去氢骆驼蓬碱联合rad51抑制剂对细粒棘球蚴体外作用及DNA损伤水平的影响

doi:10.12140/j.issn.1000-7423.2024.06.006

中国寄生虫学与寄生虫病杂志 ›› 2024, Vol. 42 ›› Issue (6): 726-736.doi: 10.12140/j.issn.1000-7423.2024.06.006

去氢骆驼蓬碱联合rad51抑制剂对细粒棘球蚴体外作用及DNA损伤水平的影响

巩月红¹^,²^,³(), 潘美驰⁴, 孙佳佳⁵, 马瑞佳⁶, 吾斯曼江·艾买提⁷, 赵一聪⁴, 赵军¹^,²^,³, 王建华¹^,²^,³^,^*()

1 新疆医科大学第一附属医院药学部，新疆乌鲁木齐 830011
2 新疆医科大学省部共建中亚高发病成因与防治国家重点实验室，新疆乌鲁木齐 830011
3 新疆药物临床研究重点实验室，新疆乌鲁木齐 830011
4 新疆医科大学药学院，新疆乌鲁木齐 830054
5 新疆医科大学临床医学部，新疆乌鲁木齐 830054
6 新疆医科大学第七附属医院药学部，新疆乌鲁木齐 830092
7 新疆喀什地区第二人民医院药学部，新疆喀什 844000

收稿日期:2024-05-22 修回日期:2024-07-19 出版日期:2024-12-30 发布日期:2025-01-14
通讯作者: *王建华（1964—），女，研究生，主任药师。从事抗棘球蚴病新药与作用机制研究。E-mail：jhw716@163.com
作者简介:巩月红（1976—），女，研究生，副主任药师。从事抗棘球蚴病新药与作用机制研究。E-mail：gongyh0602@126.com
基金资助:
新疆维吾尔自治区科学技术厅自然科学基金重点项目(2021D01D15);新疆维吾尔自治区天山英才青年骨干项目(TSYC202301B095);省部共建国家重点实验室开放课题(SKL-HIDCA-2022-9)

Effect of harmine combined with rad51 inhibitor on the Echinococcus granulosus larvae and its DNA damage in vitro

GONG Yuehong¹^,²^,³(), PAN Meichi⁴, SUN Jiajia⁵, MA Ruijia⁶, WUSMANJIANG Aimaiti⁷, ZHAO Yicong⁴, ZHAO Jun¹^,²^,³, WANG Jianhua¹^,²^,³^,^*()

1 Department of Pharmacy, The First Affiliated Hospital of Xinjiang Medical University, Urumqi 830011, Xinjiang, China
2 State Key Laboratory of Causes and Prevention of High Morbidity in Central Asia, Xinjiang Medical University, Urumqi 830011, Xinjiang, China
3 Xinjiang Key Laboratory of Clinical Drug Research, Urumqi 830011, Xinjiang, China
4 Department of Pharmacognosy, School of Pharmacy, Xinjiang Medical University, Urumqi 830054, Xinjiang, China
5 Department of Medicine, School of Pharmacy, Xinjiang Medical University, Urumqi 830054, Xinjiang, China
6 Department of Pharmacy, The Seventh Affiliated Hospital of Xinjiang Medical University,Urumqi 830092, Xinjiang, China
7 Department of Pharmacy, The Second People’s Hospital of Kashgar, Xinjiang, Kashi 844000, Xinjiang, China

Received:2024-05-22 Revised:2024-07-19 Online:2024-12-30 Published:2025-01-14
Contact: *E-mail: jhw716@163.com
Supported by:
Natural Science Foundation of Xinjiang Uygur Autonomous Region(2021D01D15);“Tianshan Talents” Program for Training High-level Talents in Medicine and Healthcare(TSYC202301B095);State Key Laboratory of Pathogenesis, Prevention and Treatment of Central Asia High Incidence Diseases fund(SKL-HIDCA-2022-9)

