四环素类污染物毒性的微观机制研究
摘要
蛋白质是生命的物质基础,它与各种形式的生命活动紧密联系在一起,机体中的每一个细胞和所有重要组成部分都有蛋白质参与。细胞是生物有机体进行新陈代谢活动的基本单位,外环境中的有害因子,如物理性因子(电离辐射、噪声、紫外线等)、化学性因子和生物性因子(细菌、病毒等)等,通过不同途径(如呼吸道、消化道、皮肤及伤口等)作用于机体,能诱发机体结构与功能发生改变,而这些改变无不反映细胞结构与功能的变化。细胞结构与功能的改变是机体受到外源性有害物质作用所致损伤的基础。
四环素类药物在畜牧业和水产养殖业中有广泛应用。由于生物利用率较低,50-80%的四环素类药物未经代谢而进入环境成为污染物。残留在土壤、地表水、地下水、甚至饮用水等环境以及动物源食品(如蛋、奶、肉等)中的四环素类污染物能经由食物链或以饮食方式进入人体,对人类健康形成威胁。四环素类药物残留的污染问题及其毒性已引起了世界范围内的关注,并已有大量相关报道,但国内外已有的研究成果还不能彻底阐释环境中药物残留对生态及人类健康的内在作用机制。本论文在已报道的相关研究成果的基础上,以四环素类污染物致机体毒性的作用靶点功能蛋白质和细胞为对象,研究了常见四环素类污染物(土霉素OTC、四环素TC和金霉素CTC, TCs)毒性的微观机制,得到以下研究结果：
1OTC和TC与血清白蛋白相互作用的机理研究
血清白蛋白是各种内源性和外源性化合物在血液中运输的载体。本文在利用公式校正荧光内滤效应的基础上研究了OTC和TC与血清白蛋白(BSA和HSA)的相互作用。分子探针的研究结果表明,OTC和TC与位于血清白蛋白子域ⅢA的位点Ⅱ结合。计算得到的△H°矿和△S°分别为负值和正值,说明OTC和TC与血清白蛋白非共价结合的主要作用力为静电作用力。利用分子模拟方法进一步确定OTC和TC的结合位置为位于位点Ⅱ的正电荷氨基酸残基(对于BSA为ARG433或ARG436,对于HSA为ARG410或LYS414)。紫外可见吸收光谱、同步荧光光谱和圆二色谱的实验结果表明,结合的OTC和TC导致血清白蛋白的二级结构和色氨酸残基微环境发生改变。相关研究结果已分别发表在Biomacromolecules和Journal of Agricultural and Food Chemistry上。
2TCs与其毒性相关的功能蛋白酶的作用机理研究
已有研究结果表明,TCs能使过氧化氢酶、溶菌酶和胰蛋白酶等功能蛋白酶的活性下降。本文利用光谱学技术结合分子对接研究了TCs毒性的微观机制。实验结果表明：(1)OTC以一个结合位点通过范德华力和氢键作用力与过氧化氢酶作用形成复合物。结合的OTC使过氧化氢酶的二级结构和色氨酸残基微环境发生改变,使过氧化氢酶活性受到抑制；(2) OTC、TC和CTC以一个结合位点与位于溶菌酶表面裂缝的活性中心中的两个关键氨基酸残基(Glu35或Asp52)作用,竞争性抑制溶菌酶活性,结合强度的顺序为：CTC>TC>OTC。分子对接和热力学分析的结果均表明,静电作用力在TCs与溶菌酶的作用过程中占主导地位。结合的TCs使溶菌酶的二级结构和色氨酸残基的微环境发生改变。(3)OTC、TC和CTC均能以一个结合位点与胰蛋白酶通过范德华力和氢键作用力作用形成复合物,结合强度的顺序为：TC>OTC>CTC。结合的TCs能抑制胰蛋白酶活性,抑制程度大小顺序为：CTC>OTC>TC。分子对接和胰蛋白酶活性实验的结果均表明OTC和TC与胰蛋白酶的S1结合口袋结合,竞争性抑制酶活性；由于在CTC苯环上的氯原子阻碍苯环进入S1结合口袋,CTC与胰蛋白酶的非酶活性中心位点结合,非竞争性抑制胰蛋白酶活性。结合的TCs使胰蛋白酶的二级结构和色氨酸残基的微环境发生改变,但不同的结合位置使CTC对胰蛋白酶二级结构的影响与OTC和TC相反。相关工作已分别发表在Science of The Total Environment, Chemosphere和PLoS ONE上。
3TCs对人血红细胞毒性的作用机理研究
常见的TCs (OTC和TC)均能进入红细胞,本文考察了其对红细胞毒性的微观作用机理。研究结果表明：(1)OTC能引起红细胞抗氧化防御体系功能下降,导致红细胞氧化应激,导致以下毒性效应：使红细胞的形态发生变化,并进一步导致红细胞溶血(OTC浓度大于8×10-5mol L-1)。在低浓度下(≤4×10-5mol L-1), OTC能使红细胞ATP酶活性增强；随浓度进一步增大,OTC能抑制ATP酶活性,影响细胞功能；(2)利用流式细胞术探索性建立反映红细胞抗氧化性的指标(谷胱甘肽和活性氧)的检测方法,并考察了TC对其含量的影响。结果表明,TC能导致红细胞谷胱甘肽含量减少,从而使细胞抗氧化防御体系功能降低,导致细胞氧化/抗氧化平衡稳态被破坏,进而使ROS浓度升高,造成氧化应激,能引起细胞结构和功能的损伤；(3)OTC和TC均以一个作用位点与血红蛋白通过范德华力和氢键作用力结合形成复合物。同步荧光实验和分子对接均表明,OTC和TC在血红蛋白上的结合位置为四个亚基之间的中央空穴。结合的OTC和TC能改变血红蛋白的结构和酪氨酸残基的微环境。部分研究结果已经在Journal of Hazardous Materials上发表。
本论文对TCs致机体毒性的微观机制进行了探索性研究,取得了具有创新性的研究成果,有利于深入认识TCs的毒性；论文建立的研究TCs毒性作用机理的新方法可为其他环境污染物的毒性评价提供方法学的参考和技术支持。
