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Article(id=1226956549407552258, tenantId=1146029695717560320, journalId=1192105938417971205, issueId=1226956547847275311, articleNumber=null, orderNo=null, doi=10.13343/j.cnki.wsxb.20250085, pmid=null, cstr=null, oa=null, hot=null, price=null, onlineType=0, articleFormat=0, articleType=null, articleTypeStr=research-article, receivedDate=1738857600000, receivedDateStr=2025-02-07, revisedDate=null, revisedDateStr=null, acceptedDate=1746288000000, acceptedDateStr=2025-05-04, onlineDate=1770458837129, onlineDateStr=2026-02-07, pubDate=1756915200000, pubDateStr=2025-09-04, doiRegisterDate=null, doiRegisterDateStr=null, onlineIssueDate=1770458837129, onlineIssueDateStr=2026-02-07, onlineJustAcceptDate=null, onlineJustAcceptDateStr=null, onlineFirstDate=null, onlineFirstDateStr=null, sourceXml=null, magXml=null, createTime=1770458837129, creator=13701087609, updateTime=1770458837129, updator=13701087609, issue=Issue{id=1226956547847275311, tenantId=1146029695717560320, journalId=1192105938417971205, year='2025', volume='65', issue='9', pageStart='3821', pageEnd='4232', issueExtLink='null', onlineDate='null', pubDate='null', beforeIssueId=null, nextIssueId=null, price=null, status=1, issueComplete=1, articleOrder=1, issueType=-1, specialIssue=null, createTime=1770458836757, creator=13701087609, updateTime=1770459153781, updator=13701087609, preIssue=null, nextIssue=null, ext={EN=IssueExt(id=1226957877613605816, tenantId=1146029695717560320, journalId=1192105938417971205, issueId=1226956547847275311, language=EN, specialIssueTitle=, coverIllustrator=null, specialIssueEditor=, specialIssueAbout=), CN=IssueExt(id=1226957877613605817, tenantId=1146029695717560320, journalId=1192105938417971205, issueId=1226956547847275311, language=CN, specialIssueTitle=, coverIllustrator=null, specialIssueEditor=, specialIssueAbout=)}, issueFiles=null}, startPage=3935, endPage=3945, ext={EN=ArticleExt(id=1226956550087029512, articleId=1226956549407552258, tenantId=1146029695717560320, journalId=1192105938417971205, language=EN, title=Voltage dependent anion-selective channel 2 promotes interferon response to inhibit foot-and-mouth disease virus replication, columnId=1192149543992045670, journalTitle=Acta Microbiologica Sinica, columnName=Research Article, runingTitle=null, highlight=null, articleAbstract=

Foot-and-mouth disease (FMD) is a highly contagious disease caused by foot-and-mouth disease virus (FMDV) in cloven-hoofed animals. FMDV is a single-stranded positive-sense non-enveloped RNA virus with icosahedral symmetry. FMDV can cause innate and adaptive immunity of the host, and it has evolved a variety of immune escape ways. The FMDV infection is a complicated process involving various host proteins. However, the related mechanisms remain largely unknown. Voltage dependent anion-selective channel 2 (VDAC2) is a mitochondrial channel protein, and the specific mechanism by which VDAC2 regulates FMDV replication remains unclear. [Objective] To confirm the regulatory effects between VDAC2 and FMDV and reveal the molecular mechanism by which VDAC2 inhibits FMDV replication. [Methods] The subcellular localization of VDAC2 was determined by the indirect immunofluorescence assay. The effects of FMDV on the translation and transcription levels of VDAC2 were determined by Western blotting and qPCR, respectively. The effect of VDAC2 overexpression on FMDV replication in BHK-21 cells was measured based on the virus titer. The effects of VDAC2 overexpression and knockdown on the levels of IL-1β, ISG15, OAS1, mtDNA, and gDNA during FMDV infection were evaluated by qPCR. [Results] VDAC2 was localized in the cytoplasm. FMDV infection down-regulated the expression of VDAC2. The overexpression of VDAC2 inhibited FMDV replication in a dose-dependent manner, while the knockdown of VDAC2 promoted FMDV replication. The overexpression of VDAC2 enhanced FMDV-induced interferon-I (IFN-I) response, while the knockdown of VDAC2 inhibited FMDV-induced IFN-I response. In addition, the overexpression of VDAC2 increased the release of mtDNA. [Conclusion] FMDV infection can downregulate the transcription and translation of VDAC2, as VDAC2 can exert antiviral effects by regulating mtDNA release and promoting the expression of antiviral factors such as IL-1β, ISG15, and OAS1. This study indicates that upon FMDV infection, host cells can regulate the virus replication by enhancing IFN-I response via VDAC2 to exert antiviral effects.

