دورية أكاديمية

The endocytic recycling compartment serves as a viral factory for hepatitis E virus.

التفاصيل البيبلوغرافية
العنوان: The endocytic recycling compartment serves as a viral factory for hepatitis E virus.
المؤلفون: Bentaleb C; University of Lille, CNRS, Inserm, CHU Lille, Pasteur Institute of Lille, U1019-UMR 9017-CIIL-Center for Infection and Immunity of Lille, 59000, Lille, France., Hervouet K; University of Lille, CNRS, Inserm, CHU Lille, Pasteur Institute of Lille, U1019-UMR 9017-CIIL-Center for Infection and Immunity of Lille, 59000, Lille, France., Montpellier C; University of Lille, CNRS, Inserm, CHU Lille, Pasteur Institute of Lille, U1019-UMR 9017-CIIL-Center for Infection and Immunity of Lille, 59000, Lille, France., Camuzet C; University of Lille, CNRS, Inserm, CHU Lille, Pasteur Institute of Lille, U1019-UMR 9017-CIIL-Center for Infection and Immunity of Lille, 59000, Lille, France., Ferrié M; University of Lille, CNRS, Inserm, CHU Lille, Pasteur Institute of Lille, U1019-UMR 9017-CIIL-Center for Infection and Immunity of Lille, 59000, Lille, France., Burlaud-Gaillard J; Inserm U1259, Morphogénèse et Antigénicité du VIH et des Virus des Hépatites (MAVIVH), Université de Tours and CHRU de Tours, 37032, Tours, France.; Université de Tours et CHRU de Tours, Plateforme IBiSA de Microscopie Electronique, Tours, France., Bressanelli S; Université Paris-Saclay, CEA, CNRS, Institute for Integrative Biology of the Cell (I2BC), Gif-Sur-Yvette, France., Metzger K; University of Lille, CNRS, Inserm, CHU Lille, Pasteur Institute of Lille, U1019-UMR 9017-CIIL-Center for Infection and Immunity of Lille, 59000, Lille, France., Werkmeister E; Univ. Lille, CNRS, Inserm, CHU Lille, Institut Pasteur de Lille, UMR2014-US41-PLBS-Plateformes Lilloises de Biologie and Santé, Lille, France., Ankavay M; University of Lille, CNRS, Inserm, CHU Lille, Pasteur Institute of Lille, U1019-UMR 9017-CIIL-Center for Infection and Immunity of Lille, 59000, Lille, France.; Division of Gastroenterology and Hepatology, Institute of Microbiology, Lausanne, Switzerland., Janampa NL; Inserm U1259, Morphogénèse et Antigénicité du VIH et des Virus des Hépatites (MAVIVH), Université de Tours and CHRU de Tours, 37032, Tours, France., Marlet J; Inserm U1259, Morphogénèse et Antigénicité du VIH et des Virus des Hépatites (MAVIVH), Université de Tours and CHRU de Tours, 37032, Tours, France., Roux J; BIOTEM, Apprieu, France., Deffaud C; BIOTEM, Apprieu, France., Goffard A; University of Lille, CNRS, Inserm, CHU Lille, Pasteur Institute of Lille, U1019-UMR 9017-CIIL-Center for Infection and Immunity of Lille, 59000, Lille, France., Rouillé Y; University of Lille, CNRS, Inserm, CHU Lille, Pasteur Institute of Lille, U1019-UMR 9017-CIIL-Center for Infection and Immunity of Lille, 59000, Lille, France., Dubuisson J; University of Lille, CNRS, Inserm, CHU Lille, Pasteur Institute of Lille, U1019-UMR 9017-CIIL-Center for Infection and Immunity of Lille, 59000, Lille, France., Roingeard P; Inserm U1259, Morphogénèse et Antigénicité du VIH et des Virus des Hépatites (MAVIVH), Université de Tours and CHRU de Tours, 37032, Tours, France.; Université de Tours et CHRU de Tours, Plateforme IBiSA de Microscopie Electronique, Tours, France., Aliouat-Denis CM; University of Lille, CNRS, Inserm, CHU Lille, Pasteur Institute of Lille, U1019-UMR 9017-CIIL-Center for Infection and Immunity of Lille, 59000, Lille, France., Cocquerel L; University of Lille, CNRS, Inserm, CHU Lille, Pasteur Institute of Lille, U1019-UMR 9017-CIIL-Center for Infection and Immunity of Lille, 59000, Lille, France. laurence.cocquerel@cnrs.fr.
