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Published in: Medical Microbiology and Immunology 4/2020

Open Access 01-08-2020 | Hepatitis C | Original Investigation

Single-nucleotide variants in human CD81 influence hepatitis C virus infection of hepatoma cells

Authors: María Pía Alberione, Rebecca Moeller, Jared Kirui, Corinne Ginkel, Mandy Doepke, Luisa J. Ströh, Jan-Philipp Machtens, Thomas Pietschmann, Gisa Gerold

Published in: Medical Microbiology and Immunology | Issue 4/2020

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Abstract

An estimated number of 71 million people are living with chronic hepatitis C virus (HCV) infection worldwide and 400,000 annual deaths are related to the infection. HCV entry into the hepatocytes is complex and involves several host factors. The tetraspanin human CD81 (hCD81) is one of the four essential entry factors and is composed of one large extracellular loop, one small extracellular loop, four transmembrane domains, one intracellular loop and two intracellular tails. The large extracellular loop interacts with the E2 glycoprotein of HCV. Regions outside the large extracellular loop (backbone) of hCD81 have a critical role in post-binding entry steps and determine susceptibility of hepatocytes to HCV. Here, we investigated the effect of five non-synonymous single-nucleotide variants in the backbone of hCD81 on HCV susceptibility. We generated cell lines that stably express the hCD81 variants and infected the cells using HCV pseudoparticles and cell culture-derived HCV. Our results show that all the tested hCD81 variants support HCV pseudoparticle entry with similar efficiency as wild-type hCD81. In contrast, variants A54V, V211M and M220I are less supportive to cell culture-derived HCV infection. This altered susceptibility is HCV genotype dependent and specifically affected the cell entry step. Our findings identify three hCD81 genetic variants that are impaired in their function as HCV host factors for specific viral genotypes. This study provides additional evidence that genetic host variation contributes to inter-individual differences in HCV infection and outcome.
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Literature
2.
go back to reference Di Bisceglie AM (2000) Natural history of hepatitis C: its impact on clinical management. Hepatology 31:1014–1018PubMedCrossRef Di Bisceglie AM (2000) Natural history of hepatitis C: its impact on clinical management. Hepatology 31:1014–1018PubMedCrossRef
3.
go back to reference Simmonds P, Bukh J, Combet C, Deléage G, Enomoto N, Feinstone S, Halfon P, Inchauspé G, Kuiken C, Maertens G et al (2005) Consensus proposals for a unified system of nomenclature of hepatitis C virus genotypes. Hepatology 42:962–973PubMedCrossRef Simmonds P, Bukh J, Combet C, Deléage G, Enomoto N, Feinstone S, Halfon P, Inchauspé G, Kuiken C, Maertens G et al (2005) Consensus proposals for a unified system of nomenclature of hepatitis C virus genotypes. Hepatology 42:962–973PubMedCrossRef
4.
go back to reference Scarselli E, Ansuini H, Cerino R, Roccasecca RM, Acali S, Filocamo G, Traboni C, Nicosia A, Cortese R, Vitelli A (2002) The human scavenger receptor class B type I is a novel candidate receptor for the hepatitis C virus. EMBO J 21:5017–5025PubMedPubMedCentralCrossRef Scarselli E, Ansuini H, Cerino R, Roccasecca RM, Acali S, Filocamo G, Traboni C, Nicosia A, Cortese R, Vitelli A (2002) The human scavenger receptor class B type I is a novel candidate receptor for the hepatitis C virus. EMBO J 21:5017–5025PubMedPubMedCentralCrossRef
5.
go back to reference Pileri P, Uematsu Y, Campagnoli S, Galli G, Falugi F, Petracca R, Weiner AJ, Houghton M, Rosa D, Grandi G et al (1998) Binding of hepatitis C virus to CD81. Science 282:938–941PubMedCrossRef Pileri P, Uematsu Y, Campagnoli S, Galli G, Falugi F, Petracca R, Weiner AJ, Houghton M, Rosa D, Grandi G et al (1998) Binding of hepatitis C virus to CD81. Science 282:938–941PubMedCrossRef
6.