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*E-mail: BAO Shijun,
ZHU Zixiang,
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口蹄疫(foot-and-mouth disease, FMD)是由口蹄疫病毒(foot-and-mouth disease virus, FMDV)感染偶蹄动物引起的一种烈性动物传染病。FMDV是一种单股正链无囊膜RNA病毒，具有二十面体对称结构。FMDV入侵宿主后会引起宿主的先天性免疫和适应性免疫反应，而FMDV已经进化出多种途径来逃避免疫。FMDV的感染致病机制复杂，目前对于参与调控病毒感染复制的宿主因子的认知仍然非常有限。宿主线粒体通道蛋白(voltage dependent anion-selective channel 2, VDAC2)是一种线粒体通道蛋白，目前关于VDAC2对FMDV复制调控的具体机制尚不清楚。 【目的】 确证VDAC2与FMDV之间的调控作用，并揭示VDAC2抑制FMDV复制的分子机制。 【方法】 通过间接免疫荧光方法确定VDAC2在细胞内的定位；利用Western blotting以及荧光定量PCR方法检测FMDV对VDAC2蛋白水平和转录水平的影响；在BHK-21细胞上利用病毒滴度测定法检测过表达VDAC2对FMDV复制的影响；利用qPCR方法检测上调或下调VDAC2后FMDV感染对细胞内IL-1β、ISG15、OAS1、mtDNA和gDNA水平的影响。 【结果】 结果显示VDAC2亚细胞定位于细胞质中；FMDV感染可以降低VDAC2的表达；过表达VDAC2显著抑制FMDV的复制，并呈现剂量依赖关系；干扰VDAC2能够促进FMDV的复制；过表达VDAC2可增强FMDV诱导的IFN-Ⅰ反应；干扰VDAC2可抑制FMDV诱导的IFN-Ⅰ反应；过表达VDAC2可以促进mtDNA的释放。 【结论】 本研究表明FMDV感染可以下调VDAC2的转录与蛋白表达，而VDAC2可通过调节mtDNA的释放促进IL-1β、ISG15和OAS1等抗病毒因子的表达，从而发挥抗病毒作用。当FMDV入侵宿主细胞时，宿主细胞可以通过VDAC2增强IFN-Ⅰ反应，对病毒复制进行调控，发挥抗病毒作用。

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作者贡献声明

蔡镇远：数据收集与监管，数据分析，完成呈现，撰写文章；陈文哲：监督管理，数据分析；杨发誉：审阅文章；魏衍全：监督管理；何继军：监督管理；郑海学：项目管理；包世俊：监督管理；朱紫祥：提出概念，提供资源，审阅文章。

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Study on mechanism of host protein VDAC1 inhibiting replication of foot-and-mouth disease virus[J]. Chinese Veterinary Science, 2024, 54(12): 1563-1568 (in Chinese)., articleTitle=null, refAbstract=null), Reference(id=1226964064086179983, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1226956549407552258, doi=null, pmid=null, pmcid=null, year=2021, volume=49, issue=6, pageStart=2787, pageEnd=2795, url=null, language=null, rfNumber=[14], rfOrder=15, authorNames=YUAN Z, DEWSON G, CZABOTAR PE, BIRKINSHAW RW, journalName=Biochemical Society Transactions, refType=null, unstructuredReference=YUAN Z, DEWSON G, CZABOTAR PE, BIRKINSHAW RW. VDAC2 and the BCL-2 family of proteins[J]. 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A: Subcellular localization of HA-VDAC2; B: DAPI staining of the nucleus; C: Merge staining of the nucleus and cytoplasm., figureFileSmall=KdI7dBkYix5E0RKh/nTybg==, figureFileBig=OGwq6WdOmjX+wzZRXvghhg==, tableContent=null), ArticleFig(id=1226964056414798701, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1226956549407552258, language=CN, label=图1, caption=pcDNA-HA-VDAC2质粒的细胞定位, figureFileSmall=KdI7dBkYix5E0RKh/nTybg==, figureFileBig=OGwq6WdOmjX+wzZRXvghhg==, tableContent=null), ArticleFig(id=1226964056582570874, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1226956549407552258, language=EN, label=Figure 2, caption=FMDV infection decreased the expression of endogenous VDAC2. A: VDAC2 protein levels were detected after FMDV infection; B: VDAC2 mRNA level was detected after FMDV infection. NC: Negative control. *: Significant difference (P<0.05)., figureFileSmall=pFRRu7x04DX+AXY8GbOf4g==, figureFileBig=EUy4xM+syJ9IIQqfNMAMlw==, tableContent=null), ArticleFig(id=1226964056670651261, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1226956549407552258, language=CN, label=图2, caption=FMDV感染调控内源蛋白VDAC2的表达, figureFileSmall=pFRRu7x04DX+AXY8GbOf4g==, figureFileBig=EUy4xM+syJ9IIQqfNMAMlw==, tableContent=null), ArticleFig(id=1226964056779703173, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1226956549407552258, language=EN, label=Figure 3, caption=Overexpression of VDAC2 suppressed FMDV replication. A: FMDV protein levels were detected in VDAC2 overexpressing cells after FMDV infection; B: FMDV VP1 mRNA levels were detected in VDAC2 overexpressing cells; C: Determination of viral titers using BHK-21 cells. *: P<0.05; **: P<0.01., figureFileSmall=qSNi70U/4T1ESvWJmh7Wpg==, figureFileBig=e4RHaTlPfTuYUh+thA9CXA==, tableContent=null), ArticleFig(id=1226964056871977866, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1226956549407552258, language=CN, label=图3, caption=过表达VDAC2抑制FMDV的复制, figureFileSmall=qSNi70U/4T1ESvWJmh7Wpg==, figureFileBig=e4RHaTlPfTuYUh+thA9CXA==, tableContent=null), ArticleFig(id=1226964056951669650, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1226956549407552258, language=EN, label=Figure 4, caption=Downregulation of VDAC2 expression promotes FMDV replication. A: Detection of silence ratio of VDAC2 siRNA; B: FMDV protein levels were detected after downregulation of VDAC2 expression; C: FMDV VP1 mRNA levels were detected after downregulation of VDAC2 expression; D: VDAC2 mRNA levels were detected after downregulation of VDAC2 expression. NC: Negative control. *: P<0.05; ***: P<0.001., figureFileSmall=sOC0qHbdjOvf8oW0hpMlDg==, figureFileBig=wzg4Y7sIqSM7tdw2y2UKjw==, tableContent=null), ArticleFig(id=1226964057052332952, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1226956549407552258, language=CN, label=图4, caption=下调VDAC2促进FMDV的复制, figureFileSmall=sOC0qHbdjOvf8oW0hpMlDg==, figureFileBig=wzg4Y7sIqSM7tdw2y2UKjw==, tableContent=null), ArticleFig(id=1226964057157190557, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1226956549407552258, language=EN, label=Figure 5, caption=Overexpression of VDAC2 promoted IFN-I response induced by FMDV. A: The mRNA level of IL-1β was detected by qPCR; B: The mRNA level of ISG15 was detected by qPCR; C: The mRNA level of OAS1 was detected by qPCR. **: P<0.01; ****: P<0.000 1., figureFileSmall=I70/wJneV6miha6TfuUmVg==, figureFileBig=pEg+M7g2A3dsmnpjBlWJ1A==, tableContent=null), ArticleFig(id=1226964057245270949, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1226956549407552258, language=CN, label=图5, caption=过表达VDAC2促进FMDV诱导的IFN-Ⅰ反应, figureFileSmall=I70/wJneV6miha6TfuUmVg==, figureFileBig=pEg+M7g2A3dsmnpjBlWJ1A==, tableContent=null), ArticleFig(id=1226964057333351339, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1226956549407552258, language=EN, label=Figure 6, caption=Downregulation of VDAC2 inhibited IFN-I response induced by FMDV. A: The mRNA level of IL-1β was detected by qPCR; B: The mRNA level of ISG15 was detected by qPCR; C: The mRNA level of OAS1 was detected by qPCR. **: P<0.01; ****: P<0.000 1., figureFileSmall=d4IvGjto5YBd32vs0MgqmA==, figureFileBig=M0twIVmFvkfhO/bR/E4KWQ==, tableContent=null), ArticleFig(id=1226964057459180463, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1226956549407552258, language=CN, label=图6, caption=下调VDAC2抑制FMDV诱导的IFN-Ⅰ反应, figureFileSmall=d4IvGjto5YBd32vs0MgqmA==, figureFileBig=M0twIVmFvkfhO/bR/E4KWQ==, tableContent=null), ArticleFig(id=1226964057618564022, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1226956549407552258, language=EN, label=Figure 7, caption=Overexpression of VDAC2 promotes mtDNA release. A: Detection of mtDNA levels; B: Detection of gDNA levels. ns: No significant difference (P>0.05); *: Significant difference (P<0.05)., figureFileSmall=IDHxECy1DqXNh7embqsuuQ==, figureFileBig=NwA6iHXbo8ORwjKseZ06bg==, tableContent=null), ArticleFig(id=1226964057803113404, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1226956549407552258, language=CN, label=图7, caption=过表达VDAC2促进mtDNA的释放, figureFileSmall=IDHxECy1DqXNh7embqsuuQ==, figureFileBig=NwA6iHXbo8ORwjKseZ06bg==, tableContent=null), ArticleFig(id=1226964057941525447, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1226956549407552258, language=EN, label=Figure 8, caption=Overexpression of VDAC2 promotes the expression of p-STAT1., figureFileSmall=YWwsoobBHMXKI2V4qTaMkQ==, figureFileBig=47kXnKovJPBqPMYy5WbFnA==, tableContent=null), ArticleFig(id=1226964058042188743, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1226956549407552258, language=CN, label=图8, caption=过表达VDAC2促进p-STAT1的表达, figureFileSmall=YWwsoobBHMXKI2V4qTaMkQ==, figureFileBig=47kXnKovJPBqPMYy5WbFnA==, tableContent=null), ArticleFig(id=1226964058151240654, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1226956549407552258, language=EN, label=Table 1, caption=

