多齿围沙蚕（Periereis nuntia Savigy）对苯并（a）芘的毒性响应
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摘要
多环芳烃(PAHs)是一类广泛分布并稳定存在于自然环境中的含两个以上苯环的有机污染物。苯并(a)芘(B(a)P)分布广泛,性质稳定,致癌性强,是PAHs中最具代表且研究最多的毒物之一,目前也已成为国内外环境监测的重要指标之一。B(a)P具较高的亲脂性,一旦进入海洋环境易累积在生物体和沉积物中,对底栖生物产生短期或长期的毒性效应。B(a)P对脊椎动物如鱼类等已有相当多的毒性及相关机制报道,而无脊椎方面却很少有所涉及。
多毛类动物如沙蚕科动物在海洋食物链中的是一个重要环节,在整个海洋食物网中占有重要位置,在海洋生态系统的物质循环和能量流动中起着重要作用,是海洋生物调查的重要组分,是沿海国家最常见、最具经济价值的海洋动物。本研究以水陆交错带栖息常见无脊椎动物多毛类优势种多齿围沙蚕为研究对象,以PAHs的典型污染物苯并(a)芘为污染物,以海水和溶剂DMSO作为对照,以2.5μg/L和50μg/L B(a)P对多齿围沙蚕进行14天毒性暴露,研究发现多齿围沙蚕表现出明显的对苯并(a)芘的毒性响应,包括脂质过氧化、抗氧化酶系统和解毒酶系统的诱导、DNA损伤、凋亡和组织病理学变化等。
脂质过氧化方面,2.5μg/L和50μg/L B(a)P暴露组MDA含量均极度显著的升高(P<0.01),说明沙蚕在2.5μg/L和50μg/L B(a)P暴露时均出现显著的脂质过氧化。抗氧化系统酶方面,低浓度B(a)P(2.5μg/L)时SOD(P<0.01)、GSH-PX(P<0.05)和GST(P<0.05)活性被显著性诱导;而GSH(P<0.01)被显著性抑制。高浓度B(a)P(50μg/L):SOD(P<0.01)、CAT(P<0.01)、GR(P<0.01)、GSH-PX(P<0.01)活性被显著性诱导;而GSH(P<0.01)同样被显著性抑制。
解毒酶方面,I相解毒酶系统-CYP450基因CYP2u、CYP3A和CYP4A在分子水平上均表现不同的诱导:经实时定量PCR检测,CYP2u、CYP3A和CYP4A在2.5μg/L B(a)P时均出现极度显著性诱导(P<0.01),分别为对照的23.3、23.5和1203倍;CYP3A在50μg/L B(a)P的水平与2.5μg/L B(a)P时相比显著性下降,但仍为对照组的6倍。而高浓度B(a)P (50μg/L)组,CYP2u、CYP3A和CYP4A基因分子水平的显著性下降(P<0.01),基本处于对照组水平。2.5μg/L和50μg/L B(a)P对CYP4B基因在分子水平上无明显变化,说明在B(a)P对沙蚕的毒性暴露阶段,CYP4B基因可能不参与细胞色素P450的解毒效应。II相解毒酶-GST在酶活性上进行了探讨:2.5μg/L B(a)P对GST出现显著性诱导(P<0.01),50μg/L B(a)P虽未出现显著性,但与对照组相比仍增加2.31倍。
通过采用Tunel Assay法和DNA Laddering法研究B(a)P对多齿围沙蚕DNA损伤情况。Tunel Assay法分析检测到2.5μg/LB(a)P组出现少量凋亡细胞;50μg/L B(a)P组则出现大量凋亡细胞,且主要集中于体腔内。DNA Laddering法检测2.5μg/L B(a)P组沙蚕总DNA未出现明显断裂,亦未出现180bp-laddering现象;50μg/L B(a)P组沙蚕总DNA出现明显断裂和损伤,但不是显著180bp-laddering现象。多齿围沙蚕凋亡相关基因如Caspase8和PDCD10基因分子水平上,低浓度B(a)P(2.5μg/L)均显著性诱导(P<0.01),高浓度B(a)P(50μg/L)时,Caspase 8和PDCD10基因无明显变化。
常规HE染色组织病理学观察发现,经过14天毒性暴露后,B(a)P对多齿围沙蚕的毒性效应主要体现在肌肉外层(纵肌层)和体腔细胞。2.5μg/L B(a)P组与对照相比均有所明显增厚,肌肉外层(纵肌层)显著性增厚,肌肉内层(环肌层)无明显变化;50μg/L B(a)P组与对照相比,肌肉外层(纵肌层)出现多层环绕,肌肉层显著性增厚,肌肉内层(环肌层)亦无明显变化。2.5μg/L B(a)P组体腔细胞大多破裂,仅剩细胞空壳,出现细胞簇;50μg/L B(a)P细胞完全破裂,空壳明显增多,无细胞簇现象,胞内物质聚集形成淀粉层。
本研究首次以底栖无脊椎动物多毛类优势种多齿围沙蚕为研究对象,以PAHs的典型污染物苯并(a)芘为暴露物,经过14天毒性暴露,多齿围沙蚕表现出对B(a)P显著性的毒性响应。苯并(a)芘进入生物机体后,先经过一系列的代谢过程形成中间或终产物,刺激多齿围沙蚕机体内部产生ROS,如:02-、H2O2、HO·等,间接对机体内产生氧化损伤,如脂质过氧化的出现(MDA显著性升高);进而抗氧化酶系统的显著性升高,如SOD、CAT、GSH、GR、GSH-PX等;体内两相解毒酶的显著性升高:I相解毒酶-细胞色素P450基因水平显著性升高;II相解毒酶-GST酶活性显著性升高;最后导致DNA损伤严重、细胞凋亡的出现和相关凋亡基因分子水平;组织病理学分析观察亦见到明显的病理学变化。
本研究首次将Real-Time PCR等相关分子手段运用到无脊椎动物多齿围沙蚕的毒性响应的研究中,弥补了该项工作的空白,为潮间带环境污染修复和底栖生物毒理性研究等工作提供理论依据,并为水陆交错带的生态毒理学研究方法及其理论发展提供新的思路。
