Integrin beta 1 facilitates non-enveloped hepatitis E virus cell entry through the recycling endosome

Abstract Hepatitis E virus (HEV) is a major cause of acute hepatitis and mainly transmitted faecal-orally. HEV particles present in faeces are naked (nHEV), whereas those found in the blood are quasi-enveloped (eHEV) with a cell-derived lipid membrane. Despite its global health impact, the cellular...

Full description

Saved in:
Bibliographic Details
Main Authors: Rebecca Fu, Paula Jordan, Zoe Engels, Jasmin Alara Weihs, Josias Mürle, Huanting Chi, Sebastian Burbano de Lara, Barbara Helm, Mara Klöhn, Jungen Hu, Andrew Freistaedter, Tobias Boettler, Marco Binder, Ursula Klingmüller, Eike Steinmann, Pierre-Yves Lozach, Thibault Tubiana, Stanley M. Lemon, Viet Loan Dao Thi
Format: Article
Language:English
Published: Nature Portfolio 2025-06-01
Series:Nature Communications
Online Access:https://doi.org/10.1038/s41467-025-61071-y
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1849432634559561728
author Rebecca Fu
Paula Jordan
Zoe Engels
Jasmin Alara Weihs
Josias Mürle
Huanting Chi
Sebastian Burbano de Lara
Barbara Helm
Mara Klöhn
Jungen Hu
Andrew Freistaedter
Tobias Boettler
Marco Binder
Ursula Klingmüller
Eike Steinmann
Pierre-Yves Lozach
Thibault Tubiana
Stanley M. Lemon
Viet Loan Dao Thi
author_facet Rebecca Fu
Paula Jordan
Zoe Engels
Jasmin Alara Weihs
Josias Mürle
Huanting Chi
Sebastian Burbano de Lara
Barbara Helm
Mara Klöhn
Jungen Hu
Andrew Freistaedter
Tobias Boettler
Marco Binder
Ursula Klingmüller
Eike Steinmann
Pierre-Yves Lozach
Thibault Tubiana
Stanley M. Lemon
Viet Loan Dao Thi
author_sort Rebecca Fu
collection DOAJ
description Abstract Hepatitis E virus (HEV) is a major cause of acute hepatitis and mainly transmitted faecal-orally. HEV particles present in faeces are naked (nHEV), whereas those found in the blood are quasi-enveloped (eHEV) with a cell-derived lipid membrane. Despite its global health impact, the cellular life cycle of HEV remains poorly understood, particularly regarding the mechanisms of viral entry into host cells. To address this knowledge gap, we develop a high content RNA-FISH-based imaging assay that allows for the investigation of the entry pathways of both naked and quasi-enveloped HEV particles. Surprisingly, we find that integrin α3, previously implicated in nHEV cell entry, is not expressed in the cell types that are most permissive for HEV infection. Instead, we identify integrin β1 (ITGB1) pairing with different α-integrins as the key player mediating nHEV cell entry. Our results indicate that the interaction of nHEV with ITGB1 facilitates entry through Rab11-positive recycling endosomes. In contrast, eHEV particles do not interact with ITGB1 and enter cells using a classical endocytic route via Rab5a-positive early endosomes. The entry of both types of HEV particles requires endosomal acidification and proteolytic cleavage by lysosomal cathepsins, which ultimately results in delivery of the HEV genome to the cytoplasm.
format Article
id doaj-art-48a92abeba284c918d151f88840a87c2
institution Kabale University
issn 2041-1723
language English
publishDate 2025-06-01
publisher Nature Portfolio
record_format Article
series Nature Communications
spelling doaj-art-48a92abeba284c918d151f88840a87c22025-08-20T03:27:18ZengNature PortfolioNature Communications2041-17232025-06-0116111810.1038/s41467-025-61071-yIntegrin beta 1 facilitates non-enveloped hepatitis E virus cell entry through the recycling endosomeRebecca Fu0Paula Jordan1Zoe Engels2Jasmin Alara Weihs3Josias Mürle4Huanting Chi5Sebastian Burbano de Lara6Barbara Helm7Mara Klöhn8Jungen Hu9Andrew Freistaedter10Tobias Boettler11Marco Binder12Ursula Klingmüller13Eike Steinmann14Pierre-Yves Lozach15Thibault Tubiana16Stanley M. Lemon17Viet Loan Dao Thi18Schaller Research Group, Department of Infectious Diseases, Virology, Heidelberg University, Medical Faculty HeidelbergSchaller Research Group, Department of Infectious Diseases, Virology, Heidelberg University, Medical Faculty HeidelbergSchaller Research Group, Department of Infectious Diseases, Virology, Heidelberg University, Medical Faculty HeidelbergSchaller Research Group, Department of Infectious Diseases, Virology, Heidelberg University, Medical Faculty HeidelbergSchaller Research Group, Department of Infectious Diseases, Virology, Heidelberg University, Medical Faculty HeidelbergGerman Centre for Infection Research (DZIF), Partner Site HeidelbergDivision of Systems Biology of Signal Transduction (B200), German Cancer Research Center (DKFZ)Division of Systems Biology of Signal Transduction (B200), German Cancer Research Center (DKFZ)Department of Molecular and Medical Virology, Ruhr University BochumSchaller Research Group, Department of Infectious Diseases, Virology, Heidelberg University, Medical Faculty HeidelbergSchaller Research Group, Department of Infectious Diseases, Virology, Heidelberg University, Medical Faculty HeidelbergDepartment of Medicine II, Medical Center – University of FreiburgResearch Group “Dynamics of Early Viral Infection and the Innate Antiviral Response”, Division Virus-Associated