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Article(id=1194617494641021242, tenantId=1146029695717560320, journalId=1189873630562394117, issueId=1194617490446721194, articleNumber=null, orderNo=null, doi=10.11855/j.issn.0577-7402.1567.2024.0418, pmid=null, cstr=null, oa=null, hot=null, price=null, onlineType=0, articleFormat=0, articleType=null, articleTypeStr=research-article, receivedDate=1701014400000, receivedDateStr=2023-11-27, revisedDate=null, revisedDateStr=null, acceptedDate=1706544000000, acceptedDateStr=2024-01-30, onlineDate=1762748605642, onlineDateStr=2025-11-10, pubDate=1740672000000, pubDateStr=2025-02-28, doiRegisterDate=null, doiRegisterDateStr=null, onlineIssueDate=1762748605642, onlineIssueDateStr=2025-11-10, onlineJustAcceptDate=null, onlineJustAcceptDateStr=null, onlineFirstDate=null, onlineFirstDateStr=null, sourceXml=null, magXml=null, createTime=1762748605642, creator=13701087609, updateTime=1762748605642, updator=13701087609, issue=Issue{id=1194617490446721194, tenantId=1146029695717560320, journalId=1189873630562394117, year='2025', volume='50', issue='2', pageStart='123', pageEnd='244', issueExtLink='null', onlineDate='null', pubDate='null', beforeIssueId=null, nextIssueId=null, price=null, status=1, issueComplete=1, articleOrder=1, issueType=-1, specialIssue=0, createTime=1762748604641, creator=13701087609, updateTime=1762749162199, updator=13701087609, preIssue=null, nextIssue=null, ext={EN=IssueExt(id=1194619829073191185, tenantId=1146029695717560320, journalId=1189873630562394117, issueId=1194617490446721194, language=EN, specialIssueTitle=, coverIllustrator=null, specialIssueEditor=, specialIssueAbout=), CN=IssueExt(id=1194619829073191186, tenantId=1146029695717560320, journalId=1189873630562394117, issueId=1194617490446721194, language=CN, specialIssueTitle=, coverIllustrator=null, specialIssueEditor=, specialIssueAbout=)}, issueFiles=null}, startPage=214, endPage=220, ext={EN=ArticleExt(id=1194617494980759868, articleId=1194617494641021242, tenantId=1146029695717560320, journalId=1189873630562394117, language=EN, title=Protective effect and its mechanism of low-dose interleukin-2 against hepatocyte injury in mice with autoimmune hepatitis, columnId=1190310110212751762, journalTitle=Medical Journal of Chinese People’s Liberation Army, columnName=Basic Research, runingTitle=null, highlight=null, articleAbstract=

Objective To investigate the protective effect and its mechanism of low-dose interleukin-2 (IL-2) against hepatocyte injury in Concanavalin A (Con A)-induced autoimmune hepatitis (AIH) mice. Methods Eighteen SPF female C57BL/6 mice were randomly divided into normal group, model group and treatment group, each group with 6 mice. Mice in the treatment group were subcutaneously injected with 300 μl 10,000 U IL-2 for 12 d, once a day. 2 h after the last dose, Con A (15 mg/kg) was injected through the tail vein in the model group and treatment group. After 8 h of modeling, the histopathological changes in the mouse liver were observed using HE staining, and the serum levels of aspartate aminotransferase (AST), alanine aminotransferase (ALT), tumor necrosis factor-α (TNF-α), and interferon-γ (IFN-γ) were detected using ELISA method; the expression of apoptotic protein caspase 8/9/3 was detected by Western blotting; and the percentages of Treg and Th1 cells were observed by flow cytometry. Results Compared with normal group, the liver index, spleen index, the percentage of necrotic area of liver tissue, the serum levels of ALT, AST, TNF-α and IFN-γ, and the expression of apoptosis protein caspase 8/9/3 significantly increased in the model group (P<0.05 or P<0.01); Compared with model group, the liver index, spleen index, the percentage of necrotic area of liver tissue, the serum levels of ALT, TNF-α and IFN-γ, and the expression of apoptosis protein caspase 8/9/3 significantly decreased in the treatment group (P<0.05 or P<0.01). The flow cytometry results showed that compared with normal group, the percentages of Treg and Th1 cells and Th1/Treg ratio increased in the model group (P<0.05 or P<0.01); Compared with the model group, the percentage of Treg cells further increased (P<0.01), Th1/Treg ratio decreased significantly in the treatment group (P<0.05), but there was no significant difference in the percentage of Th1 cells between two groups (P>0.05). Conclusion Low-dose of IL-2 can effectively improve liver injury in AIH mice, and the mechanism of action may be related to inducible Treg cell activation.