go back to reference Eva-ns MJ, von Hahn T, Tscherne DM, Syder AJ, Panis M, Wölk B, Hatziioannou T, McKeating JA, Bieniasz PD, Rice CM (2007) Claudin-1 is a hepatitis C virus co-receptor required for a late step in entry. Nature 446:801–805CrossRef Eva-ns MJ, von Hahn T, Tscherne DM, Syder AJ, Panis M, Wölk B, Hatziioannou T, McKeating JA, Bieniasz PD, Rice CM (2007) Claudin-1 is a hepatitis C virus co-receptor required for a late step in entry. Nature 446:801–805CrossRef
7.
go back to reference Ploss A, Evans MJ, Gaysinskaya VA, Panis M, You H, de Jong YP, Rice CM (2009) Human occludin is a hepatitis C virus entry factor required for infection of mouse cells. Nature 457:882–886PubMedPubMedCentralCrossRef Ploss A, Evans MJ, Gaysinskaya VA, Panis M, You H, de Jong YP, Rice CM (2009) Human occludin is a hepatitis C virus entry factor required for infection of mouse cells. Nature 457:882–886PubMedPubMedCentralCrossRef
8.
go back to reference Blanchard E, Belouzard S, Goueslain L, Wakita T, Dubuisson J, Wychowski C, Rouillé Y (2006) Hepatitis C virus entry depends on clathrin-mediated endocytosis. J Virol 80:6964–6972PubMedPubMedCentralCrossRef Blanchard E, Belouzard S, Goueslain L, Wakita T, Dubuisson J, Wychowski C, Rouillé Y (2006) Hepatitis C virus entry depends on clathrin-mediated endocytosis. J Virol 80:6964–6972PubMedPubMedCentralCrossRef
9.
go back to reference Ge D, Fellay J, Thompson AJ, Simon JS, Shianna KV, Urban TJ, Heinzen EL, Qiu P, Bertelsen AH, Muir AJ et al (2009) Genetic variation in IL28B predicts hepatitis C treatment-induced viral clearance. Nature 461:399–401PubMedCrossRef Ge D, Fellay J, Thompson AJ, Simon JS, Shianna KV, Urban TJ, Heinzen EL, Qiu P, Bertelsen AH, Muir AJ et al (2009) Genetic variation in IL28B predicts hepatitis C treatment-induced viral clearance. Nature 461:399–401PubMedCrossRef
10.
go back to reference Thomas DL, Thio CL, Martin MP, Qi Y, Ge D, O’Huigin C, Kidd J, Kidd K, Khakoo SI, Alexander G et al (2009) Genetic variation in IL28B and spontaneous clearance of hepatitis C virus. Nature 461:798–801PubMedPubMedCentralCrossRef Thomas DL, Thio CL, Martin MP, Qi Y, Ge D, O’Huigin C, Kidd J, Kidd K, Khakoo SI, Alexander G et al (2009) Genetic variation in IL28B and spontaneous clearance of hepatitis C virus. Nature 461:798–801PubMedPubMedCentralCrossRef
11.
12.
go back to reference Ciesek S, Westhaus S, Wicht M, Wappler I, Henschen S, Sarrazin C, Hamdi N, Abdelaziz AI, Strassburg CP, Wedemeyer H et al (2011) Impact of intra- and interspecies variation of occludin on its function as coreceptor for authentic hepatitis C virus particles. J Virol 85:7613–7621PubMedPubMedCentralCrossRef Ciesek S, Westhaus S, Wicht M, Wappler I, Henschen S, Sarrazin C, Hamdi N, Abdelaziz AI, Strassburg CP, Wedemeyer H et al (2011) Impact of intra- and interspecies variation of occludin on its function as coreceptor for authentic hepatitis C virus particles. J Virol 85:7613–7621PubMedPubMedCentralCrossRef
13.
go back to reference Westhaus S, Deest M, Nguyen ATX, Stanke F, Heckl D, Costa R, Schambach A, Manns MP, Berg T, Vondran FWR et al (2017) Scavenger receptor class B member 1 (SCARB1) variants modulate hepatitis C virus replication cycle and viral load. J Hepatol 67:237–245PubMedCrossRef Westhaus S, Deest M, Nguyen ATX, Stanke F, Heckl D, Costa R, Schambach A, Manns MP, Berg T, Vondran FWR et al (2017) Scavenger receptor class B member 1 (SCARB1) variants modulate hepatitis C virus replication cycle and viral load. J Hepatol 67:237–245PubMedCrossRef
14.
