典型有机磷和拟除虫菊酯对PC12胞毒性的氧化应激机制及对映体选择性
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摘要
近几年来,一些科研工作者对手性农药的环境安全性进行了研究,并发现手性农药在环境归趋、内分泌干扰、生殖毒性以及免疫毒性等方面均具有对映体选择性。然而,到目前为止对单一对映异构体引起的毒性作用的分子机制的研究还比较有限。为了更为准确地评估手性农药的环境风险性,有必要开展典型手性农药的环境风险性评价,并深入研究对映体选择性毒性的分子机制。因此,本文主要以丙溴磷和联苯菊酯为手性有机磷和拟除虫菊酯的代表,以大鼠嗜铬细胞瘤株(PC12)细胞作为体外细胞模型,在细胞和分子水平上研究由氧化应激介导的有机磷和拟除虫菊酯类农药对PC12细胞的毒性机制及对映体差异性。研究主要取得以下结果：
(1)以典型手性拟除虫菊酯联苯菊酯(BF)为研究对象,考察了cis-BF引起PC12细胞细胞毒性和氧化应激的对映体差异性。实验结果显示,当浓度为10-5mol L-1及以上时,cis-BF对PC12细胞的毒性效应及氧化应激存在显著的对映体选择性差异,对映体1S-cis-BF的作用明显强于对映体1R-cis-BF.1S-cis-BF可以更显著性地抑制PC12细胞活性,诱导细胞外乳酸脱氢酶(LDH)；同时1S-cis-BF使PC12细胞内活性氧(ROS)和丙二醛(MDA)水平明显升高,细胞内超氧化物歧化酶(SOD)活性受到显著抑制。可见,cis-BF可以对映体特异性地诱导细胞毒性以及氧化应激,并且1S-cis-BF是其引起细胞毒性和氧化应激的主要贡献者。
(2)在得到了cis-BF可以对映体选择性地诱导氧化应激的结果的基础上,采用荧光定量PCR (qRT-PCR)法进一步深入研究了cis-BF对氧化应激以及热休克蛋白相关基因表达的影响及对映体选择性。研究结果显示,当浓度大于5×10-6mol-1时,1S-cis-BF可以显著性地诱导HSP90、HSP70、HSP60、Cu-ZnSOD、 MnSOD、CAT以及GST基因表达上调,而1R-cis-BF对相关基因表达的影响明显弱于1S-cis-BF。1S-xis-BF对Cu-ZnSOD、MnSOD、GST和CAT基因表达的诱导可能主要是通过激活p38通路和ERK通路,对HSP90、HSP70和HSP60基因表达的诱导主要是通过激活p38通路。
(3)以丙溴磷作为手性有机磷农药的代表,在对映体层面上研究丙溴磷由氧化应激介导的PC12细胞的细胞毒性的机制及对映体差异性。MTT、LDH和彗星实验的结果显示,丙澳磷外消旋体及其对映体对细胞活性、LDH释放以及细胞彗尾长度的影响具有剂量和时间依赖性,对映体(-)-丙溴磷的毒性明显高于(+)-丙溴磷和rac-丙溴磷。(-)-丙溴磷可以剂量和时间依赖性刺激ROS和MDA产生,同时诱导Cu-ZnSOD、GST、CAT、HSP70以及HSP90基因表达上调。而(+)-丙溴磷对相关基因表达的影响明显弱于(-)-丙溴磷及rac-丙澳磷。维生素E(6×10-4mol L-1)预处理可以剂量依赖性地降低细胞活性抑制率,使彗尾长度,ROS和MDA水平恢复至正常水平,进一步证实了氧化应激对细胞毒性的介导。除此之外,我们的研究结果显示氧化应激的产生先于细胞毒性和DNA损伤的产生,表明氧化应激是丙溴磷产生细胞毒性和基因毒性的起因而不是结果。
(4)比较了甲胺磷、乙酰甲胺磷、氯胺磷、马拉硫磷及马拉氧磷5种有机磷农药诱导PC12细胞的细胞毒性、DNA损伤以及氧化应激的能力。MTT的结果显示,这5种有机磷在最高浓度80mg L-1时,对PC12细胞活性均有显著抑制,抑制率从大到小排序为马拉氧磷(32.1%)>甲胺磷(23.3%)>马拉硫磷(22.1%)>氯胺磷(4.0%)>乙酰甲胺磷(3.2%)。彗星实验的结果显示,当浓度为40mg L-时,暴露于有机磷中的细胞的彗尾长度和空白对照的比值从高到低依次为：马拉氧磷(3.02倍)>甲胺磷(2.35倍)>马拉硫磷(1.71倍)>乙酰甲胺磷(1.44倍)>氯胺磷(1.07倍)。在对氧化应激相关检测终点的检测中发现,甲胺磷、乙酰甲胺磷、马拉硫磷和马拉氧磷可以不同程度地诱导ROS和MDA的增加,并抑制SOD、过氧化氢酶(CAT)和谷胱甘肽(GSH)活性。维生素E预处理可以降低细胞活性抑制率,减弱DNA损伤,同时,可以使有机磷诱导的ROS、 MDA水平的上升以及CAT、SOD和GSH等抗氧化物酶活性的抑制得到恢复。
综上,我们的研究结果表明,手性农药可以对映体选择性地诱导细胞产生氧化应激,并进一步诱导产生对映体选择性的细胞毒性和DNA损伤。本论文的研究为筛选出既具有高靶标生物药效又对生物低毒安全的手性农药对映体单体提供了科学依据,为我国环保型农药的研制开发提供了理论参考。