Protein is the material base for life, being involved in every cell and all important part of body and closely linked to various forms of life activities. The cell is the basic unit of the metabolic activity of biological organism. The harmful factors in the external environment, such as physical (ionizing radiation, noise, ultraviolet, etc.), chemical and biological (bacteria, viruses, etc.) ones, can act on the body through various means (such as respiratory tract, digestive tract, skin and wound), inducing changes in body structure and function, all reflecting those in cell structure and function. So the changes in cell structure and function are the basis for the injuries to the body induced by exogenous harmful substances.
Tetracyclines are widely used in animal husbandry and aquaculture. Because of their low bioavailability,50-80%of the applied dose enters the environment without metabolism, becomes a pollutant. The tetracycline residues in the environment such as soil, surface water, groundwater, even drinking water, and animal food (egg, milk, meat, etc.) can enter human bodies by food chain or diet, being potentially harmful. The pollution of tetracycline residues and their toxicity has attracted worldwide attention. There have been many related reports, but the existing research results can not completely explain the inner mechanism of the residues in the environment to ecology and human health. In this thesis, on the basis of the existing related research results, with the targets of the tetracyclines induced toxicity (functional proteins and cell) as the object, we investigated the micromechanism of the toxicity of the common tetracyclines (oxytetracycline (OTC), tetracycline (TC) and chlortetracycline (CTC)) and obtained the following findings:
1The interaction mechanism of OTC and TC with serum albumins
Serum albumins are the carrier of a wide variety of endogenous and exogenous compounds in blood. We studied the interaction of OTC and TC with serum albumins based on the elimination of inner filter effect with the correction equation. The site marker competition experiments revealed that OTC and TC bind to site Ⅱ (subdomain ⅢA) of serum albumins, mainly with electrostatic interaction indicated by the calculated negative ΔH°and positive ΔS°. The molecular modeling methods were applied to further define that the binding site for OTC and TC was the positively charged amino acid residues in site II (ARG433or ARG436for BSA, ARG410and LYS414for HSA). The UV-visible absorption, synchronous fluorescence and circular dichroism results showed that the bound OTC and TC can change the secondary structure and the microenvironment of the tryptophan residues of BSA and HSA. The research results were published on Biomacromolecules and Journal of Agricultural and Food Chemistry.
