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Article(id=1226554100679094333, tenantId=1146029695717560320, journalId=1192105938417971205, issueId=1226554095926952065, articleNumber=null, orderNo=null, doi=10.13343/j.cnki.wsxb.20250043, pmid=null, cstr=null, oa=null, hot=null, price=null, onlineType=0, articleFormat=0, articleType=null, articleTypeStr=research-article, receivedDate=1736870400000, receivedDateStr=2025-01-15, revisedDate=null, revisedDateStr=null, acceptedDate=1741017600000, acceptedDateStr=2025-03-04, onlineDate=1770362885875, onlineDateStr=2026-02-06, pubDate=1751558400000, pubDateStr=2025-07-04, doiRegisterDate=null, doiRegisterDateStr=null, onlineIssueDate=1770362885875, onlineIssueDateStr=2026-02-06, onlineJustAcceptDate=null, onlineJustAcceptDateStr=null, onlineFirstDate=null, onlineFirstDateStr=null, sourceXml=null, magXml=null, createTime=1770362885875, creator=13701087609, updateTime=1770362885875, updator=13701087609, issue=Issue{id=1226554095926952065, tenantId=1146029695717560320, journalId=1192105938417971205, year='2025', volume='65', issue='7', pageStart='2771', pageEnd='3233', issueExtLink='null', onlineDate='null', pubDate='null', beforeIssueId=null, nextIssueId=null, price=null, status=1, issueComplete=1, articleOrder=1, issueType=-1, specialIssue=null, createTime=1770362884741, creator=13701087609, updateTime=1770363575040, updator=13701087609, preIssue=null, nextIssue=null, ext={EN=IssueExt(id=1226556991309529548, tenantId=1146029695717560320, journalId=1192105938417971205, issueId=1226554095926952065, language=EN, specialIssueTitle=, coverIllustrator=null, specialIssueEditor=, specialIssueAbout=), CN=IssueExt(id=1226556991309529549, tenantId=1146029695717560320, journalId=1192105938417971205, issueId=1226554095926952065, language=CN, specialIssueTitle=, coverIllustrator=null, specialIssueEditor=, specialIssueAbout=)}, issueFiles=null}, startPage=3195, endPage=3207, ext={EN=ArticleExt(id=1226554100968501333, articleId=1226554100679094333, tenantId=1146029695717560320, journalId=1192105938417971205, language=EN, title=African swine fever virus protein E423R induces autophagy, columnId=1192149543992045670, journalTitle=Acta Microbiologica Sinica, columnName=Research Article, runingTitle=null, highlight=null, articleAbstract=

[Objective] To explore the autophagy induced by the African swine fever virus (ASFV) protein E423R. [Methods] The RFP-LC3 fluorescent spots following the transfection of HeLa-DifluoTM hLC3 cells with pCMV-Myc-E423R was quantified by the High-Content Analysis System, and the autophagic flux was assessed. The expression levels of key autophagy proteins, LC3-Ⅱ and SQSTM1/p62, in HeLa cells were analyzed via Western blotting. Co-localization of autophagosomes and lysosomes was examined by laser confocal microscopy. Additionally, Western blotting was employed to investigate the dose-dependent effect of E423R on LC3-Ⅱ expression and the regulatory effect of E423R on the AKT/mTOR/ULK1 signaling pathway. [Results] The High-Content Analysis System demonstrated a significant increase in RFP-LC3 fluorescence spots in the reporter cells expressing E423R, suggesting that E423R induced the activation of autophagy. Western blotting further confirmed that the expression of E423R significantly elevated the LC3-Ⅱ/β-actin ratio while decreasing the expression level of p62. Confocal microscopy results indicated that E423R enhanced the expression of GFP-LC3, promoted the co-localization of GFP-LC3 with Lyso-Tracker Red, and facilitated the fusion of autophagosomes and lysosomes. Additionally, the expression level of E423R exhibited a positive correlation with the expression level of LC3-Ⅱ in HeLa cells. Furthermore, E423R down-regulated the expression of p-AKT, p-mTOR, and p-ULK1 (Ser757) in the mTOR signaling pathway. [Conclusion] This study demonstrates that the ASFV E423R protein induces complete autophagy via the AKT/mTOR/ULK1 signaling pathway, exhibiting a dose-dependent effect on LC3-Ⅱ expression to a certain degree. These findings provide a foundation for further investigation into the infection and pathogenic mechanisms of ASFV.