Previous studies have demonstrated the occurrence of enantioselectivity of chiral pesticides in environmental fate, endocrine disruption, reproductive toxicity and immune toxicity. However, research on the molecular mechanisms of enantioselective toxicity of chiral pesticides has been limited. Therefore, it is important to investigate the environmental risk of the chiral pesticides, and explore the toxic mechanism in-depth. In this study, we used the rat pheochromocytoma PC12cell line as an in vitro model to evaluate the involvement of the oxidative stress pathway in enantioselective toxicity of several common used chiral pesticides, represented by bifenthrin (BF) and profenofos (PFF). Both the underlying mechanisms and enantioselectivity of toxicities were investigated using molecular biology methods. The major results were listed as follows:
(1) In this part, cis-BF was chosen to evaluate the involvement of the oxidative stress in enantioselective cytotoxicity of cis-BF. Following exposure of cells to cis-BF and its enantiomers, a significant reduction in cell survival and superoxide dismutase (SOD), as well as increased production of lactate dehydrogenase (LDH), intracellular reactive oxygen species (ROS) and malondialdehyde (MDA), was observed in1S-cis-BF, while1R-cis-BF exhibited these effects to a lesser degree. These results demonstrated that enantiomer-specific cis-BF-induced oxidative stress is possibly the mechanism of cis-BF-induced enantioselective cytotoxicity.
(2) Based on the result that cis-BF could enantioselectively induce oxidative stress, the expression patterns of different genes encoding heat shock protein and antioxidant enzymes were investigated by real-time quantitative PCR in PC12cells after exposure to cis-BF and its enantiomers. The results showed that exposure to1S-cis-BF resulted in increased transcription of HSP90、HSP70、HSP60. Cu-Zn-superoxide dismutase (Cu-ZnSOD)、Mn-superoxide dismutase (MnSOD)、 catalase (CAT) and glutathione-s-transferase (GST) at a concentration of5×10-6mol L-1and the above, while exposure to1R-cis-BF and rac-cis-BF exhibited these effects to lesser degrees. In addition, induction of antioxidant enzyme gene expression produced by1S-cis-BF might occur, at least in part through activation of p38MAPK and ERK, while increase of stress protein response produced by1S-cis-BF might occur through p38MAPK signaling pathway.
