DBDCT致肝毒性的蛋白质组学及Trxl介导的氧化应激机制研究
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摘要
目的：建立[二-(4-氯苯甲酰异羟肟酸)二正丁基合锡](DBDCT)体内与体外的肝毒性模型，采用蛋白质组学技术分别对其作用前后蛋白质表达谱的改变进行分析及鉴定，通过对差异蛋白的验证及其功能分析，推测DBDCT引起肝毒性的主要作用机制。通过对由差异蛋白Trx1介导的氧化应激信号通路的研究，探讨DBDCT引起肝毒性的氧化应激作用机制及其毒性靶蛋白。
方法：（1）SD大鼠腹腔注射DBDCT，并记录动物体重变化及其肝脏系数，分别检测血浆肝功生化指标，肝组织病理学变化以及锡的肝脏蓄积，以确定其对大鼠的肝脏毒性。（2）采用2-DE-TOF-TOF-MS分别对正常组和DBDCT染毒组大鼠肝脏膜蛋白和核蛋白表达谱进行分析，鉴定及其验证。（3）分别采用MTT法，透射电镜，比色法以及流式细胞术检测DBDCT对HL02肝细胞的抑制活性，细胞形态变化，胞外LDH含量，细胞凋亡、周期以及胞内ROS含量，初步探讨DBDCT对HL02细胞的毒性作用及其机制。（4）采用2-DE-TOF-TOF-MS对DBDCT处理前后HL02细胞总蛋白表达谱进行分析，鉴定，并采用比色法、Western blot和RT-PCR方法对差异蛋白的功能及其表达进行验证。（5）采用Western blot和RT-PCR方法对差异蛋白Trx1，PARK7介导的氧化应激通路下游因子ASK1，JNK和P38进行检测；同时采用抗氧化剂乙酰-L-半胱氨酸(NAC)与DBDCT体外共同孵育，检测细胞存活率，ROS含量及其上述因子的蛋白变化水平。
结果：（1）大鼠腹腔注射DBDCT2.3、3.2、4.5mg/kg后，动物体重逐渐增加，且随着给药次数的增加，动物出现不同程度的腹水现象，自发活动减少，嗜睡，高剂量组部分动物死亡；肝脏系数随着给药浓度的增加逐渐减少；DBDCT中高剂量染毒组AST，AKP和ACP水平明显升高，而ALT水平随着给药剂量的增加逐渐降低；病理切片可见DBDCT中剂量组有散发肝细胞嗜酸性变，核固缩，高剂量组被膜增生，部分肝细胞嗜酸性变，核固缩；原子吸收结果显示锡在大鼠肝脏形成一定的蓄积，且呈现明显的量效关系。（2）采用2-DE-TOF-TOF-MS共分析并鉴定出6个膜蛋白和10个核蛋白，包括甘油醛-3-磷酸脱氢酶(RGD1565368)，磷脂酰乙醇胺凝结蛋白(Pebp1)，醋酸盐水解酶1(Iah1)，S-腺苷甲硫氨酸合酶(Mat1a)，谷氨酸脱氢酶1(Glud1)，翻译起始因子5A-1(Eif5a)，腺苷酸激酶2(KAD2)，蛋白质二硫化物异构酶A3(PDIA3)，丁二酸脱氢酶(DHSA)，乙醛脱氢酶(ALDH2)，谷胱甘肽S-转移酶(GSTM2)，热休克蛋白(HS90B)，二甲基甘氨酸脱氢酶(M2GD)，4-羟苯(基)丙酮酸双(加)氧酶(HPPD)，鸟氨酸转氨酶(OAT)。上述差异蛋白主要参与氧化还原/氧化应激，线粒体呼吸链电子传递，酶代谢以及氨基酸合成等生命过程。（3）体外肝毒性研究结果显示DBDCT对HL02细胞的IC50值为5.77μM，且细胞固缩变圆，结构模糊，核膜破裂，胞外LDH水平明显升高。流式细胞术检测结果显示DBDCT染毒组细胞出现不同程度的凋亡与坏死，G2/M期发生阻滞，且胞内ROS含量逐渐升高。根据上述结果初步推测DBDCT的细胞肝毒性与细胞凋亡，周期阻滞及其氧化应激有关。（4）通过2-DE-TOF-TOF-MS对DBDCT作用前后HL02肝细胞总蛋白分析鉴定共得到9个差异蛋白，硫氧还蛋白(Trx1)，核苷酸结合蛋白(HINT1)，蛋白DJ1(PARK7)，细胞色素C氧化酶亚型5A(COX5A)，半乳糖凝集素-1(Gal-1)，过氧化物酶2(PRDX2)，过氧化物歧化酶(SODM)，3-羟酰辅酶A脱氢酶2(HCD2)，NADH脱氢酶(NDUS8)，且Western blot和RT-PCR对差异蛋白Trx1和PARK7的验证结果与2-DE结果一致。鉴定的差异蛋白主要参与细胞的氧化还原/氧化应激，线粒体相关功能，细胞凋亡、增殖与分化以及微管的调节等过程，其中氧化应激反应占据重要地位。（5）由Trx1介导的氧化应激通路研究显示DBDCT干预细胞后，Trx1、DJ1、ASK1的蛋白表达和mRNA表达水平均升高， JNK和P38发生了蛋白磷酸化修饰，且呈现明显的时效与量效关系。N-乙酰-L-半胱氨酸(NAC)与DBDCT共同孵育细胞后，ROS表达水平明显下降，而细胞存活率上升，Trx1，DJ1蛋白的表达较DBDCT组降低，且JNK和P38的磷酸化水平也明显下降。