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*E-mail: KANG Xilong,
PAN Zhiming,
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【目的】 探究非洲猪瘟病毒(African swine fever virus, ASFV)蛋白E423R诱导细胞自噬的功能。 【方法】 通过高内涵分析系统量化分析pCMV-Myc-E423R转染自噬报告细胞HeLa-DifluoTM hLC3后的RFP-LC3荧光斑点数，评估自噬通量；利用Western blotting分析HeLa细胞中自噬关键蛋白LC3-Ⅱ、SQSTM1/p62的表达水平；采用激光共聚焦技术观察自噬体与溶酶体的共定位情况；通过Western blotting检测E423R蛋白与LC3-Ⅱ表达的剂量依赖效应以及对AKT/mTOR/ULK1信号通路的调控作用。 【结果】 高内涵细胞分析实验显示，表达E423R蛋白的报告细胞中RFP-LC3荧光斑点明显增多，表明E423R蛋白可以诱导自噬发生活化；Western blotting分析证实，E423R蛋白表达促使LC3-Ⅱ/β-actin显著升高，p62的表达水平显著下调；共聚焦结果显示E423R蛋白可增强GFP-LC3的表达，促使GFP-LC3与Lyso-Tracker Red荧光共定位明显增多，诱导自噬体与溶酶体融合；同时，E423R蛋白表达水平与HeLa细胞中的LC3-Ⅱ表达水平呈正相关，E423R蛋白能下调mTOR信号通路中p-AKT、p-mTOR、p-ULK1 (Ser757)的表达。 【结论】 本研究揭示了ASFV E423R蛋白通过AKT/mTOR/ULK1信号通路诱导完整的细胞自噬过程，E423R与LC3-Ⅱ的表达呈一定程度的剂量依赖效应，为深入研究自噬在ASFV感染与致病机制中的功能奠定了基础。

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作者贡献声明

黄静怡：实验执行，数据分析和论文撰写；康喜龙：实验设计，数据分析和论文修改；黄霞：实验执行；周懿：协助实验操作，数据分析；刘弘知：提供技术支持，参与论文讨论；焦新安：指导论文思路，论文修改；潘志明：研究构思和设计，论文修改。

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2.Jiangsu Co-innovation Center for Prevention and Control of Important Animal Infectious Diseases and Zoonoses, Yangzhou University, Yangzhou, Jiangsu, China
3.Key Laboratory of Prevention and Control of Biological Hazard Factors (Animal Origin) for Agrifood Safety and Quality, Ministry of Agriculture and Rural Affairs, Yangzhou University, Yangzhou, Jiangsu, China
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2.扬州大学，江苏省高校动物重要疫病与人兽共患病防控协同创新中心，江苏 扬州
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2.Jiangsu Co-innovation Center for Prevention and Control of Important Animal Infectious Diseases and Zoonoses, Yangzhou University, Yangzhou, Jiangsu, China
3.Key Laboratory of Prevention and Control of Biological Hazard Factors (Animal Origin) for Agrifood Safety and Quality, Ministry of Agriculture and Rural Affairs, Yangzhou University, Yangzhou, Jiangsu, China
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2.扬州大学，江苏省高校动物重要疫病与人兽共患病防控协同创新中心，江苏 扬州
3.扬州大学，农业农村部农产品质量安全生物性危害因子(动物源)控制重点实验室，江苏 扬州
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2.Jiangsu Co-innovation Center for Prevention and Control of Important Animal Infectious Diseases and Zoonoses, Yangzhou University, Yangzhou, Jiangsu, China
3.Key Laboratory of Prevention and Control of Biological Hazard Factors (Animal Origin) for Agrifood Safety and Quality, Ministry of Agriculture and Rural Affairs, Yangzhou University, Yangzhou, Jiangsu, China
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2.扬州大学，江苏省高校动物重要疫病与人兽共患病防控协同创新中心，江苏 扬州
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3.Key Laboratory of Prevention and Control of Biological Hazard Factors (Animal Origin) for Agrifood Safety and Quality, Ministry of Agriculture and Rural Affairs, Yangzhou University, Yangzhou, Jiangsu, China
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3.Key Laboratory of Prevention and Control of Biological Hazard Factors (Animal Origin) for Agrifood Safety and Quality, Ministry of Agriculture and Rural Affairs, Yangzhou University, Yangzhou, Jiangsu, China
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PLoS One, 2019, 14(11): e0223955., articleTitle=Mechanisms of African swine fever virus pathogenesis and immune evasion inferred from gene expression changes in infected swine macrophages, refAbstract=null)], funds=[Fund(id=1227681732573458680, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1226554100679094333, awardId=BE2021331, language=EN, fundingSource=Key Research and Development Program (Modern Agriculture) Project of Jiangsu Province(BE2021331), fundOrder=null, country=null), Fund(id=1227681732690899202, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1226554100679094333, awardId=BE2021331, language=CN, fundingSource=江苏省重点研发计划(现代农业)项目(BE2021331), fundOrder=null, country=null), Fund(id=1227681732783173898, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1226554100679094333, awardId=KYCX24_3823, language=EN, fundingSource=Postgraduate Research and Practice Innovation Program of Jiangsu Province(KYCX24_3823), 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Education, Yangzhou University, Yangzhou, Jiangsu, China), AuthorCompanyExt(id=1227681719017468615, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1226554100679094333, companyId=1227681719004885701, language=CN, country=null, province=null, city=null, postcode=null, companyName=null, departmentName=null, remark=4.