, correspAuthors=Yang Liu, authorNote=null, correspAuthorsNote=
E-mail:
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目的 探讨低剂量白细胞介素-2(IL-2)对刀豆蛋白A(Con A)诱导的自身免疫性肝炎(AIH)小鼠的肝保护作用及其机制。方法 SPF级雌性C57BL/6小鼠18只随机分为正常组、模型组与治疗组，每组6只。治疗组小鼠皮下注射300 μl 10 000 U IL-2，给药频率为1次/d，连续12 d。末次给药2 h后，模型组和治疗组均尾静脉注射Con A(15 mg/kg)。造模8 h后，采用HE染色观察小鼠肝脏病理形态变化，ELISA法检测小鼠血清中谷草转氨酶(AST)、谷丙转氨酶(ALT)、肿瘤坏死因子-α(TNF-α)和γ干扰素(IFN-γ)水平，Western blotting检测凋亡蛋白胱天蛋白酶(caspase 8/9/3)的表达情况，流式细胞术检测调节性T细胞(Treg)、Th1细胞百分比。结果 与正常组比较，模型组小鼠肝脏指数，脾脏指数，肝组织坏死面积百分比，血清ALT、AST、TNF-α、IFN-γ水平，凋亡蛋白caspase 8/9/3的表达均明显升高(P<0.05或P<0.01)；与模型组比较，治疗组小鼠肝脏指数，脾脏指数，肝组织坏死面积百分比，血清ALT、TNF-α、IFN-γ水平，凋亡蛋白caspase 8/9/3的表达均明显降低(P<0.05或P<0.01)。流式细胞术检测结果显示，与正常组比较，模型组小鼠Treg、Th1细胞百分比以及Th1/Treg比例均明显升高(P<0.05或P<0.01)；与模型组比较，治疗组小鼠Treg细胞百分比进一步升高(P<0.01)，Th1细胞百分比差异无统计学意义(P>0.05)，Th1/Treg比例明显降低(P<0.05)。结论 低剂量IL-2可有效缓解AIH小鼠的肝损伤，其作用机制可能与诱导Tregs活化有关。

, correspAuthors=刘杨, authorNote=null, correspAuthorsNote=
刘杨，E-mail：
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陈晨，硕士研究生，主要从事自身免疫性肝炎方面的研究

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陈晨，硕士研究生，主要从事自身免疫性肝炎方面的研究

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陈晨，硕士研究生，主要从事自身免疫性肝炎方面的研究

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Annu Rev Immunol, 2021, 39: 759-790., articleTitle=Dendritic cell regulation of T helper cells, refAbstract=null)], funds=[Fund(id=1194646668541923415, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1194617494641021242, awardId=202104041101013, language=EN, fundingSource=Shanxi Provincial Key Country Science and Technology Cooperation Project, Shanxi Provincial Science and Technology Department(202104041101013), fundOrder=null, country=null), Fund(id=1194646668596449368, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1194617494641021242, awardId=202104041101013, language=CN, fundingSource=山西省科学技术厅山西省重点国别科技合作项目(202104041101013), fundOrder=null, country=null), Fund(id=1194646668655169625, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1194617494641021242, awardId=202204051002033, language=EN, fundingSource=Key Team of Science and Technology Innovation Talents of Shanxi Province for Prevention and Treatment of Rheumatological and Immunological Diseases by Integrated Chinese and Western Medicine(202204051002033), fundOrder=null, country=null), Fund(id=1194646668705501274, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1194617494641021242, awardId=202204051002033, language=CN, fundingSource=中西医结合防治风湿免疫病山西省科技创新人才重点团队(202204051002033), fundOrder=null, country=null), Fund(id=1194646668755832923, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1194617494641021242, awardId=2022TD2003, language=EN, fundingSource=Science and Technology Innovation Team Project of Shanxi University of Traditional Chinese Medicine(2022TD2003), fundOrder=null, country=null), Fund(id=1194646668814553180, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1194617494641021242, awardId=2022TD2003, language=CN, fundingSource=山西中医药大学科技创新团队项目(2022TD2003), fundOrder=null, country=null), Fund(id=1194646668890050653, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1194617494641021242, awardId=2023XKJS-03, language=EN, fundingSource=Discipline Construction Project of Shanxi University of Traditional Chinese Medicine(2023XKJS-03), fundOrder=null, country=null), Fund(id=1194646669934432350, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1194617494641021242, awardId=2023XKJS-03, language=CN, fundingSource=山西中医药大学学科建设项目(2023XKJS-03), fundOrder=null, country=null)], companyList=[AuthorCompany(id=1194646664242761757, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1194617494641021242, xref=null, ext=[AuthorCompanyExt(id=1194646664251150366, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1194617494641021242, companyId=1194646664242761757, language=EN, country=null, province=null, city=null, postcode=null, companyName=null, departmentName=null, remark=School of Basic Medical Sciences, Shanxi University of Traditional Chinese Medicine, Jinzhong, Shanxi 030619, China), AuthorCompanyExt(id=1194646664255344671, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1194617494641021242, companyId=1194646664242761757, language=CN, country=null, province=null, city=null, postcode=null, companyName=null, departmentName=null, remark=山西中医药大学基础医学院，山西晋中 030619)])], figs=[ArticleFig(id=1194646667510124619, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1194617494641021242, language=EN, label=Fig.1, caption=Changes of liver index and spleen index of mice in each group (n=6), figureFileSmall=iMSWH2kZYEw5j4xJDr1tYQ==, figureFileBig=hOtlKKYu5UxNnNh3AGgdlA==, tableContent=null), ArticleFig(id=1194646667594010700, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1194617494641021242, language=CN, label=图1, caption=各组小鼠肝脏指数、脾脏指数变化情况(n=6)