其可能的作用机制为DBDCT诱导细胞自由基水平升高，使得Trx1蛋白表达升高以抵抗氧化应激作用，此时的Trx1逐渐失去了与ASK1的结合能力，使得ASK1游离；同时作为氧化应激的伴侣蛋白，DJ1也被激活并与死亡蛋白Daxx结合，进而抑制Daxx与ASK1的结合，使得游离的ASK1表达升高，激活MAPK通路中的JNK和P38，最终导致细胞凋亡与坏死。结论：（1）体内外研究证明，DBDCT可引起明显的肝毒性。（2）氧化应激反应在毒性作用中占据重要地位，且主要通过升高胞内自由基水平，激活由Trx1介导的氧化应激通路来实现的。（3）抗氧化剂NAC可通过降低胞内ROS水平，进而影响Trx1介导的氧化应激通路以抵抗DBDCT引起的肝毒性。（4）Trx1蛋白可作为DBDCT引发肝毒性的早期监测指标。
Objective: To investigate di-n-butyl-di-(4-chlorobenzohydroxamato) tin (IV)(DBDCT) induced hepatotoxic mechanism using proteomics methods. To study thedifferentially expressed protein-Trx1mediated oxidative stress signaling pathway. Tosearch the potential biomarkers for the early diagnosis of hepatotoxicity.
Methods:(1) SD rats were treated with DBDCT intraperitoneally, and the bodyweight, liver weight ratio, plasma biochemistry, liver histopathology and total Snwere recorded and determined.(2)2-DE-TOF-TOF-MS was performed to analyzeand identify the differentially expressed proteins between control and DBDCT-treatedgroups in vivo.(3) Cytotoxicities of DBDCT to HL-02cells were assessed using MTTmethod. The morphology was examined under transmission electron microscope. Theextracellular level of LDH was determined using colorimetric method. The cellapoptosis, cell circles and the intracellular level of ROS were detected by flowcytometrye.(4) The total protein of HL02cell line was separated by2-DE, and thedifferentially expressed proteins between DBDCT-treated and untreated groups wereidentified by MALDI-TOF-TOF-MS. Meanwhile, the expression and function of twoidentified proteins were verified by Western blot and RT-PCR methods.(5) Theexpression of ASK1, JNK and P38, the downstream factors of Trx1-medited oxidativestress signaling pathway, were determined in DBDCT-treated group using Westernblot and RT-PCR methods. The cell viability, the level of ROS and the expression ofabove factors were detected after the treatment of antioxidant NAC and DBDCT.
