邻苯二甲酸酯对小鼠植入前胚胎体外发育的影响及作用机制的研究
摘要
邻苯二甲酸酯(phthalate esters, PEs),是一类普遍使用的化学工业品,主要用作增塑剂,其中邻苯二甲酸二乙基己基酯(Di-2-ethylhexyl phthalate, DEHP)和邻苯二甲酸二丁酯(Dibutyl phthalate, DBP)是使用较为广泛的增塑剂。邻苯二甲酸-单-乙基己基酯(Mono-2-ethylhexyl phthalate, MEHP)和邻苯二甲酸单丁酯(Mono-n-butyl phthalate, MBP)分别是DEHP和DBP的主要代谢物。使用过程中,邻苯二甲酸酯会通过各种途径进入环境中,人类可经由食品、水和土壤接触邻苯二甲酸酯。现已发现邻苯二甲酸酯具有很强的生殖和发育毒性,能损害生物的生育力。然而,目前我们对于MEHP和MBP对植入前胚胎发育的影响仍知之甚少。
为了研究MEHP对植入前胚胎发育的影响,我们用0,10-5,10-4,10-3M MEHP处理受精卵,发现10-3M MEHP会引起小鼠胚胎发生2-细胞阻滞。10-3M MEHP暴露24h后,小鼠胚胎细胞内活性氧水平显著升高。然而,抗氧化物(CAT和SOD)可以降低胚胎细胞中活性氧的水平,提高胚胎的存活率,但是没有恢复发生2-细胞阻滞胚胎的发育。进一步的实验结果表明,MEHP暴露后,只有死亡胚胎的凋亡水平升高了,但活的2-细胞阻滞的胚胎凋亡水平没有明显变化。这些结果提示ROS水平的升高和胚胎细胞凋亡并不是发生2-细胞发育胎阻滞的主要原因。通过分析胚胎基因组激活(embryonic genome activation, EGA)的关键基因(Hsc70, MuERV-L, Hsp70.1, eIF-1A和Zscan4)以及母源效应基因(OCT4和SOX2),我们发现胚胎2-细胞到4-细胞阶段,MEHP暴露显著降低了基因Hsc70、MuERV-L和SOX2的表达水平,提高了Hsp70.1、eIF-1A、Zscan4和OCT4的表达水平。添加抗氧化物(CAT和SOD)没能改变这些基因的表达趋势。由此可见,MEHP-诱导的胚胎发育阻滞是由母体向胚胎转换异常介导的,而不是氧化应激和细胞凋亡。
为了研究MBP对植入前胚胎发育的影响,我们用0,10-5,10-4,10-3M MBP处理受精卵,发现10-3和10-4M MBP暴露96h,囊胚的数量均显著降低,当延迟培养24h时,即120h,10-3M MBP暴露组桑椹胚继续发育到囊胚的胚胎数量显著高于对照组,但96h和120h囊胚的总数仍显著低于对照组,并且10-3M MBP暴露显著降低了孵化囊胚的数量,这些结果显示了10-3M MBP会损害小鼠植入前胚胎的发育潜能,10-4M MBP暴露只是延缓了胚胎的发育进程。10-3M MBP暴露48h后,胚胎细胞内ROS水平显著升高,并通过促进线粒体释放细胞色素c提高了凋亡水平。免疫荧光染色分析显示MBP处理以剂量依赖(10-5,10-4,10-3M)的方式降低了DNA甲基化水平。这些结果显示MBP可能通过诱导氧化应激、细胞凋亡或抑制DNA甲基化降低胚胎的发育潜能。
总之,本研究首次揭示了PEs暴露能对植入前胚胎发育造成损害。MEHP能够引起胚胎2-细胞发育阻滞,其主要是由于EGA启动失败和母源效应基因表达异常引起,与ROS和凋亡水平无显著相关性。MBP能够降低植入前胚胎的发育潜能,其主要与ROS和细胞凋亡相关,还可能与DNA甲基化水平的降低有关。
Phthalates (PEs) are a family of industrial chemicals that have been used as plasticizers. Among phthalates, the di-(2-ethylhexyl) phthalate (DEHP) and dibutyl phthalate (DBP) are most widely used PEs. During use, they leach, migrate, or evaporate into environment over time and humans are potentially exposed to PEs through food, water, and soil. They are thought as an environmental contaminant, which is known to cause many serious diseases, especially in reproductive system. Mono-2-ethylhexyl phthalate (MEHP) and Mono-n-butyl phthalate (MBP) are metabolite of DEHP and DBP respectively. However, little is known about the effect of MEHP and MBP on preimplantation embryo development.