Benzo[a]Pyrene (B(a)P) is one of polycyclic aromatic hydrocarbons (PAHs), which are widely distributed and persistent in the aquatic environment. This contaminant has been shown to be genotoxic, endocrine-toxic, imuno-toxic, nerve-toxic, teratogenic and carcinogenic to a broad range of organisms. Data to date show that the level of B(a)P in the sediment has been in a high level that may pose threats to the deposit-feeders such as polychaetes. Polychaetes such as sandworms play an important role on the marine food chain in terms of their great contribution to the material cycling and energy flowing of the marine ecosystem. However, the studies about the toxicity of B(a)P to these animals are very limited until now. In the present study, we employed the sandworm Periereis nuntia Savigy, one of the most common benthic polychaetes in Chinese coastal area, as the model to stduy the potential effects of B(a)P on deposit-feeders. The sandworms Periereis nuntia Savigy were exposed to 2.5μg/L and 50μg/L B(a)P for 14 days, and samples were then collected for analysis of lipid peroxidation, antioxidative enzymes, detoxification enzymes, DNA damage, apoptosis and histological changes etc.. The mechanisms laid behind were also discussed.
The results showed that both concentrations of B(a)P caused significant increase in lipid peroxidation compared the DMSO treated group (P<0.01). The antioxidative enzymes, including SOD, GSH-PX and GST were also enhanced significantly in both exposure groups (P<0.05). GSH concentration (P<0.01) decreased significantly in both exposure groups.
The quantitative PCR results showed that the levels of CYP450 genes, including CYP2u, CYP3A and CYP4A, which played important roles in phase I detoxification, were all significantly induced in the 2.5μg/L B(a)P exposed group (P<0.01), which were 23.3-, 23.5- and 1203-folds to the control, respectively. However, in the 50μg/L B(a)P exposed group, these three enzymes were less induced compared to the low concentration group and no significant increases or decreases were observed. There was no significant changes detected in the level of CYP4B gene for both exposure groups, which might imply that the CYP4B gene and its coded protein is not involved in the detoxification of B(a)P in the sandworms. GST activity, which was orientated in the phase II detoxification, was induced significantly (P<0.01) only in the 2.5μg/L B(a)P exposed group but not in the 50μg/L exposure group.