扬州大学，教育部农业与农产品安全国际合作联合实验室，江苏 扬州)])], figs=[ArticleFig(id=1227681727540293738, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1226554100679094333, language=EN, label=Figure 1, caption=Identification of expression of E423R, E199L and DP238L proteins. A: Western blotting was used to detect the expression of E423R protein (Lane M: 180 kDa Prestained Protein Marker; Lane 1: pCMV-Myc; Lane 2: pCMV-Myc-E423R); B: Western blotting was used to detect the expression of E199L protein (Lane M: 180 kDa Plus Prestained Protein Marker; Lane 1: pCMV-Myc; Lane 2: pCMV-Myc-E199L); C: Western blotting was used to detect the expression of DP238L protein (Lane M: 180 kDa Prestained Protein Marker; Lane 1: pCMV-Myc; Lane 2: pCMV-Myc-DP238L)., figureFileSmall=gVBHeb6txpHrOjwFh8Y4CA==, figureFileBig=62myldfz5qJC8UPrr53y3Q==, tableContent=null), ArticleFig(id=1227681727653539959, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1226554100679094333, language=CN, label=图1, caption=E423R、E199L、DP238L蛋白表达的鉴定, figureFileSmall=gVBHeb6txpHrOjwFh8Y4CA==, figureFileBig=62myldfz5qJC8UPrr53y3Q==, tableContent=null), ArticleFig(id=1227681727770980480, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1226554100679094333, language=EN, label=Figure 2, caption=E423R protein promotes the formation of autophagosomes. A: The impact of E423R protein on autophagosome formation was assessed using High-Content Analysis System; B: Quantitative analysis of High-Content Analysis results. Mock: Blank control; Rapamycin: 25 μmol/L rapamycin stimulation; EV: pCMV-Myc; DP238L: pCMV-Myc-DP238L; E199L: pCMV-Myc-E199L; E423R: pCMV-Myc-E423R. *: P<0.05., figureFileSmall=W93E2I82RkGFC0uqk/etcg==, figureFileBig=EVTRvfSU3Q0n0Hno97xeow==, tableContent=null), ArticleFig(id=1227681727892615310, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1226554100679094333, language=CN, label=图2, caption=E423R蛋白诱导自噬体形成, figureFileSmall=W93E2I82RkGFC0uqk/etcg==, figureFileBig=EVTRvfSU3Q0n0Hno97xeow==, tableContent=null), ArticleFig(id=1227681727989084309, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1226554100679094333, language=EN, label=Figure 3, caption=Complete autophagy induced by ASFV E423R protein. A: Western blotting was used to detect the effect of E423R protein on the expression of autophagy-related proteins LC3 and p62; B: The gray values of the protein LC3-Ⅱ; C: The gray values of the protein p62; D: Western blotting was employed to assess the autophagic function of E423R in response to stimulation by bafilomycin A1; E: The gray values of LC3-Ⅱ stimulated by bafilomycin A1; F: The gray values of p62 stimulated by bafilomycin A1. *: P<0.05; **: P<0.01; ***: P<0.001., figureFileSmall=VjQf7UZJpHUlgUHGnj0GVw==, figureFileBig=YhaDqUYgHAz4hR9TcwIZAA==, tableContent=null), ArticleFig(id=1227681728140079267, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1226554100679094333, language=CN, label=图3, caption=ASFV E423R蛋白诱导完整的细胞自噬过程, figureFileSmall=VjQf7UZJpHUlgUHGnj0GVw==, figureFileBig=YhaDqUYgHAz4hR9TcwIZAA==, tableContent=null), ArticleFig(id=1227681728265908394, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1226554100679094333, language=EN, label=Figure 4, caption=E423R protein induces autophagosome-lysosomal colocalization in HeLa cells. A: The acid lysosomes were stained with Lyso-Tracker Red, and the HeLa cells were immunolabeled with LC3 (green fluorescence) and ASFV recombinant plasmid (blue fluorescence) after transfection for 24 h; B: LC3 spots were counted using ImageJ software; C: Autophagosomes and lysosomes colocalization were counted using ImageJ software. Scale: 50 μm. **: P<0.01. ***: P<0.001., figureFileSmall=2pY/4f7rtk7EARVahsQZSQ==, figureFileBig=UrxfeOJFtW8EAQQdsdzDEw==, tableContent=null), ArticleFig(id=1227681728400126135, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1226554100679094333, language=CN, label=图4, caption=E423R蛋白诱导自噬体与溶酶体在HeLa细胞中的共定位, figureFileSmall=2pY/4f7rtk7EARVahsQZSQ==, figureFileBig=UrxfeOJFtW8EAQQdsdzDEw==, tableContent=null), ArticleFig(id=1227681729884909763, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1226554100679094333, language=EN, label=Figure 5, caption=E423R protein can induce the expression of LC3-Ⅱ in a dose-dependent manner. A: Western blotting was used to detect the effect of gradient overexpression of LC3-Ⅱ on the expression of E423R in HeLa cells; B: Grayscale analysis of Western blotting results., figureFileSmall=4cQpIFF4b7c7hOtMd5RBnw==, figureFileBig=vsrkhPlsnSYP4AI8b6/w4Q==, tableContent=null), ArticleFig(id=1227681730119790801, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1226554100679094333, language=CN, label=图5, caption=E423R蛋白诱导自噬关键蛋白LC3-Ⅱ表达并呈剂量依赖性, figureFileSmall=4cQpIFF4b7c7hOtMd5RBnw==, figureFileBig=vsrkhPlsnSYP4AI8b6/w4Q==, tableContent=null), ArticleFig(id=1227681730233037019, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1226554100679094333, language=EN, label=Figure 6, caption=E423R protein activates autophagy through the AKT/mTOR/ULK1 signaling pathway., figureFileSmall=hVxJMJ2a/3F0Xmwn4qhMwQ==, figureFileBig=2DMrmk4WUBjcUVCtvIxSYw==, tableContent=null), ArticleFig(id=1227681732221137125, tenantId=1146029695717560320, 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非洲猪瘟病毒E423R蛋白诱导细胞自噬的功能