(3) The role of oxidative stress in enantiomer-specific, profenofos (PFF)-induced cytotoxicity and genotoxicity was investigated using PC12cells. The results demonstrated that PFF enantioselectively induced inhibition of cell viability and DNA damage in PC12cells. A concentration-and time-dependent significant induction of reactive oxygen species, malondialdehyde and gene expression encoding antioxidant enzyme (Cu-ZnSOD, GST and CAT) and stress protein (HSP70and HSP90), was observed in (-)-PFF, while (+)-PFF and rac-PFF exhibited these effects to lesser degrees. Pre-treatment with vitamin E (6×10mol L-1) caused a significant attenuation in the toxic effect; reversing subsequent PFF-induced elevation of ROS and MDA levels, further strengthening the involvement of oxidative stress in PFF mediated toxicity. In addition, the results also showed that PFF-dependent ROS accumulation, MDA release and oxidative stress gene expression preceded the loss of cell viability and induction of DNA damage, and already significantly changed at concentrations which are not yet cytotoxic or genotoxic. These results indicate that oxidative stress may contribute to PFF induced toxicity and was not a consequence of it.
(4) The primary objective of this part is to compare the ability of acephate (ACE), methamidophos (MET), chloramidophos (CHL), malathion (MAT) and malaoxon (MAO) to induce cytotoxicity, DNA damage and oxidative stress at5mg L-1～80mg L-1in PC12cells. The results demonstrated that MET、MAT and MAO caused significant inhibition of cell viability and increased DNA damage in PC12cells at40mg L-1. MAO was more toxic than the other organophosphorous (OP) compounds. ACE、 MET、MAT and MAO increased the levels of intracellular ROS and MDA, and decreased the activity of SOD、CAT and GSH at20mg L-1and40mg L-1to different degrees. Pre-treatment with vitamin E (6×10-4mol L-1) caused a significant attenuation in the cytotoxic and genotoxic effect; reversing subsequent OP-induced elevation of peroxidation products and the decline of anti-oxidant enzyme activities. These results indicate that oxidative damage contributes to the OP-induced cytotoxicity and DNA damage.
Overall, results of our study suggest that enantiomer-specific chiral pesticide-induced oxidative stress is possibly the mechanism of chiral pesticide-induced enantioselective cytotoxicity and genotoxicity.1S-cis-BF and (-)-PFF are the major contributors. This paper provided a scientific basis for screening out the monomer of chiral pesticides which both has high pesticide effect to target organism and has low toxicity to non-target organism, and provided a theoretical reference for researching and developing the environment-friendly pesticides.
(1)以典型手性拟除虫菊酯联苯菊酯(BF)为研究对象,考察了cis-BF引起PC12细胞细胞毒性和氧化应激的对映体差异性。实验结果显示,当浓度为10-5mol L-1及以上时,cis-BF对PC12细胞的毒性效应及氧化应激存在显著的对映体选择性差异,对映体1S-cis-BF的作用明显强于对映体1R-cis-BF.1S-cis-BF可以更显著性地抑制PC12细胞活性,诱导细胞外乳酸脱氢酶(LDH)；同时1S-cis-BF使PC12细胞内活性氧(ROS)和丙二醛(MDA)水平明显升高,细胞内超氧化物歧化酶(SOD)活性受到显著抑制。可见,cis-BF可以对映体特异性地诱导细胞毒性以及氧化应激,并且1S-cis-BF是其引起细胞毒性和氧化应激的主要贡献者。