siRNAs targeting the VDAC2 gene

, figureFileSmall=null, figureFileBig=null, tableContent=
Name of siRNAsPrimer sequences (5′→3′)
si-VDAC2-1

Sense: GGUUCAUCUAAUACAGACA

Antisense: UGUCUGUAUUAGAUGAACC

si-VDAC2-2

Sense: GAUCUUGACACUUCAGUAA

Antisense: UUACUGAAGUGUCAAGAUC

), ArticleFig(id=1226964059564721116, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1226956549407552258, language=CN, label=表1, caption=

靶向VDAC2的siRNA序列

, figureFileSmall=null, figureFileBig=null, tableContent=
Name of siRNAsPrimer sequences (5′→3′)
si-VDAC2-1

Sense: GGUUCAUCUAAUACAGACA

Antisense: UGUCUGUAUUAGAUGAACC

si-VDAC2-2

Sense: GAUCUUGACACUUCAGUAA

Antisense: UUACUGAAGUGUCAAGAUC

), ArticleFig(id=1226964059690550243, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1226956549407552258, language=EN, label=Table 2, caption=

The primers used in this study

, figureFileSmall=null, figureFileBig=null, tableContent=
GenePrimer sequences (5′→3′)
FMDV

Forward: TTCGGCCTTTGATGCTAACCACTG

Reverse: GCATCCCGCCCTAACAACAAT

VDAC2

Forward: TCAAGTCTTCTTACAAGAGGGA

Reverse: TCAAAGGTCATCTGGTACCCAG

IL-1β

Forward: AGCGACATGGAGAAGCGATTT

Reverse: TTCTGCTTGAGAGGTGCTGATG

ISG15

Forward: GATCGGTGTGCCTGCCTTC

Reverse: CGTTGCTGCGACCCTTGT

OAS1

Forward: AAGCATCAGAAGCTTTGCATCTT

Reverse: CAGGCCTGGGTTTCTTGAGTT

GAPDH

Forward: ACATGGCCTCCAAGGAGTAAGA

Reverse: GATCGAGTTGGGGCTGTGACT

), ArticleFig(id=1226964059812185065, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1226956549407552258, language=CN, label=表2, caption=

本研究所用引物

, figureFileSmall=null, figureFileBig=null, tableContent=
GenePrimer sequences (5′→3′)
FMDV