Carcinogenesis (D430), German Cancer Research Center (DKFZ)Division of Systems Biology of Signal Transduction (B200), German Cancer Research Center (DKFZ)Department of Molecular and Medical Virology, Ruhr University BochumUniv. Lyon, INRAE, EPHE, IVPCInstitute for Integrative Biology of the Cell (I2BC), Université Paris-Saclay, CEA, CNRSDepartments of Medicine and Microbiology & Immunology, The University of North Carolina at Chapel HillSchaller Research Group, Department of Infectious Diseases, Virology, Heidelberg University, Medical Faculty HeidelbergAbstract Hepatitis E virus (HEV) is a major cause of acute hepatitis and mainly transmitted faecal-orally. HEV particles present in faeces are naked (nHEV), whereas those found in the blood are quasi-enveloped (eHEV) with a cell-derived lipid membrane. Despite its global health impact, the cellular life cycle of HEV remains poorly understood, particularly regarding the mechanisms of viral entry into host cells. To address this knowledge gap, we develop a high content RNA-FISH-based imaging assay that allows for the investigation of the entry pathways of both naked and quasi-enveloped HEV particles. Surprisingly, we find that integrin α3, previously implicated in nHEV cell entry, is not expressed in the cell types that are most permissive for HEV infection. Instead, we identify integrin β1 (ITGB1) pairing with different α-integrins as the key player mediating nHEV cell entry. Our results indicate that the interaction of nHEV with ITGB1 facilitates entry through Rab11-positive recycling endosomes. In contrast, eHEV particles do not interact with ITGB1 and enter cells using a classical endocytic route via Rab5a-positive early endosomes. The entry of both types of HEV particles requires endosomal acidification and proteolytic cleavage by lysosomal cathepsins, which ultimately results in delivery of the HEV genome to the cytoplasm.https://doi.org/10.1038/s41467-025-61071-y
spellingShingle Rebecca Fu
Paula Jordan
Zoe Engels
Jasmin Alara Weihs
Josias Mürle
Huanting Chi
Sebastian Burbano de Lara
Barbara Helm
Mara Klöhn
Jungen Hu
Andrew Freistaedter
Tobias Boettler
Marco Binder
Ursula Klingmüller
Eike Steinmann
Pierre-Yves Lozach
Thibault Tubiana
Stanley M. Lemon
Viet Loan Dao Thi
Integrin beta 1 facilitates non-enveloped hepatitis E virus cell entry through the recycling endosome
Nature Communications
title Integrin beta 1 facilitates non-enveloped hepatitis E virus cell entry through the recycling endosome
title_full Integrin beta 1 facilitates non-enveloped hepatitis E virus cell entry through the recycling endosome
title_fullStr Integrin beta 1 facilitates non-enveloped hepatitis E virus cell entry through the recycling endosome
title_full_unstemmed Integrin beta 1 facilitates non-enveloped hepatitis E virus cell entry through the recycling endosome
title_short Integrin beta 1 facilitates non-enveloped hepatitis E virus cell entry through the recycling endosome
title_sort integrin beta 1 facilitates non enveloped hepatitis e virus cell entry through the recycling endosome
url https://doi.org/10.1038/s41467-025-61071-y
work_keys_str_mv AT rebeccafu integrinbeta1facilitatesnonenvelopedhepatitiseviruscellentrythroughtherecyclingendosome
AT paulajordan integrinbeta1facilitatesnonenvelopedhepatitiseviruscellentrythroughtherecyclingendosome
AT zoeengels integrinbeta1facilitatesnonenvelopedhepatitiseviruscellentrythroughtherecyclingendosome
AT jasminalaraweihs integrinbeta1facilitatesnonenvelopedhepatitiseviruscellentrythroughtherecyclingendosome
AT josiasmurle integrinbeta1facilitatesnonenvelopedhepatitiseviruscellentrythroughtherecyclingendosome
AT huantingchi integrinbeta1facilitatesnonenvelopedhepatitiseviruscellentrythroughtherecyclingendosome
AT sebastianburbanodelara integrinbeta1facilitatesnonenvelopedhepatitiseviruscellentrythroughtherecyclingendosome
AT barbarahelm integrinbeta1facilitatesnonenvelopedhepatitiseviruscellentrythroughtherecyclingendosome
AT maraklohn integrinbeta1facilitatesnonenvelopedhepatitiseviruscellentrythroughtherecyclingendosome
AT jungenhu integrinbeta1facilitatesnonenvelopedhepatitiseviruscellentrythroughtherecyclingendosome
AT andrewfreistaedter integrinbeta1facilitatesnonenvelopedhepatitiseviruscellentrythroughtherecyclingendosome
AT tobiasboettler integrinbeta1facilitatesnonenvelopedhepatitiseviruscellentrythroughtherecyclingendosome
AT marcobinder integrinbeta1facilitatesnonenvelopedhepatitiseviruscellentrythroughtherecyclingendosome
AT ursulaklingmuller integrinbeta1facilitatesnonenvelopedhepatitiseviruscellentrythroughtherecyclingendosome
AT eikesteinmann integrinbeta1facilitatesnonenvelopedhepatitiseviruscellentrythroughtherecyclingendosome
AT pierreyveslozach integrinbeta1facilitatesnonenvelopedhepatitiseviruscellentrythroughtherecyclingendosome
AT thibaulttubiana integrinbeta1facilitatesnonenvelopedhepatitiseviruscellentrythroughtherecyclingendosome
AT stanleymlemon integrinbeta1facilitatesnonenvelopedhepatitiseviruscellentrythroughtherecyclingendosome
AT vietloandaothi integrinbeta1facilitatesnonenvelopedhepatitiseviruscellentrythroughtherecyclingendosome