环境内分泌干扰物4-壬基苯酚对无脊椎动物家蚕的生殖毒性及分子机理研究
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摘要
4-壬基苯酚（4-NP）是一种环境内分泌干扰物，对包括哺乳动物的多种动物生殖系统发育都表现出复杂的毒性效应。迄今为止，还未见4-NP对陆生无脊椎动物生殖发育的影响报告。本研究以无脊椎模式昆虫家蚕为实验模型，采用全龄幼虫饲料添毒方式，通过组织病理切片、生理生化检测、基因表达谱分析、蛋白IHC、HPLC分析、组织和细胞培养等实验技术，调查了4-NP对家蚕的生殖毒性，并探讨了其分子作用机制。在传统的动物体生殖毒理试验基础上，研究建立了简单方便快捷的NP类环境内分泌干扰物的陆生无脊椎动物离体毒性试验模型。获得的主要结果如下：
1.4-NP经口暴露对家蚕具有生殖毒性
家蚕幼虫全龄饲料添加4-NP0.05～0.4g kg~(-1)，对家蚕蛹的雌雄性比没有影响（P>0.05），但两性的生殖腺指数降低了70.0%～48.7%；成虫的雌雄性比在0.4g kg~(-1)时显著下降了29.2%，产卵数和子代孵化率分别比对照下降了80.7%和91.8%；组织病理学检测出4-NP暴露后家蚕5龄幼虫的精巢生殖细胞发育滞后，细胞结构出现损伤。0.2g kg~(-1)4-NP暴露的家蚕5龄幼虫体内，HPLC检测出有4-NP累积，脂肪体中的累积系数高于中肠、表皮和生殖腺组织；雌蚕的累积系数高于雄蚕。表明4-NP经口暴露对家蚕具有生殖毒性。
2.家蚕生殖腺中氧化保护酶系统对4-NP暴露敏感
家蚕幼虫全龄饲料添加4-NP0.05～0.4g kg~(-1)，诱导生殖腺脂质过氧化产物MDA增多，耗竭GSH，降低SOD、CAT和GPx活性，引起细胞氧化与抗氧化失衡，导致细胞损伤；同时GSH和GST协同作用参与了对4-NP的解毒。成虫期和蛹期生殖腺中的抗氧化酶系统比5龄幼虫期反应更加敏感，表明家蚕生殖细胞快速发育和成熟过程中抗氧化酶系统仍然对幼虫期的4-NP暴露具有反应；从性别而言，4-NP暴露后，雄性生殖腺的抗氧化酶活性更易被激活，并具备更好的GSH和GST协同作用机制，雌性家蚕抗氧化酶活性下降引起的组织细胞脂质过氧化更加严重。表明4-NP能够通过氧化损伤途径对家蚕雌性生殖发育产生更大的毒性效应，成虫期是可用于从生理指标上来检测4-NP暴露对家蚕生殖毒性效应的敏感时期。
3.4-NP对雌雄家蚕生殖毒性影响具有不同的分子机理
4-NP暴露使雌性家蚕生殖发育特异Vg和Esp基因的表达发生变化，IHC显示0.1g kg~(-1)4-NP暴露卵巢中卵黄蛋白的生成量下降。4-NP暴露通过下调雌性家蚕内分泌系统中蜕皮激素受体基因EcR的表达，减少卵黄蛋白由脂肪体向卵巢的转运与发育卵对卵黄蛋白的吸收；4-NP也通过下调JNK信号途径中Jun基因的表达水平来影响卵的发育。
家蚕幼虫全龄饲料添加4-NP0.05～0.4g kg~(-1)，诱导了雌特异Vg基因在雄性幼虫、蛹和成虫期的表达和IHC显示0.05g kg~(-1)4-NP暴露组Vg蛋白在雄性蛹期的表达，表明4-NP对雄性家蚕具有类雌激素效应。利用Vg可以作为评估4-NP和相关酚类等环境内分泌干扰物对家蚕生殖毒性效应的有效生物标志物。4-NP暴露显著抑制雄性家蚕中生殖细胞发育相关的SoxE和Stat基因表达，而EcR基因的表达水平没有受影响。推测4-NP暴露对雄性家蚕生殖腺或生殖细胞发育的影响可能与JAK／STAT信号通路有关。
4.家蚕精巢组织和生精囊细胞体外培养毒性模型能够快速检测4-NP的雄性生殖毒性家蚕精巢组织直接暴露于7.0～28.0mg L~(-1)4-NP，组织内抗氧化防御系统的平衡受到破坏，但对生殖发育的相关基因SoxE没有显著影响。
使用接近国内太湖流域生态环境中检测到的4-NP浓度0.02～2.0μg L~(-1)暴露，体外培养的家蚕生精囊生长受到明显抑制作用，表明家蚕雄性生殖细胞对4-NP非常敏感。体外培养生精囊细胞模型可用于检测4-NP的雄性生殖毒性。
结论：家蚕是研究4-NP生殖毒性效应的一种良好无脊椎模式动物。
As an environmental endocrine disruptor,4-nonylphenol (4-NP) severely affects the developmentof the reproductive system within various animals, including mammals. Right until now there is noreport on the effect of4-NP on reproductive development of terrestrial invertebrates. Bombyx mori (B.mori) was set as an invertebrate insect model, adopting the full-instar larvae diet exposed to4-NP,employed by histopathology, physiological and biochemical detection, gene expression profile analysis,IHC, HPLC analysis, tissue and cell culture and other experimental technologies, the reproductivetoxicity of4-NP to B. mori and its molecular mechanism were investigated. On the basis of thetraditional reproductive toxicity testing in vivo, a easy-handed, fast and convenient in vitro toxicitytesting model was estabished which could be used to detect the endocrine disruptor such as4-NP. Themajor results are as follows:
1.4-NP through oral exposure has reproductive toxic effects on silkworm, B. mori
Added with0.05～0.4g kg~(-1)4-NP in diet at B. mori’s larval stage, there was no significantdifference in the sex ratio (female/male) at pupal stage, while the gonad somatic index decreased by70.0%～48.7%; At the adult stage, the sex ratio (female/male) fell by29.2%in the group exposed to0.4g kg~(-1)4-NP, the fecundity and the hatching rate decreased by80.7%and91.8%, respectively.Histopathology demonstrated that the growth of testis germ cells of B. mori was retarded and the cellstructure was injured in4-NP exposed groups.4-NP could be accumulated in the silkworm tissues, andthe content of4-NP in fat body was higher than in intestine, epidermis and gonads; the content of4-NPin females was higher than that in males. The results showed that4-NP through oral exposure hadreproductive toxic effects on B. mori.