Forward: TTCGGCCTTTGATGCTAACCACTG

Reverse: GCATCCCGCCCTAACAACAAT

VDAC2

Forward: TCAAGTCTTCTTACAAGAGGGA

Reverse: TCAAAGGTCATCTGGTACCCAG

IL-1β

Forward: AGCGACATGGAGAAGCGATTT

Reverse: TTCTGCTTGAGAGGTGCTGATG

ISG15

Forward: GATCGGTGTGCCTGCCTTC

Reverse: CGTTGCTGCGACCCTTGT

OAS1

Forward: AAGCATCAGAAGCTTTGCATCTT

Reverse: CAGGCCTGGGTTTCTTGAGTT

GAPDH

Forward: ACATGGCCTCCAAGGAGTAAGA

Reverse: GATCGAGTTGGGGCTGTGACT

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宿主线粒体通道蛋白促进干扰素应答抑制口蹄疫病毒复制的分子机制
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蔡镇远 1, 2 , 陈文哲 2 , 杨发誉 2 , 魏衍全 1 , 何继军 2 , 郑海学 2 , 包世俊 1 , 朱紫祥 1, 2
微生物学报 | 研究报告 2025,65(9): 3935-3945
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微生物学报 | 研究报告 2025, 65(9): 3935-3945
宿主线粒体通道蛋白促进干扰素应答抑制口蹄疫病毒复制的分子机制
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蔡镇远1, 2, 陈文哲2, 杨发誉2, 魏衍全1, 何继军2, 郑海学2, 包世俊1 , 朱紫祥1, 2
作者信息
  • 1 甘肃农业大学 动物医学院，甘肃 兰州
  • 2 中国农业科学院兰州兽医研究所/兰州大学 动物医学与生物安全学院，动物疫病防控全国重点实验室，甘肃 兰州
Voltage dependent anion-selective channel 2 promotes interferon response to inhibit foot-and-mouth disease virus replication
Zhenyuan CAI1, 2, Wenzhe CHEN2, Fayu YANG2, Yanquan WEI1, Jijun HE2, Haixue ZHENG2, Shijun BAO1 , Zixiang ZHU1, 2
Affiliations
  • 1 College of Veterinary Medicine, Gansu Agricultural University, Lanzhou, Gansu, China
  • 2 State Key Laboratory for Animal Disease Control and Prevention, College of Veterinary Medicine and Biosafety, Lanzhou University, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Lanzhou, Gansu, China
出版时间: 2025-09-04 doi: 10.13343/j.cnki.wsxb.20250085
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摘要
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口蹄疫(foot-and-mouth disease, FMD)是由口蹄疫病毒(foot-and-mouth disease virus, FMDV)感染偶蹄动物引起的一种烈性动物传染病。FMDV是一种单股正链无囊膜RNA病毒，具有二十面体对称结构。FMDV入侵宿主后会引起宿主的先天性免疫和适应性免疫反应，而FMDV已经进化出多种途径来逃避免疫。FMDV的感染致病机制复杂，目前对于参与调控病毒感染复制的宿主因子的认知仍然非常有限。宿主线粒体通道蛋白(voltage dependent anion-selective channel 2, VDAC2)是一种线粒体通道蛋白，目前关于VDAC2对FMDV复制调控的具体机制尚不清楚。 【目的】 确证VDAC2与FMDV之间的调控作用，并揭示VDAC2抑制FMDV复制的分子机制。 【方法】 通过间接免疫荧光方法确定VDAC2在细胞内的定位；利用Western blotting以及荧光定量PCR方法检测FMDV对VDAC2蛋白水平和转录水平的影响；在BHK-21细胞上利用病毒滴度测定法检测过表达VDAC2对FMDV复制的影响；利用qPCR方法检测上调或下调VDAC2后FMDV感染对细胞内IL-1β、ISG15、OAS1、mtDNA和gDNA水平的影响。 【结果】 结果显示VDAC2亚细胞定位于细胞质中；FMDV感染可以降低VDAC2的表达；过表达VDAC2显著抑制FMDV的复制，并呈现剂量依赖关系；干扰VDAC2能够促进FMDV的复制；过表达VDAC2可增强FMDV诱导的IFN-Ⅰ反应；干扰VDAC2可抑制FMDV诱导的IFN-Ⅰ反应；过表达VDAC2可以促进mtDNA的释放。 【结论】 本研究表明FMDV感染可以下调VDAC2的转录与蛋白表达，而VDAC2可通过调节mtDNA的释放促进IL-1β、ISG15和OAS1等抗病毒因子的表达，从而发挥抗病毒作用。当FMDV入侵宿主细胞时，宿主细胞可以通过VDAC2增强IFN-Ⅰ反应，对病毒复制进行调控，发挥抗病毒作用。

口蹄疫病毒  /  VDAC2蛋白  /  IFN应答

Foot-and-mouth disease (FMD) is a highly contagious disease caused by foot-and-mouth disease virus (FMDV) in cloven-hoofed animals. FMDV is a single-stranded positive-sense non-enveloped RNA virus with icosahedral symmetry. FMDV can cause innate and adaptive immunity of the host, and it has evolved a variety of immune escape ways. The FMDV infection is a complicated process involving various host proteins. However, the related mechanisms remain largely unknown. Voltage dependent anion-selective channel 2 (VDAC2) is a mitochondrial channel protein, and the specific mechanism by which VDAC2 regulates FMDV replication remains unclear. [Objective] To confirm the regulatory effects between VDAC2 and FMDV and reveal the molecular mechanism by which VDAC2 inhibits FMDV replication. [Methods] The subcellular localization of VDAC2 was determined by the indirect immunofluorescence assay. The effects of FMDV on the translation and transcription levels of VDAC2 were determined by Western blotting and qPCR, respectively. The effect of VDAC2 overexpression on FMDV replication in BHK-21 cells was measured based on the virus titer. The effects of VDAC2 overexpression and knockdown on the levels of IL-1β, ISG15, OAS1, mtDNA, and gDNA during FMDV infection were evaluated by qPCR. [Results] VDAC2 was localized in the cytoplasm. FMDV infection down-regulated the expression of VDAC2. The overexpression of VDAC2 inhibited FMDV replication in a dose-dependent manner, while the knockdown of VDAC2 promoted FMDV replication. The overexpression of VDAC2 enhanced FMDV-induced interferon-I (IFN-I) response, while the knockdown of VDAC2 inhibited FMDV-induced IFN-I response. In addition, the overexpression of VDAC2 increased the release of mtDNA. [Conclusion] FMDV infection can downregulate the transcription and translation of VDAC2, as VDAC2 can exert antiviral effects by regulating mtDNA release and promoting the expression of antiviral factors such as IL-1β, ISG15, and OAS1. This study indicates that upon FMDV infection, host cells can regulate the virus replication by enhancing IFN-I response via VDAC2 to exert antiviral effects.

