Wang Zhen-Dong, Han Shan, Gu Ji-Hong, Huang Zhi-Feng, Liu Mei-Xian, Zhuo Yue
Science and Technology Innovation Center,Guangzhou University of Chinese Medicine Guangzhou 510405,China.
the First Affiliated Hospital of Guangzhou University of Chinese Medicine Guangzhou 510405,China.
Zhongguo Zhong Yao Za Zhi. 2024 Sep;49(17):4744-4754. doi: 10.19540/j.cnki.cjcmm.20240516.702.
Salt-processed Psoraleae Fructus is a commonly used tonic in clinical practice. However, its usage is restricted due to the inherent toxicity. The covalent modification of proteins by reactive metabolites(RMs) plays a role in the hepatotoxicity of salt-processed Psoraleae Fructus. This study delves into the protein covalent modification by RMs generated from psoralen/isopsoralen, the primary toxic components of salt-processed Psoraleae Fructus, by liquid chromatography-mass spectrometry(LC-MS), aiming to elucidate the mechanism underlying the hepatic injury induced by salt-processed Psoraleae Fructus. Biochemical methods were utilized to measure the levels of alanine aminotransferase(ALT), aspartate aminotransferase(AST), catalase(CAT), malondialdehyde(MDA), superoxide dismutase(SOD), reduced glutathione(GSH), and glutathione S-transferase(GST) in mice. The pathological changes in the liver were observed by hematoxylin-eosin(HE) staining. Subsequently, ultra performance liquid chromatography-quadrupole-time-of-flight-mass spectrometry(UPLC-Q-TOF-MS) was employed to identify the primary toxic components of psoralen/isopsoralen and the RMs in salt-processed Psoraleae Fructus. Covalent bonding adducts of the toxic components/RMs with GSH and free amino acids were identified to investigate the effects of the toxic components on modification sites and patterns of amino acids. The modifications of RMs were incorporated into the variable modifications of Proteome Discoverer, and the target proteins of psoralen/isopsoralen were detected by liquid chromatography-quadrupole exactive-mass spectrometry. Lastly, Label-free quantitative proteomics was adopted to screen differential proteins, which were further subjected to KEGG and GO enrichment analyses and confirmed by qPCR. The results indicated that compared with the control group, salt-processed Psoraleae Fructus significantly elevated the ALT, AST, and MDA levels and lowered the SOD, CAT, GSH, and GST levels in a dose-dependent manner, while causing obvious vacuolization and inflammatory cell infiltration in mouse hepatocytes. Furthermore, the livers of mice in the salt-processed Psoraleae Fructus group showed the presence of five RMs of psoralen/isopsoralen, two adducts with GSH, and one adduct with cysteine. In addition, 10 proteins modified by the RMs of psoralen/isopsoralen were identified. A total of 133 differential proteins were detected in the livers of mice in the salt-processed Psoraleae Fructus group, including 92 with up-regulated expression and 41 with down-regulated expression. These differential proteins mainly involved ribosomes, rRNAs, and glutathione, affecting the proteasome pathway. The qPCR results were consistent with the differential proteins. These findings suggest that the RMs of psoralen/isopsoralen can covalently bind to GSH and modify cysteine and lysine residues of liver proteins. This covalent modification of proteins by harmful substances can potentially result in liver damage. Therefore, it can be inferred that the oxidative stress damage induced by salt-processed Psoraleae Fructus may be associated with the abnormality of proteasome and its complex, biosynthesis of ribosomes and their nucleoprotein complex, rRNA binding, and glutathione binding.
盐炙补骨脂是临床常用的滋补药。然而,由于其固有的毒性,其使用受到限制。活性代谢产物(RMs)对蛋白质的共价修饰在盐炙补骨脂的肝毒性中起作用。本研究通过液相色谱-质谱联用(LC-MS)深入研究补骨脂素/异补骨脂素(盐炙补骨脂的主要毒性成分)产生的RMs对蛋白质的共价修饰,旨在阐明盐炙补骨脂引起肝损伤的机制。采用生化方法检测小鼠血清中谷丙转氨酶(ALT)、谷草转氨酶(AST)、过氧化氢酶(CAT)、丙二醛(MDA)、超氧化物歧化酶(SOD)、还原型谷胱甘肽(GSH)和谷胱甘肽S-转移酶(GST)水平。通过苏木精-伊红(HE)染色观察肝脏的病理变化。随后,采用超高效液相色谱-四极杆-飞行时间质谱(UPLC-Q-TOF-MS)鉴定补骨脂素/异补骨脂素的主要毒性成分及盐炙补骨脂中的RMs。鉴定毒性成分/RMs与GSH和游离氨基酸的共价结合加合物,以研究毒性成分对氨基酸修饰位点和模式的影响。将RMs的修饰纳入Proteome Discoverer的可变修饰中,通过液相色谱-四极杆精确质量质谱检测补骨脂素/异补骨脂素的靶蛋白。最后,采用无标记定量蛋白质组学筛选差异蛋白,对差异蛋白进行KEGG和GO富集分析,并通过qPCR进行验证。结果表明,与对照组相比,盐炙补骨脂可使小鼠ALT、AST和MDA水平显著升高,SOD、CAT、GSH和GST水平呈剂量依赖性降低,同时引起小鼠肝细胞明显空泡化和炎性细胞浸润。此外,盐炙补骨脂组小鼠肝脏中存在补骨脂素/异补骨脂素的5种RMs、2种与GSH的加合物和1种与半胱氨酸的加合物。此外,鉴定出10种被补骨脂素/异补骨脂素的RMs修饰的蛋白质。盐炙补骨脂组小鼠肝脏共检测到133种差异蛋白,其中表达上调92种,表达下调41种。这些差异蛋白主要涉及核糖体、rRNA和谷胱甘肽,影响蛋白酶体途径。qPCR结果与差异蛋白结果一致。这些发现表明,补骨脂素/异补骨脂素的RMs可与GSH共价结合,修饰肝脏蛋白质的半胱氨酸和赖氨酸残基。有害物质对蛋白质的这种共价修饰可能导致肝脏损伤。因此,可以推断盐炙补骨脂诱导的氧化应激损伤可能与蛋白酶体及其复合物异常、核糖体及其核蛋白复合物的生物合成、rRNA结合和谷胱甘肽结合有关。