2The interaction mechanism of tetracyclines with the functional enzymes related to tetracyclines toxicity
It have been reported that tetracyclines can result in the decrease of the activity of catalase, lysozyme and trypsin. We investigated the micromechanism of the toxicity of tetracyclines by multispectroscopic techniques and molecular modeling method. The experimental results indicated that:(1) OTC can interact with catalase to form a complex mainly by van der Waals'interactions and hydrogen bonds with one binding site. The binding of OTC can result in change of the secondary structure and the microenvironment of the tryptophan residues of catalase. The activity of catalase was also inhibited for the bound OTC.(2) All the three tetracyclines OTC, TC and CTC can bind into lysozyme cleft and interact with the key active-site residues Glu35or Asp52with one binding site, with the affinity order:CTC>TC>OTC, resulting in competitive inhibition of lysozyme activity. Both the spectroscopic technique and the molecular modeling method revealed that tetracyclines interact with lysozyme mainly through electrostatic forces. The binding of tetracyclines can cause the secondary structure and the microenvironment of the tryptophan residues of lysozyme.(3) All the three tetracyclines (OTC, TC and CTC) can interact with trypsin with one binding site to form tetracyclines-trypsin complex, mainly through van der Waals'interactions and hydrogen bonds with the affinity order:TC>OTC>CTC. The bound tetracyclines can result in inhibition of trypsin activity with the inhibition order:CTC>OTC>TC. Both the molecular docking study and the trypsin activity experiment revealed that OTC and TC bound into S1binding pocket, competitively inhibiting the enzyme activity, and CTC was a non-competitive inhibitor which bound to a non-active site of trypsin, different from TC and OTC due to the Cl atom on the benzene ring of CTC which hinders CTC entering into the S1binding pocket. The secondary structure and the microenvironment of the tryptophan residues of trypsin were also changed because of the bound tetracyclines. However, the effect of CTC on the secondary structure content of trypsin was contrary to those of TC and OTC. The related research results were published on Science of the Total Environment, Chemosphere and PLoS ONE.
3The toxic interaction mechanism of tetracyclines with human red blood cells
The common tetracyclines OTC and TC can enter red blood cells (RBCs). We studied the micromechanism of the toxicity of tetracyclines to RBCs. The experimental results revealed that:(1) OTC can reduce the antioxidant capacity of RBCs and induce oxidative stress, causing the following toxic effects:OTC can change the morphology of RBCs and further resulting in hemolysis (OTC concentration higher than8×10-5mol L-1). At low OTC dose, the ATPase activity increased. However, at higher dose, OTC can inhibit the activity of ATPase, affecting cell function.(2) Utilizing the flow cytometry, we established the detection methods for the indicators of antioxidant activity of RBCs (glutathione and reactive oxygen species (ROS)) and investigated the impact of TC on their content in RBCs. The experimental results indicated that TC can result in the reduction of glutathione content in RBCs to reduce the function of the antioxidant defense system of RBCs. The cellular oxidative/antioxidant balance was destroyed, so the ROS concentration in RBCs increased, causing oxidative stress which can lead to the damage of cellular structure and function.(3) OTC and TC can interact with hemoglobin with one binding site to form complex, mainly through van der Waals and hydrogen bond interactions. Both the synchronous fluorescence experiment and the molecular modeling study revealed that OTC and TC bind into hemoglobin central cavity. The bound OTC and TC can change the secondary structure and the microenvironment of the tyrosine residues of hemoglobin. A part of the research results were published on Journal of Hazardous Materials.