与正常组比较，(1)P<0.01；与模型组比较，(2)P<0.01

, figureFileSmall=iMSWH2kZYEw5j4xJDr1tYQ==, figureFileBig=hOtlKKYu5UxNnNh3AGgdlA==, tableContent=null), ArticleFig(id=1194646667698868301, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1194617494641021242, language=EN, label=Fig.2, caption=Morphological changes of the liver of mice in each group, figureFileSmall=mhalRl3BQ7PUaoqt7Ncmgw==, figureFileBig=+/AsUhuApC/ksPdH4P3inA==, tableContent=null), ArticleFig(id=1194646667765977166, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1194617494641021242, language=CN, label=图2, caption=各组小鼠肝脏形态学改变情况

A. 各组小鼠肝组织病理学变化(HE染色)，圆圈示坏死区域，箭头示炎性细胞浸润；B. 各组小鼠肝组织坏死面积百分比(n=6)；与正常组比较，(1)P<0.01；与模型组比较，(2)P<0.01

, figureFileSmall=mhalRl3BQ7PUaoqt7Ncmgw==, figureFileBig=+/AsUhuApC/ksPdH4P3inA==, tableContent=null), ArticleFig(id=1194646667862446159, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1194617494641021242, language=EN, label=Fig.3, caption=Comparison of AST and ALT levels in the serum of mice in each group (n=6), figureFileSmall=lFCDrKeDcs8hI8xyPo6pig==, figureFileBig=QAzejuqjQU++TPDh6rz+Kw==, tableContent=null), ArticleFig(id=1194646667963109456, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1194617494641021242, language=CN, label=图3, caption=各组小鼠血清AST、ALT水平比较(n=6)

AST. 谷草转氨酶；ALT. 谷丙转氨酶；与正常组比较，(1)P<0.01；与模型组比较，(2)P<0.01

, figureFileSmall=lFCDrKeDcs8hI8xyPo6pig==, figureFileBig=QAzejuqjQU++TPDh6rz+Kw==, tableContent=null), ArticleFig(id=1194646668021829713, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1194617494641021242, language=EN, label=Fig.4, caption=Comparison of TNF-α and IFN-γ levels in the serum of mice in each group (n=6), figureFileSmall=CNf24xfAyN7edhq9ECc0fg==, figureFileBig=i49vsj/aS/qvaY/O2sRKwA==, tableContent=null), ArticleFig(id=1194646668088938578, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1194617494641021242, language=CN, label=图4, caption=各组小鼠血清TNF-α、IFN-γ水平比较(n=6)

TNF-α. 肿瘤坏死因子-α；IFN-γ. γ干扰素；与正常组比较，(1)P<0.05，(2)P<0.01；与模型组比较，(3)P<0.05，(4)P<0.01

, figureFileSmall=CNf24xfAyN7edhq9ECc0fg==, figureFileBig=i49vsj/aS/qvaY/O2sRKwA==, tableContent=null), ArticleFig(id=1194646668189601875, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1194617494641021242, language=EN, label=Fig.5, caption=Changes in apoptosis protein caspase 8/9/3 expression in each group of mice (n=6), figureFileSmall=E2gij9ZM5LUQood4HOwstg==, figureFileBig=X03zPlhObQKi9gj23JK+ZA==, tableContent=null), ArticleFig(id=1194646668244127828, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1194617494641021242, language=CN, label=图5, caption=各组小鼠凋亡蛋白caspase 8/9/3表达变化(n=6)

与正常组比较，(1)P<0.01；与模型组比较，(2)P<0.01

, figureFileSmall=E2gij9ZM5LUQood4HOwstg==, figureFileBig=X03zPlhObQKi9gj23JK+ZA==, tableContent=null), ArticleFig(id=1194646668319625301, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1194617494641021242, language=EN, label=Fig.6, caption=Changes in the percentage of Treg cells and Th1 cells in each group of mice (n=6), figureFileSmall=OVgs8uxcIBfJzoSfpDMU7w==, figureFileBig=DBLNBzKOeEVxhkt/Ng9qxA==, tableContent=null), ArticleFig(id=1194646668420288598, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1194617494641021242, language=CN, label=图6, caption=各组小鼠Treg、Th1细胞百分比变化情况(n=6)

Treg. 调节性T细胞；A. 流式细胞术检测各组小鼠Tregs表达情况；B. 流式细胞术检测各组小鼠Th1细胞表达情况；C. 各组小鼠Treg、Th1细胞百分比以及Th1/Treg比例；与正常组比较，(1)P<0.05，(2)P<0.01；与模型组比较，(3)P<0.05，(4)P<0.01

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低剂量白细胞介素-2对自身免疫性肝炎小鼠的肝保护作用及其机制
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陈晨 , 李竹蓉 , 吕思学 , 郭地 , 武嘉文 , 杨娜 , 刘杨 *
解放军医学杂志 | 基础研究 2025,50(2): 214-220
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解放军医学杂志 | 基础研究 2025, 50(2): 214-220
低剂量白细胞介素-2对自身免疫性肝炎小鼠的肝保护作用及其机制
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陈晨, 李竹蓉, 吕思学, 郭地, 武嘉文, 杨娜, 刘杨*
作者信息
  • 山西中医药大学基础医学院，山西晋中 030619

