.22	1.03 ± 0.26
miR-340-5p野生	0.29 ± 0.06^a	1.02 ± 0.27
t值	7.627	0.065
P值	< 0.001	0.949

表6 HCT116/OXA细胞相对荧光素酶活性值（n = 6，

± s）

分组	CircEZH2过表达	CircEZH2空载
miR-340-5p突变	1.00 ± 0.22	1.03 ± 0.26
miR-340-5p野生	0.29 ± 0.06^a	1.02 ± 0.27
t值	7.627	0.065
P值	< 0.001	0.949

图6 查询Starbase数据库所得CircEZH2与miR-340-5p间的结合位点

表7 HCT116/OXA细胞相对荧光素酶活性值（n = 6，

± s）

分组	miR-340-5p mimics	miR-340-5p mimics阴性对照
PUM1突变	1.03 ± 0.19	1.00 ± 0.28
PUM1野生	0.27 ± 0.03^a	0.99 ± 0.20
t值	9.678	0.071
P值	< 0.001	0.945

表7 HCT116/OXA细胞相对荧光素酶活性值（n = 6，

± s）

分组	miR-340-5p mimics	miR-340-5p mimics阴性对照
PUM1突变	1.03 ± 0.19	1.00 ± 0.28
PUM1野生	0.27 ± 0.03^a	0.99 ± 0.20
t值	9.678	0.071
P值	< 0.001	0.945

图7 查询Starbase数据库所得miR-340-5p与PUM1间的结合位点

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The effect of CircEZH2 on oxaliplatin resistance in colon cancer cells by regulating the miR- 340- 5p/PUM1 axis

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The effect of CircEZH2 on oxaliplatin resistance in colon cancer cells by regulating the miR- 340- 5p/PUM1 axis