المصدر: Cellular and molecular life sciences : CMLS [Cell Mol Life Sci] 2022 Dec 03; Vol. 79 (12), pp. 615. Date of Electronic Publication: 2022 Dec 03.
نوع المنشور: Journal Article
اللغة: English
بيانات الدورية: Publisher: Springer Country of Publication: Switzerland NLM ID: 9705402 Publication Model: Electronic Cited Medium: Internet ISSN: 1420-9071 (Electronic) Linking ISSN: 1420682X NLM ISO Abbreviation: Cell Mol Life Sci Subsets: MEDLINE
أسماء مطبوعة: Publication: Basel : Springer
Original Publication: Basel ; Boston : Birkhauser, c1997-
مواضيع طبية MeSH: Hepatitis E virus*/genetics, Humans ; Viral Replication Compartments ; Capsid Proteins ; Biological Transport ; Antibodies, Monoclonal
مستخلص: Although hepatitis E virus (HEV) is the major leading cause of enterically transmitted viral hepatitis worldwide, many gaps remain in the understanding of the HEV lifecycle. Notably, viral factories induced by HEV have not been documented yet, and it is currently unknown whether HEV infection leads to cellular membrane modeling as many positive-strand RNA viruses. HEV genome encodes the ORF1 replicase, the ORF2 capsid protein and the ORF3 protein involved in virion egress. Previously, we demonstrated that HEV produces different ORF2 isoforms including the virion-associated ORF2i form. Here, we generated monoclonal antibodies that specifically recognize the ORF2i form and antibodies that recognize the different ORF2 isoforms. One antibody, named P1H1 and targeting the ORF2i N-terminus, recognized delipidated HEV particles from cell culture and patient sera. Importantly, AlphaFold2 modeling demonstrated that the P1H1 epitope is exposed on HEV particles. Next, antibodies were used to probe viral factories in HEV-producing/infected cells. By confocal microscopy, we identified subcellular nugget-like structures enriched in ORF1, ORF2 and ORF3 proteins and viral RNA. Electron microscopy analyses revealed an unprecedented HEV-induced membrane network containing tubular and vesicular structures. We showed that these structures are dependent on ORF2i capsid protein assembly and ORF3 expression. An extensive colocalization study of viral proteins with subcellular markers, and silencing experiments demonstrated that these structures are derived from the endocytic recycling compartment (ERC) for which Rab11 is a central player. Hence, HEV hijacks the ERC and forms a membrane network of vesicular and tubular structures that might be the hallmark of HEV infection.
(© 2022. The Author(s).)