go back to reference Levy S, Todd SC, Maecker HT (1998) CD81 (TAPA-1): a molecule involved in signal transduction and cell adhesion in the immune system. Annu Rev Immunol 16:89–109PubMedCrossRef Levy S, Todd SC, Maecker HT (1998) CD81 (TAPA-1): a molecule involved in signal transduction and cell adhesion in the immune system. Annu Rev Immunol 16:89–109PubMedCrossRef
15.
go back to reference Tham TN, Gouin E, Rubinstein E, Boucheix C, Cossart P, Pizarro-Cerda J (2010) Tetraspanin CD81 is required for Listeria monocytogenes invasion. Infect Immun 78:204–209PubMedCrossRef Tham TN, Gouin E, Rubinstein E, Boucheix C, Cossart P, Pizarro-Cerda J (2010) Tetraspanin CD81 is required for Listeria monocytogenes invasion. Infect Immun 78:204–209PubMedCrossRef
16.
go back to reference Silvie O, Rubinstein E, Franetich J-F, Prenant M, Belnoue E, Rénia L, Hannoun L, Eling W, Levy S, Boucheix C et al (2003) Hepatocyte CD81 is required for Plasmodium falciparum and Plasmodium yoelii sporozoite infectivity. Nat Med 9:93–96PubMedCrossRef Silvie O, Rubinstein E, Franetich J-F, Prenant M, Belnoue E, Rénia L, Hannoun L, Eling W, Levy S, Boucheix C et al (2003) Hepatocyte CD81 is required for Plasmodium falciparum and Plasmodium yoelii sporozoite infectivity. Nat Med 9:93–96PubMedCrossRef
17.
18.
go back to reference Gordón-Alonso M, Yañez-Mó M, Barreiro O, Alvarez S, Muñoz-Fernández MA, Valenzuela-Fernández A, Sánchez-Madrid F (2006) Tetraspanins CD9 and CD81 modulate HIV-1-induced membrane fusion. J Immunol 177:5129–5137PubMedCrossRef Gordón-Alonso M, Yañez-Mó M, Barreiro O, Alvarez S, Muñoz-Fernández MA, Valenzuela-Fernández A, Sánchez-Madrid F (2006) Tetraspanins CD9 and CD81 modulate HIV-1-induced membrane fusion. J Immunol 177:5129–5137PubMedCrossRef
19.
go back to reference Gray LR, Turville SG, Hitchen TL, Cheng W-J, Ellett AM, Salimi H, Roche MJ, Wesselingh SL, Gorry PR, Churchill MJ (2014) HIV-1 entry and trans-infection of astrocytes involves CD81 vesicles. PLoS One 9:e90620PubMedPubMedCentralCrossRef Gray LR, Turville SG, Hitchen TL, Cheng W-J, Ellett AM, Salimi H, Roche MJ, Wesselingh SL, Gorry PR, Churchill MJ (2014) HIV-1 entry and trans-infection of astrocytes involves CD81 vesicles. PLoS One 9:e90620PubMedPubMedCentralCrossRef
21.
go back to reference Deest M, Westhaus S, Steinmann E, Manns MP, von Hahn T, Ciesek S (2014) Impact of single nucleotide polymorphisms in the essential HCV entry factor CD81 on HCV infectivity and neutralization. Antivir Res 101:37–44PubMedCrossRef Deest M, Westhaus S, Steinmann E, Manns MP, von Hahn T, Ciesek S (2014) Impact of single nucleotide polymorphisms in the essential HCV entry factor CD81 on HCV infectivity and neutralization. Antivir Res 101:37–44PubMedCrossRef
22.