The thesis makes exploratory research on the micromechanism of the toxicity of tetracyclines and obtains innovative research results, which is conducive to in-depth understanding of the toxicity of tetracyclines. The established new methods for the research on the toxic mechanism of tetracyclines can provide the methodological reference and technical support for the toxicity evaluation of other pollutants.
四环素类药物在畜牧业和水产养殖业中有广泛应用。由于生物利用率较低,50-80%的四环素类药物未经代谢而进入环境成为污染物。残留在土壤、地表水、地下水、甚至饮用水等环境以及动物源食品(如蛋、奶、肉等)中的四环素类污染物能经由食物链或以饮食方式进入人体,对人类健康形成威胁。四环素类药物残留的污染问题及其毒性已引起了世界范围内的关注,并已有大量相关报道,但国内外已有的研究成果还不能彻底阐释环境中药物残留对生态及人类健康的内在作用机制。本论文在已报道的相关研究成果的基础上,以四环素类污染物致机体毒性的作用靶点功能蛋白质和细胞为对象,研究了常见四环素类污染物(土霉素OTC、四环素TC和金霉素CTC, TCs)毒性的微观机制,得到以下研究结果：
1OTC和TC与血清白蛋白相互作用的机理研究
血清白蛋白是各种内源性和外源性化合物在血液中运输的载体。本文在利用公式校正荧光内滤效应的基础上研究了OTC和TC与血清白蛋白(BSA和HSA)的相互作用。分子探针的研究结果表明,OTC和TC与位于血清白蛋白子域ⅢA的位点Ⅱ结合。计算得到的△H°矿和△S°分别为负值和正值,说明OTC和TC与血清白蛋白非共价结合的主要作用力为静电作用力。利用分子模拟方法进一步确定OTC和TC的结合位置为位于位点Ⅱ的正电荷氨基酸残基(对于BSA为ARG433或ARG436,对于HSA为ARG410或LYS414)。紫外可见吸收光谱、同步荧光光谱和圆二色谱的实验结果表明,结合的OTC和TC导致血清白蛋白的二级结构和色氨酸残基微环境发生改变。相关研究结果已分别发表在Biomacromolecules和Journal of Agricultural and Food Chemistry上。
2TCs与其毒性相关的功能蛋白酶的作用机理研究
已有研究结果表明,TCs能使过氧化氢酶、溶菌酶和胰蛋白酶等功能蛋白酶的活性下降。本文利用光谱学技术结合分子对接研究了TCs毒性的微观机制。实验结果表明：(1)OTC以一个结合位点通过范德华力和氢键作用力与过氧化氢酶作用形成复合物。结合的OTC使过氧化氢酶的二级结构和色氨酸残基微环境发生改变,使过氧化氢酶活性受到抑制；(2) OTC、TC和CTC以一个结合位点与位于溶菌酶表面裂缝的活性中心中的两个关键氨基酸残基(Glu35或Asp52)作用,竞争性抑制溶菌酶活性,结合强度的顺序为：CTC>TC>OTC。分子对接和热力学分析的结果均表明,静电作用力在TCs与溶菌酶的作用过程中占主导地位。结合的TCs使溶菌酶的二级结构和色氨酸残基的微环境发生改变。(3)OTC、TC和CTC均能以一个结合位点与胰蛋白酶通过范德华力和氢键作用力作用形成复合物,结合强度的顺序为：TC>OTC>CTC。结合的TCs能抑制胰蛋白酶活性,抑制程度大小顺序为：CTC>OTC>TC。分子对接和胰蛋白酶活性实验的结果均表明OTC和TC与胰蛋白酶的S1结合口袋结合,竞争性抑制酶活性；由于在CTC苯环上的氯原子阻碍苯环进入S1结合口袋,CTC与胰蛋白酶的非酶活性中心位点结合,非竞争性抑制胰蛋白酶活性。结合的TCs使胰蛋白酶的二级结构和色氨酸残基的微环境发生改变,但不同的结合位置使CTC对胰蛋白酶二级结构的影响与OTC和TC相反。相关工作已分别发表在Science of The Total Environment, Chemosphere和PLoS ONE上。
3TCs对人血红细胞毒性的作用机理研究
常见的TCs (OTC和TC)均能进入红细胞,本文考察了其对红细胞毒性的微观作用机理。研究结果表明：(1)OTC能引起红细胞抗氧化防御体系功能下降,导致红细胞氧化应激,导致以下毒性效应：使红细胞的形态发生变化,并进一步导致红细胞溶血(OTC浓度大于8×10-5mol L-1)。在低浓度下(≤4×10-5mol L-1), OTC能使红细胞ATP酶活性增强；随浓度进一步增大,OTC能抑制ATP酶活性,影响细胞功能；(2)利用流式细胞术探索性建立反映红细胞抗氧化性的指标(谷胱甘肽和活性氧)的检测方法,并考察了TC对其含量的影响。结果表明,TC能导致红细胞谷胱甘肽含量减少,从而使细胞抗氧化防御体系功能降低,导致细胞氧化/抗氧化平衡稳态被破坏,进而使ROS浓度升高,造成氧化应激,能引起细胞结构和功能的损伤；(3)OTC和TC均以一个作用位点与血红蛋白通过范德华力和氢键作用力结合形成复合物。同步荧光实验和分子对接均表明,OTC和TC在血红蛋白上的结合位置为四个亚基之间的中央空穴。结合的OTC和TC能改变血红蛋白的结构和酪氨酸残基的微环境。部分研究结果已经在Journal of Hazardous Materials上发表。
本论文对TCs致机体毒性的微观机制进行了探索性研究,取得了具有创新性的研究成果,有利于深入认识TCs的毒性；论文建立的研究TCs毒性作用机理的新方法可为其他环境污染物的毒性评价提供方法学的参考和技术支持。
