Hepatitis B surface antigen hijacks TANK-binding kinase 1 to suppress type I interferon and induce early autophagy

Abstract There are close links between innate immunity and autophagy. However, the crosstalk between innate immunity and autophagy in host cells infected with hepatitis B virus (HBV) remains unclear. Here, we reported that HBsAg suppressed type I interferon production and induced the accumulation of...

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Main Authors: Chuanjin Luo, Caijiao Ma, Gang Xu, Chengbo Lu, June Ma, Yu Huang, Longyu Nie, Chen Yu, Yongfang Xia, Zhiqiang Liu, Ying Zhu, Shi Liu
Format: Article
Language:English
Published: Nature Publishing Group 2025-04-01
Series:Cell Death and Disease
Online Access:https://doi.org/10.1038/s41419-025-07605-0
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author Chuanjin Luo
Caijiao Ma
Gang Xu
Chengbo Lu
June Ma
Yu Huang
Longyu Nie
Chen Yu
Yongfang Xia
Zhiqiang Liu
Ying Zhu
Shi Liu
author_facet Chuanjin Luo
Caijiao Ma
Gang Xu
Chengbo Lu
June Ma
Yu Huang
Longyu Nie
Chen Yu
Yongfang Xia
Zhiqiang Liu
Ying Zhu
Shi Liu
author_sort Chuanjin Luo
collection DOAJ
description Abstract There are close links between innate immunity and autophagy. However, the crosstalk between innate immunity and autophagy in host cells infected with hepatitis B virus (HBV) remains unclear. Here, we reported that HBsAg suppressed type I interferon production and induced the accumulation of autophagosomes. HBsAg boosted TANK-binding kinase 1 (TBK1) phosphorylation and depressed interferon regulatory factor 3 (IRF3) phosphorylation ex vivo and in vivo. Mechanistic studies showed that HBsAg interaction with the kinase domain (KD) of TBK1 augmented its dimerization but disrupted TBK1–IRF3 complexes. Using the TBK1 inhibitor, BX795, we discovered that HBsAg-enhanced TBK1 dimerization, promoting sequestosome-1 (p62) phosphorylation, was necessary for HBV-induced autophagy and HBV replication. Moreover, HBsAg blocked autophagosome–lysosome fusion by inhibiting the synaptosomal-associated protein 29 (SNAP29) promoter. Notably, liver tissues from HBsAg transgenic mice or chronic HBV patients revealed that IFNβ signaling was inhibited and incomplete autophagy was induced. These findings suggest a novel mechanism by which HBsAg targets TBK1 to inhibit type I interferon and induce early autophagy, possibly leading to persistent HBV infection. Molecular mechanisms of HBsAg suppression of the IFNβ signaling pathway and triggering of early autophagy. HBsAg targets the kinase domain of TBK1, thereby disrupting the TBK1–IRF3 complex and inhibiting type I interferon production. On the other hand, HBsAg enhances TBK1 dimerization and phosphorylation, which upregulates the phosphorylation of p62 to induce p62-mediated autophagy. Furthermore, HBV infection causes the accumulation of autophagosomes. This is achieved by HBsAg suppressing the SNAP29 promoter activity, which blocks autophagosome–lysosome fusion.