foot-and-mouth disease virus (FMDV)  /  voltage dependent anion-selective channel 2 (VDAC2)  /  interferon (IFN) response
蔡镇远, 陈文哲, 杨发誉, 魏衍全, 何继军, 郑海学, 包世俊, 朱紫祥. 宿主线粒体通道蛋白促进干扰素应答抑制口蹄疫病毒复制的分子机制. 微生物学报, 2025 , 65 (9) : 3935 -3945 . DOI: 10.13343/j.cnki.wsxb.20250085
Zhenyuan CAI, Wenzhe CHEN, Fayu YANG, Yanquan WEI, Jijun HE, Haixue ZHENG, Shijun BAO, Zixiang ZHU. Voltage dependent anion-selective channel 2 promotes interferon response to inhibit foot-and-mouth disease virus replication[J]. Acta Microbiologica Sinica, 2025 , 65 (9) : 3935 -3945 . DOI: 10.13343/j.cnki.wsxb.20250085
正文
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口蹄疫(foot-and-mouth disease, FMD)是由口蹄疫病毒(foot-and-mouth disease virus, FMDV)引起的一种高度传染性偶蹄动物疾病。FMDV感染会引起口腔、鼻腔和足部的水疱病变，并伴随发烧、流涎和跛行等症状[1-2]。口蹄疫的流行会对国家经济和贸易带来严重影响，尽管接种灭活疫苗对口蹄疫的流行起到了一定的控制作用，但疫病流行的风险仍然存在[3]。FMDV是一种单股正链RNA病毒，具有二十面体对称的无包膜结构[4]。由于RNA复制的稳定性较差，基因组突变率较高，FMDV有7种不同的血清型，分别为A、O、C、Asia1、SAT1、SAT2和SAT3，血清型的多样性导致疫苗免疫缺乏交叉保护[5]。FMDV的基因组长度约为8 kb，其中开放阅读框(open reading frame, ORF)包含4种结构蛋白(分别为VP1、VP2、VP3和VP4)以及编码11种非结构蛋白的序列[6]。
线粒体在细胞信号传导、细胞衰老、细胞增殖、疾病和细胞死亡中起着至关重要的作用。电压依赖性阴离子通道(voltage dependent anion-selective channel, VDAC)是线粒体外膜上的一类孔蛋白，在线粒体代谢中发挥着关键作用[7]。据报道，VDACs参与多种病理反应过程，这可能是由于VDACs功能紊乱导致细胞质和线粒体之间的物质代谢障碍以及细胞凋亡调节异常所致[8]。VDACs家族有3种亚型，分别是VDAC1、VDAC2和VDAC3，其中VDAC2存在主要的结构差异，其N端区域比VDAC1和VDAC3延伸了12个氨基酸[9]。VDACs通道的关闭可导致代谢物交换停止。VDACs可以与Bcl-2家族蛋白相互作用，调节细胞凋亡的发生，VDAC2通过与BAK相互作用调控BAK依赖的细胞凋亡，缺失VDAC2可增强BAK寡聚化，促进细胞凋亡；而过表达VDAC2能够抑制BAK激活，进而抑制线粒体凋亡的发生[10]。
VDAC2是一种对FMDV复制具有显著调控作用的线粒体通道蛋白。为探究宿主VDAC2蛋白对FMDV复制的影响及其在FMDV感染期间的功能，本研究利用过表达和RNA干扰等方法，探讨了VDAC2对FMDV诱导的I型干扰素反应的影响，以期为宿主抗FMDV感染机制的阐明提供新的理论依据。
1 材料与方法
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1.1 细胞和病毒
PK-15和BHK-21细胞由中国农业科学院兰州兽医研究所口蹄疫与新发病流行病学实验室提供。细胞在含有5% CO2、37 ℃恒温培养箱内静置培养。口蹄疫O/BY/CHA/2010毒株由中国农业科学院兰州兽医研究所统一保存提供。
1.2 主要试剂和仪器
小鼠抗HA单克隆抗体和鼠抗β-actin单克隆抗体，Sigma-Aldrich公司；山羊抗小鼠IgG的辣根过氧化物酶偶联二抗和山羊抗兔IgG的辣根过氧化物酶偶联二抗，武汉博士德生物工程有限公司；VDAC2、STAT1、p-STAT1和针对cGAS (环状GMP-AMP合酶)的兔源多克隆抗体，ABclonal公司；VDAC2表达质粒，苏州金唯智生物科技有限公司构建；针对FMDV的VP1和3D抗体由本实验室制备；ECL显色剂、Goat anti-Mouse IgG (H+L) Cross-Adsorbed Secondary Antibody和AlexaFluorTm 594，ThermoFisher Scientific公司；EDTA胰酶溶液、DMEM培养基和胎牛血清(fetal bovine serum, FBS)，Gibco公司；PBS溶液，上海碧云天生物技术股份有限公司；蛋白marker，TaKaRa公司；转染试剂JetPRIME，Polyplus-transfection公司；RNA抽提试剂TRIzol，Invitrogen公司；qRT SuperMix反转录试剂和SYBR Mix，南京诺唯赞生物科技股份有限公司；4′,6-二脒基-2-苯基吲哚(4′,6-diamidino-2-phenylindole, DAPI)荧光染料，Beyotime公司。
激光共聚焦显微镜，Leica公司。
1.3 细胞转染
