没食子酸与氯硝柳胺联合灭螺作用研究

doi:10.12140/j.issn.1000-7423.2024.02.017

中国寄生虫学与寄生虫病杂志 ›› 2024, Vol. 42 ›› Issue (2): 251-258.doi: 10.12140/j.issn.1000-7423.2024.02.017

没食子酸与氯硝柳胺联合灭螺作用研究

郑涛(), 刘佳豪, 李彬, 李佳珊, 聂娟, 熊涛^*()

湖南中医药大学医学院病原生物学教研室，长沙 410006

收稿日期:2023-10-30 修回日期:2023-12-24 出版日期:2024-04-30 发布日期:2024-04-26
通讯作者: * 熊涛（1988—），男，博士，讲师，从事血吸虫宿主生物学与分子生物学研究。E-mail：xiongtao_28@126.com
作者简介:郑涛（2002—），男，本科生，从事血吸虫宿主生物学与分子生物学研究。E-mail：ZhengTao_107@163.com
基金资助:
中国博士后科学基金委面上项目(2021M791078);湖南省自然科学基金青年项目(2022JJ40311);湖南省教育厅科学研究项目青年项目(21B0388);湖南省卫健委科研项目一般项目(202201054363);湖南省中医药管理局科研计划项目青年项目(2021163);湖南中医药大学创新训练项目

Molluscicidal efficacy of gallic acid in combination with niclosamide

ZHENG Tao(), LIU Jiahao, LI Bin, LI Jiashan, NIE Juan, XIONG Tao^*()

Department of Microbiology, School of Medicine, Hunan University of Chinese Medicine

Received:2023-10-30 Revised:2023-12-24 Online:2024-04-30 Published:2024-04-26
Contact: * E-mail: xiongtao_28@126.com
Supported by:
China Postdoctoral Science Foundation Funded Project(2021M791078);Natural Science Foundation of Hunan Province(2022JJ40311);Scientific Research Fund of Hunan Provincial Education Department(21B0388);Scientific Research Fund of Hunan Provincial Health Commission(202201054363);Scientific Research Plan Fund of Hunan Provincial Administration of Traditional Chinese Medicine(2021163);Innovation Training Project Supported by Hunan University of Chinese Medicine

摘要/Abstract

摘要：

目的本研究旨在探讨具有交替氧化酶（AOX）抑制活性的中药单体分子没食子酸和氯硝柳胺的联合灭螺效果及其灭螺机制。方法阴性钉螺采自湖北省公安县，随机分为7组，空白对照组（H₂O），实验组分别为氯硝柳胺（N1组：0.06 mg/L，N2组：0.1 mg/L）和没食子酸（G1组：0.8 g/L，G2组：1.6 g/L）单独使用，及联合使用（M1组：0.06 mg/L氯硝柳胺 + 0.8 g/L没食子酸，M2组：0.06 mg/L氯硝柳胺 + 1.6 g/L没食子酸）。检测各组钉螺经药物浸杀12、24和48 h后的存活率，液氮包埋后切片并染色，光学显微镜下观察并定量分析，检测钉螺软体切片中细胞色素C氧化酶（CCO）和乳酸脱氢酶（LDH）的相对酶活力值，以平均光密度值表示。钉螺匀浆后离心、取上清，DCFH-DA探针共孵育，用BCA蛋白定量试剂盒测定总蛋白含量，多功能酶标仪检测荧光强度，ROS值以样品测得的荧光强度（FI）除以蛋白质浓度（μg）的值表示，用总超氧化物歧化酶（SOD）活性检测试剂盒测定SOD水平。钉螺死亡率的差异分析采用卡方检验；CCO活性和氧化应激水平的数据用Levene’s Test确定方差齐性后，用Tukey HSD的多重比较方法进行不同组间的两两比较。结果 G1和G2组浸杀后未表现出显著的灭螺效应。M1组和M2组在浸杀48 h后的钉螺死亡率分别达到70.0%（56/80）和84.2%（101/120），均高于N1组（44.4%，32/72）（χ² = 9.13、32.52，均P < 0.05）；与N2组相比，钉螺死亡率差异均无统计学意义（χ² = 0.11、2.58，均P > 0.05）。N1和N2组钉螺的LDH活性呈下降趋势；M1组和M2组钉螺体内CCO和LDH活性均降低（均P < 0.05），48 h后M1组的LDH活性在肌肉组织和肝脏分别为0.152 ± 0.002和0.172 ± 0.016 ，CCO活性分别为0.180 ± 0.022和0.335 ± 0.014；M2组的LDH活性为0.166 ± 0.008和0.173 ± 0.022，CCO活性为0.199 ± 0.009和0.294 ± 0.015，与空白对照组LDH活性（0.229 ± 0.006和0.227 ± 0.010）、CCO活性（0.259 ± 0.008和0.428 ± 0.024 ）的差异均有统计学意义（均P < 0.05）。M1组在处理后24 h的SOD活性为（5.56 ± 0.91）UI/g，高于空白对照组的（5.26 ± 0.08 ）UI/g（P < 0.05）；M2组的SOD活性在处理后12、24和48 h呈现先升高后降低的趋势[（2.40 ± 0.45）、（8.14 ± 0.15）、（1.60 ± 0.21）UI/g]，与空白对照组在相应时间点的（3.54 ± 0.94）、（5.26 ± 0.08）、（5.10 ± 0.87） UI/g相比，变化趋势显著（均P < 0.05）。M1组在处理后24 h和48 h的ROS水平分别为（1 619.00 ± 168.25）FI/μg和（1 866.65 ± 211.79 ）FI/μg，M2组在48 h后的ROS水平达到（2 451.29 ± 195.91）FI/μg，均高于空白对照组在相应时间点的（802.37 ± 114.69）、（1 393.81 ± 86.12）FI/μg（均P < 0.05）。结论没食子酸显著增强了低浓度氯硝柳胺的灭螺效果，其灭螺机制为通过阻断AOX的代偿上调，进一步加重了钉螺能量代谢失衡和氧化应激压力。