The Tunnel assay and DNA laddering were employed to detect the DNA damage in this study. The results of Tunnel assay showed that there were only a little apoptotic cells in the lower concentration (2.5μg/L B(a)P), while a lot of in the higher (50μg/L B(a)P). All of the apoptotic cells were found to occur in the celom. DNA laddering results showed that there were lots of DNA fragments which could be seen clearly through the gel in the 50μg/L B(a)P, though no clear 180-DNA-ladderring, while there was fragments recorded in the lower concentration group(2.5μg/L B(a)P). In addition, two of important apoptosis genes, caspase 8 and PDCD 10 were analyzed through the quantitative Real-Time PCR. Data showed that the level of both genes were all significantly induced in the lower concentration (2.5μg/L B(a)P), but there were no changes in the higher concentration group (50μg/L B(a)P).
For the histological examination, after 14 days B(a)P exposure, there were some obvious changes in the outer muscle layers (longitudinal muscle) and celom cells, detected by regular HE-dyeing of histopathology analysis. In the 2.5μg/L B(a)P exposed group, the outer muscle layers became thicker clearly compared to the control, while there was no difference in the inner muscle layers. Most of the celom cells broke up, and the inclusion was released, whereas some cells agglomerated to be a big cell-cluster. In the 50μg/L B(a)P exposed group, the outer muscle layers were surrounded by several annulations, and the layer became thicker significantly. All of the celom cells broke up, and the the inclusion was released into the celom which gathered up to be a amylaceous fabric and no cell clusters were obeserved.
This was the first time to use the polychaete Periereis nuntia Savigy to detect the potential effects of B(a)P on the marine deposit-feeding invertebrates. After 14 days B(a)P exposure, there were some obvious toxic performances on the polychaete Periereis nuntia Savigy. As intake of the B(a)P, a series of metabolites were produced, resulting in generation of some reactive oxygen species, such as O2-, H2O2 , HO·and so on, which was indicated by some obvious oxidative damages, e.g. lipid peroxidation in this study. The significant increase of antioxidative enzyme systems (SOD, CAT, GSH, GR, GSH-PX); the significant induction of detoxification systems, such as the molecular levels of CYP450s of phase I and the GST activity of the phase II; finally, the oxidative damage of DNA and the appearance of apoptosis; of course, there were some obvious damage to the celom cells and issues. The results here laid basic foundation for possible future’s marine biomonitoring by using polychaetes.
多毛类动物如沙蚕科动物在海洋食物链中的是一个重要环节,在整个海洋食物网中占有重要位置,在海洋生态系统的物质循环和能量流动中起着重要作用,是海洋生物调查的重要组分,是沿海国家最常见、最具经济价值的海洋动物。本研究以水陆交错带栖息常见无脊椎动物多毛类优势种多齿围沙蚕为研究对象,以PAHs的典型污染物苯并(a)芘为污染物,以海水和溶剂DMSO作为对照,以2.5μg/L和50μg/L B(a)P对多齿围沙蚕进行14天毒性暴露,研究发现多齿围沙蚕表现出明显的对苯并(a)芘的毒性响应,包括脂质过氧化、抗氧化酶系统和解毒酶系统的诱导、DNA损伤、凋亡和组织病理学变化等。