In order to study the effect of MEHP on preimplantation embryos of mouse, embryos were treated by0,10-5,10-4,10-3M MEHP. We found that the development of mouse2-cell embryo was blocked by10-3M MEHP. A significant increase in the level of reactive oxygen species (ROS) was observed in arrested2-cell embryo following10-3M MEHP treatment for24h. However, antioxidants, catalase (CAT), and superoxide dismutase (SOD), reduced intracellular ROS and protected MEHP-exposed embryos from death but failed to return the arrested embryos. Further experiments demonstrated that the level of apoptosis was not altered in live arrested2-cell embryo and increased in dead arrested2-cell embryo after MEHP treatment, which implied that ROS and apoptosis were not related with2-cell block.
During analysis of the indicators of embryonic genome activation (EGA) initiation (Hsc70, MuERV-L, Hsp70.1, eIF-1A, and Zscan4) and maternal-effect genes (OCT4and SOX2), we found that MEHP treatment could significantly decline Hsc70, MuERV-L mRNA level and SOX2protein level, and markedly enhance Hsp70.1, eIF-1A, Zscan4mRNA level, and OCT4protein level at2-cell to4-cell stage. Supplementation of CAT and SOD did not reverse the expression tendency of EGA related genes.
In order to study the effect of MBP on preimplantation embryos of mouse, embryos were treated by0,10-5,10-4,10-3M MBP. We found the rate of blastocyst formation was significantly reduced following96h exposure to10-4and10-3M MBP compared with the control group. After96h culture, the blastocysts were removed and the remaining embryos were cultured for a further24h. After120h in culture, the rate of blastocyst formation was obviously increased in the10-3M MBP-treated group. However, exposure to10-3M MBP significantly decreased the total blastocyst rate (i.e. the sum of blastocysts at96and120h) and the formation of hatching/hatched embryos compared with that in the control group. These findings suggested that treatment of embryos with10"3M MBP impaired developmental competency, whereas exposure to10-4M MBP delayed the progression of preimplantation embryos to the blastocyst stage. Furthermore, reactive oxygen species (ROS) levels in embryos were significantly increased following treatment with10"3M MBP. In addition,10-3M MBP increased apoptosis via the release of cytochrome c, whereas immunofluorescent analysis revealed that exposure of preimplantation embryos to MBP concentration-dependently (10-5,10-4and10-3M) decreased DNA methylation.
Collectively, this study demonstrates for the first time that there is a possible relationship between PEs exposure and developmental failure in preimplantation embryos. An intracellular redox imbalance and apoptosis are involved in this process. But, MEHP-induced2-cell block is mediated by the failure of EGA onset and maternal-effect genes, not oxidative stress and apoptosis. Redox imbalance and apoptosis are related with MBP-induced reductions in the developmental competency of preimplantation embryos. In addition, reductions in DNA methylation may be another mechanism.
为了研究MEHP对植入前胚胎发育的影响,我们用0,10-5,10-4,10-3M MEHP处理受精卵,发现10-3M MEHP会引起小鼠胚胎发生2-细胞阻滞。10-3M MEHP暴露24h后,小鼠胚胎细胞内活性氧水平显著升高。然而,抗氧化物(CAT和SOD)可以降低胚胎细胞中活性氧的水平,提高胚胎的存活率,但是没有恢复发生2-细胞阻滞胚胎的发育。进一步的实验结果表明,MEHP暴露后,只有死亡胚胎的凋亡水平升高了,但活的2-细胞阻滞的胚胎凋亡水平没有明显变化。这些结果提示ROS水平的升高和胚胎细胞凋亡并不是发生2-细胞发育胎阻滞的主要原因。通过分析胚胎基因组激活(embryonic genome activation, EGA)的关键基因(Hsc70, MuERV-L, Hsp70.1, eIF-1A和Zscan4)以及母源效应基因(OCT4和SOX2),我们发现胚胎2-细胞到4-细胞阶段,MEHP暴露显著降低了基因Hsc70、MuERV-L和SOX2的表达水平,提高了Hsp70.1、eIF-1A、Zscan4和OCT4的表达水平。添加抗氧化物(CAT和SOD)没能改变这些基因的表达趋势。由此可见,MEHP-诱导的胚胎发育阻滞是由母体向胚胎转换异常介导的,而不是氧化应激和细胞凋亡。
为了研究MBP对植入前胚胎发育的影响,我们用0,10-5,10-4,10-3M MBP处理受精卵,发现10-3和10-4M MBP暴露96h,囊胚的数量均显著降低,当延迟培养24h时,即120h,10-3M MBP暴露组桑椹胚继续发育到囊胚的胚胎数量显著高于对照组,但96h和120h囊胚的总数仍显著低于对照组,并且10-3M MBP暴露显著降低了孵化囊胚的数量,这些结果显示了10-3M MBP会损害小鼠植入前胚胎的发育潜能,10-4M MBP暴露只是延缓了胚胎的发育进程。10-3M MBP暴露48h后,胚胎细胞内ROS水平显著升高,并通过促进线粒体释放细胞色素c提高了凋亡水平。免疫荧光染色分析显示MBP处理以剂量依赖(10-5,10-4,10-3M)的方式降低了DNA甲基化水平。这些结果显示MBP可能通过诱导氧化应激、细胞凋亡或抑制DNA甲基化降低胚胎的发育潜能。