关键词: 湖北钉螺, 没食子酸, 氯硝柳胺, 灭螺效果, 葡萄糖代谢酶活性, 氧化应激水平

Abstract:

Objective To investigate the combined snail killing effect and mechanism of traditional Chinese medicine monomers gallic acid and niclosamide, which have alternating oxidase (AOX) inhibitory activity. Methods Negative snails were collected from Gong’an County, Hubei Province and randomly divided into 7 groups: a blank control group (H₂O), experimental groups were treated with niclosamide (N1 group: 0.06 mg/L, N2 group: 0.1 mg/L) and gallic acid (G1 group: 0.8 g/L, G2 group: 1.6 g/L) alone or in combination (M1 group: 0.06 mg/L niclosamide + 0.8 g/L gallic acid, M2 group: 0.06 mg/L niclosamide + 1.6 g/L gallic acid). Detect the survival rates of each group of snails after drug immersion for 12, 24, and 48 hours. Slice and stain them after liquid nitrogen embedding, observe and quantitatively analyze them under an optical microscope. Measure the relative enzyme activity values of cytochrome C oxidase (CCO) and lactate dehydrogenase (LDH) in the soft sections of snails, expressed as average optical density values. After homogenizing the snail, centrifuge and take the supernatant. Incubate with DCFH-DA probe, determine the total protein content using a BCA protein quantification kit, detect fluorescence intensity (FI) using a multifunctional enzyme-linked immunosorbent assay (ELISA), and divide the ROS value by the FI measured in the sample by the protein concentration (μg). The value represents the determination of superoxide dismutase (SOD) levels using a total SOD activity detection kit. The difference analysis of snail mortality rate was conducted using χ² test. After determining the homogeneity of variance using Levene’s Test, the data on CCO activity and oxidative stress levels were compared pairwise between different groups using Tukey HSD’s multiple comparison method. Results The G1 and G2 groups did not show significant snail killing effects after immersion. The mortality rates of snails in the M1 and M2 groups after 48 h of immersion reached 70.0% (56/80) and 84.2% (101/120), respectively, higher than those in the N1 group (44.4%, 32/72) (χ² = 9.13, 32.52; P < 0.05); Compared with the N2 group, there was no statistically significant difference in snail mortality rate (χ² = 0.11, 2.58; P > 0.05). The LDH activity of snails in N1 and N2 groups showed a decreasing trend; The activities of CCO and LDH in the screw bodies of M1 and M2 groups decreased (P < 0.05). After 48 hours, the LDH activities in muscle tissue and liver of M1 group were 0.152 ± 0.002 and 0.172 ± 0.016, respectively, and the CCO activities were 0.180 ± 0.022 and 0.335 ± 0.014, respectively; The LDH activity of the M2 group was 0.166 ± 0.008 and 0.173 ± 0.022, and the CCO activity was 0.199 ± 0.009 and 0.294 ± 0.015, respectively. There was a statistically significant difference (P < 0.05) between the two groups and the blank control group (LDH activity was 0.229 ± 0.006 and 0.227 ± 0.010, and CCO activity was 0.259 ± 0.008 and 0.428 ± 0.024, respectively). The SOD activity of the M1 group at 24 hours after treatment was (5.56 ± 0.91) UI/g, which was higher than that of the blank control group at (5.26 ± 0.08) UI/g (P < 0.05); The SOD activity of the M2 group showed a trend of first increasing and then decreasing [(2.40 ± 0.45), (8.14 ± 0.15), (1.60 ± 0.21) UI/g] at 12, 24 and 48 h after treatment. Compared with the UI/g of the blank control group at the corresponding time points [(3.54 ± 0.94), (5.26 ± 0.08), (5.10 ± 0.87) UI/g], the trend of change was significant (P < 0.05). The ROS levels in the M1 group were (1 619.00 ± 168.25) FI/μg and (1 866.65 ± 211.79) FI/μg, respectively, at 24 and 48 h after treatment. The ROS levels in the M2 group reached (2 451.29 ± 195.91) FI/μg after 48 hours, which were higher than those in the blank control group at the corresponding time points [(802.37 ± 114.69), (1 393.81 ± 86.12) FI/μg] (P < 0.05). Conclusion Gallic acid significantly enhances the snail killing effect of low concentration chloramphenicol. By blocking the compensatory upregulation of AOX, it further exacerbates the energy metabolism imbalance and oxidative stress in snails. This may be an important mechanism by which gallic acid has an auxiliary snail killing effect.