Protein is the material base for life, being involved in every cell and all important part of body and closely linked to various forms of life activities. The cell is the basic unit of the metabolic activity of biological organism. The harmful factors in the external environment, such as physical (ionizing radiation, noise, ultraviolet, etc.), chemical and biological (bacteria, viruses, etc.) ones, can act on the body through various means (such as respiratory tract, digestive tract, skin and wound), inducing changes in body structure and function, all reflecting those in cell structure and function. So the changes in cell structure and function are the basis for the injuries to the body induced by exogenous harmful substances.
Tetracyclines are widely used in animal husbandry and aquaculture. Because of their low bioavailability,50-80%of the applied dose enters the environment without metabolism, becomes a pollutant. The tetracycline residues in the environment such as soil, surface water, groundwater, even drinking water, and animal food (egg, milk, meat, etc.) can enter human bodies by food chain or diet, being potentially harmful. The pollution of tetracycline residues and their toxicity has attracted worldwide attention. There have been many related reports, but the existing research results can not completely explain the inner mechanism of the residues in the environment to ecology and human health. In this thesis, on the basis of the existing related research results, with the targets of the tetracyclines induced toxicity (functional proteins and cell) as the object, we investigated the micromechanism of the toxicity of the common tetracyclines (oxytetracycline (OTC), tetracycline (TC) and chlortetracycline (CTC)) and obtained the following findings:
1The interaction mechanism of OTC and TC with serum albumins
Serum albumins are the carrier of a wide variety of endogenous and exogenous compounds in blood. We studied the interaction of OTC and TC with serum albumins based on the elimination of inner filter effect with the correction equation. The site marker competition experiments revealed that OTC and TC bind to site Ⅱ (subdomain ⅢA) of serum albumins, mainly with electrostatic interaction indicated by the calculated negative ΔH°and positive ΔS°. The molecular modeling methods were applied to further define that the binding site for OTC and TC was the positively charged amino acid residues in site II (ARG433or ARG436for BSA, ARG410and LYS414for HSA). The UV-visible absorption, synchronous fluorescence and circular dichroism results showed that the bound OTC and TC can change the secondary structure and the microenvironment of the tryptophan residues of BSA and HSA. The research results were published on Biomacromolecules and Journal of Agricultural and Food Chemistry.