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spelling doaj-art-9ff3a310b0924e7abeefcca9e417d4842025-08-20T02:17:49ZengNature Publishing GroupCell Death and Disease2041-48892025-04-0116111610.1038/s41419-025-07605-0Hepatitis B surface antigen hijacks TANK-binding kinase 1 to suppress type I interferon and induce early autophagyChuanjin Luo0Caijiao Ma1Gang Xu2Chengbo Lu3June Ma4Yu Huang5Longyu Nie6Chen Yu7Yongfang Xia8Zhiqiang Liu9Ying Zhu10Shi Liu11State Key Laboratory of Virology, Modern Virology Research Center, College of Life Sciences, Wuhan UniversityState Key Laboratory of Virology, Modern Virology Research Center, College of Life Sciences, Wuhan UniversityState Key Laboratory of Virology, Modern Virology Research Center, College of Life Sciences, Wuhan UniversityState Key Laboratory of Virology, Modern Virology Research Center, College of Life Sciences, Wuhan UniversityDepartment of Clinical Laboratory, Maternal and Child Health Hospital of Hubei Province, Tongji Medical College, Huazhong University of Science and TechnologyState Key Laboratory of Virology, Modern Virology Research Center, College of Life Sciences, Wuhan UniversityState Key Laboratory of Virology, Modern Virology Research Center, College of Life Sciences, Wuhan UniversityState Key Laboratory of Virology, Modern Virology Research Center, College of Life Sciences, Wuhan UniversityState Key Laboratory of Virology, Modern Virology Research Center, College of Life Sciences, Wuhan UniversityState Key Laboratory of Virology, Modern Virology Research Center, College of Life Sciences, Wuhan UniversityState Key Laboratory of Virology, Modern Virology Research Center, College of Life Sciences, Wuhan UniversityState Key Laboratory of Virology, Modern Virology Research Center, College of Life Sciences, Wuhan UniversityAbstract There are close links between innate immunity and autophagy. However, the crosstalk between innate immunity and autophagy in host cells infected with hepatitis B virus (HBV) remains unclear. Here, we reported that HBsAg suppressed type I interferon production and induced the accumulation of autophagosomes. HBsAg boosted TANK-binding kinase 1 (TBK1) phosphorylation and depressed interferon regulatory factor 3 (IRF3) phosphorylation ex vivo and in vivo. Mechanistic studies showed that HBsAg interaction with the kinase domain (KD) of TBK1 augmented its dimerization but disrupted TBK1–IRF3 complexes. Using the TBK1 inhibitor, BX795, we discovered that HBsAg-enhanced TBK1 dimerization, promoting sequestosome-1 (p62) phosphorylation, was necessary for HBV-induced autophagy and HBV replication. Moreover, HBsAg blocked autophagosome–lysosome fusion by inhibiting the synaptosomal-associated protein 29 (SNAP29) promoter. Notably, liver tissues from HBsAg transgenic mice or chronic HBV patients revealed that IFNβ signaling was inhibited and incomplete autophagy was induced. These findings suggest a novel mechanism by which HBsAg targets TBK1 to inhibit type I interferon and induce early autophagy, possibly leading to persistent HBV infection. Molecular mechanisms of HBsAg suppression of the IFNβ signaling pathway and triggering of early autophagy. HBsAg targets the kinase domain of TBK1, thereby disrupting the TBK1–IRF3 complex and inhibiting type I interferon production. On the other hand, HBsAg enhances TBK1 dimerization and phosphorylation, which upregulates the phosphorylation of p62 to induce p62-mediated autophagy. Furthermore, HBV infection causes the accumulation of autophagosomes. This is achieved by HBsAg suppressing the SNAP29 promoter activity, which blocks autophagosome–lysosome fusion.https://doi.org/10.1038/s41419-025-07605-0
spellingShingle Chuanjin Luo
Caijiao Ma
Gang Xu
Chengbo Lu
June Ma
Yu Huang
Longyu Nie
Chen Yu
Yongfang Xia
Zhiqiang Liu
Ying Zhu
Shi Liu
Hepatitis B surface antigen hijacks TANK-binding kinase 1 to suppress type I interferon and induce early autophagy
Cell Death and Disease
title Hepatitis B surface antigen hijacks TANK-binding kinase 1 to suppress type I interferon and induce early autophagy
title_full Hepatitis B surface antigen hijacks TANK-binding kinase 1 to suppress type I interferon and induce early autophagy
title_fullStr Hepatitis B surface antigen hijacks TANK-binding kinase 1 to suppress type I interferon and induce early autophagy
title_full_unstemmed Hepatitis B surface antigen hijacks TANK-binding kinase 1 to suppress type I interferon and induce early autophagy
title_short Hepatitis B surface antigen hijacks TANK-binding kinase 1 to suppress type I interferon and induce early autophagy
title_sort hepatitis b surface antigen hijacks tank binding kinase 1 to suppress type i interferon and induce early autophagy
url https://doi.org/10.1038/s41419-025-07605-0
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