细胞转染使用JetPRIME转染试剂，在实验之前将消化混匀后的细胞加入所需的孔板内，并在5% CO2、37 ℃恒温培养箱内静置培养。待细胞密度达到70%-80%时进行转染，取1.5 mL无RNase离心管，加入转染缓冲液，按说明书比例先后加入各组分，用移液枪吹吸混匀后静置10 min。将细胞孔板从培养箱中取出，在生物安全柜内使用真空泵吸去培养基，加入新的培养基，然后将质粒和转染试剂的混合物缓慢加入培养基中，水平前后缓慢摇晃孔板，使转染试剂均匀分布后，再将其放回5% CO2、37 ℃恒温培养箱中继续培养。转染12 h后，弃去旧培养基，加入新的完全培养基，继续培养12 h后收取细胞样品并进行相应处理。
1.4 siRNA干扰实验
VDAC2的特异性siRNA序列由北京擎科生物科技股份有限公司合成(表1)。将消化好的PK-15细胞均匀铺于12孔板内，待细胞密度达到70%-80%时，将VDAC2特异性siRNA转染到PK-15细胞中，干扰48 h后按照病毒感染复数(multiplicity of infection, MOI)=0.1感染FMDV，12 h后弃去上清，收集细胞，对VDAC2和FMDV mRNA的表达水平差异进行分析。
1.5 蛋白免疫印记试验(Western blotting)
收集细胞样品，金属浴100 ℃加热12 min进行蛋白变性，随后12 000 r/min离心5 min。将样品和蛋白marker分别加入蛋白胶梳孔中，调节电压为80 V，运行30 min。待SDS loading buffer形成整齐的线性且离开上层胶后，将电压调整至120 V，继续运行以分离蛋白，直至目的条带清晰分离为止。在100 V恒压下，于冰水混合物中进行1 h的转膜操作。室温下封闭1 h，用TBST洗涤3次。一抗(1:2 000稀释)在4 ℃、50 r/min孵育过夜，随后用TBST洗涤3次。二抗(1:5 000稀释)在室温下50 r/min孵育1 h，之后用TBST洗涤3次，最后用ECL化学发光显色液进行显色。
1.6 间接免疫荧光(indirect fluorescence assay, IFA)
将0.01% (100 μg/mL)的多聚赖氨酸溶液加入共聚焦小皿中，在5% CO2、37 ℃培养箱中包被30 min。铺PK-15细胞，待细胞生长至60%-80%时进行转染，随后置于培养箱中继续培养24 h后处理样品。弃去培养基，用PBS清洗；使用提前冷却备用的4%多聚甲醛固定 30 min，再用PBS清洗；在室温条件下用0.2% Triton X-100通透15 min，随后用PBS清洗；用5% BSA在室温下封闭1 h，再用PBS清洗 1次；加入一抗(用5% BSA稀释)，在4 ℃孵育过夜；用PBST洗涤3次，加入荧光二抗(用5% BSA稀释)，在避光条件下孵育1 h，随后用PBST洗涤3次；用DAPI在避光条件下染色10 min，最后用PBS清洗。在避光条件下，使用激光共聚焦显微镜进行观察并拍照。
1.7 实时荧光定量PCR (qPCR)
采用TRIzol法提取PK-15细胞总RNA。弃去细胞孔板内的培养液，用PBS漂洗后在通风橱内加入500 μL TRIzol (12孔板/孔)，室温裂解5 min。反复吹打以促使细胞脱落，将裂解液转移至RNase-free离心管，室温静置5 min。按体积比5:1加入氯仿(100 μL)，涡旋振荡至溶液呈均质粉红色，4 ℃静置5 min。在4 ℃、12 000 r/min离心15 min，分离水相与有机相。吸取200 μL上层水相至新的离心管，加入等体积异丙醇，轻柔混匀后置于-40 ℃静置30 min。在4 ℃、12 000 r/min离心15 min，收集RNA沉淀，弃上清，加入1 mL预冷75%乙醇洗涤沉淀，在4 ℃、12 000 r/min离心5 min。彻底吸弃乙醇，室温干燥沉淀至半透明状。加入20 μL DEPC水溶解RNA，冰上暂存，测定浓度后置于-80 ℃冻存。使用qRT SuperMix反转录试剂对提取的细胞总RNA进行反转录为cDNA。反应体系(10 μL)：RNA 2 μL，RNase-free ddH2O 6 μL，5×PrimerScript RT Master Mix 2 μL。反应条件：50 ℃ 15 min，85 ℃ 10 s，4 ℃保存。
使用SYBR Green Master Mix进行qPCR。反应体系：上、下游引物(10 μmol/L)各0.5 μL，SYBR Premix 5 μL，cDNA 1 μL，DEPC水 3 μL。反应条件：95 ℃ 5 min；95 ℃ 10 s，60 ℃ 30 s，进行40个循环；60 ℃ 1 min，95 ℃ 15 s，4 ℃保存。目的基因相对表达量使用2⁻ΔΔCt公式进行计算。本研究所用引物如表2所示。
1.8 病毒滴度测定(TCID50)
将BHK-21细胞铺于96孔板中，用含1%血清的DMEM培养基对FMDV上清进行梯度稀释。感染72 h后，在显微镜下观察每列细胞中产生细胞病变效应(cytopathic effect, CPE)的细胞孔数量，计算TCID50值。进行3次生物学重复观察测量，最后取其平均值作为最终的病毒效价。
1.9 IP-cGAS检测mtDNA
将PK-15细胞铺于6孔板中，空白对照组和实验组分别以MOI=0.1接毒8-10 h后，用PBS洗1次。每孔加入300 μL含蛋白酶抑制剂的裂解液，冰上裂解15 min，随后以12 000 r/min离心15 min。在1.5 mL离心管中加入10 μL protein G，用lysis buffer洗涤2次，8 000 r/min离心30 s。将上清液加入离心管中，每管加入0.4 μL cGAS抗体。在4 ℃旋转混匀仪上孵育4-6 h，用lysis buffer洗涤2次，加入50 μL DEPC水，37 ℃静置10-30 min。每管加入50-100 ng EGFP质粒，用枪尖研磨底部beads，提取上清液保存或进行qPCR实验。检测mtDNA、gDNA (GAPDH)和EGFP引物。其中，EGFP作为内参，gDNA (GAPDH)表示总DNA含量，mtDNA表示释放的线粒体DNA量。在gDNA含量一致的情况下，比较mtDNA的变化。