脂质过氧化方面,2.5μg/L和50μg/L B(a)P暴露组MDA含量均极度显著的升高(P<0.01),说明沙蚕在2.5μg/L和50μg/L B(a)P暴露时均出现显著的脂质过氧化。抗氧化系统酶方面,低浓度B(a)P(2.5μg/L)时SOD(P<0.01)、GSH-PX(P<0.05)和GST(P<0.05)活性被显著性诱导;而GSH(P<0.01)被显著性抑制。高浓度B(a)P(50μg/L):SOD(P<0.01)、CAT(P<0.01)、GR(P<0.01)、GSH-PX(P<0.01)活性被显著性诱导;而GSH(P<0.01)同样被显著性抑制。
解毒酶方面,I相解毒酶系统-CYP450基因CYP2u、CYP3A和CYP4A在分子水平上均表现不同的诱导:经实时定量PCR检测,CYP2u、CYP3A和CYP4A在2.5μg/L B(a)P时均出现极度显著性诱导(P<0.01),分别为对照的23.3、23.5和1203倍;CYP3A在50μg/L B(a)P的水平与2.5μg/L B(a)P时相比显著性下降,但仍为对照组的6倍。而高浓度B(a)P (50μg/L)组,CYP2u、CYP3A和CYP4A基因分子水平的显著性下降(P<0.01),基本处于对照组水平。2.5μg/L和50μg/L B(a)P对CYP4B基因在分子水平上无明显变化,说明在B(a)P对沙蚕的毒性暴露阶段,CYP4B基因可能不参与细胞色素P450的解毒效应。II相解毒酶-GST在酶活性上进行了探讨:2.5μg/L B(a)P对GST出现显著性诱导(P<0.01),50μg/L B(a)P虽未出现显著性,但与对照组相比仍增加2.31倍。
通过采用Tunel Assay法和DNA Laddering法研究B(a)P对多齿围沙蚕DNA损伤情况。Tunel Assay法分析检测到2.5μg/LB(a)P组出现少量凋亡细胞;50μg/L B(a)P组则出现大量凋亡细胞,且主要集中于体腔内。DNA Laddering法检测2.5μg/L B(a)P组沙蚕总DNA未出现明显断裂,亦未出现180bp-laddering现象;50μg/L B(a)P组沙蚕总DNA出现明显断裂和损伤,但不是显著180bp-laddering现象。多齿围沙蚕凋亡相关基因如Caspase8和PDCD10基因分子水平上,低浓度B(a)P(2.5μg/L)均显著性诱导(P<0.01),高浓度B(a)P(50μg/L)时,Caspase 8和PDCD10基因无明显变化。
常规HE染色组织病理学观察发现,经过14天毒性暴露后,B(a)P对多齿围沙蚕的毒性效应主要体现在肌肉外层(纵肌层)和体腔细胞。2.5μg/L B(a)P组与对照相比均有所明显增厚,肌肉外层(纵肌层)显著性增厚,肌肉内层(环肌层)无明显变化;50μg/L B(a)P组与对照相比,肌肉外层(纵肌层)出现多层环绕,肌肉层显著性增厚,肌肉内层(环肌层)亦无明显变化。2.5μg/L B(a)P组体腔细胞大多破裂,仅剩细胞空壳,出现细胞簇;50μg/L B(a)P细胞完全破裂,空壳明显增多,无细胞簇现象,胞内物质聚集形成淀粉层。
本研究首次以底栖无脊椎动物多毛类优势种多齿围沙蚕为研究对象,以PAHs的典型污染物苯并(a)芘为暴露物,经过14天毒性暴露,多齿围沙蚕表现出对B(a)P显著性的毒性响应。苯并(a)芘进入生物机体后,先经过一系列的代谢过程形成中间或终产物,刺激多齿围沙蚕机体内部产生ROS,如:02-、H2O2、HO·等,间接对机体内产生氧化损伤,如脂质过氧化的出现(MDA显著性升高);进而抗氧化酶系统的显著性升高,如SOD、CAT、GSH、GR、GSH-PX等;体内两相解毒酶的显著性升高:I相解毒酶-细胞色素P450基因水平显著性升高;II相解毒酶-GST酶活性显著性升高;最后导致DNA损伤严重、细胞凋亡的出现和相关凋亡基因分子水平;组织病理学分析观察亦见到明显的病理学变化。
本研究首次将Real-Time PCR等相关分子手段运用到无脊椎动物多齿围沙蚕的毒性响应的研究中,弥补了该项工作的空白,为潮间带环境污染修复和底栖生物毒理性研究等工作提供理论依据,并为水陆交错带的生态毒理学研究方法及其理论发展提供新的思路。
Benzo[a]Pyrene (B(a)P) is one of polycyclic aromatic hydrocarbons (PAHs), which are widely distributed and persistent in the aquatic environment. This contaminant has been shown to be genotoxic, endocrine-toxic, imuno-toxic, nerve-toxic, teratogenic and carcinogenic to a broad range of organisms. Data to date show that the level of B(a)P in the sediment has been in a high level that may pose threats to the deposit-feeders such as polychaetes. Polychaetes such as sandworms play an important role on the marine food chain in terms of their great contribution to the material cycling and energy flowing of the marine ecosystem. However, the studies about the toxicity of B(a)P to these animals are very limited until now. In the present study, we employed the sandworm Periereis nuntia Savigy, one of the most common benthic polychaetes in Chinese coastal area, as the model to stduy the potential effects of B(a)P on deposit-feeders. The sandworms Periereis nuntia Savigy were exposed to 2.5μg/L and 50μg/L B(a)P for 14 days, and samples were then collected for analysis of lipid peroxidation, antioxidative enzymes, detoxification enzymes, DNA damage, apoptosis and histological changes etc.. The mechanisms laid behind were also discussed.