    • 陈晨，硕士研究生，主要从事自身免疫性肝炎方面的研究

通讯作者:

刘杨，E-mail：
Protective effect and its mechanism of low-dose interleukin-2 against hepatocyte injury in mice with autoimmune hepatitis
Chen Chen, Zhu-Rong Li, Si-Xue Lyu, Di Guo, Jia-Wen Wu, Na Yang, Yang Liu*
Affiliations
  • School of Basic Medical Sciences, Shanxi University of Traditional Chinese Medicine, Jinzhong, Shanxi 030619, China
出版时间: 2025-02-28 doi: 10.11855/j.issn.0577-7402.1567.2024.0418
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摘要
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目的 探讨低剂量白细胞介素-2(IL-2)对刀豆蛋白A(Con A)诱导的自身免疫性肝炎(AIH)小鼠的肝保护作用及其机制。方法 SPF级雌性C57BL/6小鼠18只随机分为正常组、模型组与治疗组，每组6只。治疗组小鼠皮下注射300 μl 10 000 U IL-2，给药频率为1次/d，连续12 d。末次给药2 h后，模型组和治疗组均尾静脉注射Con A(15 mg/kg)。造模8 h后，采用HE染色观察小鼠肝脏病理形态变化，ELISA法检测小鼠血清中谷草转氨酶(AST)、谷丙转氨酶(ALT)、肿瘤坏死因子-α(TNF-α)和γ干扰素(IFN-γ)水平，Western blotting检测凋亡蛋白胱天蛋白酶(caspase 8/9/3)的表达情况，流式细胞术检测调节性T细胞(Treg)、Th1细胞百分比。结果 与正常组比较，模型组小鼠肝脏指数，脾脏指数，肝组织坏死面积百分比，血清ALT、AST、TNF-α、IFN-γ水平，凋亡蛋白caspase 8/9/3的表达均明显升高(P<0.05或P<0.01)；与模型组比较，治疗组小鼠肝脏指数，脾脏指数，肝组织坏死面积百分比，血清ALT、TNF-α、IFN-γ水平，凋亡蛋白caspase 8/9/3的表达均明显降低(P<0.05或P<0.01)。流式细胞术检测结果显示，与正常组比较，模型组小鼠Treg、Th1细胞百分比以及Th1/Treg比例均明显升高(P<0.05或P<0.01)；与模型组比较，治疗组小鼠Treg细胞百分比进一步升高(P<0.01)，Th1细胞百分比差异无统计学意义(P>0.05)，Th1/Treg比例明显降低(P<0.05)。结论 低剂量IL-2可有效缓解AIH小鼠的肝损伤，其作用机制可能与诱导Tregs活化有关。

自身免疫性肝炎  /  白细胞介素-2  /  调节性T细胞  /  Th1细胞

Objective To investigate the protective effect and its mechanism of low-dose interleukin-2 (IL-2) against hepatocyte injury in Concanavalin A (Con A)-induced autoimmune hepatitis (AIH) mice. Methods Eighteen SPF female C57BL/6 mice were randomly divided into normal group, model group and treatment group, each group with 6 mice. Mice in the treatment group were subcutaneously injected with 300 μl 10,000 U IL-2 for 12 d, once a day. 2 h after the last dose, Con A (15 mg/kg) was injected through the tail vein in the model group and treatment group. After 8 h of modeling, the histopathological changes in the mouse liver were observed using HE staining, and the serum levels of aspartate aminotransferase (AST), alanine aminotransferase (ALT), tumor necrosis factor-α (TNF-α), and interferon-γ (IFN-γ) were detected using ELISA method; the expression of apoptotic protein caspase 8/9/3 was detected by Western blotting; and the percentages of Treg and Th1 cells were observed by flow cytometry. Results Compared with normal group, the liver index, spleen index, the percentage of necrotic area of liver tissue, the serum levels of ALT, AST, TNF-α and IFN-γ, and the expression of apoptosis protein caspase 8/9/3 significantly increased in the model group (P<0.05 or P<0.01); Compared with model group, the liver index, spleen index, the percentage of necrotic area of liver tissue, the serum levels of ALT, TNF-α and IFN-γ, and the expression of apoptosis protein caspase 8/9/3 significantly decreased in the treatment group (P<0.05 or P<0.01). The flow cytometry results showed that compared with normal group, the percentages of Treg and Th1 cells and Th1/Treg ratio increased in the model group (P<0.05 or P<0.01); Compared with the model group, the percentage of Treg cells further increased (P<0.01), Th1/Treg ratio decreased significantly in the treatment group (P<0.05), but there was no significant difference in the percentage of Th1 cells between two groups (P>0.05). Conclusion Low-dose of IL-2 can effectively improve liver injury in AIH mice, and the mechanism of action may be related to inducible Treg cell activation.