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黄静怡 1, 2, 3, 4 , 康喜龙 1, 2, 3, 4 , 黄霞 1, 2, 3, 4 , 周懿 1, 2, 3, 4 , 刘弘知 1, 2, 3, 4 , 焦新安 1, 2, 3, 4 , 潘志明 1, 2, 3, 4
微生物学报 | 研究报告 2025,65(7): 3195-3207
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微生物学报 | 研究报告 2025, 65(7): 3195-3207
非洲猪瘟病毒E423R蛋白诱导细胞自噬的功能
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黄静怡1, 2, 3, 4, 康喜龙1, 2, 3, 4 , 黄霞1, 2, 3, 4, 周懿1, 2, 3, 4, 刘弘知1, 2, 3, 4, 焦新安1, 2, 3, 4, 潘志明1, 2, 3, 4
作者信息
  • 1.扬州大学，江苏省人兽共患病学重点实验室，江苏 扬州
  • 2.扬州大学，江苏省高校动物重要疫病与人兽共患病防控协同创新中心，江苏 扬州
  • 3.扬州大学，农业农村部农产品质量安全生物性危害因子(动物源)控制重点实验室，江苏 扬州
  • 4.扬州大学，教育部农业与农产品安全国际合作联合实验室，江苏 扬州
African swine fever virus protein E423R induces autophagy
Jingyi HUANG1, 2, 3, 4, Xilong KANG1, 2, 3, 4 , Xia HUANG1, 2, 3, 4, Yi ZHOU1, 2, 3, 4, Hongzhi LIU1, 2, 3, 4, Xin’an JIAO1, 2, 3, 4, Zhiming PAN1, 2, 3, 4
Affiliations
  • 1.Jiangsu Key Laboratory of Zoonosis, Yangzhou University, Yangzhou, Jiangsu, China
  • 2.Jiangsu Co-innovation Center for Prevention and Control of Important Animal Infectious Diseases and Zoonoses, Yangzhou University, Yangzhou, Jiangsu, China
  • 3.Key Laboratory of Prevention and Control of Biological Hazard Factors (Animal Origin) for Agrifood Safety and Quality, Ministry of Agriculture and Rural Affairs, Yangzhou University, Yangzhou, Jiangsu, China
  • 4.Joint International Research Laboratory of Agriculture and Agri-product Safety of the Ministry of Education, Yangzhou University, Yangzhou, Jiangsu, China
出版时间: 2025-07-04 doi: 10.13343/j.cnki.wsxb.20250043
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【目的】 探究非洲猪瘟病毒(African swine fever virus, ASFV)蛋白E423R诱导细胞自噬的功能。 【方法】 通过高内涵分析系统量化分析pCMV-Myc-E423R转染自噬报告细胞HeLa-DifluoTM hLC3后的RFP-LC3荧光斑点数，评估自噬通量；利用Western blotting分析HeLa细胞中自噬关键蛋白LC3-Ⅱ、SQSTM1/p62的表达水平；采用激光共聚焦技术观察自噬体与溶酶体的共定位情况；通过Western blotting检测E423R蛋白与LC3-Ⅱ表达的剂量依赖效应以及对AKT/mTOR/ULK1信号通路的调控作用。 【结果】 高内涵细胞分析实验显示，表达E423R蛋白的报告细胞中RFP-LC3荧光斑点明显增多，表明E423R蛋白可以诱导自噬发生活化；Western blotting分析证实，E423R蛋白表达促使LC3-Ⅱ/β-actin显著升高，p62的表达水平显著下调；共聚焦结果显示E423R蛋白可增强GFP-LC3的表达，促使GFP-LC3与Lyso-Tracker Red荧光共定位明显增多，诱导自噬体与溶酶体融合；同时，E423R蛋白表达水平与HeLa细胞中的LC3-Ⅱ表达水平呈正相关，E423R蛋白能下调mTOR信号通路中p-AKT、p-mTOR、p-ULK1 (Ser757)的表达。 【结论】 本研究揭示了ASFV E423R蛋白通过AKT/mTOR/ULK1信号通路诱导完整的细胞自噬过程，E423R与LC3-Ⅱ的表达呈一定程度的剂量依赖效应，为深入研究自噬在ASFV感染与致病机制中的功能奠定了基础。

非洲猪瘟病毒  /  E423R  /  自噬  /  AKT/mTOR/ULK1信号通路

[Objective] To explore the autophagy induced by the African swine fever virus (ASFV) protein E423R. [Methods] The RFP-LC3 fluorescent spots following the transfection of HeLa-DifluoTM hLC3 cells with pCMV-Myc-E423R was quantified by the High-Content Analysis System, and the autophagic flux was assessed. The expression levels of key autophagy proteins, LC3-Ⅱ and SQSTM1/p62, in HeLa cells were analyzed via Western blotting. Co-localization of autophagosomes and lysosomes was examined by laser confocal microscopy. Additionally, Western blotting was employed to investigate the dose-dependent effect of E423R on LC3-Ⅱ expression and the regulatory effect of E423R on the AKT/mTOR/ULK1 signaling pathway. [Results] The High-Content Analysis System demonstrated a significant increase in RFP-LC3 fluorescence spots in the reporter cells expressing E423R, suggesting that E423R induced the activation of autophagy. Western blotting further confirmed that the expression of E423R significantly elevated the LC3-Ⅱ/β-actin ratio while decreasing the expression level of p62. Confocal microscopy results indicated that E423R enhanced the expression of GFP-LC3, promoted the co-localization of GFP-LC3 with Lyso-Tracker Red, and facilitated the fusion of autophagosomes and lysosomes. Additionally, the expression level of E423R exhibited a positive correlation with the expression level of LC3-Ⅱ in HeLa cells. Furthermore, E423R down-regulated the expression of p-AKT, p-mTOR, and p-ULK1 (Ser757) in the mTOR signaling pathway. [Conclusion] This study demonstrates that the ASFV E423R protein induces complete autophagy via the AKT/mTOR/ULK1 signaling pathway, exhibiting a dose-dependent effect on LC3-Ⅱ expression to a certain degree. These findings provide a foundation for further investigation into the infection and pathogenic mechanisms of ASFV.