摘要/Abstract

摘要：

目的探讨去氢骆驼蓬碱联合rad51抑制剂（RI-1）对细粒棘球蚴体外作用及DNA损伤水平的影响。方法从绵羊肝脏的棘球蚴包囊中收集细粒棘球蚴，随机分组，各组分别用去氢骆驼蓬碱（0、20、30、40、50、100 μg/ml）与RI-1（0、5、10、20、40、80 μg/ml）培养5 d，0.1%亚甲基蓝染色计算存活率，选择接近去氢骆驼蓬碱抗细粒棘球蚴半抑制浓度组别的浓度为固定浓度，分别以去氢骆驼蓬碱与RI-1比例分别为40∶5、40∶10、40∶20的混合药物干预细粒棘球蚴，筛选最佳协同比例。设置去氢骆驼蓬碱和RI-1混合药物组，同浓度单独作用的去氢骆驼蓬碱组和RI-1组，并设置阳性对照组（添加阿苯达唑亚砜）与空白对照组，观察干预3 d后细粒棘球蚴与囊泡形态。DCFH-DA法检测各组干预后细粒棘球蚴活性氧含量；各组进行彗星实验（阳性对照为阿霉素），分析并测定Olive尾矩；试剂盒检测药物干预后细粒棘球蚴氧化应激水平及Caspase-3含量，以及三磷酸腺苷（ATP）和乳酸脱氢酶（LDH）含量；qRT-PCR反应检测DNA损伤修复相关基因的mRNA相对表达水平。结果 0、20、30、40、50、100 μg/ml的去氢骆驼蓬碱干预5 d后细粒棘球蚴存活率分别为（94.67 ± 1.25）%、（83.00 ± 3.27）%、（64.67 ± 3.86）%、（55.33 ± 3.40）%、（29.67 ± 2.49）%、（9.33 ± 1.70）%，0、5、10、20、40、80 μg/ml的RI-1干预5 d后细粒棘球蚴存活率分别为（94.33 ± 0.94）%、（70.00 ± 2.94）%、（55.67 ± 3.86）%、（30.00 ± 5.09）%、（2.67 ± 1.25）%、0。以40 μg/ml∶10 μg/ml作为混合药物最佳协同比例干预细粒棘球蚴3 d后，混合药物组存活率为（48.67 ± 2.62）%，与空白对照组[（96.33 ± 1.25）%]、阳性对照组[（91.67 ± 1.25）%]、去氢骆驼蓬碱组[（72.67 ± 4.50）%]相比均下降（F = 78.85，P < 0.01；F = 437.92, P < 0.05；F = 42.49，P < 0.01）。混合药物组虫体结构塌陷，形态破坏严重，虫体显著缩小且表皮层呈现虫蚀样改变。混合药物组活性氧平均荧光强度（45.71 ± 1.52）与空白对照组（3.40 ± 0.55）、阳性对照组（12.98 ± 0.67）、去氢骆驼蓬碱组（39.79 ± 1.11）相比均增强（F = 339.795、773.96、76.99，均P < 0.01）。混合药物组Olive尾矩值（17.73 ± 1.11）高于空白对照组（0.03 ± 0.02）、阳性对照组（6.46 ± 0.56）和去氢骆驼蓬碱组（8.80 ± 0.61）（F = 230.32、165.59、151.44，均P < 0.01）。混合药物组总超氧化物歧化酶（SOD）含量为（0.71 ± 0.07）U/mg，与空白对照组[（2.32 ± 0.24）U/mg]、去氢骆驼蓬碱组[（1.26 ± 0.12）U/mg]相比均降低（F = 39.57、 15.74，均P < 0.01）；混合药物组丙二醛（MDA）含量为（0.62 ± 0.03）mmol/mg，与空白对照组[（0.82 ± 0.05）mmol/mg]、去氢骆驼蓬碱组[（0.70 ± 0.03）mmol/mg]相比均降低（F = 22.78、28.37，P < 0.01）；混合药物组Caspase-3水平为（1.82 ± 0.05）U/mg，与空白对照组[（0.70 ± 0.02）U/mg]、去氢骆驼蓬碱组为[（1.36 ± 0.19）U/mg]相比均升高（F = 26.24，P < 0.01；F = 7.52，P < 0.05）。混合药物组细粒棘球蚴线粒体ATP水平为（112.21 ± 2.72）µmol/ml，与空白对照组[（157.50 ± 5.23）µmol/ml]、去氢骆驼蓬碱组[（123.10 ± 4.73）µmol/ml]相比均降低（F = 60.73，P < 0.01；F = 67.42，P < 0.05）。混合药物组细粒棘球蚴LDH释放量为（1.83 ± 0.09）mU，与空白对照组[（0.70 ± 0.05）mU]相比升高（F = 146.79，P < 0.01），与去氢骆驼蓬碱组[（1.51 ± 0.05）mU]相比差异无统计学意义（F = 62.78，P > 0.05）。混合药物组细粒棘球蚴h2ax、rad51、brca1、mre11基因相对表达水平分别为2.34 ± 0.15、1.19 ± 0.14、1.35 ± 0.08、1.43 ± 0.10，与空白对照组（均为1.00 ± 0.00）相比均上调（F = 23.79，P < 0.01；F = 8.96，P < 0.05；F = 30.75，P < 0.05；F = 39.81，P < 0.01）。结论去氢骆驼蓬碱联合rad51抑制剂RI-1可增强去氢骆驼蓬碱体外抗细粒棘球蚴的作用，同时增强细粒棘球蚴DNA损伤。