autoimmune hepatitis  /  interleukin-2  /  regulatory T cells  /  Th1 cells
陈晨, 李竹蓉, 吕思学, 郭地, 武嘉文, 杨娜, 刘杨. 低剂量白细胞介素-2对自身免疫性肝炎小鼠的肝保护作用及其机制. 解放军医学杂志, 2025 , 50 (2) : 214 -220 . DOI: 10.11855/j.issn.0577-7402.1567.2024.0418
Chen Chen, Zhu-Rong Li, Si-Xue Lyu, Di Guo, Jia-Wen Wu, Na Yang, Yang Liu. Protective effect and its mechanism of low-dose interleukin-2 against hepatocyte injury in mice with autoimmune hepatitis[J]. Medical Journal of Chinese People’s Liberation Army, 2025 , 50 (2) : 214 -220 . DOI: 10.11855/j.issn.0577-7402.1567.2024.0418
正文
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自身免疫性肝炎(autoimmune hepatitis，AIH)是一种由免疫介导的慢性肝细胞炎症性疾病，通常源于产生炎性细胞因子的细胞过度活化，伴随着免疫调节通路的中断，导致对自我抗原的持续反应[1-2]。AIH以肝脏内存在界面性肝炎伴淋巴细胞浸润、高γ球蛋白血症、血清氨基转移酶异常以及自身抗体阳性为基本特征[3-4]。AIH好发于女性，男性发病率也在逐步上升，但发病机制仍不明确，遗传易感性和环境因素是公认的疾病诱发因素，免疫细胞、免疫因子等其他因素也逐渐受到关注[5-7]。临床治疗AIH以糖皮质激素联合硫唑嘌呤的非特异性免疫抑制治疗为主，但存在停用后复发等不良反应。有研究表明，在类固醇治疗逐渐减量的过程中AIH患者可能出现神经肉瘤等病症[8]。目前，许多新型治疗方法被提出，如消除在各种自身免疫性疾病中检测到的高水平T记忆干细胞可为治疗自身免疫性疾病提供新机会[9]；环孢霉素可通过抑制白细胞增殖及白细胞介素-2(IL-2)的合成来缓解二氧化硅诱导的AIH[10]。同时，有研究发现AIH患者外周血中调节性T细胞(regulatory T cells，Tregs)数量减少且功能受损，这种缺陷可能与疾病的发生和进展有关[1]。生物制剂类，如低剂量重组IL-2可通过扩大Treg群体提高治疗效果[11]，因此Tregs在AIH治疗中扮演重要角色。
Tregs是T细胞亚群之一，主要通过抑制免疫细胞过度反应防止自身免疫性疾病的发生发展。IL-2是白细胞介素家族成员之一，对Tregs的激活起至关重要的作用。高剂量IL-2可促进效应T细胞和记忆T细胞的分化增殖，增强CD8+效应T细胞和自然杀伤细胞的扩增和溶解活性，主要在机体抗肿瘤方面发挥重要作用[12]。相反，CD25是在Tregs上高表达的IL-2受体，因其与IL-2的超高亲和力使得Tregs在亚生理浓度下也可优先激活和扩展，同时避免效应记忆T细胞的意外激活和Th1细胞[13-14]产生促炎因子。因此，本研究通过观察Tregs数量变化探讨低剂量IL-2对刀豆蛋白A(Con A)诱导的AIH小鼠的肝保护作用机制，以期为使用低剂量IL-2防治AIH提供新思路。
1 材料与方法
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1.1 主要试剂
注射用IL-2(PWL130，大连美仑生物技术有限公司)；Con A(C8110，北京索莱宝生物技术有限公司)；谷草转氨酶(AST；C0010 3-1)、谷丙转氨酶(ALT；C009 3-1)测试盒(南京建成生物工程研究所)；小鼠肿瘤坏死因子-α(TNF-α；MU30030)、γ干扰素(IFN-γ；MU30038) ELISA试剂盒(武汉贝茵莱生物科技公司)；异硫氰酸荧光素(fluorescein isothiocyanate，FITC)标记的抗CD4单克隆抗体(102006)、藻红蛋白(phycoerythrin，PE)标记的抗CD25单克隆抗体(100406)、别藻蓝蛋白(allophycocyanin，APC)标记的FOXP3单克隆抗体(320014)、APC标记的IFN-γ单克隆抗体(505810，美国Biolegend公司)；Peridinin叶绿素蛋白复合物(Peridinin chlorophyll protein，PerCP)标记的CD3单克隆抗体(E-AB-F1013F，中国Elabscience公司)；小鼠抗胱天蛋白酶(caspase) 3单克隆抗体(66470-2-Ig)、兔抗caspase 8多克隆抗体(13423-1-AP)、兔抗caspase 9多克隆抗体(10380-1-AP，美国Proteintech公司)；兔抗GAPDH抗体(AB0037)、兔抗β‑tubulin 抗体(AB0039，上海埃必威生物技术有限公司)；辣根过氧化物酶(HRP)标记山羊抗兔IgG二抗(A21020)、HRP标记山羊抗小鼠IgG二抗(A21010，美国Abbkine公司)；6× 蛋白上样缓冲液(P0015F，上海碧云天生物科技有限公司)；一抗二抗稀释液(AR1017，武汉博士德生物工程有限公司)；戊巴比妥麻醉剂来源为山西中医药大学实验室管理中心申请所得，剩余麻醉药按照麻醉药品管理制度交回管理人员。