2. Oxidation protective enzyme system in the gonads of silkworm, B. mori is sensitiveto4-NP exposure
B. mori exposed to0.05～0.4g kg~(-1)4-NP in whole larval stage, the lipid peroxide MDA content ingonads was induced, and the GSH level was exhausted, the enzyme activities of SOD, CAT and GPXwere decreased,4-NP broke the balance of cell oxidation and antioxidant and led to cell injury.Meanwhile, the cooperation of GSH and GST played a role in4-NP detoxification.
The antioxidant enzymatic systems in gonads of pupae and adults were more sensitive than inlarvae, suggesting that the oxidation protective enzymatic systems in the pupae and adults when germcells developed quickly, were still reactive to the4-NP exposed in larvae.
The antioxidant enzymatic activities in the gonads of male could be activated easier than in femalegonads, because the male gonads had a better mechanism in cooperation of GSH and GST, and theattenuation of antioxidant enzyme activities in female gonads aggravated the lipid peroxidation of cells.The results suggested that4-NP could produce more reproductive toxicity in female silkworm throughoxidative damage. The adult was the sensitive stage which could be selected as the best period fordetecting insect reproductive toxicity.
3.4-NP has different molecular mechanisms in affecting the reproductive toxicity ofmale and female silkworm, B. mori
4-NP exposure induced the expression levels of female special genes Vg and Esp, in which Vgprotein content in ovaries was reduced in0.1g kg~(-1)4-NP exposed group analyzed by IHC. Takentogether, these results showed that4-NP impacted the expression level of the EcR gene which mightlead to reduced activity of ecdysteroids in the ovary and subsequent disturbance of the Vg productionpathway thus affecting its transfer from the fat body to the ovary in this in vivo model. Also,4-NP couldaffect the egg development by down-regulated the expression level of Jun in JNK signal.
Vg gene expression in male gonad silent in normal stage was induced in larval, pupal and adultstage, while4-NP was added in diet in whole larval stage. Vg protein in testis of pupae was detected in0.05g kg~(-1)4-NP exposure group by IHC assay. The results suggested that4-NP had estronic effect onmale silkworm. Vg gene expression could be used as a typical biomarker in evaluating the reproductivetoxicity of B. mori exposed to4-NP and other related environment endocrine disruptors. The expressionlevel of SoxE and Stat in gonad of male B. mori was significantly reduced in4-NP exposure groups,while the expression level of EcR was not affected. The effects of4-NP on the development of malegonad or germ cells might be related to the JAK/STAT signal pathway.
4. Establishing the model of B. mori’s testis and spermatotheca in vitro toxicityculture, which can be used to analyze the male reproductive toxicity of4-NP in insects
Testes of silkworm were exposed to7～28mg L~(-1)4-NP in vitro, and the balance of antioxidantdefense system in tissue were damaged but the expression level of SoxE gene were not affected much.
