Abstract
Hepatitis C and malaria, two of the most prevalent infectious diseases in the world, are caused by Hepatitis C virus (HCV) and Plasmodium parasites, respectively. Both HCV particles and Plasmodium sporozoites, the mosquito-transmitted stage of the malaria parasite, infect and replicate in the liver. Whereas HCV enters cells by clathrin-mediated endocytosis, Plasmodium sporozoite invasion is a specific active process that relies on the parasite motility machinery. Remarkably, both pathogens critically depend on the host tetraspanin CD81 to enter hepatocytes. In this chapter, we summarize the current knowledge on the role of CD81, tetraspanin-enriched microdomains and CD81-associated partners during HCV and Plasmodium liver infection.
Keywords
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- AMA-1:
-
Apical membrane antigen 1
- ApoB:
-
Apolipoprotein B
- ApoE:
-
Apolipoprotein E
- CLDN-1:
-
Claudin-1
- CSP:
-
Circumsporozoite protein
- EC1:
-
First extracellular loop
- EEFs:
-
Exo-erythrocytic forms
- ER:
-
Endoplasmic reticulum
- hCD81:
-
Human CD81
- HCV:
-
Hepatitis C virus
- HCVcc:
-
HCV produced in cell culture
- HCVpc:
-
HCV from primary culture
- HCVpp:
-
HCV pseudoparticles
- HCVs:
-
HCV from infectious serum
- HDL:
-
High-density lipoproteins
- HSPGs:
-
Heparan sulfate proteoglycans
- HTLV-1:
-
Human T-lymphotropic virus 1
- HVR1:
-
Hypervariable region 1
- LDL:
-
Low-density lipoproteins
- LDL-R:
-
Low-density lipoproteins receptor
- LEL:
-
Large extracellular loop
- LS:
-
Liver stages
- LVPs:
-
Lipo-viro-particles
- mCD81:
-
Mouse CD81
- MβCD:
-
Methyl-beta-cyclo-dextrin
- NS:
-
Non structural
- PCSK9:
-
Proprotein convertase subtilisin/kexin type 9
- PHH:
-
Primary human hepatocytes
- sE2:
-
Soluble E2
- SR-BI:
-
Scavenger receptor class B type I
- TEM:
-
Tetraspanin-enriched microdomains
- TRAP:
-
Thrombospondin-related anonymous protein
- VLDL:
-
Very-low-density lipoproteins
References
Agnello V, Abel G, Elfahal M, Knight GB, Zhang Q-X (1999) Hepatitis C virus and other flaviviridae viruses enter cells via low density lipoprotein receptor. Proc Natl Acad Sci USA 96:12766–12771
Akazawa D, Date T, Morikawa K, Murayama A, Miyamoto M, Kaga M, Barth H, Baumert TF, Dubuisson J, Wakita T (2007) CD81 expression is important for the permissiveness of Huh7 cell clones for heterogeneous hepatitis C virus infection. J Virol 81:5036–5045
Albecka A, Belouzard S, de Beeck AO, Descamps V, Goueslain L, Bertrand-Michel J, Terce F, Duverlie G, Rouille Y, Dubuisson J (2012) Role of low-density lipoprotein receptor in the hepatitis C virus life cycle. Hepatology 55:998–1007
Allander T, Forns X, Emerson SU, Purcell RH, Bukh J (2000) Hepatitis C virus envelope protein E2 binds to CD81 of tamarins. Virology 277:358–367
Aly AS, Vaughan AM, Kappe SH (2009) Malaria parasite development in the mosquito and infection of the mammalian host. Annu Rev Microbiol 63:195–221
Amino R, Thiberge S, Martin B, Celli S, Shorte S, Frischknecht F, Menard R (2006) Quantitative imaging of Plasmodium transmission from mosquito to mammal. Nat Med 12:220–224
Andre P, Komurian-Pradel F, Deforges S, Perret M, Berland JL, Sodoyer M, Pol S, Brechot C, Paranhos-Baccala G, Lotteau V (2002) Characterization of low- and very-low-density hepatitis C virus RNA-containing particles. J Virol 76:6919–6928
Andre P, Perlemuter G, Budkowska A, Brechot C, Lotteau V (2005) Hepatitis C virus particles and lipoprotein metabolism. Semin Liver Dis 25:93–104
Andreo U, Maillard P, Kalinina O, Walic M, Meurs E, Martinot M, Marcellin P, Budkowska A (2007) Lipoprotein lipase mediates hepatitis C virus (HCV) cell entry and inhibits HCV infection. Cell Microbiol 9:2445–2456
Bankwitz D, Steinmann E, Bitzegeio J, Ciesek S, Friesland M, Herrmann E, Zeisel MB, Baumert TF, Keck ZY, Foung SK, Pecheur EI, Pietschmann T (2010) Hepatitis C virus hypervariable region 1 modulates receptor interactions, conceals the CD81 binding site, and protects conserved neutralizing epitopes. J Virol 84:5751–5763
Bano N, Romano JD, Jayabalasingham B, Coppens I (2007) Cellular interactions of Plasmodium liver stage with its host mammalian cell. Int J Parasitol 37:1329–1341
Barth H, Schafer C, Adah MI, Zhang F, Linhardt RJ, Toyoda H, Kinoshita-Toyoda A, Toida T, Van Kuppevelt TH, Depla E, Von Weizsacker F, Blum HE, Baumert TF (2003) Cellular binding of hepatitis C virus envelope glycoprotein E2 requires cell surface heparan sulfate. J Biol Chem 278:41003–41012
