Hepatitis B Virus Utilizes a Retrograde Trafficking Route via the Trans-Golgi Network to Avoid Lysosomal Degradation.


Journal

Cellular and molecular gastroenterology and hepatology
ISSN: 2352-345X
Titre abrégé: Cell Mol Gastroenterol Hepatol
Pays: United States
ID NLM: 101648302

Informations de publication

Date de publication:
2023
Historique:
received: 24 12 2021
revised: 11 10 2022
accepted: 12 10 2022
pubmed: 22 10 2022
medline: 25 2 2023
entrez: 21 10 2022
Statut: ppublish

Résumé

Hepatitis B virus (HBV) infection is difficult to cure owing to the persistence of covalently closed circular viral DNA (cccDNA). We performed single-cell transcriptome analysis of newly established HBV-positive and HBV-negative hepatocellular carcinoma cell lines and found that dedicator of cytokinesis 11 (DOCK11) was crucially involved in HBV persistence. However, the roles of DOCK11 in the HBV lifecycle have not been clarified. The cccDNA levels were measured by Southern blotting and real-time detection polymerase chain reaction in various hepatocytes including PXB cells by using an HBV-infected model. The retrograde trafficking route of HBV capsid was investigated by super-resolution microscopy, proximity ligation assay, and time-lapse analysis. The downstream molecules of DOCK11 and underlying mechanism were examined by liquid chromatography-tandem mass spectrometry, immunoblotting, and enzyme-linked immunosorbent assay. The cccDNA levels were strongly increased by DOCK11 overexpression and repressed by DOCK11 suppression. Interestingly, DOCK11 functionally associated with retrograde trafficking proteins in the trans-Golgi network (TGN), Arf-GAP with GTPase domain, ankyrin repeat, and pleckstrin homology domain-containing protein 2 (AGAP2), and ADP-ribosylation factor 1 (ARF1), together with HBV capsid, to open an alternative retrograde trafficking route for HBV from early endosomes (EEs) to the TGN and then to the endoplasmic reticulum (ER), thereby avoiding lysosomal degradation. Clinically, DOCK11 levels in liver biopsies from patients with chronic hepatitis B were significantly reduced by entecavir treatment, and this reduction correlated with HBV surface antigen levels. HBV uses a retrograde trafficking route via EEs-TGN-ER for infection that is facilitated by DOCK11 and serves to maintain cccDNA. Therefore, DOCK11 is a potential therapeutic target to prevent persistent HBV infection.

Sections du résumé

BACKGROUND & AIMS
Hepatitis B virus (HBV) infection is difficult to cure owing to the persistence of covalently closed circular viral DNA (cccDNA). We performed single-cell transcriptome analysis of newly established HBV-positive and HBV-negative hepatocellular carcinoma cell lines and found that dedicator of cytokinesis 11 (DOCK11) was crucially involved in HBV persistence. However, the roles of DOCK11 in the HBV lifecycle have not been clarified.
METHODS
The cccDNA levels were measured by Southern blotting and real-time detection polymerase chain reaction in various hepatocytes including PXB cells by using an HBV-infected model. The retrograde trafficking route of HBV capsid was investigated by super-resolution microscopy, proximity ligation assay, and time-lapse analysis. The downstream molecules of DOCK11 and underlying mechanism were examined by liquid chromatography-tandem mass spectrometry, immunoblotting, and enzyme-linked immunosorbent assay.
RESULTS
The cccDNA levels were strongly increased by DOCK11 overexpression and repressed by DOCK11 suppression. Interestingly, DOCK11 functionally associated with retrograde trafficking proteins in the trans-Golgi network (TGN), Arf-GAP with GTPase domain, ankyrin repeat, and pleckstrin homology domain-containing protein 2 (AGAP2), and ADP-ribosylation factor 1 (ARF1), together with HBV capsid, to open an alternative retrograde trafficking route for HBV from early endosomes (EEs) to the TGN and then to the endoplasmic reticulum (ER), thereby avoiding lysosomal degradation. Clinically, DOCK11 levels in liver biopsies from patients with chronic hepatitis B were significantly reduced by entecavir treatment, and this reduction correlated with HBV surface antigen levels.
CONCLUSIONS
HBV uses a retrograde trafficking route via EEs-TGN-ER for infection that is facilitated by DOCK11 and serves to maintain cccDNA. Therefore, DOCK11 is a potential therapeutic target to prevent persistent HBV infection.