关键词: 细粒棘球蚴, 去氢骆驼蓬碱, rad51抑制剂, 存活率, DNA损伤

Abstract:

Objective To investigate the effect of harmine combined with rad51 inhibitor (RI-1) on Echinococcus granulosus in vitro and the level of DNA damage. Methods E. granulosus from the cysts of sheep liver were collected and randomly divided into groups. Each group contains a mixture of harmine (0, 20, 30, 40, 50, 100 μg/ml) and RI-1 (0, 5, 10, 20, 40, 80 μg/ml), cultured for 5 days, and stained with 0.1% methylene blue to calculate the survival rate. The group which is close to the half inhibitory concentration of harmine against E. granulosus was selected as the fixed concentration. The groups were treated against E. granulosus with a mixture of harmine and RI-1 in ratios of 40∶5, 40∶10 and 40∶20, respectively. The optimal synergistic ratio was screened. Set up a mixed drug group of harmine and RI-1, a harmine group and RI-1 group acting alone at the same concentration, and set up a positive control group (adding albendazole sulfoxide) and a blank control group. Observe the morphology of E. granulosus and vesicles after 3 days of intervention. DCFH-DA method was used to detect the reactive oxygen species content of E. granulosus after intervention in each group. Each group underwent comet assay (the positive control was doxorubicin), and the Olive tail moment was analyzed and measured. The reagent kit is used to detect the oxidative stress level and Caspase-3 content of E. granulosus after drug intervention, as well as the levels of adenosine triphosphate (ATP) and lactate dehydrogenase (LDH). qRT-PCR reaction is used to detect the mRNA expression levels of DNA damage repair related genes. Results The survival rates of E. granulosus after 5 days of intervention with 0, 20, 30, 40, 50 and 100 μg/ml harmine were (94.67 ± 1.25)%, (83.00 ± 3.27)%, (64.67 ± 3.86)%, (55.33 ± 3.40)%, (29.67 ± 2.49)%, and (9.33 ± 1.70)%, respectively. The survival rates of E. granulosus after 5 days of intervention with 0, 5, 10, 20, 40 and 80 μg/ml RI were (94.33 ± 0.94)%, (70.00 ± 2.94)%, (55.67 ± 3.86)%, and (30.00 ± 1.70)%, 5.09%, (2.67 ± 1.25)% and 0, respectively. After 3 days of intervention with a mixed drug ratio of 40 μg/ml∶10 μg/ml as the optimal synergistic ratio for E. granulosus, the survival rate of the mixed drug group was (48.67 ± 2.62)%, which was lower than that of the blank control group [(96.33 ± 1.25)%], positive control group [(91.67 ± 1.25)%], and harmine group [(72.67 ± 4.50)%] (F = 78.85, P < 0.01; F = 437.92, P < 0.05; F = 42.49, P < 0.01). The structure of the mixed drug group’s worm body collapsed, with severe morphological damage, significant shrinkage of the worm body, and insect like changes in the epidermal layer. The average fluorescence intensity of reactive oxygen species in the mixed drug group (45.71 ± 1.52) was enhanced compared with the blank control group (3.40 ± 0.55), the positive control group (12.98 ± 0.67), and the dehydroberberine group (39.79 ± 1.11) (F = 339.795, 773.96, 76.99, all P < 0.01). The Olive tail moment value of the mixed drug group (17.73 ± 1.11) was higher than that of the blank control group (0.03 ± 0.02), positive control group (6.46 ± 0.56), and dehydrocamel base group (8.80 ± 0.61) (F = 230.32, 165.59, 151.44, all P < 0.01). The SOD content in the mixed drug group was (0.71 ± 0.07) U/mg, which was lower than that in the blank control group [(2.32 ± 0.24) U/mg] and the dehydroberberine group [(1.26 ± 0.12) U/mg] (F = 39.57, 15.74, both P < 0.01). The MDA content in the mixed drug group was (0.62 ± 0.03) mmol/mg, which was lower than that in the blank control group [(0.82 ± 0.05) mmol/mg] and the dehydroberberine group [(0.70 ± 0.03) mmol/mg] (F = 22.78, 28.37, P < 0.01). The level of Caspase-3 in the mixed drug group was (1.82 ± 0.05) U/mg, which was higher than that in the blank control group [(0.70 ± 0.02) U/mg] and the dehydroberberine group [(1.36 ± 0.19) U/mg] (F = 26.24, P < 0.01; F = 7.52, P < 0.05). The mitochondrial ATP level of E. granulosus in the mixed drug group was (112.21 ± 2.72) µmol/ml, which was lower than that of the blank control group [(157.50 ± 5.23) µmol/ml] and the dehydrocoumarin group [(123.10 ± 4.73) µmol/ml] (F = 60.73, P < 0.01; F = 67.42, P < 0.05). The release of LDH from E. granulosus in the mixed drug group was (1.83 ± 0.09) mU, which was higher than that in the blank control group [(0.70 ± 0.05) mU] (F = 146.79, P < 0.01), but there was no statistically significant difference compared with the dehydrocoumarin group [(1.51 ± 0.05) mU] (F = 62.78, P > 0.05). The relative expression levels of h2ax, rad51, brca1 and mrel1 genes in the mixed drug group of E. granulosus were 2.34 ± 0.15, 1.19 ± 0.14, 1.35 ± 0.08, and 1.43 ± 0.10, respectively, which were upregulated compared with the blank control group (all 1.00 ± 0.00) (F = 23.79, P < 0.01; F = 8.96, P < 0.05; F = 30.75, P < 0.05; F = 39.81, P < 0.01). Conclusion The combination of harmine and rad51 inhibitor RI-1 can enhance the in vitro efficacy of harmine against E. granulosus, while also increasing DNA damage in E. granulosus.