4-NP was restrained in the growth development of spermatocyst in vitro which could be used as amodel in analyzing male reproductive toxicity of4-NP. The concentration of4-NP used in detectionwas0.02～2μg L~(-1), which was close to that reported in the actual environment in TaiHu. It meant themale reproductive cells of B. mori were sensitive to4-NP and could be used for the quick analysis of4-NP’s male reproductive toxicity.
Conclusion: Silkworm, B. mori is a good invertebrate model organism in studying reproductivetoxicity of4-NP.
1.4-NP经口暴露对家蚕具有生殖毒性
家蚕幼虫全龄饲料添加4-NP0.05～0.4g kg~(-1)，对家蚕蛹的雌雄性比没有影响（P>0.05），但两性的生殖腺指数降低了70.0%～48.7%；成虫的雌雄性比在0.4g kg~(-1)时显著下降了29.2%，产卵数和子代孵化率分别比对照下降了80.7%和91.8%；组织病理学检测出4-NP暴露后家蚕5龄幼虫的精巢生殖细胞发育滞后，细胞结构出现损伤。0.2g kg~(-1)4-NP暴露的家蚕5龄幼虫体内，HPLC检测出有4-NP累积，脂肪体中的累积系数高于中肠、表皮和生殖腺组织；雌蚕的累积系数高于雄蚕。表明4-NP经口暴露对家蚕具有生殖毒性。
2.家蚕生殖腺中氧化保护酶系统对4-NP暴露敏感
家蚕幼虫全龄饲料添加4-NP0.05～0.4g kg~(-1)，诱导生殖腺脂质过氧化产物MDA增多，耗竭GSH，降低SOD、CAT和GPx活性，引起细胞氧化与抗氧化失衡，导致细胞损伤；同时GSH和GST协同作用参与了对4-NP的解毒。成虫期和蛹期生殖腺中的抗氧化酶系统比5龄幼虫期反应更加敏感，表明家蚕生殖细胞快速发育和成熟过程中抗氧化酶系统仍然对幼虫期的4-NP暴露具有反应；从性别而言，4-NP暴露后，雄性生殖腺的抗氧化酶活性更易被激活，并具备更好的GSH和GST协同作用机制，雌性家蚕抗氧化酶活性下降引起的组织细胞脂质过氧化更加严重。表明4-NP能够通过氧化损伤途径对家蚕雌性生殖发育产生更大的毒性效应，成虫期是可用于从生理指标上来检测4-NP暴露对家蚕生殖毒性效应的敏感时期。
3.4-NP对雌雄家蚕生殖毒性影响具有不同的分子机理
4-NP暴露使雌性家蚕生殖发育特异Vg和Esp基因的表达发生变化，IHC显示0.1g kg~(-1)4-NP暴露卵巢中卵黄蛋白的生成量下降。4-NP暴露通过下调雌性家蚕内分泌系统中蜕皮激素受体基因EcR的表达，减少卵黄蛋白由脂肪体向卵巢的转运与发育卵对卵黄蛋白的吸收；4-NP也通过下调JNK信号途径中Jun基因的表达水平来影响卵的发育。
家蚕幼虫全龄饲料添加4-NP0.05～0.4g kg~(-1)，诱导了雌特异Vg基因在雄性幼虫、蛹和成虫期的表达和IHC显示0.05g kg~(-1)4-NP暴露组Vg蛋白在雄性蛹期的表达，表明4-NP对雄性家蚕具有类雌激素效应。利用Vg可以作为评估4-NP和相关酚类等环境内分泌干扰物对家蚕生殖毒性效应的有效生物标志物。4-NP暴露显著抑制雄性家蚕中生殖细胞发育相关的SoxE和Stat基因表达，而EcR基因的表达水平没有受影响。推测4-NP暴露对雄性家蚕生殖腺或生殖细胞发育的影响可能与JAK／STAT信号通路有关。
4.家蚕精巢组织和生精囊细胞体外培养毒性模型能够快速检测4-NP的雄性生殖毒性家蚕精巢组织直接暴露于7.0～28.0mg L~(-1)4-NP，组织内抗氧化防御系统的平衡受到破坏，但对生殖发育的相关基因SoxE没有显著影响。
使用接近国内太湖流域生态环境中检测到的4-NP浓度0.02～2.0μg L~(-1)暴露，体外培养的家蚕生精囊生长受到明显抑制作用，表明家蚕雄性生殖细胞对4-NP非常敏感。体外培养生精囊细胞模型可用于检测4-NP的雄性生殖毒性。
结论：家蚕是研究4-NP生殖毒性效应的一种良好无脊椎模式动物。
As an environmental endocrine disruptor,4-nonylphenol (4-NP) severely affects the developmentof the reproductive system within various animals, including mammals. Right until now there is noreport on the effect of4-NP on reproductive development of terrestrial invertebrates. Bombyx mori (B.mori) was set as an invertebrate insect model, adopting the full-instar larvae diet exposed to4-NP,employed by histopathology, physiological and biochemical detection, gene expression profile analysis,IHC, HPLC analysis, tissue and cell culture and other experimental technologies, the reproductivetoxicity of4-NP to B. mori and its molecular mechanism were investigated. On the basis of thetraditional reproductive toxicity testing in vivo, a easy-handed, fast and convenient in vitro toxicitytesting model was estabished which could be used to detect the endocrine disruptor such as4-NP. Themajor results are as follows:
1.4-NP through oral exposure has reproductive toxic effects on silkworm, B. mori
Added with0.05～0.4g kg~(-1)4-NP in diet at B. mori’s larval stage, there was no significantdifference in the sex ratio (female/male) at pupal stage, while the gonad somatic index decreased by70.0%～48.7%; At the adult stage, the sex ratio (female/male) fell by29.2%in the group exposed to0.4g kg~(-1)4-NP, the fecundity and the hatching rate decreased by80.7%and91.8%, respectively.Histopathology demonstrated that the growth of testis germ cells of B. mori was retarded and the cellstructure was injured in4-NP exposed groups.4-NP could be accumulated in the silkworm tissues, andthe content of4-NP in fat body was higher than in intestine, epidermis and gonads; the content of4-NPin females was higher than that in males. The results showed that4-NP through oral exposure hadreproductive toxic effects on B. mori.