African swine fever virus (ASFV)  /  E423R  /  autophagy  /  AKT/mTOR/ULK1 signaling pathway
黄静怡, 康喜龙, 黄霞, 周懿, 刘弘知, 焦新安, 潘志明. 非洲猪瘟病毒E423R蛋白诱导细胞自噬的功能. 微生物学报, 2025 , 65 (7) : 3195 -3207 . DOI: 10.13343/j.cnki.wsxb.20250043
Jingyi HUANG, Xilong KANG, Xia HUANG, Yi ZHOU, Hongzhi LIU, Xin’an JIAO, Zhiming PAN. African swine fever virus protein E423R induces autophagy[J]. Acta Microbiologica Sinica, 2025 , 65 (7) : 3195 -3207 . DOI: 10.13343/j.cnki.wsxb.20250043
正文
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非洲猪瘟(African swine fever, ASF)是由非洲猪瘟病毒(African swine fever virus, ASFV)感染引起的一种急性、出血性传染病。患病家猪和野猪表现出高热、皮肤及内脏器官出血性病变等症状。由于尚无有效的疫苗和特效治疗药物，非洲猪瘟疫情难以控制，严重影响着我国乃至全球养猪业的运营与发展[1-2]。ASFV是一种包膜、胞质的双链DNA病毒，基因组为170-193 kb，编码68种结构蛋白和100多种非结构蛋白[3]，参与调节病毒复制、装配、蛋白质修饰以及与宿主细胞的交互作用等多个过程[4-5]。例如：p150、p37、p14、p34、p35和p15是病毒粒子核衣壳的主要成分，参与病毒装配[6]；CD2v使红细胞吸附到被感染的细胞表面，促进病毒进一步感染[7]；p30是一种早期膜蛋白，能够诱导机体发生快速且强烈的免疫应答，被视为ASFV感染早期的检测标志[8]。然而，ASFV编码的大多数蛋白的功能仍然未知。
自噬对维持细胞稳态至关重要。细胞能够通过自噬清除入侵的病原体，从而抵抗病毒感染[9-11]。研究显示，ASFV可以参与调节宿主细胞自噬[12]。其中，ASFV E199L蛋白可通过与PYCR2相互作用，降低PYCR2的表达，诱导细胞自噬[13]；ASFV K205R蛋白通过诱导内质网应激激活自噬通路[14]；ASFV p17蛋白与宿主胞内蛋白TOMM70结合，促进线粒体自噬受体SQSTM1与TOMM70的结合，从而诱导线粒体自噬[15]。然而，ASFV致病机制复杂，编码蛋白众多，其与自噬的关系仍未被完全阐明。
ASFV E423R蛋白是一种未表征蛋白，由Cackett等[16]通过高通量测序手段发现，其在ASFV复制周期后期表达。Rodríguez等[17]通过氨基酸序列比对发现，E423R蛋白可能与双组分信号传导蛋白组氨酸激酶相关，参与调控DpiA等转录调控蛋白的磷酸化。目前有关ASFV E423R蛋白的相关研究报道非常少。为了探究E423R与细胞自噬的关系，本研究通过高内涵细胞分析技术，分析ASFV E423R蛋白对自噬体形成的影响；使用Western blotting检测自噬关键蛋白LC3-Ⅱ、p62的表达；利用激光共聚焦技术观察E423R表达下自噬小体与溶酶体的共定位；通过Western blotting探索E423R蛋白与LC3-Ⅱ是否存在剂量依赖效应，以及E423R参与细胞自噬的具体通路，以期为深入研究ASFV病毒蛋白调节细胞自噬的机制提供理论依据。
1 材料与方法
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1.1 细胞和质粒
HeLa细胞、HeLa-DifluoTM hLC3自噬报告细胞系均由本实验室保存，使用含10%胎牛血清(fetal bovine serum, FBS)的DMEM培养基进行培养。其中，HeLa-DifluoTM hLC3自噬报告细胞系在含有100 µg/mL ZeocinTM的生长培养基中进行培养和细胞传代。pCMV-Myc载体由本实验室保存。
1.2 主要试剂
无内毒素质粒小提中量试剂盒，Tiangen公司；细胞培养基DMEM、胎牛血清、胰酶、Opti-MEM (转染用培养基)，Gibco公司；Lip2000 Transfection Reagent，Biosharp公司；180 kDa Prestained Protein Marker、180 kDa Plus Prestained Protein Marker，Vazyme公司；SDS-PAGE蛋白上样缓冲液(5×)、Myc抗体(小鼠单抗)、β-Actin Mouse Monoclonal Antibody、mTOR Rabbit Monoclonal Antibody、山羊抗兔Alexa Fluor 488、山羊抗小鼠DyLight 405抗体，上海碧云天生物技术股份有限公司；LC3 Polyclonal Antibody，武汉三鹰生物技术有限公司；SQSTM1/p62 Recombinant Rabbit Monoclonal Antibody、AKT1/2/3 Recombinant Rabbit Monoclonal Antibody、Phospho-AKT (S473) Recombinant Rabbit Monoclonal Antibody、Anti-ULK1 Recombinant Rabbit Monoclonal Antibody、Phospho-mTOR (S2448) Mouse Monoclonal Antibody，杭州华安生物技术有限公司；Goat Anti Rabbit IgG HRP、Goat Anti Mouse IgG HRP，ABclone公司；ULK1 (Phospho Ser757) Rabbit Polyclonal Antibody，苏州博特龙免疫技术有限公司。
1.3 ASFV E423R、ASFV E199L、ASFV DP238L真核表达质粒的构建及表达