(2)在得到了cis-BF可以对映体选择性地诱导氧化应激的结果的基础上,采用荧光定量PCR (qRT-PCR)法进一步深入研究了cis-BF对氧化应激以及热休克蛋白相关基因表达的影响及对映体选择性。研究结果显示,当浓度大于5×10-6mol-1时,1S-cis-BF可以显著性地诱导HSP90、HSP70、HSP60、Cu-ZnSOD、 MnSOD、CAT以及GST基因表达上调,而1R-cis-BF对相关基因表达的影响明显弱于1S-cis-BF。1S-xis-BF对Cu-ZnSOD、MnSOD、GST和CAT基因表达的诱导可能主要是通过激活p38通路和ERK通路,对HSP90、HSP70和HSP60基因表达的诱导主要是通过激活p38通路。
(3)以丙溴磷作为手性有机磷农药的代表,在对映体层面上研究丙溴磷由氧化应激介导的PC12细胞的细胞毒性的机制及对映体差异性。MTT、LDH和彗星实验的结果显示,丙澳磷外消旋体及其对映体对细胞活性、LDH释放以及细胞彗尾长度的影响具有剂量和时间依赖性,对映体(-)-丙溴磷的毒性明显高于(+)-丙溴磷和rac-丙溴磷。(-)-丙溴磷可以剂量和时间依赖性刺激ROS和MDA产生,同时诱导Cu-ZnSOD、GST、CAT、HSP70以及HSP90基因表达上调。而(+)-丙溴磷对相关基因表达的影响明显弱于(-)-丙溴磷及rac-丙澳磷。维生素E(6×10-4mol L-1)预处理可以剂量依赖性地降低细胞活性抑制率,使彗尾长度,ROS和MDA水平恢复至正常水平,进一步证实了氧化应激对细胞毒性的介导。除此之外,我们的研究结果显示氧化应激的产生先于细胞毒性和DNA损伤的产生,表明氧化应激是丙溴磷产生细胞毒性和基因毒性的起因而不是结果。
(4)比较了甲胺磷、乙酰甲胺磷、氯胺磷、马拉硫磷及马拉氧磷5种有机磷农药诱导PC12细胞的细胞毒性、DNA损伤以及氧化应激的能力。MTT的结果显示,这5种有机磷在最高浓度80mg L-1时,对PC12细胞活性均有显著抑制,抑制率从大到小排序为马拉氧磷(32.1%)>甲胺磷(23.3%)>马拉硫磷(22.1%)>氯胺磷(4.0%)>乙酰甲胺磷(3.2%)。彗星实验的结果显示,当浓度为40mg L-时,暴露于有机磷中的细胞的彗尾长度和空白对照的比值从高到低依次为：马拉氧磷(3.02倍)>甲胺磷(2.35倍)>马拉硫磷(1.71倍)>乙酰甲胺磷(1.44倍)>氯胺磷(1.07倍)。在对氧化应激相关检测终点的检测中发现,甲胺磷、乙酰甲胺磷、马拉硫磷和马拉氧磷可以不同程度地诱导ROS和MDA的增加,并抑制SOD、过氧化氢酶(CAT)和谷胱甘肽(GSH)活性。维生素E预处理可以降低细胞活性抑制率,减弱DNA损伤,同时,可以使有机磷诱导的ROS、 MDA水平的上升以及CAT、SOD和GSH等抗氧化物酶活性的抑制得到恢复。
综上,我们的研究结果表明,手性农药可以对映体选择性地诱导细胞产生氧化应激,并进一步诱导产生对映体选择性的细胞毒性和DNA损伤。本论文的研究为筛选出既具有高靶标生物药效又对生物低毒安全的手性农药对映体单体提供了科学依据,为我国环保型农药的研制开发提供了理论参考。
Previous studies have demonstrated the occurrence of enantioselectivity of chiral pesticides in environmental fate, endocrine disruption, reproductive toxicity and immune toxicity. However, research on the molecular mechanisms of enantioselective toxicity of chiral pesticides has been limited. Therefore, it is important to investigate the environmental risk of the chiral pesticides, and explore the toxic mechanism in-depth. In this study, we used the rat pheochromocytoma PC12cell line as an in vitro model to evaluate the involvement of the oxidative stress pathway in enantioselective toxicity of several common used chiral pesticides, represented by bifenthrin (BF) and profenofos (PFF). Both the underlying mechanisms and enantioselectivity of toxicities were investigated using molecular biology methods. The major results were listed as follows:
(1) In this part, cis-BF was chosen to evaluate the involvement of the oxidative stress in enantioselective cytotoxicity of cis-BF. Following exposure of cells to cis-BF and its enantiomers, a significant reduction in cell survival and superoxide dismutase (SOD), as well as increased production of lactate dehydrogenase (LDH), intracellular reactive oxygen species (ROS) and malondialdehyde (MDA), was observed in1S-cis-BF, while1R-cis-BF exhibited these effects to a lesser degree. These results demonstrated that enantiomer-specific cis-BF-induced oxidative stress is possibly the mechanism of cis-BF-induced enantioselective cytotoxicity.