Results:(1) The body weight was increased followed with ascites, lethargy anddecreased spontaneous activity in DBDCT treated groups, and several animals weredied in high-dose group. The liver weight ratio was decreased in DBDCT-treatedgroups with an obvious does-effect relationship. The levels of AST，AKP and ACPwere increased significantly in middle and high-dose treated groups. However, the ALT level was decreased. The liver cells eosinophilic change and karyopyknosis wereobserved in middle and high-dose treated groups. The atomic absorption resultsshowed that there was a certain accumulation of tin in rat liver and observed in a dosedependent manner.(2) Sixteen proteins were indentified according to the2-DE-TOF-TOF-MS, including glyceraldehyde-3-phosphate dehydrogenase(RGD1565368). Phosphatidylethanolamine-binding protein1(Pebp1), Isoamylacetate-hydrolyzing esterase1homolog (Iah1), S-adenosylmethionine synthaseisoform type-1(Mat1a), Glutamate dehydrogenase1(Glud1), Eukaryotic translationinitiation factor5A-1(Eif5a), Isoform2of Adenylate kinase2(KAD2), Proteindisulfide-isomerase A3(PDIA3), Succinate dehydrogenase (DHSA), Aldehydedehydrogenase (ALDH2), Glutathione S-transferase Mu2(GSTM2), Heat shockprotein HSP90-beta (HS90B), Dimethylglycine dehydrogenase (M2GD),4-hydroxyphenylpyruvate dioxygenase (HPPD), Ornithine aminotransferase (OAT).The identified proteins were participated in the process of oxidoreduction/oxidativestress, electronical transmission of mitochondrial respiratory chain, enzymaticmetabolism and synthesis of amino acid.(3) The IC50value of DBDCT to HL-7702cells was5.77μM at24h. The morphology showed that the cell contour becameblurred gradually, the nuclear membrane was fractured followed with the highexpression of extracellular LDH in DBDCT-treated group. Compared with the controlgroup, DBDCT could obvious increase the cell apoptosis, the release of ROS andcould induce the cycle arrest. The results indicated that cell apoptosis, oxidative stressand cycle arrest might be the major hepatotoxic mechanism.(4) Nine proteins wereindentified according to the2-DE-TOF-TOF-MS in vitro, including Thioredoxin1(Trx1), Histidine triad nucleotide-binding protein1(HINT1), Protein DJ-1(PARK7),Cytochrome c oxidase subunit5A (COX5A), Galectin-1(Gal-1), Peroxiredoxin-2(PRDX2), Superoxide di (SODM), Isoform1of3-hydroxyacyl-CoA dehydrogenasetype-2(HCD2), and NADH dehydrogenase [ubiquinone] iron-sulfur protein8(NDUS8). The expression of Trx1and PARK7were checked by Western blot andRT-PCR methods to gain the identical results with2-DE. The identified proteins wereparticipated in the process of oxidoreduction/oxidative stress, electronical transmission of mitochondrial respiratory chain, regulation of microtubule, cellapoptosis, proliferation and differentiation.(5) The study on Trx1-mediated oxidativestress pathway showed that the expression of Trx1, DJ1, ASK1, JNK and P38wereincreased significantly with an obvious dose and time dependent manner on bothprotein and mRNA levels. However, after the co-treated with NAC, the cell viabilitywas increased followed with the decreased expression of ROS. Meanwhile, the levelsof Trx1, DJ1, JNK and P38were decreased significantly. According to the results, wepresumed that oxidative stress was the major hepatotoxic mechanism. DBDCT couldinduce the high expression of free radical, then Trx1was dissociated from ASK1toresist the redundant free radical, regulated the JNK/P38signaling pathway resultingin cell apoptosis. Meanwhile, as a chaperonin of oxidative stress, DJ1was also highexpressed to bind with Daxx which was integrated with ASK1in normal cells.Therefore, ASK1was liberated to activate the JNK/P38signaling pathway.