ASFV E423R基因(GenBank登录号为AAA65355.1)、ASFV E199L基因(GenBank登录号为AAA65358.1)、ASFV DP238L基因(GenBank登录号为AAA65373.1)均由生工生物工程(上海)股份有限公司合成，并插入到pCMV-Myc表达载体的EcoR Ⅰ和Eag Ⅰ酶切位点之间。将pCMV-Myc、pCMV-Myc-E423R、pCMV-Myc-E199L、pCMV-Myc-DP238L分别转染至HeLa细胞，24 h后使用Western及IP细胞裂解液裂解细胞，收集总蛋白。使用Myc抗体(小鼠单抗)作为一抗，通过Western blotting检测E423R、E199L、DP238L蛋白的表达情况。
1.4 E423R蛋白对自噬体形成的影响
将自噬报告细胞HeLa-Difluo™ hLC3接种于96孔板，37 ℃、5% CO2培养过夜。待细胞生长至70%后，转染200 ng pCMV-Myc-E423R，24 h后使用1:1混匀的甲醇:丙酮进行固定，PBS清洗3遍，加入DAPI荧光染料37 ℃避光标记8 min。设置如下对照：Mock组(空白对照，不进行质粒转染、Rapamycin处理)，EV组(阴性对照，200 ng pCMV-Myc转染)，Rapamycin组(阳性对照，使用25 μmol/L Rapamycin处理细胞，2 h后再进行固定等后续操作)，E199L组(阳性对照，使用pCMV-Myc-E199L质粒进行转染)，DP238L组(无关对照，使用pCMV-Myc-DP238L质粒进行转染）。使用Operetta CLS高内涵细胞成像仪HCA进行自噬体与荧光共定位观察。
1.5 E423R蛋白对自噬关键蛋白LC3、SQSTM1/p62表达的影响
为了评价E423R蛋白对自噬关键蛋白LC3、SQSTM1/p62的影响，将HeLa细胞接种于24孔培养板，进行如下处理：分别使用800 ng pCMV-Myc、pCMV-Myc-E423R、pCMV-Myc-E199L转染HeLa细胞。收样前2 h更换含25 μmol/L雷帕霉素或100 nmol/L巴佛洛霉素A1的DMEM，继续培养至24 h，收取总蛋白。通过Western blotting检测LC3、SQSTM1/p62的表达水平。
1.6 E423R蛋白对自噬流的影响
为了进一步探究E423R蛋白对自噬过程的影响，将HeLa细胞接种于放有细胞爬片的24孔板中，于37 ℃、5% CO2培养过夜。使用800 ng pCMV-Myc-E423R进行转染，24 h后加入PBS清洗细胞。使用37 ℃预热的4%多聚甲醛，室温固定15-20 min，PBS清洗，加入0.5% Triton X-100 400 μL常温破膜20 min。将细胞在含5% BSA的PBS中37 ℃封闭2 h，依次孵育LC3 Polyclonal Antibody、Myc抗体(小鼠单抗)，置于4 ℃、40 r/min的水平摇床上过夜。PBS清洗4次，每次5 min，加入山羊抗兔Alexa Fluor 488、山羊抗小鼠DyLight 405 37 ℃孵育2 h，PBS清洗4次，每次5 min，加入甘油、指甲油封片。设置如下对照：Mock组(空白对照，不进行质粒转染、Rapamycin处理)，EV组(阴性对照，使用800 ng pCMV-Myc转染)，EV+Rapamycin组(阳性对照，使用800 ng pCMV-Myc进行转染)，22 h后使用25 μmol/L雷帕霉素处理2 h再进行固定等后续操作。
1.7 E423R蛋白诱导自噬剂量依赖效应探究
为了检测E423R与LC3-Ⅱ蛋白之间是否存在剂量依赖效应，使用24孔板接种HeLa细胞，分别将600 ng pCMV-Myc转染HeLa细胞作为对照组，将200、400、600、800、1 000 ng pCMV-Myc-E423R转染到HeLa细胞，24 h后收取总蛋白。使用Myc抗体(小鼠单抗)、LC3 Polyclonal Antibody作为一抗，通过Western blotting检测E423R、LC3的表达水平。
1.8 E423R蛋白对AKT/mTOR/ULK1信号通路的调控作用
为了探究E423R蛋白诱导细胞自噬所涉及的信号通路，使用24孔板接种HeLa细胞，将pCMV-Myc-E423R分别以200、400、600、800、1 000 ng的剂量转染到HeLa细胞；同时设立对照组，将pCMV-Myc以600 ng的剂量转染到HeLa细胞。24 h后，进行裂解、收样。使用AKT1/2/3 Recombinant Rabbit Monoclonal Antibody、Phospho-AKT (S473) Recombinant Rabbit Monoclonal Antibody、mTOR Rabbit Monoclonal Antibody、Phospho-mTOR (S2448) Mouse Monoclonal Antibody、Anti-ULK1 Recombinant Rabbit Monoclonal Antibody、ULK1 (Phospho Ser757) Rabbit Polyclonal Antibody作为一抗，通过Western blotting检测AKT、p-AKT、mTOR、p-mTOR、ULK1等蛋白的表达水平。
1.9 统计学分析
将试验所得数据通过GraphPad Prism 8软件进行t检验分析，统计学差异用P值表示，*：P<0.05；**：P<0.01，***：P<0.001。所有涉及统计学分析的数据至少重复3次。
2 结果与分析
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2.1 E423R、E199L、DP238L蛋白表达的鉴定
为检测pCMV-Myc-E423R、pCMV-Myc-E199L、pCMV-Myc-DP238L质粒是否表达，分别将pCMV-Myc-E423R、pCMV-Myc-E199L、pCMV-Myc-DP238L质粒转染HeLa细胞，24 h后收取总蛋白，以Myc抗体(小鼠单抗)作为一抗进行Western blotting。结果如图1所示，pCMV-Myc-E423R转染组在48 kDa左右有明显可见的条带(图1A)，pCMV-Myc-E199L转染组在22 kDa左右有明显可见的条带(图1B)，pCMV-Myc-DP238L转染组在27 kDa左右有明显可见的条带(图1C)，与预期结果一致，而空载体转染组未见条带，表明E423R、E199L、DP238L蛋白在真核细胞中成功表达。