go back to reference Davis C, Harris HJ, Hu K, Drummer HE, McKeating JA, Mullins JGL, Balfe P (2012) In silico directed mutagenesis identifies the CD81/claudin-1 hepatitis C virus receptor interface. Cell Microbiol 14:1892–1903PubMedPubMedCentralCrossRef Davis C, Harris HJ, Hu K, Drummer HE, McKeating JA, Mullins JGL, Balfe P (2012) In silico directed mutagenesis identifies the CD81/claudin-1 hepatitis C virus receptor interface. Cell Microbiol 14:1892–1903PubMedPubMedCentralCrossRef
23.
go back to reference Zona L, Lupberger J, Sidahmed-Adrar N, Thumann C, Harris HJ, Barnes A, Florentin J, Tawar RG, Xiao F, Turek M et al (2013) HRas signal transduction promotes hepatitis C virus cell entry by triggering assembly of the host tetraspanin receptor complex. Cell Host Microbe 13:302–313PubMedCrossRef Zona L, Lupberger J, Sidahmed-Adrar N, Thumann C, Harris HJ, Barnes A, Florentin J, Tawar RG, Xiao F, Turek M et al (2013) HRas signal transduction promotes hepatitis C virus cell entry by triggering assembly of the host tetraspanin receptor complex. Cell Host Microbe 13:302–313PubMedCrossRef
24.
go back to reference Gerold G, Meissner F, Bruening J, Welsch K, Perin PM, Baumert TF, Vondran FW, Kaderali L, Marcotrigiano J, Khan AG et al (2015) Quantitative proteomics identifies serum response factor binding protein 1 as a host factor for hepatitis C virus entry. Cell Rep 12:864–878PubMedPubMedCentralCrossRef Gerold G, Meissner F, Bruening J, Welsch K, Perin PM, Baumert TF, Vondran FW, Kaderali L, Marcotrigiano J, Khan AG et al (2015) Quantitative proteomics identifies serum response factor binding protein 1 as a host factor for hepatitis C virus entry. Cell Rep 12:864–878PubMedPubMedCentralCrossRef
25.
go back to reference Bruening J, Lasswitz L, Banse P, Kahl S, Marinach C, Vondran FW, Kaderali L, Silvie O, Pietschmann T, Meissner F et al (2018) Hepatitis C virus enters liver cells using the CD81 receptor complex proteins calpain-5 and CBLB. PLoS Pathog 14:e1007111PubMedPubMedCentralCrossRef Bruening J, Lasswitz L, Banse P, Kahl S, Marinach C, Vondran FW, Kaderali L, Silvie O, Pietschmann T, Meissner F et al (2018) Hepatitis C virus enters liver cells using the CD81 receptor complex proteins calpain-5 and CBLB. PLoS Pathog 14:e1007111PubMedPubMedCentralCrossRef
26.
go back to reference Banse P, Moeller R, Bruening J, Lasswitz L, Kahl S, Khan AG, Marcotrigiano J, Pietschmann T, Gerold G (2018) CD81 receptor regions outside the large extracellular loop determine hepatitis C virus entry into hepatoma cells. Viruses 10(4):207PubMedPubMedCentralCrossRef Banse P, Moeller R, Bruening J, Lasswitz L, Kahl S, Khan AG, Marcotrigiano J, Pietschmann T, Gerold G (2018) CD81 receptor regions outside the large extracellular loop determine hepatitis C virus entry into hepatoma cells. Viruses 10(4):207PubMedPubMedCentralCrossRef
27.
go back to reference Zimmerman B, Kelly B, McMillan BJ, Seegar TCM, Dror RO, Kruse AC, Blacklow SC (2016) Crystal structure of a full-length human tetraspanin reveals a cholesterol-binding pocket. Cell 167:1041–1051.e11PubMedPubMedCentralCrossRef Zimmerman B, Kelly B, McMillan BJ, Seegar TCM, Dror RO, Kruse AC, Blacklow SC (2016) Crystal structure of a full-length human tetraspanin reveals a cholesterol-binding pocket. Cell 167:1041–1051.e11PubMedPubMedCentralCrossRef
28.