Barth H, Ulsenheimer A, Pape GR, Diepolder HM, Hoffmann M, Neumann-Haefelin C, Thimme R, Henneke P, Klein R, Paranhos-Baccala G, Depla E, Liang TJ, Blum HE, Baumert TF (2005) Uptake and presentation of hepatitis C virus-like particles by human dendritic cells. Blood 105:3605–3614
Barth H, Liang TJ, Baumert TF (2006) Hepatitis C virus entry: molecular biology and clinical implications. Hepatology 44:527–535
Bartosch B, Cosset FL (2006) Cell entry of hepatitis C virus. Virology 348:1–12
Bartosch B, Bukh J, Meunier JC, Granier C, Engle RE, Blackwelder WC, Emerson SU, Cosset FL, Purcell RH (2003a) In vitro assay for neutralizing antibody to hepatitis C virus: evidence for broadly conserved neutralization epitopes. Proc Natl Acad Sci USA 100:14199–14204
Bartosch B, Dubuisson J, Cosset F-L (2003b) Highly infectious hepatitis C pseudo-viruses containing functional E1E2 envelope protein complexes. J Exp Med 197:633–642
Bartosch B, Vitelli A, Granier C, Goujon C, Dubuisson J, Pascale S, Scarselli E, Cortese R, Nicosia A, Cosset FL (2003c) Cell entry of hepatitis C virus requires a set of co-receptors that include the CD81 tetraspanin and the SR-B1 scavenger receptor. J Biol Chem 278:41624–41630
Bartosch B, Verney G, Dreux M, Donot P, Morice Y, Penin F, Pawlotsky JM, Lavillette D, Cosset FL (2005) An interplay between hypervariable region 1 of the hepatitis C virus E2 glycoprotein, the scavenger receptor BI, and high-density lipoprotein promotes both enhancement of infection and protection against neutralizing antibodies. J Virol 79:8217–8229
Basu A, Kanda T, Beyene A, Saito K, Meyer K, Ray R (2007) Sulfated homologues of heparin inhibit hepatitis C virus entry into mammalian cells. J Virol 81:3933–3941
Baum J, Gilberger TW, Frischknecht F, Meissner M (2008) Host-cell invasion by malaria parasites: insights from Plasmodium and Toxoplasma. Trends Parasitol 24:557–563
Benedicto I, Molina-Jimenez F, Bartosch B, Cosset FL, Lavillette D, Prieto J, Moreno-Otero R, Valenzuela-Fernandez A, Aldabe R, Lopez-Cabrera M, Majano PL (2009) The tight junction-associated protein occludin is required for a postbinding step in hepatitis C virus entry and infection. J Virol 83:8012–8020
Benga WJ, Krieger SE, Dimitrova M, Zeisel MB, Parnot M, Lupberger J, Hildt E, Luo G, McLauchlan J, Baumert TF, Schuster C (2010) Apolipoprotein E interacts with hepatitis C virus nonstructural protein 5A and determines assembly of infectious particles. Hepatology 51:43–53
Berditchevski F, Odintsova E, Sawada S, Gilbert E (2002) Expression of the palmitoylation-deficient CD151 weakens the association of alpha 3 beta 1 integrin with the tetraspanin-enriched microdomains and affects integrin-dependent signaling. J Biol Chem 277:36991–37000
Bertaux C, Dragic T (2006) Different domains of CD81 mediate distinct stages of hepatitis C virus pseudoparticle entry. J Virol 80:4940–4948
Blanchard E, Belouzard S, Goueslain L, Wakita T, Dubuisson J, Wychowski C, Rouille Y (2006) Hepatitis C virus entry depends on clathrin-mediated endocytosis. J Virol 80:6964–6972
Bollinger CR, Teichgraber V, Gulbins E (2005) Ceramide-enriched membrane domains. Biochim Biophys Acta 1746:284–294
Bonnafous P, Perrault M, Le Bihan O, Bartosch B, Lavillette D, Penin F, Lambert O, Pecheur EI (2010) Characterization of hepatitis C viral pseudoparticles by cryo-electron microscopy using functionalized magnetic nanobeads. J Gen Virol 91(Pt8):1919–1930
Boo I, Tewierik K, Douam F, Lavillette D, Poumbourios P, Drummer HE (2012) Distinct roles in folding, CD81 receptor binding and viral entry for conserved histidine residues of hepatitis C virus glycoprotein E1 and E2. Biochem J 443:85–94
Boucheix C, Rubinstein E (2001) Tetraspanins. Cell Mol Life Sci 58:1189–1205
Brazzoli M, Helenius A, Foung SK, Houghton M, Abrignani S, Merola M (2005) Folding and dimerization of hepatitis C virus E1 and E2 glycoproteins in stably transfected CHO cells. Virology 332:438–453
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 82:8316–8329
Buck M (2008) Direct infection and replication of naturally occurring hepatitis C virus genotypes 1, 2, 3 and 4 in normal human hepatocyte cultures. PLoS One 3:e2660