1.10 统计学分析
统计分析结果均以mean±SD表示，每组实验至少进行3次生物学重复。使用GraphPad Prism 8.0进行t检验分析，对数据均值之间的统计差异进行分析，其中：*表示P<0.05；**表示P<0.01；***表示P<0.001；****表示P<0.000 1。
2 结果与分析
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2.1 VDAC2的定位
为了验证VDAC2的亚细胞定位，将pcDNA-HA-VDAC2真核表达质粒转染至生长密度为70%-80%的BHK-21细胞中，转染24 h后进行观察。结果如图1所示，红色为HA-VDAC2，蓝色为细胞核，VDAC2主要定位于细胞质中。
2.2 FMDV感染调控VDAC2的表达
为了研究FMDV感染对VDAC2表达的影响，设计了0、2、4、8、12 h的时间点。当待PK-15细胞生长至单层时，以MOI=0.1进行感染，分别在5个细胞孔中进行Western blotting和12 h时间点的qPCR实验。结果显示，FMDV感染会导致VDAC2的蛋白表达水平和转录水平呈下降趋势(图2A、2B)。这表明FMDV感染可以降低VDAC2的表达水平。
2.3 过表达VDAC2抑制FMDV的复制
为了验证过表达VDAC2对FMDV复制的影响，将PK-15细胞转染不同剂量的VDAC2表达质粒(0、250、500 ng)，转染24 h后以MOI=0.1感染FMDV，12 h后分别收集细胞和上清进行实验。结果表明，随着VDAC2表达量的增加，FMDV的蛋白水平和mRNA水平显著降低(图3A、3B)。对收集的上清进行滴度测定，TCID50结果显示过表达VDAC2能抑制FMDV的复制，并呈现剂量依赖关系(图3C)。
2.4 干扰VDAC2促进FMDV的复制
对合成的2对猪源VDAC2特异性siRNA进行mRNA水平的筛选，选择干扰效率较高的siRNA进行后续实验。PK-15细胞转染VDAC2的siRNA和空白对照48 h后，以MOI=0.1感染FMDV 12 h，收集细胞样品进行检测。结果显示，si-VDAC2-2的干扰效率较高(图4A)。VDAC2 siRNA的转染导致FMDV VP1蛋白水平和mRNA水平升高(图4B、4C)，同时VDAC2的表达量降低(图4D)，表明干扰VDAC2能够促进FMDV的复制。
2.5 过表达VDAC2促进FMDV诱导的IFN-I反应
为探究过表达VDAC2抑制FMDV复制的分子机制，将VDAC2质粒转染至PK-15细胞24 h后，以MOI=0.1感染12 h。通过qPCR实验检测IL-1β、ISG15和OAS1的mRNA水平。结果显示，IL-1β、ISG15和OAS1的mRNA水平显著提高(图5)。这表明过表达VDAC2可以增强FMDV诱导的IFN-I反应。
2.6 干扰VDAC2抑制FMDV诱导的IFN-I反应
为探究干扰VDAC2促进FMDV复制的分子机制，设置实验组和对照组，在PK-15细胞中分别转染siRNA和空白对照siRNA 24 h后，以MOI=0.1感染12 h，检测mRNA水平。通过qPCR实验检测IL-1β、ISG15和OAS1的mRNA水平。结果显示，IL-1β、ISG15和OAS1的mRNA水平显著降低(图6)。这表明干扰VDAC2可以抑制FMDV诱导的IFN-I反应。
2.7 过表达VDAC2对mtDNA和gDNA的影响
线粒体损伤或功能障碍会导致mtDNA释放到细胞质中，并被cGAS识别。本研究中通过IP-cGAS对过表达样品进行处理，以EGFP为内参，检测了过表达VDAC2后FMDV对mtDNA释放的影响。结果显示，FMDV感染过表达VDAC2的细胞后，显著促进了mtDNA的释放，但不影响基因组DNA (gDNA)的释放(图7A、7B)。这一结果与过表达VDAC2能够增强FMDV诱导的IFN-I反应相呼应。
2.8 过表达VDAC2后对STAT1磷酸化蛋白水平的检测
通过Western blotting技术检测了过表达VDAC2后FMDV感染细胞中STAT1及其磷酸化形式(p-STAT1)的表达水平。实验结果表明，VDAC2的过表达显著增强了STAT1的磷酸化水平(p-STAT1)，提示其可能通过激活JAK-STAT信号通路的关键节点促进宿主的抗病毒反应，功能实验证实VDAC2介导的STAT1磷酸化增强能够有效抑制FMDV在细胞内的复制(图8)。
3 讨论
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口蹄疫是一种极具传染性的动物传染病，其流行对养殖业造成了严重的危害，并导致了巨大的经济损失。口蹄疫病毒具有高度变异性，这使得疫情反复发生，给动物养殖、贸易出口以及疫病防控带来了极为严峻的挑战。FMDV能够快速突破宿主的天然免疫系统，并借助宿主细胞内的机制进行快速复制，其发病机制极为复杂。病毒与宿主免疫系统之间复杂的作用关系决定了病毒能否被宿主细胞清除。宿主主要通过先天性免疫和适应性免疫来对抗病毒感染，其中I型干扰素的作用以及中和抗体的产生发挥着极为重要的作用[11-12]。如果宿主无法及时清除病毒，病毒就可能在机体内形成持续性感染。在一定条件下，病毒可能再次排毒，从而引发新的疫情。为了对抗宿主的抗病毒应答，FMDV可以通过多种途径进行免疫逃避。因此深入了解宿主与病毒之间的相互作用机制对于口蹄疫的防控具有重要的指导意义。