1.2 实验动物
SPF级雌性C57BL/6小鼠18只，8周龄，体重(20±2) g，购自斯贝福(北京)生物技术有限公司[实验动物生产许可证号：SCXK(京)2019-0010]，分笼饲养，自由摄食饮水。饲养环境为室温20－25 ℃，湿度55%。本研究经山西中医药大学动物福利伦理委员会批准(2019LL41)。
1.3 AIH小鼠模型建立及分组　小鼠适应性饲养
1周后，随机分为正常组、模型组与治疗组，每组6只。正常组、模型组常规饲养；治疗组按10 000 U浓度预先皮下注射300 μl IL-2[15-16]，给药频率为1次/d，连续12 d，正常组和模型组以等剂量0.9%氯化钠溶液进行皮下注射。末次给药2 h后，模型组和治疗组均通过尾静脉注射Con A(15 mg/kg)进行造模，正常组尾静脉注射等剂量0.9%氯化钠溶液。造模8 h后各组小鼠使用戊巴比妥进行麻醉，麻醉剂按30 mg/kg体重实施基础给药，麻醉后立即眼球取血，收集外周血后采用颈椎脱臼法处死全部小鼠。
1.4 肝脏指数、脾脏指数计算
小鼠处死前进行称重，取材后称量肝脏、脾脏重量，并计算肝脏指数和脾脏指数。肝脏指数(mg/g)=1000×肝脏重(g)/小鼠体重(g)；脾脏指数(mg/g)=1000×脾脏重(g)/小鼠体重(g)。
1.5 ELISA法检测肝功能相关指标
取小鼠外周血室温下静置30 min，2000 r/min离心20 min分离并收集血清，根据ELISA试剂盒说明书进行检测，使用酶标仪(1550-801138，美国Thermoscientific公司)测定各组小鼠血清中AST、ALT、TNF-α、IFN-γ水平。
1.6 HE染色观察肝组织病理变化
无菌环境下提取小鼠肝脏，将部分肝组织分离并置于4%多聚甲醛溶液中固定，经梯度乙醇脱水、二甲苯透明、石蜡包埋、切片、HE染色等步骤完成HE染色。光镜下观察肝组织的形态学改变。
肝组织坏死面积计算：光学显微镜100倍视野下观察肝组织，每个样本随机选取5个视野，计算5个视野下坏死区域面积总和，将坏死区域的总面积除以每组的视野总数即为该样本肝组织坏死面积[17]。
1.7 Western blotting检测caspase 8/9/3的表达
根据裂解液说明书加入含1%蛋白酶抑制剂的RIPA裂解液，加入比例为每20 mg肝组织加入250 μl裂解液，混匀进行组织匀浆，离心取上清。SDS-PAGE凝胶电泳后转移到PVDF膜上，5%脱脂奶粉封闭2 h，孵育一抗(caspase 8/9/3，稀释倍数为1:750、1:750、1:1000)和对应内参，摇床室温10 min后，置于4 ℃冰箱过夜。TBST洗3次，将膜放入二抗(稀释倍数1:10 000)中，室温下摇床孵育2 h。TBST洗3次，使用ECL显色液避光滴于膜上充分覆盖，用显影仪成像。条带灰度值采用ImageJ软件分析。
1.8 流式细胞术检测Treg、Th1细胞百分比
无菌环境下取出新鲜小鼠脾，生理盐水洗涤并去除多余组织后，将脾脏转移至金属滤网研磨。收集细胞至离心管，550 g离心5 min后弃上清液，细胞悬液中加入3 ml红细胞裂解稀释液(10×)，混匀，冰上裂解3 min后加入3 ml PBS终止裂解并清洗。
缓冲液清洗后收集细胞至流式管，加50 μl封闭液与CD4 FITC、CD3 PerCP抗体各5 μl在4 ℃环境下孵育30 min进行表面染色，缓冲液清洗细胞后进行破膜固定；加入50 μl封闭液与FOXP3 APC、IFN-γ APC抗体各5 μl进行胞内染色，4 ℃环境下孵育30 min后清洗细胞，PBS重悬细胞，过筛后使用BD Accuric6流式仪检测脾脏Treg、Th1细胞染色情况，数据采用Flowjo10.8.1分析。
1.9 统计学处理
采用SPSS 26.0软件进行统计分析。所有实验数据均以$\bar{x}±s$表示，多组间比较采用单因素方差分析，进一步两两比较采用LSD-t检验。
P<0.05为差异有统计学意义。
2 结果
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2.1 低剂量IL-2对AIH小鼠肝、脾形态的影响
与正常组比较，模型组小鼠肝脏指数、脾脏指数明显升高(P<0.01)；与模型组比较，治疗组小鼠肝脏指数、脾脏指数明显降低(P<0.01，图1)。
2.2 低剂量IL-2对AIH小鼠肝脏形态学的影响
HE染色结果显示，正常组小鼠肝小叶结构清晰，无炎性细胞浸润；模型组小鼠出现大量炎性细胞浸润，肝小叶结构模糊，肝细胞大量坏死；与模型组比较，治疗组小鼠肝组织坏死面积减小且炎性细胞浸润减轻(图2A)。与正常组比较，模型组小鼠肝组织坏死面积百分比明显增高(P<0.01)；与模型组比较，治疗组小鼠肝组织坏死面积百分比明显降低(P<0.01，图2B)。
2.3 低剂量IL-2对AIH小鼠血清ALT、AST水平的影响