Cai Z, Cai L, Jiang J, Chang KS, van der Westhuyzen DR, Luo G (2007) Human serum amyloid A protein inhibits hepatitis C virus entry into cells. J Virol 81:6128–6133
Callens N, Ciczora Y, Bartosch B, Vu-Dac N, Cosset FL, Pawlotsky JM, Penin F, Dubuisson J (2005) Basic residues in hypervariable region 1 of hepatitis C virus envelope glycoprotein e2 contribute to virus entry. J Virol 79:15331–15341
Calvo-Calle JM, Moreno A, Eling WM, Nardin EH (1994) In vitro development of infectious liver stages of P. yoelii and P. berghei malaria in human cell lines. Exp Parasitol 79:362–373
Carloni G, Iacovacci S, Sargiacomo M, Ravagnan G, Ponzetto A, Peschle C, Battaglia M (1993) Susceptibility of human liver cell cultures to hepatitis C virus infection. Arch Virol Suppl 8:31–39
Catanese MT, Graziani R, von Hahn T, Moreau M, Huby T, Paonessa G, Santini C, Luzzago A, Rice CM, Cortese R, Vitelli A, Nicosia A (2007) High-avidity monoclonal antibodies against the human scavenger class B type I receptor efficiently block hepatitis C virus infection in the presence of high-density lipoprotein. J Virol 81:8063–8071
Catanese MT, Ansuini H, Graziani R, Huby T, Moreau M, Ball JK, Paonessa G, Rice CM, Cortese R, Vitelli A, Nicosia A (2010) Role of scavenger receptor class B type I in hepatitis C virus entry: kinetics and molecular determinants. J Virol 84:34–43
Chang KS, Jiang J, Cai Z, Luo G (2007) Human apolipoprotein e is required for infectivity and production of hepatitis C virus in cell culture. J Virol 81:13783–13793
Charrin S, Le Naour F, Oualid M, Billard M, Faure G, Hanash SM, Boucheix C, Rubinstein E (2001) The major CD9 and CD81 molecular partner. Identification and characterization of the complexes. J Biol Chem 276:14329–14337
Charrin S, Le Naour F, Labas V, Billard M, Le Caer JP, Emile JF, Petit MA, Boucheix C, Rubinstein E (2003a) EWI-2 is a new component of the tetraspanin web in hepatocytes and lymphoid cells. Biochem J 373:409–421
Charrin S, Manie S, Thiele C, Billard M, Gerlier D, Boucheix C, Rubinstein E (2003b) A physical and functional link between cholesterol and tetraspanins. Eur J Immunol 33:2479–2489
Charrin S, le Naour F, Silvie O, Milhiet PE, Boucheix C, Rubinstein E (2009a) Lateral organization of membrane proteins: tetraspanins spin their web. Biochem J 420:133–154
Charrin S, Yalaoui S, Bartosch B, Cocquerel L, Franetich JF, Boucheix C, Mazier D, Rubinstein E, Silvie O (2009b) The Ig domain protein CD9P-1 down-regulates CD81 ability to support Plasmodium yoelii infection. J Biol Chem 284:31572–31578
Ciccaglione AR, Costantino A, Marcantonio C, Equestre M, Geraci A, Rapicetta M (2001) Mutagenesis of hepatitis C virus E1 protein affects its membrane-permeabilizing activity. J Gen Virol 82:2243–2250
Ciczora Y, Callens N, Montpellier C, Bartosch B, Cosset FL, Op de Beeck A, Dubuisson J (2005) Contribution of the charged residues of hepatitis C virus glycoprotein E2 transmembrane domain to the functions of the E1E2 heterodimer. J Gen Virol 86:2793–2798
Clark KL, Zeng Z, Langford AL, Bowen SM, Todd SC (2001) PGRL is a major CD81-associated protein on lymphocytes and distinguishes a new family of cell surface proteins. J Immunol 167:5115–5121
Cocquerel L, Meunier JC, Pillez A, Wychowski C, Dubuisson J (1998) A retention signal necessary and sufficient for endoplasmic reticulum localization maps to the transmembrane domain of hepatitis C virus glycoprotein E2. J Virol 72:2183–2191
Cocquerel L, Duvet S, Meunier JC, Pillez A, Cacan R, Wychowski C, Dubuisson J (1999) The transmembrane domain of hepatitis C virus glycoprotein E1 is a signal for static retention in the endoplasmic reticulum. J Virol 73:2641–2649
Cocquerel L, Wychowski C, Minner F, Penin F, Dubuisson J (2000) Charged residues in the transmembrane domains of hepatitis C virus glycoproteins play a major role in the processing, subcellular localization, and assembly of these envelope proteins. J Virol 74:3623–3633
Cocquerel L, Meunier JC, Op de Beeck A, Bonte D, Wychowski C, Dubuisson J (2001) Coexpression of hepatitis C virus envelope proteins E1 and E2 in cis improves the stability of membrane insertion of E2. J Gen Virol 82:1629–1635
Cocquerel L, Op De Beeck A, Lambot M, Roussel J, Delgrange D, Pillez A, Wychowski C, Penin F, Dubuisson J (2002) Topological changes in the transmembrane domains of hepatitis C virus envelope glycoproteins. EMBO J 21:2893–2902