Key words: Oncomelania hupehensis, Gallic acid, Niclosamide, Molluscicidal effects, Glucose metabolism enzyme activity, Oxidative stress levels

中图分类号:

R978.82

郑涛, 刘佳豪, 李彬, 李佳珊, 聂娟, 熊涛. 没食子酸与氯硝柳胺联合灭螺作用研究[J]. 中国寄生虫学与寄生虫病杂志, 2024, 42(2): 251-258.

ZHENG Tao, LIU Jiahao, LI Bin, LI Jiashan, NIE Juan, XIONG Tao. Molluscicidal efficacy of gallic acid in combination with niclosamide[J]. Chinese Journal of Parasitology and Parasitic Diseases, 2024, 42(2): 251-258.

图/表 3

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组别Group	钉螺死亡率/%（比值） Snail mortality rate/% (Ratio)
组别Group	12 h	24 h	48 h
空白对照 Control	0（0/36）	5.0（2/40）	5.3（2/38）
N1	22.2（8/36）^a	21.1（8/38）	44.4（32/72）^a
G1	0（0/38）	5.0（2/40）	15.0（6/40）
M1	35.0（14/40）^a	50.0（20/40）^a，b	70.0（56/80）^a，b
N2	20.0（8/40）^a	37.5（12/32）^a	73.7（56/76）^a，b
G2	0（0/38）	10.0（4/40）	10.5（4/38）
M2	30.0（12/40）^a	31.6（12/38）^a	84.2（101/120）^a，b