Conclusions:(1) DBDCT presented obvious hepatotoxicity in vivo and in vitro.(2)DBDCT could evoke the high expression of ROS to activate Trx1-mediated oxidativestress signaling pathway to result in the cell apoptosis and necrosis. Therefore,oxidative stress played an important role in DBDCT-induced hepatotoxicity.(3)Antioxidant NAC could decrease the ROS level to intercept Trx1-mediated oxidativestress signaling pathway to resist DBDCT-induced hepatotoxiciy.(4) Trx1might be apotential biomarker for the early diagnosis of hepatotoxicity induced by DBDCT.
方法：（1）SD大鼠腹腔注射DBDCT，并记录动物体重变化及其肝脏系数，分别检测血浆肝功生化指标，肝组织病理学变化以及锡的肝脏蓄积，以确定其对大鼠的肝脏毒性。（2）采用2-DE-TOF-TOF-MS分别对正常组和DBDCT染毒组大鼠肝脏膜蛋白和核蛋白表达谱进行分析，鉴定及其验证。（3）分别采用MTT法，透射电镜，比色法以及流式细胞术检测DBDCT对HL02肝细胞的抑制活性，细胞形态变化，胞外LDH含量，细胞凋亡、周期以及胞内ROS含量，初步探讨DBDCT对HL02细胞的毒性作用及其机制。（4）采用2-DE-TOF-TOF-MS对DBDCT处理前后HL02细胞总蛋白表达谱进行分析，鉴定，并采用比色法、Western blot和RT-PCR方法对差异蛋白的功能及其表达进行验证。（5）采用Western blot和RT-PCR方法对差异蛋白Trx1，PARK7介导的氧化应激通路下游因子ASK1，JNK和P38进行检测；同时采用抗氧化剂乙酰-L-半胱氨酸(NAC)与DBDCT体外共同孵育，检测细胞存活率，ROS含量及其上述因子的蛋白变化水平。
结果：（1）大鼠腹腔注射DBDCT2.3、3.2、4.5mg/kg后，动物体重逐渐增加，且随着给药次数的增加，动物出现不同程度的腹水现象，自发活动减少，嗜睡，高剂量组部分动物死亡；肝脏系数随着给药浓度的增加逐渐减少；DBDCT中高剂量染毒组AST，AKP和ACP水平明显升高，而ALT水平随着给药剂量的增加逐渐降低；病理切片可见DBDCT中剂量组有散发肝细胞嗜酸性变，核固缩，高剂量组被膜增生，部分肝细胞嗜酸性变，核固缩；原子吸收结果显示锡在大鼠肝脏形成一定的蓄积，且呈现明显的量效关系。（2）采用2-DE-TOF-TOF-MS共分析并鉴定出6个膜蛋白和10个核蛋白，包括甘油醛-3-磷酸脱氢酶(RGD1565368)，磷脂酰乙醇胺凝结蛋白(Pebp1)，醋酸盐水解酶1(Iah1)，S-腺苷甲硫氨酸合酶(Mat1a)，谷氨酸脱氢酶1(Glud1)，翻译起始因子5A-1(Eif5a)，腺苷酸激酶2(KAD2)，蛋白质二硫化物异构酶A3(PDIA3)，丁二酸脱氢酶(DHSA)，乙醛脱氢酶(ALDH2)，谷胱甘肽S-转移酶(GSTM2)，热休克蛋白(HS90B)，二甲基甘氨酸脱氢酶(M2GD)，4-羟苯(基)丙酮酸双(加)氧酶(HPPD)，鸟氨酸转氨酶(OAT)。上述差异蛋白主要参与氧化还原/氧化应激，线粒体呼吸链电子传递，酶代谢以及氨基酸合成等生命过程。（3）体外肝毒性研究结果显示DBDCT对HL02细胞的IC50值为5.77μM，且细胞固缩变圆，结构模糊，核膜破裂，胞外LDH水平明显升高。流式细胞术检测结果显示DBDCT染毒组细胞出现不同程度的凋亡与坏死，G2/M期发生阻滞，且胞内ROS含量逐渐升高。根据上述结果初步推测DBDCT的细胞肝毒性与细胞凋亡，周期阻滞及其氧化应激有关。（4）通过2-DE-TOF-TOF-MS对DBDCT作用前后HL02肝细胞总蛋白分析鉴定共得到9个差异蛋白，硫氧还蛋白(Trx1)，核苷酸结合蛋白(HINT1)，蛋白DJ1(PARK7)，细胞色素C氧化酶亚型5A(COX5A)，半乳糖凝集素-1(Gal-1)，过氧化物酶2(PRDX2)，过氧化物歧化酶(SODM)，3-羟酰辅酶A脱氢酶2(HCD2)，NADH脱氢酶(NDUS8)，且Western blot和RT-PCR对差异蛋白Trx1和PARK7的验证结果与2-DE结果一致。鉴定的差异蛋白主要参与细胞的氧化还原/氧化应激，线粒体相关功能，细胞凋亡、增殖与分化以及微管的调节等过程，其中氧化应激反应占据重要地位。