Identifiants

pubmed: 36270602
pii: S2352-345X(22)00219-3
doi: 10.1016/j.jcmgh.2022.10.008
pmc: PMC9868690
pii:
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

533-558

Commentaires et corrections

Type : CommentIn

Informations de copyright

Copyright © 2023 The Authors. Published by Elsevier Inc. All rights reserved.

Auteurs

Ying-Yi Li (YY)

Department of Gastroenterology, Kanazawa University Graduate School of Medicine, Kanazawa, Japan.

Kazuyuki Kuroki (K)

Department of Gastroenterology, Kanazawa University Graduate School of Medicine, Kanazawa, Japan.

Tetsuro Shimakami (T)

Department of Gastroenterology, Kanazawa University Graduate School of Medicine, Kanazawa, Japan.

Kazuhisa Murai (K)

Department of Clinical Laboratory Medicine, Kanazawa University Graduate School of Health Medicine, Kanazawa, Japan.

Kazunori Kawaguchi (K)

Department of Gastroenterology, Kanazawa University Graduate School of Medicine, Kanazawa, Japan.

Takayoshi Shirasaki (T)

Department of Clinical Laboratory Medicine, Kanazawa University Graduate School of Health Medicine, Kanazawa, Japan.

Kouki Nio (K)

Department of Gastroenterology, Kanazawa University Graduate School of Medicine, Kanazawa, Japan.

Saiho Sugimoto (S)

Department of Gastroenterology, Kanazawa University Graduate School of Medicine, Kanazawa, Japan.

Tomoki Nishikawa (T)

Department of Gastroenterology, Kanazawa University Graduate School of Medicine, Kanazawa, Japan.

Hikari Okada (H)

Department of Gastroenterology, Kanazawa University Graduate School of Medicine, Kanazawa, Japan.

Noriaki Orita (N)

Department of Gastroenterology, Kanazawa University Graduate School of Medicine, Kanazawa, Japan.

Hideo Takayama (H)

Department of Gastroenterology, Kanazawa University Graduate School of Medicine, Kanazawa, Japan.

Ying Wang (Y)

Department of Clinical Laboratory Medicine, Kanazawa University Graduate School of Health Medicine, Kanazawa, Japan.

Phuong Doan Thi Bich (PD)

Department of Gastroenterology, Kanazawa University Graduate School of Medicine, Kanazawa, Japan.

Astuya Ishida (A)

Department of Gastroenterology, Kanazawa University Graduate School of Medicine, Kanazawa, Japan.

Sadahiro Iwabuchi (S)

Department of Molecular Pathophysiology, Institute of Advanced Medicine, Wakayama Medical University, Wakayama, Japan.

Shinichi Hashimoto (S)

Department of Molecular Pathophysiology, Institute of Advanced Medicine, Wakayama Medical University, Wakayama, Japan.

Takeshi Shimaoka (T)

Division of Molecular Regulation of Inflammatory and Immune Diseases, Research Institute for Biomedical Sciences, Tokyo University of Science, Chiba, Japan.

Noriko Tabata (N)

Purotech Bio Inc, Kanagawa, Japan.

Miho Watanabe-Takahashi (M)

Department of Molecular Life Sciences, Doshisha University, Kyoto, Japan.

Kiyotaka Nishikawa (K)

Department of Molecular Life Sciences, Doshisha University, Kyoto, Japan.

Hiroshi Yanagawa (H)

Purotech Bio Inc, Kanagawa, Japan.

Motoharu Seiki (M)

Department of Gastroenterology, Kanazawa University Graduate School of Medicine, Kanazawa, Japan.

Kouji Matsushima (K)

Division of Molecular Regulation of Inflammatory and Immune Diseases, Research Institute for Biomedical Sciences, Tokyo University of Science, Chiba, Japan.

Taro Yamashita (T)

Department of Gastroenterology, Kanazawa University Graduate School of Medicine, Kanazawa, Japan.

Shuichi Kaneko (S)

Department of Gastroenterology, Kanazawa University Graduate School of Medicine, Kanazawa, Japan.

Masao Honda (M)

Department of Gastroenterology, Kanazawa University Graduate School of Medicine, Kanazawa, Japan; Department of Clinical Laboratory Medicine, Kanazawa University Graduate School of Health Medicine, Kanazawa, Japan. Electronic address: mhonda@m-kanazawa.jp.

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