与正常组比较，模型组小鼠血清AST、ALT水平明显增高(P<0.01)；与模型组比较，治疗组小鼠血清ALT水平明显降低(P<0.01)，两组AST水平差异无统计学意义(P>0.05，图3)。
2.4 低剂量IL-2对AIH小鼠血清炎性因子水平的影响
与正常组比较，模型组小鼠血清TNF-α、IFN-γ水平明显增高(TNF-α：P<0.01；IFN-γ：P<0.05)；与模型组比较，治疗组小鼠血清TNF-α、IFN-γ水平明显降低(TNF-α：P<0.01；IFN-γ：P<0.05，图4)。
2.5 低剂量IL-2对AIH小鼠凋亡蛋白caspase 8/9/3表达的影响
与正常组比较，模型组小鼠凋亡蛋白caspase 8/9/3表达明显上调(P<0.01)；与模型组比较，治疗组小鼠凋亡蛋白caspase 8/9/3表达明显下调(P<0.01，图5)。
2.6 低剂量IL-2对AIH小鼠Treg、Th1细胞百分比影响
流式细胞术检测结果显示，与正常组比较，模型组小鼠Treg、Th1细胞百分比，以及Th1/Treg比例明显升高(P<0.05或P<0.01)；与模型组比较，治疗组小鼠Treg细胞百分比进一步升高(P<0.01)，Th1细胞百分比差异无统计学意义(P>0.05)，而Th1/Treg比例明显下降(P<0.05，图6)。
3 讨论
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AIH是因体内免疫功能紊乱引起的慢性炎症性肝病，可发生在所有年龄段的个体，女性发病率较高[18]。AIH病因及发病机制尚未明确，目前认为是感染、药物等外源性触发因素在遗传易感性基础上引起机体免疫耐受机制破坏，发生免疫调节异常，产生针对肝脏的自身抗原的免疫反应[19-20]。AIH的临床表现多种多样，大多起病隐匿且症状不典型，但部分患者间歇性发作或病情波动，单独使用类固醇或与其他免疫抑制剂联用是临床上AIH治疗的主要选择，而在某些情况下，症状自行缓解后可能出现严重的不良反应和疾病复发，治疗不及时可发展为肝硬化和肝衰竭[21-22]。AIH特异性治疗方法是临床研究值得开拓的领域。
IL-2是一种T细胞生长因子，在先天性和适应性免疫反应的维持和稳态中起着重要作用。IL-2通过其异三聚体受体(CD25/CD122/CD132)实现T细胞的增殖、存活和功能所需，其中IL-2与CD25(α链)呈现最高亲和力[23-24]。由于IL-2Rα(IL-2受体α亚基)可在Tregs表面持续长效表达，因此Tregs在机体无外来抗原刺激情况下，对IL-2的敏感性高于自然杀伤细胞、效应T细胞等[25-26]。近年来，由于Tregs对IL-2的超强敏感性能有效刺激Tregs发挥免疫抑制效能，低剂量IL-2在自身免疫性疾病治疗方面的作用及机制备受关注[27-28]。目前IL-2治疗自身免疫性疾病的剂量尚未统一，笔者查阅低剂量IL-2治疗自身免疫性疾病的相关文献同时比对试剂说明书选定IL-2浓度进行本研究[15-16]。
Con A是一种凝集素，因具有造模时间短、过程简单、转氨酶水平升高明显等优点被广泛应用于AIH机制研究。Con A可以激活T细胞，引发T细胞释放大量细胞因子如TNF-α、IFN-γ等，从而诱发肝细胞变性、坏死等免疫性肝损伤[29-31]。本研究结果显示，注射Con A后模型组小鼠血清ALT和AST水平明显上调，肝脏指数、脾脏指数明显升高，肝脾肿大明显。Con A激活T细胞释放大量TNF-α、IFN-γ，促进肝脏发生严重炎症反应，光学显微镜下观察模型组小鼠肝组织，可见肝细胞坏死肿胀，并伴有大量淋巴细胞浸润以及多处片状坏死区域。研究发现，TNF-α可与肝细胞表面的TNF受体(TNF receptor，TNFR)结合，启动胱天蛋白酶介导的肝细胞凋亡级联反应[32]，即活化的TNFR与caspase 8组装成死亡诱导信号复合物，招募caspase 9进入凋亡小体后，通过内源性凋亡途径激活caspase 3[33]。Caspase 3属细胞凋亡终末剪切酶，可导致核酸内切酶的活性增高，裂解核小体间的DNA，引起细胞凋亡。因此模型组小鼠注射Con A后，caspase 8/9/3蛋白表达升高。与模型组比较，治疗组小鼠血清ALT水平降低(AST水平也有所降低，但与模型组比较无统计学差异)。本研究结果显示，低剂量IL-2治疗可降低小鼠血清中促炎因子TNF-α、IFN-γ水平，有效缓解小鼠肝脏病理性损伤和炎性细胞浸润，caspase 8/9/3蛋白表达明显下调，提示低剂量IL-2能有效抑制AIH小鼠的肝损伤。