2. Oxidation protective enzyme system in the gonads of silkworm, B. mori is sensitiveto4-NP exposure
B. mori exposed to0.05～0.4g kg~(-1)4-NP in whole larval stage, the lipid peroxide MDA content ingonads was induced, and the GSH level was exhausted, the enzyme activities of SOD, CAT and GPXwere decreased,4-NP broke the balance of cell oxidation and antioxidant and led to cell injury.Meanwhile, the cooperation of GSH and GST played a role in4-NP detoxification.
The antioxidant enzymatic systems in gonads of pupae and adults were more sensitive than inlarvae, suggesting that the oxidation protective enzymatic systems in the pupae and adults when germcells developed quickly, were still reactive to the4-NP exposed in larvae.
The antioxidant enzymatic activities in the gonads of male could be activated easier than in femalegonads, because the male gonads had a better mechanism in cooperation of GSH and GST, and theattenuation of antioxidant enzyme activities in female gonads aggravated the lipid peroxidation of cells.The results suggested that4-NP could produce more reproductive toxicity in female silkworm throughoxidative damage. The adult was the sensitive stage which could be selected as the best period fordetecting insect reproductive toxicity.
3.4-NP has different molecular mechanisms in affecting the reproductive toxicity ofmale and female silkworm, B. mori
4-NP exposure induced the expression levels of female special genes Vg and Esp, in which Vgprotein content in ovaries was reduced in0.1g kg~(-1)4-NP exposed group analyzed by IHC. Takentogether, these results showed that4-NP impacted the expression level of the EcR gene which mightlead to reduced activity of ecdysteroids in the ovary and subsequent disturbance of the Vg productionpathway thus affecting its transfer from the fat body to the ovary in this in vivo model. Also,4-NP couldaffect the egg development by down-regulated the expression level of Jun in JNK signal.
Vg gene expression in male gonad silent in normal stage was induced in larval, pupal and adultstage, while4-NP was added in diet in whole larval stage. Vg protein in testis of pupae was detected in0.05g kg~(-1)4-NP exposure group by IHC assay. The results suggested that4-NP had estronic effect onmale silkworm. Vg gene expression could be used as a typical biomarker in evaluating the reproductivetoxicity of B. mori exposed to4-NP and other related environment endocrine disruptors. The expressionlevel of SoxE and Stat in gonad of male B. mori was significantly reduced in4-NP exposure groups,while the expression level of EcR was not affected. The effects of4-NP on the development of malegonad or germ cells might be related to the JAK/STAT signal pathway.
4. Establishing the model of B. mori’s testis and spermatotheca in vitro toxicityculture, which can be used to analyze the male reproductive toxicity of4-NP in insects
Testes of silkworm were exposed to7～28mg L~(-1)4-NP in vitro, and the balance of antioxidantdefense system in tissue were damaged but the expression level of SoxE gene were not affected much.
4-NP was restrained in the growth development of spermatocyst in vitro which could be used as amodel in analyzing male reproductive toxicity of4-NP. The concentration of4-NP used in detectionwas0.02～2μg L~(-1), which was close to that reported in the actual environment in TaiHu. It meant themale reproductive cells of B. mori were sensitive to4-NP and could be used for the quick analysis of4-NP’s male reproductive toxicity.
Conclusion: Silkworm, B. mori is a good invertebrate model organism in studying reproductivetoxicity of4-NP.
引文
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