The results showed that both concentrations of B(a)P caused significant increase in lipid peroxidation compared the DMSO treated group (P<0.01). The antioxidative enzymes, including SOD, GSH-PX and GST were also enhanced significantly in both exposure groups (P<0.05). GSH concentration (P<0.01) decreased significantly in both exposure groups.
The quantitative PCR results showed that the levels of CYP450 genes, including CYP2u, CYP3A and CYP4A, which played important roles in phase I detoxification, were all significantly induced in the 2.5μg/L B(a)P exposed group (P<0.01), which were 23.3-, 23.5- and 1203-folds to the control, respectively. However, in the 50μg/L B(a)P exposed group, these three enzymes were less induced compared to the low concentration group and no significant increases or decreases were observed. There was no significant changes detected in the level of CYP4B gene for both exposure groups, which might imply that the CYP4B gene and its coded protein is not involved in the detoxification of B(a)P in the sandworms. GST activity, which was orientated in the phase II detoxification, was induced significantly (P<0.01) only in the 2.5μg/L B(a)P exposed group but not in the 50μg/L exposure group.
The Tunnel assay and DNA laddering were employed to detect the DNA damage in this study. The results of Tunnel assay showed that there were only a little apoptotic cells in the lower concentration (2.5μg/L B(a)P), while a lot of in the higher (50μg/L B(a)P). All of the apoptotic cells were found to occur in the celom. DNA laddering results showed that there were lots of DNA fragments which could be seen clearly through the gel in the 50μg/L B(a)P, though no clear 180-DNA-ladderring, while there was fragments recorded in the lower concentration group(2.5μg/L B(a)P). In addition, two of important apoptosis genes, caspase 8 and PDCD 10 were analyzed through the quantitative Real-Time PCR. Data showed that the level of both genes were all significantly induced in the lower concentration (2.5μg/L B(a)P), but there were no changes in the higher concentration group (50μg/L B(a)P).
For the histological examination, after 14 days B(a)P exposure, there were some obvious changes in the outer muscle layers (longitudinal muscle) and celom cells, detected by regular HE-dyeing of histopathology analysis. In the 2.5μg/L B(a)P exposed group, the outer muscle layers became thicker clearly compared to the control, while there was no difference in the inner muscle layers. Most of the celom cells broke up, and the inclusion was released, whereas some cells agglomerated to be a big cell-cluster. In the 50μg/L B(a)P exposed group, the outer muscle layers were surrounded by several annulations, and the layer became thicker significantly. All of the celom cells broke up, and the the inclusion was released into the celom which gathered up to be a amylaceous fabric and no cell clusters were obeserved.
This was the first time to use the polychaete Periereis nuntia Savigy to detect the potential effects of B(a)P on the marine deposit-feeding invertebrates. After 14 days B(a)P exposure, there were some obvious toxic performances on the polychaete Periereis nuntia Savigy. As intake of the B(a)P, a series of metabolites were produced, resulting in generation of some reactive oxygen species, such as O2-, H2O2 , HO·and so on, which was indicated by some obvious oxidative damages, e.g. lipid peroxidation in this study. The significant increase of antioxidative enzyme systems (SOD, CAT, GSH, GR, GSH-PX); the significant induction of detoxification systems, such as the molecular levels of CYP450s of phase I and the GST activity of the phase II; finally, the oxidative damage of DNA and the appearance of apoptosis; of course, there were some obvious damage to the celom cells and issues. The results here laid basic foundation for possible future’s marine biomonitoring by using polychaetes.
引文
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