总之,本研究首次揭示了PEs暴露能对植入前胚胎发育造成损害。MEHP能够引起胚胎2-细胞发育阻滞,其主要是由于EGA启动失败和母源效应基因表达异常引起,与ROS和凋亡水平无显著相关性。MBP能够降低植入前胚胎的发育潜能,其主要与ROS和细胞凋亡相关,还可能与DNA甲基化水平的降低有关。
Phthalates (PEs) are a family of industrial chemicals that have been used as plasticizers. Among phthalates, the di-(2-ethylhexyl) phthalate (DEHP) and dibutyl phthalate (DBP) are most widely used PEs. During use, they leach, migrate, or evaporate into environment over time and humans are potentially exposed to PEs through food, water, and soil. They are thought as an environmental contaminant, which is known to cause many serious diseases, especially in reproductive system. Mono-2-ethylhexyl phthalate (MEHP) and Mono-n-butyl phthalate (MBP) are metabolite of DEHP and DBP respectively. However, little is known about the effect of MEHP and MBP on preimplantation embryo development.
In order to study the effect of MEHP on preimplantation embryos of mouse, embryos were treated by0,10-5,10-4,10-3M MEHP. We found that the development of mouse2-cell embryo was blocked by10-3M MEHP. A significant increase in the level of reactive oxygen species (ROS) was observed in arrested2-cell embryo following10-3M MEHP treatment for24h. However, antioxidants, catalase (CAT), and superoxide dismutase (SOD), reduced intracellular ROS and protected MEHP-exposed embryos from death but failed to return the arrested embryos. Further experiments demonstrated that the level of apoptosis was not altered in live arrested2-cell embryo and increased in dead arrested2-cell embryo after MEHP treatment, which implied that ROS and apoptosis were not related with2-cell block.
During analysis of the indicators of embryonic genome activation (EGA) initiation (Hsc70, MuERV-L, Hsp70.1, eIF-1A, and Zscan4) and maternal-effect genes (OCT4and SOX2), we found that MEHP treatment could significantly decline Hsc70, MuERV-L mRNA level and SOX2protein level, and markedly enhance Hsp70.1, eIF-1A, Zscan4mRNA level, and OCT4protein level at2-cell to4-cell stage. Supplementation of CAT and SOD did not reverse the expression tendency of EGA related genes.
In order to study the effect of MBP on preimplantation embryos of mouse, embryos were treated by0,10-5,10-4,10-3M MBP. We found the rate of blastocyst formation was significantly reduced following96h exposure to10-4and10-3M MBP compared with the control group. After96h culture, the blastocysts were removed and the remaining embryos were cultured for a further24h. After120h in culture, the rate of blastocyst formation was obviously increased in the10-3M MBP-treated group. However, exposure to10-3M MBP significantly decreased the total blastocyst rate (i.e. the sum of blastocysts at96and120h) and the formation of hatching/hatched embryos compared with that in the control group. These findings suggested that treatment of embryos with10"3M MBP impaired developmental competency, whereas exposure to10-4M MBP delayed the progression of preimplantation embryos to the blastocyst stage. Furthermore, reactive oxygen species (ROS) levels in embryos were significantly increased following treatment with10"3M MBP. In addition,10-3M MBP increased apoptosis via the release of cytochrome c, whereas immunofluorescent analysis revealed that exposure of preimplantation embryos to MBP concentration-dependently (10-5,10-4and10-3M) decreased DNA methylation.
Collectively, this study demonstrates for the first time that there is a possible relationship between PEs exposure and developmental failure in preimplantation embryos. An intracellular redox imbalance and apoptosis are involved in this process. But, MEHP-induced2-cell block is mediated by the failure of EGA onset and maternal-effect genes, not oxidative stress and apoptosis. Redox imbalance and apoptosis are related with MBP-induced reductions in the developmental competency of preimplantation embryos. In addition, reductions in DNA methylation may be another mechanism.
引文
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