go back to reference Bitzegeio J, Bankwitz D, Hueging K, Haid S, Brohm C, Zeisel MB, Herrmann E, Iken M, Ott M, Baumert TF et al (2010) Adaptation of hepatitis C virus to mouse CD81 permits infection of mouse cells in the absence of human entry factors. PLoS Pathog 6:e1000978PubMedPubMedCentralCrossRef Bitzegeio J, Bankwitz D, Hueging K, Haid S, Brohm C, Zeisel MB, Herrmann E, Iken M, Ott M, Baumert TF et al (2010) Adaptation of hepatitis C virus to mouse CD81 permits infection of mouse cells in the absence of human entry factors. PLoS Pathog 6:e1000978PubMedPubMedCentralCrossRef
29.
go back to reference Jaalouk DE, Crosato M, Brodt P, Galipeau J (2006) Inhibition of histone deacetylation in 293GPG packaging cell line improves the production of self-inactivating MLV-derived retroviral vectors. Virol J 3:27PubMedPubMedCentralCrossRef Jaalouk DE, Crosato M, Brodt P, Galipeau J (2006) Inhibition of histone deacetylation in 293GPG packaging cell line improves the production of self-inactivating MLV-derived retroviral vectors. Virol J 3:27PubMedPubMedCentralCrossRef
30.
go back to reference Palsson B, Andreadis S (1997) The physico-chemical factors that govern retrovirus-mediated gene transfer. Exp Hematol 25:94–102PubMed Palsson B, Andreadis S (1997) The physico-chemical factors that govern retrovirus-mediated gene transfer. Exp Hematol 25:94–102PubMed
31.
go back to reference Webb B, Sali A (2016) Comparative protein structure modeling using MODELLER. Curr Protoc Bioinform 54:1–37CrossRef Webb B, Sali A (2016) Comparative protein structure modeling using MODELLER. Curr Protoc Bioinform 54:1–37CrossRef
32.
go back to reference Pundir S, Martin MJ, O’Donovan C (2016) UniProt tools. Curr Protoc Bioinform 53:1–15CrossRef Pundir S, Martin MJ, O’Donovan C (2016) UniProt tools. Curr Protoc Bioinform 53:1–15CrossRef
33.
34.
go back to reference Gottwein JM, Scheel TKH, Jensen TB, Lademann JB, Prentoe JC, Knudsen ML, Hoegh AM, Bukh J (2009) Development and characterization of hepatitis C virus genotype 1–7 cell culture systems: role of CD81 and scavenger receptor class B type I and effect of antiviral drugs. Hepatology 49:364–377PubMedCrossRef Gottwein JM, Scheel TKH, Jensen TB, Lademann JB, Prentoe JC, Knudsen ML, Hoegh AM, Bukh J (2009) Development and characterization of hepatitis C virus genotype 1–7 cell culture systems: role of CD81 and scavenger receptor class B type I and effect of antiviral drugs. Hepatology 49:364–377PubMedCrossRef
35.
go back to reference Haid S, Novodomská A, Gentzsch J, Grethe C, Geuenich S, Bankwitz D, Chhatwal P, Jannack B, Hennebelle T, Bailleul F et al (2012) A plant-derived flavonoid inhibits entry of all HCV genotypes into human hepatocytes. Gastroenterology 143:213–22.e5PubMedCrossRef Haid S, Novodomská A, Gentzsch J, Grethe C, Geuenich S, Bankwitz D, Chhatwal P, Jannack B, Hennebelle T, Bailleul F et al (2012) A plant-derived flavonoid inhibits entry of all HCV genotypes into human hepatocytes. Gastroenterology 143:213–22.e5PubMedCrossRef
36.
go back to reference Higginbottom A, Quinn ER, Kuo CC, Flint M, Wilson LH, Bianchi E, Nicosia A, Monk PN, McKeating JA, Levy S (2000) Identification of amino acid residues in CD81 critical for interaction with hepatitis C virus envelope glycoprotein E2. J Virol 74:3642–3649PubMedPubMedCentralCrossRef Higginbottom A, Quinn ER, Kuo CC, Flint M, Wilson LH, Bianchi E, Nicosia A, Monk PN, McKeating JA, Levy S (2000) Identification of amino acid residues in CD81 critical for interaction with hepatitis C virus envelope glycoprotein E2. J Virol 74:3642–3649PubMedPubMedCentralCrossRef
37.