机体的正常免疫功能取决于促炎因子与免疫抑制因子间的平衡，Tregs与Th1细胞是密切相关的免疫调节细胞[34]。Tregs对维持机体免疫至关重要，主要通过细胞间接触性抑制(表面共抑制受体)、非接触性抑制(细胞因子分泌)以及代谢破坏抑制等机制发挥抑制作用，从而维持免疫自耐受能力[35-36]。Th1细胞主要产生TNF-α、IFN-γ等细胞因子，能够增强巨噬细胞的吞噬活性和激活细胞毒性T细胞，从而增强细胞免疫反应[37]。当Th1细胞的促炎作用过强或Tregs的免疫抑制作用减弱时机体平衡被打破，引起一系列自身免疫性疾病。为进一步明确低剂量IL-2抑制小鼠AIH的作用机制，本研究通过流式细胞术检测AIH小鼠脾脏Treg、Th1细胞水平，结果显示Con A虽然可以诱导小鼠Treg细胞百分比升高，但同时Th1细胞百分比也升高，Tregs不足以抑制肝细胞的免疫性损伤；治疗组预先注射低剂量IL-2提前激活Tregs，致使治疗组Tregs明显增多，且升高比例高于模型组。因为低剂量IL-2与Tregs的超高亲和力在激活Tregs的同时可有效避免Th1细胞的激活，所以一定程度上减少了TNF-α的分泌，从而达到抑制肝细胞免疫性损伤的作用。上述结果提示，预先注射低剂量IL-2能够在不激活Th1细胞的情况下高效激活Tregs，提前发挥抑制功能以抑制炎性因子的分泌，从而减轻AIH小鼠过度的免疫应答，缓解AIH小鼠肝脏损伤。
综上所述，Tregs与Th1细胞的紊乱导致AIH小鼠产生一系列免疫反应，低剂量IL-2通过激活Tregs发挥免疫抑制作用来改善Tregs与Th1细胞的失衡，从而减轻Con A诱导的小鼠急性肝损伤。本研究采用流式细胞术检测低剂量IL-2干预下Con A模型小鼠Tregs、Th1细胞水平，从Tregs与Th1细胞的平衡关系入手，探讨低剂量IL-2对AIH的治疗机制，以期为AIH的发病机制以及治疗相关研究提供理论基础，并为临床治疗AIH提供新思路。但本研究存在实验周期较短等不足，因未做长期观察，故缺乏长期治疗结果进行对照；同时，本研究仅检测了低剂量IL-2对Tregs数量变化的影响，未对Tregs功能进行检测，未来研究可予以补充。
基金
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  • 山西省科学技术厅山西省重点国别科技合作项目(202104041101013)
  • 中西医结合防治风湿免疫病山西省科技创新人才重点团队(202204051002033)
  • 山西中医药大学科技创新团队项目(2022TD2003)
  • 山西中医药大学学科建设项目(2023XKJS-03)
文献
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doi: 10.11855/j.issn.0577-7402.1567.2024.0418
  • 接收时间：2023-11-27
  • 首发时间：2025-11-10
  • 出版时间：2025-02-28
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  • 收稿日期：2023-11-27
  • 录用日期：2024-01-30
基金
Shanxi Provincial Key Country Science and Technology Cooperation Project, Shanxi Provincial Science and Technology Department(202104041101013)
山西省科学技术厅山西省重点国别科技合作项目(202104041101013)
Key Team of Science and Technology Innovation Talents of Shanxi Province for Prevention and Treatment of Rheumatological and Immunological Diseases by Integrated Chinese and Western Medicine(202204051002033)
中西医结合防治风湿免疫病山西省科技创新人才重点团队(202204051002033)
Science and Technology Innovation Team Project of Shanxi University of Traditional Chinese Medicine(2022TD2003)
山西中医药大学科技创新团队项目(2022TD2003)
Discipline Construction Project of Shanxi University of Traditional Chinese Medicine(2023XKJS-03)
山西中医药大学学科建设项目(2023XKJS-03)
作者信息
    山西中医药大学基础医学院，山西晋中 030619

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Percentage of total
species (%)
鹅膏菌科Amanitaceae 2 11 5.26 鹅膏菌属 Amanita 10 4.78
小菇科 Mycenaceae 2 12 5.74 丝盖伞属 Inocybe 5 2.39
多孔菌科 Polyporaceae 8 14 6.70 蜡蘑属 Laccaria 5 2.39
红菇科 Russulaceae 3 23 11.00 小皮伞属 Marasmius 6 2.87
小菇属 Mycena 11 5.26
光柄菇属 Pluteus 5 2.39
红菇属 Russula 17 8.13
栓菌属 Trametes 5 2.39
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