References: Kamar N, Izopet J, Pavio N et al (2017) Hepatitis E virus infection. Nat Rev Dis Primers 3:17086. https://doi.org/10.1111/trf.13355. (PMID: 10.1111/trf.13355)
Doceul V, Bagdassarian E, Demange A, Pavio N (2016) Zoonotic hepatitis E virus: classification animal reservoirs and transmission routes. Viruses 8:270. https://doi.org/10.3390/v8100270. (PMID: 10.3390/v8100270)
Horvatits T, Wiesch JS, zur, Lütgehetmann M, et al (2019) The clinical perspective on hepatitis E. Viruses 11:617–619. https://doi.org/10.3390/v11070617. (PMID: 10.3390/v11070617)
Lee G-H, Tan B-H, Teo EC-Y et al (2016) Chronic infection with camelid hepatitis E virus in a liver transplant recipient who regularly consumes camel meat and milk. Gastroenterology 150:355–7.e3. https://doi.org/10.1053/j.gastro.2015.10.048. (PMID: 10.1053/j.gastro.2015.10.048)
Aslan AT, Balaban HY (2020) Hepatitis E virus: epidemiology, diagnosis, clinical manifestations, and treatment. World J Gastroentero 26:5543–5560. https://doi.org/10.3748/wjg.v26.i37.5543. (PMID: 10.3748/wjg.v26.i37.5543)
Nimgaonkar I, Ding Q, Schwartz RE, Ploss A (2018) Hepatitis E virus: advances and challenges. Nat Rev Gastroenterol Hepatol 15:96–110. https://doi.org/10.1038/nrgastro.2017.150. (PMID: 10.1038/nrgastro.2017.150)
Montpellier C, Wychowski C, Sayed IM et al (2018) Hepatitis E virus lifecycle and identification of 3 forms of the ORF2 capsid protein. Gastroenterology 154:211-223.e8. https://doi.org/10.1053/j.gastro.2017.09.020. (PMID: 10.1053/j.gastro.2017.09.020)
Yin X, Ying D, Lhomme S et al (2018) Origin, antigenicity, and function of a secreted form of ORF2 in hepatitis E virus infection. Proc Natl Acad Sci USA 3:201721345–201721346. https://doi.org/10.1073/pnas.1721345115. (PMID: 10.1073/pnas.1721345115)
Sayed IM, Verhoye L, Montpellier C et al (2019) Hepatitis E virus (HEV) open reading frame 2 antigen kinetics in human-liver chimeric mice and its impact on HEV diagnosis. J Infect Dis 220:811–819. https://doi.org/10.1093/infdis/jiz171. (PMID: 10.1093/infdis/jiz171)
Hervouet K, Ferrié M, Ankavay M et al (2022) An arginine-rich motif in the ORF2 capsid protein regulates the hepatitis e virus lifecycle and interactions with the host cell. PLoS Pathog 18:e1010798. https://doi.org/10.1371/journal.ppat.1010798. (PMID: 10.1371/journal.ppat.1010798)
Meister TL, Bruening J, Todt D, Steinmann E (2019) Cell culture systems for the study of hepatitis E virus. Antiviral Res 163:34–49. https://doi.org/10.1016/j.antiviral.2019.01.007. (PMID: 10.1016/j.antiviral.2019.01.007)
Ju X, Ding Q (2019) Hepatitis E virus assembly and release. Viruses 11:539–613. https://doi.org/10.3390/v11060539. (PMID: 10.3390/v11060539)
Harak C, Lohmann V (2015) Ultrastructure of the replication sites of positive-strand RNA viruses. Virology 479:418–433. https://doi.org/10.1016/j.virol.2015.02.029. (PMID: 10.1016/j.virol.2015.02.029)
Talmont F, Moulédous L, Baranger M et al (2019) Development and characterization of sphingosine 1-phosphate receptor 1 monoclonal antibody suitable for cell imaging and biochemical studies of endogenous receptors. PLoS ONE 14:e0213203-e213219. https://doi.org/10.1371/journal.pone.0213203. (PMID: 10.1371/journal.pone.0213203)