组别Group		钉螺相对酶活力值 Relative enzyme activity value of snails
组别Group		12 h	24 h	48 h
肌肉组织中LDH	空白对照 Control	0.234 ± 0.004	0.215 ± 0.006	0.229 ± 0.006
LDH in muscle	G1	0.228 ± 0.010	0.201 ± 0.010	0.213 ± 0.016
	N1	0.161 ± 0.005^a	0.174 ± 0.006^a	0.150 ± 0.008^a
	M1	0.116 ± 0.008^a，b，c	0.180 ± 0.013^a	0.152 ± 0.002^a，c
	G2	0.220 ± 0.014	0.221 ± 0.007	0.197 ± 0.006^a
	N2	0.191 ± 0.002^a	0.187 ± 0.016	0.143 ± 0.011^a
	M2	0.174 ± 0.014^a，c	0.197 ± 0.010	0.166 ± 0.008^a，c
肝脏中LDH	空白对照 Control	0.224 ± 0.006	0.240 ± 0.014	0.227 ± 0.010
LDH in liver	G1	0.227 ± 0.017	0.224 ± 0.018	0.255 ± 0.011
	N1	0.164 ± 0.014^a	0.257 ± 0.013	0.155 ± 0.003^a
	M1	0.202 ± 0.008^a	0.207 ± 0.005^b	0.172 ± 0.016^a，c
	G2	0.234 ± 0.007	0.256 ± 0.005	0.230 ± 0.018
	N2	0.162 ± 0.007^a	0.227 ± 0.010	0.154 ± 0.020^a
	M2	0.206 ± 0.018^b	0.210 ± 0.015^c	0.173 ± 0.022^a，c
肌肉组织中CCO	空白对照 Control	0.264 ± 0.008	0.304 ± 0.013	0.259 ± 0.008
CCO in muscle	G1	0.312 ± 0.014^a	0.315 ± 0.011	0.222 ± 0.025
	N1	0.234 ± 0.018	0.279 ± 0.013	0.156 ± 0.014^a
	M1	0.179 ± 0.011^a，b，c	0.223 ± 0.016^a，b，c	0.180 ± 0.022^a
	G2	0.269 ± 0.005	0.259 ± 0.010	0.236 ± 0.015
	N2	0.228 ± 0.004^a	0.215 ± 0.014^a	0.202 ± 0.010
	M2	0.218 ± 0.013^a，c	0.240 ± 0.017^a	0.199 ± 0.009^a
肝脏中CCO	空白对照 Control	0.453 ± 0.014	0.422 ± 0.026	0.428 ± 0.024
CCO in liver	G1	0.411 ± 0.023	0.428 ± 0.009	0.441 ± 0.014
	N1	0.287 ± 0.011^a	0.389 ± 0.031	0.310 ± 0.024^a
	M1	0.349 ± 0.016^a，b，c	0.305 ± 0.020^a，b，c	0.335 ± 0.014^a，b
	G2	0.421 ± 0.021	0.420 ± 0.016	0.390 ± 0.007
	N2	0.241 ± 0.014^a	0.265 ± 0.027^a	0.274 ± 0.022^a
	M2	0.298 ± 0.015^a，b，c	0.295 ± 0.021^a，b	0.294 ± 0.015^a，b

组别Group	软体组织匀浆中SOD/UI·g^-1SOD in soft tissue homogenate/UI·g^-1			软体组织匀浆中ROS/FI·μg^-1 ROS in soft tissue homogenate/FI·μg^-1
组别Group	12 h	24 h	48 h	12 h	24 h	48 h
空白对照 Control	3.54 ± 0.94	5.26 ± 0.08	5.10 ± 0.87	792.89 ± 50.73	802.37 ± 114.69	1 393.81 ± 86.12
G1	7.61 ± 0.54^a	10.09 ± 0.36^a	6.14 ± 0.92	853.39 ± 105.43	2 000.45 ± 472.21^a	2 662.99 ± 50.88^a
N1	4.53 ± 0.65	10.92 ± 1.24^a	6.16 ± 1.11	834.22 ± 104.89	1 300.01 ± 258.40	1 298.69 ± 43.89
M1	2.26 ± 0.75^b，c	5.56 ± 0.91^b，c	7.78 ± 0.11	838.71 ± 72.45	1 619.00 ± 168.25^a	1 866.65 ± 211.79^a，b，c
G2	8.40 ± 0.33^a	9.64 ± 1.27^a	4.88 ± 0.51	879.66 ± 105.79	1 430.35 ± 214.02	1 569.13 ± 128.93
N2	3.14 ± 0.29	9.77 ± 0.90^a	3.80 ± 0.94	534.01 ± 38.75^a	1 109.16 ± 62.23	1 998.05 ± 151.13^a
M2	2.40 ± 0.45^a，c	8.14 ± 0.15	1.60 ± 0.21^a，c	949.15 ± 84.78^b	1 272.73 ± 83.52	2 451.29 ± 195.91^a，c

没食子酸与氯硝柳胺联合灭螺作用研究

Molluscicidal efficacy of gallic acid in combination with niclosamide

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