（5）由Trx1介导的氧化应激通路研究显示DBDCT干预细胞后，Trx1、DJ1、ASK1的蛋白表达和mRNA表达水平均升高， JNK和P38发生了蛋白磷酸化修饰，且呈现明显的时效与量效关系。N-乙酰-L-半胱氨酸(NAC)与DBDCT共同孵育细胞后，ROS表达水平明显下降，而细胞存活率上升，Trx1，DJ1蛋白的表达较DBDCT组降低，且JNK和P38的磷酸化水平也明显下降。其可能的作用机制为DBDCT诱导细胞自由基水平升高，使得Trx1蛋白表达升高以抵抗氧化应激作用，此时的Trx1逐渐失去了与ASK1的结合能力，使得ASK1游离；同时作为氧化应激的伴侣蛋白，DJ1也被激活并与死亡蛋白Daxx结合，进而抑制Daxx与ASK1的结合，使得游离的ASK1表达升高，激活MAPK通路中的JNK和P38，最终导致细胞凋亡与坏死。结论：（1）体内外研究证明，DBDCT可引起明显的肝毒性。（2）氧化应激反应在毒性作用中占据重要地位，且主要通过升高胞内自由基水平，激活由Trx1介导的氧化应激通路来实现的。（3）抗氧化剂NAC可通过降低胞内ROS水平，进而影响Trx1介导的氧化应激通路以抵抗DBDCT引起的肝毒性。（4）Trx1蛋白可作为DBDCT引发肝毒性的早期监测指标。
Objective: To investigate di-n-butyl-di-(4-chlorobenzohydroxamato) tin (IV)(DBDCT) induced hepatotoxic mechanism using proteomics methods. To study thedifferentially expressed protein-Trx1mediated oxidative stress signaling pathway. Tosearch the potential biomarkers for the early diagnosis of hepatotoxicity.
Methods:(1) SD rats were treated with DBDCT intraperitoneally, and the bodyweight, liver weight ratio, plasma biochemistry, liver histopathology and total Snwere recorded and determined.(2)2-DE-TOF-TOF-MS was performed to analyzeand identify the differentially expressed proteins between control and DBDCT-treatedgroups in vivo.(3) Cytotoxicities of DBDCT to HL-02cells were assessed using MTTmethod. The morphology was examined under transmission electron microscope. Theextracellular level of LDH was determined using colorimetric method. The cellapoptosis, cell circles and the intracellular level of ROS were detected by flowcytometrye.(4) The total protein of HL02cell line was separated by2-DE, and thedifferentially expressed proteins between DBDCT-treated and untreated groups wereidentified by MALDI-TOF-TOF-MS. Meanwhile, the expression and function of twoidentified proteins were verified by Western blot and RT-PCR methods.(5) Theexpression of ASK1, JNK and P38, the downstream factors of Trx1-medited oxidativestress signaling pathway, were determined in DBDCT-treated group using Westernblot and RT-PCR methods. The cell viability, the level of ROS and the expression ofabove factors were detected after the treatment of antioxidant NAC and DBDCT.