Graff J, Nguyen H, Yu C et al (2005) The open reading frame 3 gene of hepatitis E virus contains a cis-reactive element and encodes a protein required for infection of macaques. J Virol 79:6680–6689. https://doi.org/10.1128/jvi.79.11.6680-6689.2005. (PMID: 10.1128/jvi.79.11.6680-6689.2005)
Flint M, Maidens C, Loomis-Price LD et al (1999) Characterization of hepatitis C virus E2 glycoprotein interaction with a putative cellular receptor, CD81. J Virol 73:6235–6244. (PMID: 10.1128/JVI.73.8.6235-6244.1999)
Oren R, Takahashi S, Doss C et al (1990) TAPA-1, the target of an antiproliferative antibody, defines a new family of transmembrane proteins. Mol Cell Biol 10:4007. https://doi.org/10.1128/mcb.10.8.4007. (PMID: 10.1128/mcb.10.8.4007)
Blight KJ, Mckeating JA, Rice CM (2002) Highly permissive cell lines for subgenomic and genomic hepatitis C virus RNA replication. J Virol 76:13001–13014. https://doi.org/10.1128/jvi.76.24.13001-13014.2002. (PMID: 10.1128/jvi.76.24.13001-13014.2002)
Ankavay M, Montpellier C, Sayed IM et al (2019) New insights into the ORF2 capsid protein, a key player of the hepatitis E virus lifecycle. Sci Rep 9:6243. https://doi.org/10.1038/s41598-019-42737-2. (PMID: 10.1038/s41598-019-42737-2)
Shukla P, Nguyen HT, Faulk K et al (2012) Adaptation of a genotype 3 hepatitis E virus to efficient growth in cell culture depends on an inserted human gene segment acquired by recombination. J Virol 86:5697–5707. https://doi.org/10.1128/jvi.00146-12. (PMID: 10.1128/jvi.00146-12)
Metzger K, Bentaleb C, Hervouet K et al (2022) Processing and subcellular localization of the hepatitis E virus replicase: identification of candidate viral factories. Front Microbiol 13:828636. https://doi.org/10.3389/fmicb.2022.828636. (PMID: 10.3389/fmicb.2022.828636)
Jothikumar N, Cromeans TL, Robertson BH et al (2006) A broadly reactive one-step real-time RT-PCR assay for rapid and sensitive detection of hepatitis E virus. J Virol Methods 131:65–71. https://doi.org/10.1016/j.jviromet.2005.07.004. (PMID: 10.1016/j.jviromet.2005.07.004)
Jumper J, Evans R, Pritzel A et al (2021) Highly accurate protein structure prediction with AlphaFold. Nature 596:583–589. https://doi.org/10.1038/s41586-021-03819-2. (PMID: 10.1038/s41586-021-03819-2)
Gabler F, Nam S, Till S et al (2020) Protein sequence analysis using the MPI bioinformatics toolkit. Curr Protoc Bioinform 72:e108. https://doi.org/10.1002/cpbi.108. (PMID: 10.1002/cpbi.108)
Xing L, Li TC, Mayazaki N et al (2010) Structure of hepatitis E virion-sized particle reveals an RNA-dependent viral assembly pathway. J Biol Chem 285:33175–33183. https://doi.org/10.1074/jbc.m110.106336. (PMID: 10.1074/jbc.m110.106336)
Wang F, Flanagan J, Su N et al (2012) RNAscope a novel in situ RNA analysis platform for formalin-fixed, paraffin-embedded tissues. J Mol Diagn 14:22–29. https://doi.org/10.1016/j.jmoldx.2011.08.002. (PMID: 10.1016/j.jmoldx.2011.08.002)
Liu D, Tedbury PR, Lan S et al (2019) Visualization of positive and negative sense viral RNA for probing the mechanism of direct-acting antivirals against hepatitis C virus. Viruses 11:1039. https://doi.org/10.3390/v11111039. (PMID: 10.3390/v11111039)