VDAC2作为线粒体的通道蛋白，广泛分布于真核生物线粒体外膜。当细胞处于应激状态时，线粒体外膜的通透性会发生改变，最终导致细胞凋亡的发生，在细胞命运的决定中起着关键作用。当病毒入侵时，已有研究发现VDAC2可以通过多种途径增强病毒感染。这些途径包括介导病毒进入宿主细胞、为病毒提供能量供应、增强病毒复制、通过结合或激活其他类型的蛋白质减少细胞凋亡，以及有助于抑制抗病毒免疫信号的有丝分裂诱导[13-14]。已有报道VDAC2在细胞自噬中发挥重要作用，当VDAC2基因缺失时细胞自噬更容易发生。然而，VDAC2在病毒与宿主相互作用中的具体机制尚未完全明确。在VDACs家族中，关于VDAC2的研究报道相对较少。已有研究报道过表达VDAC2抑制牛流行热病毒(bovine ephemeral fever virus, BEFV)诱导的I型干扰素的表达，而干扰VDAC2则促进BEFV诱导的I型干扰素的表达，表明VDAC2抑制BEFV诱导的I型干扰素反应。在传染性法氏囊病病毒(infectious bursal disease virus, IBDV)的感染过程中，受体激活的蛋白C激酶1 (receptor of activated protein C kinase 1, RACK1)与VDAC2和IBDV的非结构蛋白VP5相互作用形成复合物，抑制细胞凋亡，促进IBDV病毒的复制。在VDAC的3种亚型中，宿主蛋白VDAC1与FMDV的3Dpol蛋白发生互作，进而抑制3Dpol蛋白的表达，对口蹄疫病毒的复制具有抑制作用。目前关于VDAC2与FMDV之间关系的研究尚未见报道。然而，已有研究表明VDAC2在病毒的免疫逃避中可能起到一定作用。
已有文献报道，FMDV感染可以在细胞内引发mtDNA的释放。释放的mtDNA能够与cGAS结合，并激活cGAS介导的抗病毒免疫应答[15]。本研究通过在PK-15细胞中过表达VDAC2后进行病毒感染实验，发现VDAC2可以通过诱导大量mtDNA的释放，从而启动免疫系统对抗病毒感染。STAT1的磷酸化是JAK-STAT信号通路的核心调控因子，其通过级联反应将胞外信号(如干扰素、细胞因子)传递至细胞核内，激活抗病毒及免疫调控基因的表达。本研究通过检测过表达VDAC2后FMDV感染细胞的STAT1磷酸化水平，发现VDAC2介导的STAT1磷酸化增强能够有效抑制FMDV在细胞内的复制。这些发现揭示了VDAC2在FMDV感染过程中可能的调控机制。
4 结论
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本研究结果显示，在PK-15细胞中FMDV感染可以显著调控内源VDAC2的表达。这一结果表明VDAC2与FMDV之间存在必然的联系，并且VDAC2在FMDV感染后发挥着重要的抗病毒作用。本研究的发现为进一步理解VDAC2在FMDV感染中的作用机制提供了新的视角。通过深入研究VDAC2与FMDV之间的相互作用，有望为开发新的口蹄疫防控策略提供理论依据。未来的研究可以进一步探索如何通过调节VDAC2的功能来增强宿主的抗病毒能力。此外，还可以研究VDAC2与其他免疫相关分子之间的协同作用，为口蹄疫的防控提供更全面的解决方案。总之，本研究为揭示VDAC2在FMDV感染中的作用奠定了基础。
基金
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  • 国家生猪创新中心先导科技项目(NCTIP-XD/C03)
  • 国家生猪产业技术体系(CARS-35)
  • “十四五”广东省农业科技创新十大主攻方向“揭榜挂帅”项目(2022SDZG02)
文献
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参考文献 引证文献
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2025年第65卷第9期
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文章信息
doi: 10.13343/j.cnki.wsxb.20250085
  • 接收时间：2025-02-07
  • 首发时间：2026-02-07
  • 出版时间：2025-09-04
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出版历史
  • 收稿日期：2025-02-07
  • 录用日期：2025-05-04
基金
National Swine Innovation Center Pioneer Science and Technology Project(NCTIP-XD/C03)
国家生猪创新中心先导科技项目(NCTIP-XD/C03)
Pig Industry System(CARS-35)
国家生猪产业技术体系(CARS-35)
“14th Five-year Plan” Guangdong Province Agricultural Science and Technology Innovation Ten Major Directions “Listed and Commanded” Project(2022SDZG02)
“十四五”广东省农业科技创新十大主攻方向“揭榜挂帅”项目(2022SDZG02)
作者信息
    1 甘肃农业大学 动物医学院，甘肃 兰州
    2 中国农业科学院兰州兽医研究所/兰州大学 动物医学与生物安全学院，动物疫病防控全国重点实验室，甘肃 兰州
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https://castjournals.cast.org.cn/joweb/wswxb/CN/10.13343/j.cnki.wsxb.20250085
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Number of
species		 占总种数比例
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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