go back to reference Owsianka AM, Timms JM, Tarr AW, Brown RJP, Hickling TP, Szwejk A, Bienkowska-Szewczyk K, Thomson BJ, Patel AH, Ball JK (2006) Identification of conserved residues in the E2 envelope glycoprotein of the hepatitis C virus that are critical for CD81 binding. J Virol 80:8695–8704PubMedPubMedCentralCrossRef Owsianka AM, Timms JM, Tarr AW, Brown RJP, Hickling TP, Szwejk A, Bienkowska-Szewczyk K, Thomson BJ, Patel AH, Ball JK (2006) Identification of conserved residues in the E2 envelope glycoprotein of the hepatitis C virus that are critical for CD81 binding. J Virol 80:8695–8704PubMedPubMedCentralCrossRef
38.
go back to reference Kinchen VJ, Zahid MN, Flyak AI, Soliman MG, Learn GH, Wang S, Davidson E, Doranz BJ, Ray SC, Cox AL et al (2018) Broadly neutralizing antibody-mediated clearance of human hepatitis C virus infection. Cell Host Microbe 24:717–730.e5PubMedPubMedCentralCrossRef Kinchen VJ, Zahid MN, Flyak AI, Soliman MG, Learn GH, Wang S, Davidson E, Doranz BJ, Ray SC, Cox AL et al (2018) Broadly neutralizing antibody-mediated clearance of human hepatitis C virus infection. Cell Host Microbe 24:717–730.e5PubMedPubMedCentralCrossRef
39.
go back to reference Flyak AI, Ruiz S, Colbert MD, Luong T, Crowe JE, Bailey JR, Bjorkman PJ (2018) HCV broadly neutralizing antibodies use a CDRH3 disulfide motif to recognize an E2 glycoprotein site that can be targeted for vaccine design. Cell Host Microbe 24:703–716.e3PubMedPubMedCentralCrossRef Flyak AI, Ruiz S, Colbert MD, Luong T, Crowe JE, Bailey JR, Bjorkman PJ (2018) HCV broadly neutralizing antibodies use a CDRH3 disulfide motif to recognize an E2 glycoprotein site that can be targeted for vaccine design. Cell Host Microbe 24:703–716.e3PubMedPubMedCentralCrossRef
40.
go back to reference Brazzoli M, Bianchi A, Filippini S, Weiner A, Zhu Q, Pizza M, Crotta S (2008) CD81 is a central regulator of cellular events required for hepatitis C virus infection of human hepatocytes. J Virol 82:8316–8329PubMedPubMedCentralCrossRef Brazzoli M, Bianchi A, Filippini S, Weiner A, Zhu Q, Pizza M, Crotta S (2008) CD81 is a central regulator of cellular events required for hepatitis C virus infection of human hepatocytes. J Virol 82:8316–8329PubMedPubMedCentralCrossRef
41.
go back to reference Krieger SE, Zeisel MB, Davis C, Thumann C, Harris HJ, Schnober EK, Mee C, Soulier E, Royer C, Lambotin M et al (2010) Inhibition of hepatitis C virus infection by anti-claudin-1 antibodies is mediated by neutralization of E2-CD81-claudin-1 associations. Hepatology 51:1144–1157PubMedCrossRef Krieger SE, Zeisel MB, Davis C, Thumann C, Harris HJ, Schnober EK, Mee C, Soulier E, Royer C, Lambotin M et al (2010) Inhibition of hepatitis C virus infection by anti-claudin-1 antibodies is mediated by neutralization of E2-CD81-claudin-1 associations. Hepatology 51:1144–1157PubMedCrossRef
42.
go back to reference Sharma NR, Mateu G, Dreux M, Grakoui A, Cosset F-L, Melikyan GB (2011) Hepatitis C virus is primed by CD81 protein for low pH-dependent fusion. J Biol Chem 286:30361–30376PubMedPubMedCentralCrossRef Sharma NR, Mateu G, Dreux M, Grakoui A, Cosset F-L, Melikyan GB (2011) Hepatitis C virus is primed by CD81 protein for low pH-dependent fusion. J Biol Chem 286:30361–30376PubMedPubMedCentralCrossRef
44.