(2) Based on the result that cis-BF could enantioselectively induce oxidative stress, the expression patterns of different genes encoding heat shock protein and antioxidant enzymes were investigated by real-time quantitative PCR in PC12cells after exposure to cis-BF and its enantiomers. The results showed that exposure to1S-cis-BF resulted in increased transcription of HSP90、HSP70、HSP60. Cu-Zn-superoxide dismutase (Cu-ZnSOD)、Mn-superoxide dismutase (MnSOD)、 catalase (CAT) and glutathione-s-transferase (GST) at a concentration of5×10-6mol L-1and the above, while exposure to1R-cis-BF and rac-cis-BF exhibited these effects to lesser degrees. In addition, induction of antioxidant enzyme gene expression produced by1S-cis-BF might occur, at least in part through activation of p38MAPK and ERK, while increase of stress protein response produced by1S-cis-BF might occur through p38MAPK signaling pathway.
(3) The role of oxidative stress in enantiomer-specific, profenofos (PFF)-induced cytotoxicity and genotoxicity was investigated using PC12cells. The results demonstrated that PFF enantioselectively induced inhibition of cell viability and DNA damage in PC12cells. A concentration-and time-dependent significant induction of reactive oxygen species, malondialdehyde and gene expression encoding antioxidant enzyme (Cu-ZnSOD, GST and CAT) and stress protein (HSP70and HSP90), was observed in (-)-PFF, while (+)-PFF and rac-PFF exhibited these effects to lesser degrees. Pre-treatment with vitamin E (6×10mol L-1) caused a significant attenuation in the toxic effect; reversing subsequent PFF-induced elevation of ROS and MDA levels, further strengthening the involvement of oxidative stress in PFF mediated toxicity. In addition, the results also showed that PFF-dependent ROS accumulation, MDA release and oxidative stress gene expression preceded the loss of cell viability and induction of DNA damage, and already significantly changed at concentrations which are not yet cytotoxic or genotoxic. These results indicate that oxidative stress may contribute to PFF induced toxicity and was not a consequence of it.
(4) The primary objective of this part is to compare the ability of acephate (ACE), methamidophos (MET), chloramidophos (CHL), malathion (MAT) and malaoxon (MAO) to induce cytotoxicity, DNA damage and oxidative stress at5mg L-1～80mg L-1in PC12cells. The results demonstrated that MET、MAT and MAO caused significant inhibition of cell viability and increased DNA damage in PC12cells at40mg L-1. MAO was more toxic than the other organophosphorous (OP) compounds. ACE、 MET、MAT and MAO increased the levels of intracellular ROS and MDA, and decreased the activity of SOD、CAT and GSH at20mg L-1and40mg L-1to different degrees. Pre-treatment with vitamin E (6×10-4mol L-1) caused a significant attenuation in the cytotoxic and genotoxic effect; reversing subsequent OP-induced elevation of peroxidation products and the decline of anti-oxidant enzyme activities. These results indicate that oxidative damage contributes to the OP-induced cytotoxicity and DNA damage.
Overall, results of our study suggest that enantiomer-specific chiral pesticide-induced oxidative stress is possibly the mechanism of chiral pesticide-induced enantioselective cytotoxicity and genotoxicity.1S-cis-BF and (-)-PFF are the major contributors. This paper provided a scientific basis for screening out the monomer of chiral pesticides which both has high pesticide effect to target organism and has low toxicity to non-target organism, and provided a theoretical reference for researching and developing the environment-friendly pesticides.
引文
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