Results:(1) The body weight was increased followed with ascites, lethargy anddecreased spontaneous activity in DBDCT treated groups, and several animals weredied in high-dose group. The liver weight ratio was decreased in DBDCT-treatedgroups with an obvious does-effect relationship. The levels of AST，AKP and ACPwere increased significantly in middle and high-dose treated groups. However, the ALT level was decreased. The liver cells eosinophilic change and karyopyknosis wereobserved in middle and high-dose treated groups. The atomic absorption resultsshowed that there was a certain accumulation of tin in rat liver and observed in a dosedependent manner.(2) Sixteen proteins were indentified according to the2-DE-TOF-TOF-MS, including glyceraldehyde-3-phosphate dehydrogenase(RGD1565368). Phosphatidylethanolamine-binding protein1(Pebp1), Isoamylacetate-hydrolyzing esterase1homolog (Iah1), S-adenosylmethionine synthaseisoform type-1(Mat1a), Glutamate dehydrogenase1(Glud1), Eukaryotic translationinitiation factor5A-1(Eif5a), Isoform2of Adenylate kinase2(KAD2), Proteindisulfide-isomerase A3(PDIA3), Succinate dehydrogenase (DHSA), Aldehydedehydrogenase (ALDH2), Glutathione S-transferase Mu2(GSTM2), Heat shockprotein HSP90-beta (HS90B), Dimethylglycine dehydrogenase (M2GD),4-hydroxyphenylpyruvate dioxygenase (HPPD), Ornithine aminotransferase (OAT).The identified proteins were participated in the process of oxidoreduction/oxidativestress, electronical transmission of mitochondrial respiratory chain, enzymaticmetabolism and synthesis of amino acid.(3) The IC50value of DBDCT to HL-7702cells was5.77μM at24h. The morphology showed that the cell contour becameblurred gradually, the nuclear membrane was fractured followed with the highexpression of extracellular LDH in DBDCT-treated group. Compared with the controlgroup, DBDCT could obvious increase the cell apoptosis, the release of ROS andcould induce the cycle arrest. The results indicated that cell apoptosis, oxidative stressand cycle arrest might be the major hepatotoxic mechanism.(4) Nine proteins wereindentified according to the2-DE-TOF-TOF-MS in vitro, including Thioredoxin1(Trx1), Histidine triad nucleotide-binding protein1(HINT1), Protein DJ-1(PARK7),Cytochrome c oxidase subunit5A (COX5A), Galectin-1(Gal-1), Peroxiredoxin-2(PRDX2), Superoxide di (SODM), Isoform1of3-hydroxyacyl-CoA dehydrogenasetype-2(HCD2), and NADH dehydrogenase [ubiquinone] iron-sulfur protein8(NDUS8). The expression of Trx1and PARK7were checked by Western blot andRT-PCR methods to gain the identical results with2-DE. The identified proteins wereparticipated in the process of oxidoreduction/oxidative stress, electronical transmission of mitochondrial respiratory chain, regulation of microtubule, cellapoptosis, proliferation and differentiation.(5) The study on Trx1-mediated oxidativestress pathway showed that the expression of Trx1, DJ1, ASK1, JNK and P38wereincreased significantly with an obvious dose and time dependent manner on bothprotein and mRNA levels. However, after the co-treated with NAC, the cell viabilitywas increased followed with the decreased expression of ROS. Meanwhile, the levelsof Trx1, DJ1, JNK and P38were decreased significantly. According to the results, wepresumed that oxidative stress was the major hepatotoxic mechanism. DBDCT couldinduce the high expression of free radical, then Trx1was dissociated from ASK1toresist the redundant free radical, regulated the JNK/P38signaling pathway resultingin cell apoptosis. Meanwhile, as a chaperonin of oxidative stress, DJ1was also highexpressed to bind with Daxx which was integrated with ASK1in normal cells.Therefore, ASK1was liberated to activate the JNK/P38signaling pathway.
Conclusions:(1) DBDCT presented obvious hepatotoxicity in vivo and in vitro.(2)DBDCT could evoke the high expression of ROS to activate Trx1-mediated oxidativestress signaling pathway to result in the cell apoptosis and necrosis. Therefore,oxidative stress played an important role in DBDCT-induced hepatotoxicity.(3)Antioxidant NAC could decrease the ROS level to intercept Trx1-mediated oxidativestress signaling pathway to resist DBDCT-induced hepatotoxiciy.(4) Trx1might be apotential biomarker for the early diagnosis of hepatotoxicity induced by DBDCT.
引文
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