45.
go back to reference Gerold G, Pietschmann T (2014) The HCV life cycle: in vitro tissue culture systems and therapeutic targets. Dig Dis 32:525–537PubMedCrossRef Gerold G, Pietschmann T (2014) The HCV life cycle: in vitro tissue culture systems and therapeutic targets. Dig Dis 32:525–537PubMedCrossRef
46.
go back to reference Coller KE, Berger KL, Heaton NS, Cooper JD, Yoon R, Randall G (2009) RNA interference and single particle tracking analysis of hepatitis C virus endocytosis. PLoS Pathog 5:e1000702PubMedPubMedCentralCrossRef Coller KE, Berger KL, Heaton NS, Cooper JD, Yoon R, Randall G (2009) RNA interference and single particle tracking analysis of hepatitis C virus endocytosis. PLoS Pathog 5:e1000702PubMedPubMedCentralCrossRef
47.
go back to reference Baktash Y, Madhav A, Coller KE, Randall G (2018) Single particle imaging of polarized hepatoma organoids upon hepatitis C virus infection reveals an ordered and sequential entry process. Cell Host Microbe 23:382–394.e5PubMedPubMedCentralCrossRef Baktash Y, Madhav A, Coller KE, Randall G (2018) Single particle imaging of polarized hepatoma organoids upon hepatitis C virus infection reveals an ordered and sequential entry process. Cell Host Microbe 23:382–394.e5PubMedPubMedCentralCrossRef
48.
go back to reference Zahid MN, Turek M, Xiao F, Thi VLD, Guérin M, Fofana I, Bachellier P, Thompson J, Delang L, Neyts J et al (2013) The postbinding activity of scavenger receptor class B type I mediates initiation of hepatitis C virus infection and viral dissemination. Hepatology 57:492–504PubMedCrossRef Zahid MN, Turek M, Xiao F, Thi VLD, Guérin M, Fofana I, Bachellier P, Thompson J, Delang L, Neyts J et al (2013) The postbinding activity of scavenger receptor class B type I mediates initiation of hepatitis C virus infection and viral dissemination. Hepatology 57:492–504PubMedCrossRef
49.
go back to reference Bankwitz D, Vieyres G, Hueging K, Bitzegeio J, Doepke M, Chhatwal P, Haid S, Catanese MT, Zeisel MB, Nicosia A et al (2014) Role of hypervariable region 1 for the interplay of hepatitis C virus with entry factors and lipoproteins. J Virol 88:12644–12655PubMedPubMedCentralCrossRef Bankwitz D, Vieyres G, Hueging K, Bitzegeio J, Doepke M, Chhatwal P, Haid S, Catanese MT, Zeisel MB, Nicosia A et al (2014) Role of hypervariable region 1 for the interplay of hepatitis C virus with entry factors and lipoproteins. J Virol 88:12644–12655PubMedPubMedCentralCrossRef
50.
go back to reference Messina JP, Humphreys I, Flaxman A, Brown A, Cooke GS, Pybus OG, Barnes E (2015) Global distribution and prevalence of hepatitis C virus genotypes. Hepatology 61:77–87PubMedCrossRef Messina JP, Humphreys I, Flaxman A, Brown A, Cooke GS, Pybus OG, Barnes E (2015) Global distribution and prevalence of hepatitis C virus genotypes. Hepatology 61:77–87PubMedCrossRef
51.
go back to reference Simmonds P (2004) Genetic diversity and evolution of hepatitis C virus-15 years on. J Gen Virol 85:3173–3188PubMedCrossRef Simmonds P (2004) Genetic diversity and evolution of hepatitis C virus-15 years on. J Gen Virol 85:3173–3188PubMedCrossRef
52.
go back to reference Scheel TKH, Gottwein JM, Jensen TB, Prentoe JC, Hoegh AM, Alter HJ, Eugen-Olsen J, Bukh J (2008) Development of JFH1-based cell culture systems for hepatitis C virus genotype 4a and evidence for cross-genotype neutralization. Proc Natl Acad Sci USA 105:997–1002PubMedPubMedCentralCrossRef Scheel TKH, Gottwein JM, Jensen TB, Prentoe JC, Hoegh AM, Alter HJ, Eugen-Olsen J, Bukh J (2008) Development of JFH1-based cell culture systems for hepatitis C virus genotype 4a and evidence for cross-genotype neutralization. Proc Natl Acad Sci USA 105:997–1002PubMedPubMedCentralCrossRef
53.