2.2 E423R蛋白诱导自噬体形成
通过高内涵实验探究E423R蛋白对细胞自噬的影响。HeLa-DifluoTM hLC3细胞是来源于HeLa细胞系的自噬报告细胞，能够表达融合蛋白RFP::GFP::LC3，通过检测双荧光或单荧光红色LC3斑点实时监测自噬通量。在自噬早期，RFP和GFP信号都被检测到。随着自噬体与溶酶体的融合，GFP荧光减弱，只留下可见的RFP荧光。一般通过RFP-GFP阳性细胞的荧光斑点百分比或RFP阳性细胞的荧光斑点百分比评估自噬通量。如图2A所示，未处理组(Mock)、空载体组(EV)与pCMV-Myc-DP238L转染组(DP238L)中的自噬活性处于较低水平，GFP-LC3、RFP-LC3融合蛋白在胞质中主要呈弥散分布；而在雷帕霉素刺激组(Rapamycin)、pCMV-Myc-E199L转染组(E199L)和pCMV-Myc-E423R转染组(E423R)中，GFP-LC3、RFP-LC3融合蛋白积聚在自噬体膜上，形成明亮的红、绿荧光斑点。通过高内涵分析系统对HeLa-DifluoTM hLC3的RFP-LC3荧光斑点数进行量化分析(图2B)，与EV组相比，E423R组中RFP-LC3荧光斑点明显增多(P<0.05)。上述结果表明，E423R蛋白能够诱导自噬过程起始，促进早期自噬体的形成。
2.3 E423R蛋白诱导完整的细胞自噬过程
为检测E423R蛋白对细胞自噬的促进作用，采用Western blotting分析检测pCMV-Myc-E423R转染后HeLa细胞中LC3-Ⅱ、p62的表达水平。如图3A所示，与空白对照组(Mock)和空载体组(EV)相比，pCMV-Myc-E423R转染及阳性对照pCMV-Myc-E199L转染的细胞中LC3-Ⅱ水平均升高；使用ImageJ对LC3表达量进行灰度分析，与空载体组相比，pCMV-Myc-E423R转染后LC3-Ⅱ/β-actin显著升高(P<0.05) (图3B)。自噬体的累积可能是由于自噬诱导或自噬流的阻断。为测定E423R蛋白诱导的自噬过程是否完整，进一步检测p62的表达水平，与空载体组相比，在转染24 h后p62表达水平降低(图3A)；使用ImageJ对p62表达量进行灰度分析，与空载体组相比，pCMV-Myc-E423R转染后p62/β-actin显著降低(P<0.05) (图3C)。为进一步确定E423R蛋白是否影响自噬通量，使用巴佛洛霉素A1处理pCMV-Myc-E423R转染的细胞。结果显示，与未刺激组相比，添加巴佛洛霉素A1的刺激组诱导的LC3-Ⅱ积累更多，并且未引起p62降解(图3D)。同时灰度分析表明，与未刺激组相比，添加巴佛洛霉素A1的刺激组的LC3-Ⅱ/β-actin (图3E)与p62/β-actin (图3F)均上升。因此，E423R蛋白能够促进完整的细胞自噬过程。
2.4 E423R蛋白诱导自噬体与溶酶体在HeLa细胞中的共定位
为进一步证实E423R蛋白诱导自噬过程的完整性，通过激光共聚焦显微镜观察E423R蛋白诱导细胞产生自噬体积累以及自噬小体与溶酶体的共定位情况。利用pCMV-Myc-E423R转染HeLa细胞，Lyso-Tracker Red染料标记细胞的酸性溶酶体，在激光共聚焦显微镜下观察自噬体和Lyso-Tracker Red在细胞中的共定位。结果如图4A所示，在pCMV-Myc-E423R转染组(E423R)中能够观察到自噬小体与溶酶体在细胞质内共定位，说明E423R蛋白能够诱导自噬小体与溶酶体融合。利用ImageJ软件进行统计分析，pCMV-Myc-E423R转染组(E423R)中，LC3荧光斑点(图4B)、自噬体与Lyso-Tracker Red的共定位(图4C)与空载体组EV相比均明显增加(P<0.01、P<0.001)。以上结果表明，E423R蛋白能够诱导自噬体与酸性溶酶体融合，进一步验证了E423R蛋白诱导的自噬在HeLa细胞中是一个完整的过程。
2.5 E423R蛋白诱导自噬关键蛋白LC3-Ⅱ表达并呈剂量依赖
为检测E423R蛋白对细胞内自噬关键蛋白LC3-Ⅱ的促进作用，将200-1 000 ng pCMV-Myc-E423R或pCMV-Myc (EV组)分别转染到HeLa细胞中，24 h后通过Western blotting测定LC3-Ⅱ表达水平。如图5A、5B所示，在检测范围内E423R表达量越高，LC3-Ⅱ表达量越多。结果表明，E423R蛋白能够激活自噬过程，并且与LC3-Ⅱ呈现剂量依赖性。
2.6 E423R蛋白通过AKT/mTOR/ULK1信号通路激活自噬
在自噬通路中存在许多关键蛋白，这些蛋白通过相互作用对自噬进行调控。根据Western blotting结果观察到，使用200-1 000 ng pCMV-Myc-E423R转染时，随着转染剂量升高，磷酸化的AKT和mTOR逐渐降低(图6)，p-ULK1 (Ser757)的磷酸化逐渐减少，表明E423R蛋白激活了ULK1，上调自噬信号通路。这一结果表明AKT/mTOR/ULK1通路受到E423R蛋白的抑制，并且在检测浓度范围内具有剂量依赖性。综上所述，E423R蛋白通过AKT/mTOR/ULK1信号通路激活了自噬。
3 讨论与结论
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自噬是一种高度保守的分解代谢过程，通常被认为是细胞的一种保护机制。自噬体与溶酶体融合形成自噬溶酶体，导致被吞噬的成分降解并产生营养物质[18]。病毒与细胞自噬之间存在复杂的相关性。一方面，自噬可以用来降解病毒颗粒；另一方面，一些病毒阻断自噬降解，甚至通过促进细胞自噬进行复制[19]。研究显示，ASFV可以调节宿主细胞自噬，但是关于ASFV与宿主细胞自噬的关系仍未完全阐明[12]。因此，解析ASFV蛋白与宿主细胞自噬之间的关系能够为开发新的抗病毒药物提供可能的靶点线索，为深入研究ASFV感染的机制提供理论依据。