2The interaction mechanism of tetracyclines with the functional enzymes related to tetracyclines toxicity
It have been reported that tetracyclines can result in the decrease of the activity of catalase, lysozyme and trypsin. We investigated the micromechanism of the toxicity of tetracyclines by multispectroscopic techniques and molecular modeling method. The experimental results indicated that:(1) OTC can interact with catalase to form a complex mainly by van der Waals'interactions and hydrogen bonds with one binding site. The binding of OTC can result in change of the secondary structure and the microenvironment of the tryptophan residues of catalase. The activity of catalase was also inhibited for the bound OTC.(2) All the three tetracyclines OTC, TC and CTC can bind into lysozyme cleft and interact with the key active-site residues Glu35or Asp52with one binding site, with the affinity order:CTC>TC>OTC, resulting in competitive inhibition of lysozyme activity. Both the spectroscopic technique and the molecular modeling method revealed that tetracyclines interact with lysozyme mainly through electrostatic forces. The binding of tetracyclines can cause the secondary structure and the microenvironment of the tryptophan residues of lysozyme.(3) All the three tetracyclines (OTC, TC and CTC) can interact with trypsin with one binding site to form tetracyclines-trypsin complex, mainly through van der Waals'interactions and hydrogen bonds with the affinity order:TC>OTC>CTC. The bound tetracyclines can result in inhibition of trypsin activity with the inhibition order:CTC>OTC>TC. Both the molecular docking study and the trypsin activity experiment revealed that OTC and TC bound into S1binding pocket, competitively inhibiting the enzyme activity, and CTC was a non-competitive inhibitor which bound to a non-active site of trypsin, different from TC and OTC due to the Cl atom on the benzene ring of CTC which hinders CTC entering into the S1binding pocket. The secondary structure and the microenvironment of the tryptophan residues of trypsin were also changed because of the bound tetracyclines. However, the effect of CTC on the secondary structure content of trypsin was contrary to those of TC and OTC. The related research results were published on Science of the Total Environment, Chemosphere and PLoS ONE.
3The toxic interaction mechanism of tetracyclines with human red blood cells
The common tetracyclines OTC and TC can enter red blood cells (RBCs). We studied the micromechanism of the toxicity of tetracyclines to RBCs. The experimental results revealed that:(1) OTC can reduce the antioxidant capacity of RBCs and induce oxidative stress, causing the following toxic effects:OTC can change the morphology of RBCs and further resulting in hemolysis (OTC concentration higher than8×10-5mol L-1). At low OTC dose, the ATPase activity increased. However, at higher dose, OTC can inhibit the activity of ATPase, affecting cell function.(2) Utilizing the flow cytometry, we established the detection methods for the indicators of antioxidant activity of RBCs (glutathione and reactive oxygen species (ROS)) and investigated the impact of TC on their content in RBCs. The experimental results indicated that TC can result in the reduction of glutathione content in RBCs to reduce the function of the antioxidant defense system of RBCs. The cellular oxidative/antioxidant balance was destroyed, so the ROS concentration in RBCs increased, causing oxidative stress which can lead to the damage of cellular structure and function.(3) OTC and TC can interact with hemoglobin with one binding site to form complex, mainly through van der Waals and hydrogen bond interactions. Both the synchronous fluorescence experiment and the molecular modeling study revealed that OTC and TC bind into hemoglobin central cavity. The bound OTC and TC can change the secondary structure and the microenvironment of the tyrosine residues of hemoglobin. A part of the research results were published on Journal of Hazardous Materials.
The thesis makes exploratory research on the micromechanism of the toxicity of tetracyclines and obtains innovative research results, which is conducive to in-depth understanding of the toxicity of tetracyclines. The established new methods for the research on the toxic mechanism of tetracyclines can provide the methodological reference and technical support for the toxicity evaluation of other pollutants.
引文
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