Cocquerel L, Kuo CC, Dubuisson J, Levy S (2003a) CD81-dependent binding of hepatitis C virus E1E2 heterodimers. J Virol 77:10677–10683
Cocquerel L, Quinn ER, Flint M, Hadlock KG, Foung SK, Levy S (2003b) Recognition of native hepatitis C virus E1E2 heterodimers by a human monoclonal antibody. J Virol 77:1604–1609
Cocquerel L, Voisset C, Dubuisson J (2006) Hepatitis C virus entry: potential receptors and their biological functions. J Gen Virol 87:1075–1084
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:e1000702
Connelly MA, Williams DL (2004) Scavenger receptor BI: a scavenger receptor with a mission to transport high density lipoprotein lipids. Curr Opin Lipidol 15:287–295
Coppi A, Pinzon-Ortiz C, Hutter C, Sinnis P (2005) The Plasmodium circumsporozoite protein is proteolytically processed during cell invasion. J Exp Med 201:27–33
Coppi A, Tewari R, Bishop JR, Bennett BL, Lawrence R, Esko JD, Billker O, Sinnis P (2007) Heparan sulfate proteoglycans provide a signal to Plasmodium sporozoites to stop migrating and productively invade host cells. Cell Host Microbe 2:316–327
Cormier EG, Tsamis F, Kajumo F, Durso RJ, Gardner JP, Dragic T (2004) CD81 is an entry coreceptor for hepatitis C virus. Proc Natl Acad Sci USA 101:7270–7274
Coyne CB, Bergelson JM (2006) Virus-induced Abl and Fyn kinase signals permit coxsackie virus entry through epithelial tight junctions. Cell 124:119–131
Crotta S, Stilla A, Wack A, D’Andrea A, Nuti S, D’Oro U, Mosca M, Filliponi F, Brunetto RM, Bonino F, Abrignani S, Valiante NM (2002) Inhibition of natural killer cells through engagement of CD81 by the major hepatitis C virus envelope protein. J Exp Med 195:35–41
Crotta S, Ronconi V, Ulivieri C, Baldari CT, Valiante NM, Abrignani S, Wack A (2006) Cytoskeleton rearrangement induced by tetraspanin engagement modulates the activation of T and NK cells. Eur J Immunol 36:919–929
Dhillon S, Witteveldt J, Gatherer D, Owsianka AM, Zeisel MB, Zahid MN, Rychlowska M, Foung SK, Baumert TF, Angus AG, Patel AH (2010) Mutations within a conserved region of the hepatitis C virus E2 glycoprotein that influence virus-receptor interactions and sensitivity to neutralizing antibodies. J Virol 84:5494–5507
Dorner M, Horwitz JA, Robbins JB, Barry WT, Feng Q, Mu K, Jones CT, Schoggins JW, Catanese MT, Burton DR, Law M, Rice CM, Ploss A (2011) A genetically humanized mouse model for hepatitis C virus infection. Nature 474:208–211
Dreux M, Boson B, Ricard-Blum S, Molle J, Lavillette D, Bartosch B, Pecheur EI, Cosset FL (2007) The exchangeable apolipoprotein ApoC-I promotes membrane fusion of hepatitis C virus. J Biol Chem 282:32357–32369
Dreux M, Dao Thi VL, Fresquet J, Guerin M, Julia Z, Verney G, Durantel D, Zoulim F, Lavillette D, Cosset FL, Bartosch B (2009) Receptor complementation and mutagenesis reveal SR-BI as an essential HCV entry factor and functionally imply its intra- and extra-cellular domains. PLoS Pathog 5:e1000310
Drummer HE, Wilson KA, Poumbourios P (2002) Identification of the hepatitis C virus E2 glycoprotein binding site on the large extracellular loop of CD81. J Virol 76:11143–11147
Drummer HE, Maerz A, Poumbourios P (2003) Cell surface expression of functional hepatitis C virus E1 and E2 glycoproteins. FEBS Lett 546:385–390
Drummer HE, Wilson KA, Poumbourios P (2005) Determinants of CD81 dimerization and interaction with hepatitis C virus glycoprotein E2. Biochem Biophys Res Commun 328:251–257
Drummer HE, Boo I, Maerz AL, Poumbourios P (2006) A conserved Gly436-Trp-Leu-Ala-Gly-Leu-Phe-Tyr motif in hepatitis C virus glycoprotein E2 is a determinant of CD81 binding and viral entry. J Virol 80:7844–7853
Drummer HE, Boo I, Poumbourios P (2007) Mutagenesis of a conserved fusion peptide-like motif and membrane-proximal heptad-repeat region of hepatitis C virus glycoprotein E1. J Gen Virol 88:1144–1148
Dubuisson J, Rice CM (1996) Hepatitis C virus glycoprotein folding: disulfide bond formation and association with calnexin. J Virol 70:778–786
Duvet S, Cocquerel L, Pillez A, Cacan R, Verbert A, Moradpour D, Wychowski C, Dubuisson J (1998) Hepatitis C virus glycoprotein complex localization in the endoplasmic reticulum involves a determinant for retention and not retrieval. J Biol Chem 273:32088–32095
Evans MJ, von Hahn T, Tscherne DM, Syder AJ, Panis M, Wolk 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 446:801–805