ASFV与自噬之间存在复杂的相互作用，在ASFV感染过程中自噬很可能发挥抗病毒作用，然而自噬与ASFV感染之间的研究仍然不足。ASFV E423R蛋白是一种未表征蛋白，在ASFV复制周期的后期表达[16]。在本研究中，着重关注ASFV E423R蛋白对细胞自噬的调控作用。鉴定完整的自噬发生过程通常包括3个指标：LC3荧光斑点的形成、LC3-Ⅱ的积累和p62的降解[20-21]。因此，本研究通过高内涵分析系统对HeLa-DifluoTM hLC3细胞中RFP-LC3荧光斑点数进行量化分析。高内涵分析技术是一种结合了自动化细胞成像和复杂图像分析的高通量筛选技术，它兼顾了直观与批量统计分析的优点，能够通过自动化细胞成像的方法对多孔板每一个孔的细胞进行单细胞水平状态和总体趋势的分析，常用于细胞的自噬水平评估，通过RFP-LC3、GFP-LC3荧光斑点积聚判断细胞自噬水平[22]。Zhou等[23]通过高内涵分析技术对肠炎沙门菌菌株Z11的转座子突变文库进行筛选，发现RfbD基因对自噬有影响。Gao等[24]通过对107个LSCC组织和成对的癌旁正常黏膜(adjacent normal mucosal, ANM)组织进行高内涵筛选，鉴定出抑制自噬的circRNA circPARD3。同样地，本研究通过高内涵细胞分析实验评估HeLa-DifluoTM hLC3细胞的自噬水平。当E423R蛋白表达时，HeLa-DifluoTM hLC3细胞中出现了大量的RFP、GFP斑点，并且与空载体组相比，RFP斑点明显增多，说明E423R蛋白的存在使得LC3融合蛋白在自噬体上发生积聚，促进自噬的起始过程。通过Western blotting实验探究E423R蛋白诱导自噬过程的完整性，结果显示pCMV-Myc-E423R真核表达质粒转染24 h后，LC3-Ⅱ的表达量显著升高，p62降解，并且随着E423R转染剂量增加，LC3-Ⅱ的表达量增加，呈正相关。同时，通过共聚焦显微镜观察到LC3荧光斑点的形成以及与酸性溶酶体共定位。这些观察结果证实，ASFV E423R蛋白诱导自噬体形成，并与自噬溶酶体融合。因此，E423R能够诱导HeLa细胞内完整的自噬过程。
与本研究结果一致，ASFV E199L也是病毒的一种晚期表达蛋白，它可以通过与PYCR2相互作用，诱导HEK293T细胞完整的自噬发生过程[13,25]；ASFV K205R蛋白激活内质网应激，引发机体促炎反应，进而激活自噬，促进抗病毒免疫[14]；ASFV p17蛋白通过促进p62与TOMM70的相互作用促进线粒体自噬[15]。然而ASFV也存在抑制自噬的蛋白，如ASFV A179L通过与Beclin1 BH3结构域相互作用抑制自噬，从而操纵细胞凋亡控制感染[26-28]。
AKT/mTOR/ULK1作为经典自噬通路，参与调控多种病毒感染过程。正常状态下，AKT、mTOR蛋白抑制自噬，当自噬激活，AKT、mTOR蛋白去磷酸化，下游的ULK1通过改变磷酸化位点募集ATG家族蛋白，促使自噬体形成[29-30]。与ASFV同属于DNA病毒的人乳头瘤病毒(human papilloma viruses, HPV)通过表皮生长因子受体(epidermal growth factor receptor, EGFR)和PKB/AKT相互作用，导致mTOR发生磷酸化[31]。有研究证实，ASFV感染能够激活mTOR，抑制自噬相关基因Atg2A、Atg9A、Atg101、Atg4B、Atg7的表达[32]。ASFV K205R通过抑制AKT、mTOR磷酸化从而激活ULK1，激活自噬[14]。本研究结果也同样表明，E423R蛋白通过影响AKT/mTOR/ULK1信号通路调节细胞自噬。E423R蛋白能够诱导HeLa细胞自噬，并通过AKT/mTOR/ULK1信号通路增强细胞自噬的发生。
综上所述，本研究通过高内涵分析、Western blotting、激光共聚焦技术，证实了ASFV E423R蛋白具有诱导HeLa细胞自噬的功能。进一步地，Western blotting分析显示，随着E423R蛋白表达量上升，LC3-Ⅱ表达量也逐渐上升，E423R与LC3-Ⅱ之间具有剂量依赖效应。然而，E423R通过下调AKT、mTOR的磷酸化水平从而调控ULK1，诱导完整的自噬发生过程。本研究丰富了ASFV E423R蛋白的自噬功能，为研究ASFV与自噬的关系提供了有意义的参考，为开发新的抗病毒药物提供理论基础。
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作者声明不存在任何可能会影响本文所报告工作的已知经济利益或个人关系。
基金
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  • 江苏省重点研发计划(现代农业)项目(BE2021331)
  • 江苏省研究生科研与实践创新计划(KYCX24_3823)
  • 江苏高校优势学科建设工程项目
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doi: 10.13343/j.cnki.wsxb.20250043
  • 接收时间：2025-01-15
  • 首发时间：2026-02-06
  • 出版时间：2025-07-04
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  • 收稿日期：2025-01-15
  • 录用日期：2025-03-04
基金
Key Research and Development Program (Modern Agriculture) Project of Jiangsu Province(BE2021331)
江苏省重点研发计划(现代农业)项目(BE2021331)
Postgraduate Research and Practice Innovation Program of Jiangsu Province(KYCX24_3823)
江苏省研究生科研与实践创新计划(KYCX24_3823)
the Priority Academic Program Development of Jiangsu Higher Education Institutions (PAPD)
江苏高校优势学科建设工程项目
作者信息
    1.扬州大学，江苏省人兽共患病学重点实验室，江苏 扬州
    2.扬州大学，江苏省高校动物重要疫病与人兽共患病防控协同创新中心，江苏 扬州
    3.扬州大学，农业农村部农产品质量安全生物性危害因子(动物源)控制重点实验室，江苏 扬州
    4.扬州大学，教育部农业与农产品安全国际合作联合实验室，江苏 扬州
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