Ding Q, Heller B, Capuccino JMV et al (2017) Hepatitis E virus ORF3 is a functional ion channel required for release of infectious particles. Proc Natl Acad Sci USA. https://doi.org/10.1073/pnas.1614955114. (PMID: 10.1073/pnas.1614955114)
Nagashima S, Jirintai S, Takahashi M et al (2014) Hepatitis E virus egress depends on the exosomal pathway, with secretory exosomes derived from multivesicular bodies. J Gen Virol 95:2166–2175. https://doi.org/10.1099/vir.0.066910-0. (PMID: 10.1099/vir.0.066910-0)
Nagashima S, Takahashi M, Jirintai, et al (2011) A PSAP motif in the ORF3 protein of hepatitis E virus is necessary for virion release from infected cells. J Gen Virol 92:269–278. https://doi.org/10.1099/vir.0.025791-0. (PMID: 10.1099/vir.0.025791-0)
Gouttenoire J, Pollán A, Abrami L et al (2018) Palmitoylation mediates membrane association of hepatitis E virus ORF3 protein and is required for infectious particle secretion. PLoS Pathog 14:e1007471–e1007524. https://doi.org/10.1371/journal.ppat.1007471. (PMID: 10.1371/journal.ppat.1007471)
Lombardi D, Soldati T, Riederer MA et al (1993) Rab9 functions in transport between late endosomes and the trans Golgi network. Embo J 12:677–682. https://doi.org/10.1002/j.1460-2075.1993.tb05701.x. (PMID: 10.1002/j.1460-2075.1993.tb05701.x)
Hutagalung AH, Novick PJ (2011) Role of Rab GTPases in membrane traffic and cell physiology. Physiol Rev 91:119–149. https://doi.org/10.1152/physrev.00059.2009. (PMID: 10.1152/physrev.00059.2009)
Maxfield FR, McGraw TE (2004) Endocytic recycling. Nat Rev Mol Cell Biol 5:121–132. https://doi.org/10.1038/nrm1315. (PMID: 10.1038/nrm1315)
Vale-Costa S, Amorim M (2016) Recycling endosomes and viral infection. Viruses 8:29–64. https://doi.org/10.3390/v8030064. (PMID: 10.3390/v8030064)
Ullrich O, Reinsch S, Urbé S et al (1996) Rab11 regulates recycling through the pericentriolar recycling endosome. J Cell Biology 135:913–924. https://doi.org/10.1083/jcb.135.4.913. (PMID: 10.1083/jcb.135.4.913)
Stone R, Hayashi T, Bajimaya S et al (2016) Critical role of Rab11a-mediated recycling endosomes in the assembly of type I parainfluenza viruses. Virology 487:11–18. https://doi.org/10.1016/j.virol.2015.10.008. (PMID: 10.1016/j.virol.2015.10.008)
Bhuin T, Roy JK (2015) Rab11 in disease progression. Int J Mol Cell Med 4:1–8.
Guichard A, Nizet V, Bier E (2014) RAB11-mediated trafficking in host–pathogen interactions. Nat Rev Microbiol 12:624–634. https://doi.org/10.1038/nrmicro3325. (PMID: 10.1038/nrmicro3325)
Mayle KM, Le AM, Kamei DT (2012) The intracellular trafficking pathway of transferrin. Biochimica et Biophysica Acta BBA 1820:264–281. https://doi.org/10.1016/j.bbagen.2011.09.009. (PMID: 10.1016/j.bbagen.2011.09.009)
Hehnly H, Chen C-T, Powers CM et al (2012) The centrosome regulates the Rab11- dependent recycling endosome pathway at appendages of the mother centriole. Curr Biol 22:1944–1950. https://doi.org/10.1016/j.cub.2012.08.022. (PMID: 10.1016/j.cub.2012.08.022)
Yang Y-L, Nan Y-C (2021) Open reading frame 3 protein of hepatitis E virus: multi-function protein with endless potential. World J Gastroenterol 27:2458–2473. https://doi.org/10.3748/wjg.v27.i20.2458. (PMID: 10.3748/wjg.v27.i20.2458)