Falkowska E, Kajumo F, Garcia E, Reinus J, Dragic T (2007) Hepatitis C virus envelope glycoprotein E2 glycans modulate entry, CD81 binding, and neutralization. J Virol 81:8072–8079
Flint M, McKeating JA (1999) The C-terminal region of the hepatitis C virus E1 glycoprotein confers localization within the endoplasmic reticulum. J Gen Virol 80:1943–1947
Flint M, Maidens C, Loomis-Price LD, Shotton C, Dubuisson J, Monk P, Higginbottom A, Levy S, McKeating JA (1999a) Characterization of hepatitis C virus E2 glycoprotein interaction with a putative cellular receptor, CD81. J Virol 73:6235–6244
Flint M, Thomas JM, Maidens CM, Shotton C, Levy S, Barclay WS, McKeating JA (1999b) Functional analysis of cell surface-expressed hepatitis C virus E2 glycoprotein. J Virol 73:6782–6790
Flint M, von Hahn T, Zhang J, Farquhar M, Jones CT, Balfe P, Rice CM, McKeating JA (2006) Diverse CD81 proteins support hepatitis C virus infection. J Virol 80:11331–11342
Fofana I, Krieger SE, Grunert F, Glauben S, Xiao F, Fafi-Kremer S, Soulier E, Royer C, Thumann C, Mee CJ, McKeating JA, Dragic T, Pessaux P, Stoll-Keller F, Schuster C, Thompson J, Baumert TF (2010) Monoclonal anti-claudin 1 antibodies prevent hepatitis C virus infection of primary human hepatocytes. Gastroenterology 139(3):953–964, 964 e951-954
Forns X, Allander T, Rohwer-Nutter P, Bukh J (2000a) Characterization of modified hepatitis C virus E2 proteins expressed on the cell surface. Virology 274:75–85
Forns X, Thimme R, Govindarajan S, Emerson SU, Purcell RH, Chisari FV, Bukh J (2000b) Hepatitis C virus lacking the hypervariable region 1 of the second envelope protein is infectious and causes acute resolving or persistent infection in chimpanzees. Proc Natl Acad Sci USA 97:13318–13323
Fournier C, Sureau C, Coste J, Ducos J, Pageaux G, Larrey D, Domergue J, Maurel P (1998) In vitro infection of adult normal human hepatocytes in primary culture by hepatitis C virus. J Gen Virol 79:2367–2374
Frevert U, Sinnis P, Cerami C, Shreffler W, Takacs B, Nussenzweig V (1993) Malaria circumsporozoite protein binds to heparan sulfate proteoglycans associated with the surface membrane of hepatocytes. J Exp Med 177:1287–1298
Frevert U, Sinnis P, Esko JD, Nussenzweig V (1996) Cell surface glycosaminoglycans are not obligatory for Plasmodium berghei sporozoite invasion in vitro. Mol Biochem Parasitol 76:257–266
Frevert U, Engelmann S, Zougbede S, Stange J, Ng B, Matuschewski K, Liebes L, Yee H (2005) Intravital observation of Plasmodium berghei sporozoite infection of the liver. PLoS Biol 3:e192
Gantt S, Persson C, Rose K, Birkett AJ, Abagyan R, Nussenzweig V (2000) Antibodies against thrombospondin-related anonymous protein do not inhibit Plasmodium sporozoite infectivity in vivo. Infect Immun 68:3667–3673
Garry RF, Dash S (2003) Proteomics computational analyses suggest that hepatitis C virus E1 and pestivirus E2 envelope glycoproteins are truncated class II fusion proteins. Virology 307:255–265
Gastaminza P, Cheng G, Wieland S, Zhong J, Liao W, Chisari FV (2008) Cellular determinants of hepatitis C virus assembly, maturation, degradation, and secretion. J Virol 82:2120–2129
Germi R, Crance JM, Garin D, Guimet J, Lortat-Jacob H, Ruigrok RW, Zarski JP, Drouet E (2002) Cellular glycosaminoglycans and low density lipoprotein receptor are involved in hepatitis C virus adsorption. J Med Virol 68:206–215
Goffard A, Callens N, Bartosch B, Wychowski C, Cosset FL, Montpellier C, Dubuisson J (2005) Role of N-linked glycans in the functions of hepatitis C virus envelope glycoproteins. J Virol 79:8400–8409
Gottwein JM, Scheel TK, 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 49:364–377
Grove J, Huby T, Stamataki Z, Vanwolleghem T, Meuleman P, Farquhar M, Schwarz A, Moreau M, Owen JS, Leroux-Roels G, Balfe P, McKeating JA (2007) Scavenger receptor BI and BII expression levels modulate hepatitis C virus infectivity. J Virol 81:3162–3169
Haid S, Pietschmann T, Pecheur EI (2009) Low pH-dependent hepatitis C virus membrane fusion depends on E2 integrity, target lipid composition, and density of virus particles. J Biol Chem 284:17657–17667
Harris HJ, Farquhar MJ, Mee CJ, Davis C, Reynolds GM, Jennings A, Hu K, Yuan F, Deng H, Hubscher SG, Han JH, Balfe P, McKeating JA (2008) CD81 and claudin 1 coreceptor association: role in hepatitis C virus entry. J Virol 82:5007–5020