go back to reference Haid S, Grethe C, Dill MT, Heim M, Kaderali L, Pietschmann T (2014) Isolate-dependent use of claudins for cell entry by hepatitis C virus. Hepatology 59:24–34PubMedCrossRef Haid S, Grethe C, Dill MT, Heim M, Kaderali L, Pietschmann T (2014) Isolate-dependent use of claudins for cell entry by hepatitis C virus. Hepatology 59:24–34PubMedCrossRef
54.
go back to reference Pietschmann T, Kaul A, Koutsoudakis G, Shavinskaya A, Kallis S, Steinmann E, Abid K, Negro F, Dreux M, Cosset F-L et al (2006) Construction and characterization of infectious intragenotypic and intergenotypic hepatitis C virus chimeras. Proc Natl Acad Sci USA 103:7408–7413PubMedPubMedCentralCrossRef Pietschmann T, Kaul A, Koutsoudakis G, Shavinskaya A, Kallis S, Steinmann E, Abid K, Negro F, Dreux M, Cosset F-L et al (2006) Construction and characterization of infectious intragenotypic and intergenotypic hepatitis C virus chimeras. Proc Natl Acad Sci USA 103:7408–7413PubMedPubMedCentralCrossRef
56.
go back to reference Montpellier C, Tews BA, Poitrimole J, Rocha-Perugini V, D’Arienzo V, Potel J, Zhang XA, Rubinstein E, Dubuisson J, Cocquerel L (2011) Interacting regions of CD81 and two of its partners, EWI-2 and EWI-2wint, and their effect on hepatitis C virus infection. J Biol Chem 286:13954–13965PubMedPubMedCentralCrossRef Montpellier C, Tews BA, Poitrimole J, Rocha-Perugini V, D’Arienzo V, Potel J, Zhang XA, Rubinstein E, Dubuisson J, Cocquerel L (2011) Interacting regions of CD81 and two of its partners, EWI-2 and EWI-2wint, and their effect on hepatitis C virus infection. J Biol Chem 286:13954–13965PubMedPubMedCentralCrossRef
57.
go back to reference Lupberger J, Zeisel MB, Xiao F, Thumann C, Fofana I, Zona L, Davis C, Mee CJ, Turek M, Gorke S et al (2011) EGFR and EphA2 are host factors for hepatitis C virus entry and possible targets for antiviral therapy. Nat Med 17:589–595PubMedPubMedCentralCrossRef Lupberger J, Zeisel MB, Xiao F, Thumann C, Fofana I, Zona L, Davis C, Mee CJ, Turek M, Gorke S et al (2011) EGFR and EphA2 are host factors for hepatitis C virus entry and possible targets for antiviral therapy. Nat Med 17:589–595PubMedPubMedCentralCrossRef
58.
go back to reference Krammer F, Smith GJD, Fouchier RAM, Peiris M, Kedzierska K, Doherty PC, Palese P, Shaw ML, Treanor J, Webster RG et al (2018) Influenza. Nat Rev Dis Prim 4:3PubMedCrossRef Krammer F, Smith GJD, Fouchier RAM, Peiris M, Kedzierska K, Doherty PC, Palese P, Shaw ML, Treanor J, Webster RG et al (2018) Influenza. Nat Rev Dis Prim 4:3PubMedCrossRef
Metadata
Title
Single-nucleotide variants in human CD81 influence hepatitis C virus infection of hepatoma cells
Authors
María Pía Alberione
Rebecca Moeller
Jared Kirui
Corinne Ginkel
Mandy Doepke
Luisa J. Ströh
Jan-Philipp Machtens
Thomas Pietschmann
Gisa Gerold
Publication date
01-08-2020
Publisher
Springer Berlin Heidelberg
Keyword
Hepatitis C
Published in
Medical Microbiology and Immunology / Issue 4/2020
Print ISSN: 0300-8584
Electronic ISSN: 1432-1831
DOI
https://doi.org/10.1007/s00430-020-00675-1

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