Nagashima S, Takahashi M, Kobayashi T et al (2017) Characterization of the quasi-enveloped hepatitis E virus particles released by the cellular exosomal pathway. J Virol. https://doi.org/10.1128/jvi.00822-17. (PMID: 10.1128/jvi.00822-17)
Surjit M, Jameel S, Lal SK (2007) Cytoplasmic localization of the ORF2 protein of hepatitis E virus is dependent on its ability to undergo retrotranslocation from the endoplasmic reticulum. J Virol 81:3339–3345. https://doi.org/10.1128/jvi.02039-06. (PMID: 10.1128/jvi.02039-06)
Zafrullah M, Ozdener MH, Kumar R et al (1999) Mutational analysis of glycosylation, membrane translocation, and cell surface expression of the hepatitis E virus ORF2 protein. J Virol 73:4074–4082. (PMID: 10.1128/JVI.73.5.4074-4082.1999)
Lenggenhager D, Gouttenoire J, Malehmir M et al (2017) Visualization of hepatitis E virus RNA and proteins in the human liver. J Hepatol 67:471–479. https://doi.org/10.1016/j.jhep.2017.04.002. (PMID: 10.1016/j.jhep.2017.04.002)
Nagashima S, Takahashi M, Jirintai S et al (2011) Tumour susceptibility gene 101 and the vacuolar protein sorting pathway are required for the release of hepatitis E virions. J Gen Virol 92:2838–2848. https://doi.org/10.1099/vir.0.035378-0. (PMID: 10.1099/vir.0.035378-0)
Chandra V, Kar-Roy A, Kumari S et al (2008) The hepatitis E virus ORF3 protein modulates epidermal growth factor receptor trafficking, STAT3 translocation, and the acute-phase response. J Virol 82:7100–7110. https://doi.org/10.1128/jvi.00403-08. (PMID: 10.1128/jvi.00403-08)
Zafrullah M, Ozdener MH, Panda SK, Jameel S (1997) The ORF3 protein of hepatitis E virus is a phosphoprotein that associates with the cytoskeleton. J Virol 71:9045–9053. (PMID: 10.1128/jvi.71.12.9045-9053.1997)
Kannan H, Fan S, Patel D et al (2009) The hepatitis E virus open reading frame 3 product interacts with microtubules and interferes with their dynamics. J Virol 83:6375–6382. https://doi.org/10.1128/jvi.02571-08. (PMID: 10.1128/jvi.02571-08)
Szkolnicka D, Pollán A, Silva ND et al (2019) Recombinant hepatitis E viruses harboring tags in the ORF1 protein. J Virol 93:1237–1318. https://doi.org/10.1128/jvi.00459-19. (PMID: 10.1128/jvi.00459-19)
Hollinshead M, Johns HL, Sayers CL et al (2012) Endocytic tubules regulated by Rab GTPases 5 and 11 are used for envelopment of herpes simplex virus. EMBO J 31:4204–4220. https://doi.org/10.1038/emboj.2012.262. (PMID: 10.1038/emboj.2012.262)
Coller KE, Heaton NS, Berger KL et al (2012) Molecular determinants and dynamics of hepatitis C virus secretion. Plos Pathog 8:e1002466. https://doi.org/10.1371/journal.ppat.1002466. (PMID: 10.1371/journal.ppat.1002466)
معلومات مُعتمدة: MAT-PI-17006 Inserm Transfert; DiagHepE Institut Pasteur de Lille; DiagHepE Région Hauts-de-France
فهرسة مساهمة: Keywords: AlphaFold2; Antibodies; Electron microscopy; Endocytic recycling compartment; Hepatitis E virus; Infectious particles; ORF2 capsid protein; Rab11; Viral factories
المشرفين على المادة: 0 (Capsid Proteins)
0 (Antibodies, Monoclonal)
تواريخ الأحداث: Date Created: 20221202 Date Completed: 20221206 Latest Revision: 20221213
رمز التحديث: 20221214
مُعرف محوري في PubMed: PMC9718719
DOI: 10.1007/s00018-022-04646-y
PMID: 36460928
قاعدة البيانات: MEDLINE
الوصف
تدمد:1420-9071
DOI:10.1007/s00018-022-04646-y