Harris HJ, Davis C, Mullins JG, Hu K, Goodall M, Farquhar MJ, Mee CJ, McCaffrey K, Young S, Drummer H, Balfe P, McKeating JA (2010) Claudin association with CD81 defines hepatitis C virus entry. J Biol Chem 285:21092–21102
Hartsock A, Nelson WJ (2008) Adherens and tight junctions: structure, function and connections to the actin cytoskeleton. Biochim Biophys Acta 1778:660–669
Hauri AM, Armstrong GL, Hutin YJ (2004) The global burden of disease attributable to contaminated injections given in health care settings. Int J STD AIDS 15:7–16
Heiskala M, Peterson PA, Yang Y (2001) The roles of claudin superfamily proteins in paracellular transport. Traffic 2:93–98
Helle F, Goffard A, Morel V, Duverlie G, McKeating J, Keck ZY, Foung S, Penin F, Dubuisson J, Voisset C (2007) The neutralizing activity of anti-hepatitis C virus antibodies is modulated by specific glycans on the E2 envelope protein. J Virol 81:8101–8111
Helle F, Vieyres G, Elkrief L, Popescu CI, Wychowski C, Descamps V, Castelain S, Roingeard P, Duverlie G, Dubuisson J (2010) Role of N-linked glycans in the functions of hepatitis C virus envelope proteins incorporated into infectious virions. J Virol 84:11905–11915
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 74:3642–3649
Hollingdale MR, Leland P, Schwartz AL (1983) In vitro cultivation of the exoerythrocytic stage of Plasmodium berghei in a hepatoma cell line. Am J Trop Med Hyg 32:682–684
Hollingdale MR, Nardin EH, Tharavanij S, Schwartz AL, Nussenzweig RS (1984) Inhibition of entry of Plasmodium falciparum and P. vivax sporozoites into cultured cells; an in vitro assay of protective antibodies. J Immunol 132:909–913
Hsu M, Zhang J, Flint M, Logvinoff C, Cheng-Mayer C, Rice CM, McKeating JA (2003) Hepatitis C virus glycoproteins mediate pH-dependent cell entry of pseudotyped retroviral particles. Proc Natl Acad Sci USA 100:7271–7276
Huang H, Sun F, Owen DM, Li W, Chen Y, Gale M Jr, Ye J (2007) Hepatitis C virus production by human hepatocytes dependent on assembly and secretion of very low-density lipoproteins. Proc Natl Acad Sci USA 104:5848–5853
Iacovacci S, Sargiacomo M, Parolini I, Ponzetto A, Peschle C, Carloni G (1993) Replication and multiplication of hepatitis C virus genome in human foetal liver cells. Res Virol 144:275–279
Imai T, Yoshie O (1993) C33 antigen and M38 antigen recognized by monoclonal antibodies inhibitory to syncytium formation by human T cell leukemia virus type 1 are both members of the transmembrane 4 superfamily and associate with each other and with CD4 or CD8 in T cells. J Immunol 151:6470–6481
Ishino T, Chinzei Y, Yuda M (2005) Two proteins with 6-cys motifs are required for malarial parasites to commit to infection of the hepatocyte. Mol Microbiol 58:1264–1275
Janse CJ, Ramesar J, Waters AP (2006) High-efficiency transfection and drug selection of genetically transformed blood stages of the rodent malaria parasite Plasmodium berghei. Nat Protoc 1:346–356
Jiang J, Luo G (2009) Apolipoprotein E but not B is required for the formation of infectious hepatitis C virus particles. J Virol 83:12680–12691
Jones CT, Catanese MT, Law LM, Khetani SR, Syder AJ, Ploss A, Oh TS, Schoggins JW, MacDonald MR, Bhatia SN, Rice CM (2010) Real-time imaging of hepatitis C virus infection using a fluorescent cell-based reporter system. Nat Biotechnol 28:167–171
Kapadia SB, Barth H, Baumert T, McKeating JA, Chisari FV (2007) Initiation of hepatitis C virus infection is dependent on cholesterol and cooperativity between CD81 and scavenger receptor B Type I. J Virol 81:374–383
Kappe S, Bruderer T, Gantt S, Fujioka H, Nussenzweig V, Menard R (1999) Conservation of a gliding motility and cell invasion machinery in Apicomplexan parasites. J Cell Biol 147:937–944
Keck ZY, Saha A, Xia J, Wang Y, Lau P, Krey T, Rey FA, Foung SK (2011) Mapping a region of hepatitis C virus E2 that is responsible for escape from neutralizing antibodies and a core CD81-binding region that does not tolerate neutralization escape mutations. J Virol 85:10451–10463
Kitadokoro K, Bordo D, Galli G, Petracca R, Falugi F, Abrignani S, Grandi G, Bolognesi M (2001) CD81 extracellular domain 3D structure: insight into the tetraspanin superfamily structural motifs. EMBO J 20:12–18
Koutsoudakis G, Kaul A, Steinmann E, Kallis S, Lohmann V, Pietschmann T, Bartenschlager R (2006) Characterization of the early steps of hepatitis C virus infection by using luciferase reporter viruses. J Virol 80:5308–5320