Key words: Echinococcus granulosus, Harmine, rad51 inhibitor, Survival, DNA damage

中图分类号:

R383.3

巩月红, 潘美驰, 孙佳佳, 马瑞佳, 吾斯曼江·艾买提, 赵一聪, 赵军, 王建华. 去氢骆驼蓬碱联合rad51抑制剂对细粒棘球蚴体外作用及DNA损伤水平的影响[J]. 中国寄生虫学与寄生虫病杂志, 2024, 42(6): 726-736.

GONG Yuehong, PAN Meichi, SUN Jiajia, MA Ruijia, WUSMANJIANG Aimaiti, ZHAO Yicong, ZHAO Jun, WANG Jianhua. Effect of harmine combined with rad51 inhibitor on the Echinococcus granulosus larvae and its DNA damage in vitro[J]. Chinese Journal of Parasitology and Parasitic Diseases, 2024, 42(6): 726-736.

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名称 Name	序列（5'→3'） Sequences（5'→3'）
mre11	F：GAGTTCCAAGCAGTGACCAGTCTG
mre11	R：CCACTCGGCTGACGCAATCG
brca1	F：TGATTGCGACCTAAGAGAC
brca1	R：TTCCATACACAAGCCATCC
h2ax	F：TTTGGCTTCACGGCTGGCTATG
h2ax	R：TGAGTTTGCTGGAAGGGAAATGGG
rad51	F：GGCACTGATGGTGGCAATCTCC
rad51	R：CAGAAGATCCGCTCCACTTATCGC
β-actin	F：GCGATGTATGTAGCTATCCAGGCAGTGCTCTCGCT
β-actin	R：CAATCCAGACAGAGTATTTGCGTTCCGGAGGA

组别 Group	ATP/µmol·mg^-1	LDH/mU
空白对照组 Blank control group	157.50 ± 5.23	0.70 ± 0.05
去氢骆驼蓬碱组 Harmine group	123.10 ± 4.73	1.51 ± 0.05
RI-1组 RI-1 group	149.94 ± 1.94	1.16 ± 0.02
混合药物组 Mixed drug group	112.21 ± 2.72	1.83 ± 0.09

去氢骆驼蓬碱联合rad51抑制剂对细粒棘球蚴体外作用及DNA损伤水平的影响

Effect of harmine combined with rad51 inhibitor on the Echinococcus granulosus larvae and its DNA damage in vitro

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