Koutsoudakis G, Herrmann E, Kallis S, Bartenschlager R, Pietschmann T (2007) The level of CD81 cell surface expression is a key determinant for productive entry of hepatitis C virus into host cells. J Virol 81:588–598
Krey T, d’Alayer J, Kikuti CM, Saulnier A, Damier-Piolle L, Petitpas I, Johansson DX, Tawar RG, Baron B, Robert B, England P, Persson MA, Martin A, Rey FA (2010) The disulfide bonds in glycoprotein E2 of hepatitis C virus reveal the tertiary organization of the molecule. PLoS Pathog 6:e1000762
Krieger SE, Zeisel MB, Davis C, Thumann C, Harris HJ, Schnober EK, Mee C, Soulier E, Royer C, Lambotin M, Grunert F, Dao Thi VL, Dreux M, Cosset FL, McKeating JA, Schuster C, Baumert TF (2010) Inhibition of hepatitis C virus infection by anti-claudin-1 antibodies is mediated by neutralization of E2-CD81-claudin-1 associations. Hepatology 51:1144–1157
Labaied M, Harupa A, Dumpit RF, Coppens I, Mikolajczak SA, Kappe SH (2007) Plasmodium yoelii sporozoites with simultaneous deletion of P52 and P36 are completely attenuated and confer sterile immunity against infection. Infect Immun 75:3758–3768
Labonte P, Begley S, Guevin C, Asselin MC, Nassoury N, Mayer G, Prat A, Seidah NG (2009) PCSK9 impedes hepatitis C virus infection in vitro and modulates liver CD81 expression. Hepatology 50:17–24
Lavie M, Voisset C, Vu-Dac N, Zurawski V, Duverlie G, Wychowski C, Dubuisson J (2006) Serum amyloid A has antiviral activity against hepatitis C virus by inhibiting virus entry in a cell culture system. Hepatology 44:1626–1634
Lavie M, Goffard A, Dubuisson J (2007) Assembly of a functional HCV glycoprotein heterodimer. Curr Issues Mol Biol 9:71–86
Lavillette D, Tarr AW, Voisset C, Donot P, Bartosch B, Bain C, Patel AH, Dubuisson J, Ball JK, Cosset FL (2005) Characterization of host-range and cell entry properties of the major genotypes and subtypes of hepatitis C virus. Hepatology 41:265–274
Lavillette D, Bartosch B, Nourrisson D, Verney G, Cosset FL, Penin F, Pecheur EI (2006) Hepatitis C virus glycoproteins mediate low pH-dependent membrane fusion with liposomes. J Biol Chem 281:3909–3917
Lavillette D, Pecheur EI, Donot P, Fresquet J, Molle J, Corbau R, Dreux M, Penin F, Cosset FL (2007) Characterization of fusion determinants points to the involvement of three discrete regions of both E1 and E2 glycoproteins in the membrane fusion process of hepatitis C virus. J Virol 81:8752–8765
Lazaro CA, Chang M, Tang W, Campbell J, Sullivan DG, Gretch DR, Corey L, Coombs RW, Fausto N (2007) Hepatitis C virus replication in transfected and serum-infected cultured human fetal hepatocytes. Am J Pathol 170:478–489
Lemon SM, Walker C, Alter MJ, Yi M (2007) Hepatitis C virus. In: Knipe DM, Howley PM (eds) Fields virology, 5th edn. Lippincott Williams & Wilkins, Philadelphia, pp 1253–1304
Levy S, Shoham T (2005a) Protein-protein interactions in the tetraspanin web. Physiology (Bethesda) 20:218–224
Levy S, Shoham T (2005b) The tetraspanin web modulates immune-signalling complexes. Nat Rev Immunol 5:136–148
Li HF, Huang CH, Ai LS, Chuang CK, Chen SS (2009) Mutagenesis of the fusion peptide-like domain of hepatitis C virus E1 glycoprotein: involvement in cell fusion and virus entry. J Biomed Sci 16:89
Lindenbach BD, Evans MJ, Syder AJ, Wolk B, Tellinghuisen TL, Liu CC, Maruyama T, Hynes RO, Burton DR, McKeating JA, Rice CM (2005) Complete replication of hepatitis C virus in cell culture. Science 309:623–626
Lindenbach BD, Meuleman P, Ploss A, Vanwolleghem T, Syder AJ, McKeating JA, Lanford RE, Feinstone SM, Major ME, Leroux-Roels G, Rice CM (2006) Cell culture-grown hepatitis C virus is infectious in vivo and can be recultured in vitro. Proc Natl Acad Sci USA 103:3805–3809
Lindenbach BD, Thiel HJ, Rice CM (2007) Flaviviridae: the viruses and their replication. Lippincott Williams & Wilkins, Philadelphia
Liu S, Yang W, Shen L, Turner JR, Coyne CB, Wang T (2009) Tight junction proteins claudin-1 and occludin control hepatitis C virus entry and are downregulated during infection to prevent superinfection. J Virol 83:2011–2014
Lopez D (2008) PCSK9: an enigmatic protease. Biochim Biophys Acta 1781:184–191
Maecker HT, Levy S (1997) Normal lymphocyte development but delayed humoral immune response in CD81-null mice. J Exp Med 185:1505–1510
Maillard P, Huby T, Andreo U, Moreau M, Chapman J, Budkowska A (2006) The interaction of natural hepatitis C virus with human scavenger receptor SR-BI/Cla1 is mediated by ApoB-containing lipoproteins. FASEB J 20:735–737
Manns MP, Wedemeyer H, Cornberg M (2006) Treating viral hepatitis C: efficacy, side effects, and complications. Gut 55:1350–1359
Masciopinto F, Freer G, Burgio VL, Levy S, Galli-Stampino L, Bendinelli M, Houghton M, Abrignani S, Uematsu Y (2002) Expression of human CD81 in transgenic mice does not confer susceptibility to hepatitis C virus infection. Virology 304:187–196
Mazier D, Landau I, Druilhe P, Miltgen F, Guguen-Guillouzo C, Baccam D, Baxter J, Chigot JP, Gentilini M (1984) Cultivation of the liver forms of Plasmodium vivax in human hepatocytes. Nature 307:367–369
Mazier D, Beaudoin RL, Mellouk S, Druilhe P, Texier B, Trosper J, Miltgen F, Landau I, Paul C, Brandicourt O et al (1985) Complete development of hepatic stages of Plasmodium falciparum in vitro. Science 227:440–442
McKeating JA, Zhang LQ, Logvinoff C, Flint M, Zhang J, Yu J, Butera D, Ho DD, Dustin LB, Rice CM, Balfe P (2004) Diverse hepatitis C virus glycoproteins mediate viral infection in a CD81-dependent manner. J Virol 78:8496–8505
Mee CJ, Grove J, Harris HJ, Hu K, Balfe P, McKeating JA (2008) Effect of cell polarization on hepatitis C virus entry. J Virol 82:461–470
Mee CJ, Harris HJ, Farquhar MJ, Wilson G, Reynolds G, Davis C, van ISC, Balfe P, McKeating JA (2009) Polarization restricts hepatitis C virus entry into HepG2 hepatoma cells. J Virol 83:6211–6221
Meertens L, Bertaux C, Dragic T (2006) Hepatitis C virus entry requires a critical post internalization step and delivery to early endosomes via clathrin-coated vesicles. J Virol 80:11571–11578
Meertens L, Bertaux C, Cukierman L, Cormier E, Lavillette D, Cosset FL, Dragic T (2008) The tight junction proteins claudin-1, -6, and -9 are entry cofactors for hepatitis C virus. J Virol 82:3555–3560
Menard R, Janse C (1997) Gene targeting in malaria parasites. Methods (San Diego, Calif) 13:148–157
Meola A, Sbardellati A, Bruni Ercole B, Cerretani M, Pezzanera M, Ceccacci A, Vitelli A, Levy S, Nicosia A, Traboni C, McKeating J, Scarselli E (2000) Binding of hepatitis C virus E2 glycoprotein to CD81 does not correlate with species permissiveness to infection. J Virol 74:5933–5938
Meuleman P, Hesselgesser J, Paulson M, Vanwolleghem T, Desombere I, Reiser H, Leroux-Roels G (2008) Anti-CD81 antibodies can prevent a hepatitis C virus infection in vivo. Hepatology 48:1761–1768
Meunier JC, Fournillier A, Choukhi A, Cahour A, Cocquerel L, Dubuisson J, Wychowski C (1999) Analysis of the glycosylation sites of hepatitis C virus (HCV) glycoprotein E1 and the influence of E1 glycans on the formation of the HCV glycoprotein complex. J Gen Virol 80:887–896
Meunier JC, Engle RE, Faulk K, Zhao M, Bartosch B, Alter H, Emerson SU, Cosset FL, Purcell RH, Bukh J (2005) Evidence for cross-genotype neutralization of hepatitis C virus pseudo-particles and enhancement of infectivity by apolipoprotein C1. Proc Natl Acad Sci USA 102:4560–4565
Meunier JC, Russell RS, Engle RE, Faulk KN, Purcell RH, Emerson SU (2008) Apolipoprotein c1 association with hepatitis C virus. J Virol 82:9647–9656
Michalak JP, Wychowski C, Choukhi A, Meunier JC, Ung S, Rice CM, Dubuisson J (1997) Characterization of truncated forms of hepatitis C virus glycoproteins. J Gen Virol 78:2299–2306
Molina S, Castet V, Fournier-Wirth C, Pichard-Garcia L, Avner R, Harats D, Roitelman J, Barbaras R, Graber P, Ghersa P, Smolarsky M, Funaro A, Malavasi F, Larrey D, Coste J, Fabre JM, Sa-Cunha A, Maurel P (2007) The low-density lipoprotein receptor plays a role in the infection of primary human hepatocytes by hepatitis C virus. J Hepatol 46:411–419
Molina S, Castet V, Pichard-Garcia L, Wychowski C, Meurs E, Pascussi JM, Sureau C, Fabre JM, Sacunha A, Larrey D, Dubuisson J, Coste J, McKeating J, Maurel P, Fournier-Wirth C (2008) Serum-derived hepatitis C virus infection of primary human hepatocytes is tetraspanin CD81 dependent. J Virol 82:569–574
Monazahian M, Bohme I, Bonk S, Koch A, Scholz C, Grether S, Thomssen R (1999) Low density lipoprotein receptor as a candidate receptor for hepatitis C virus. J Med Virol 57:223–229
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 286:13954–13965
Morikawa K, Zhao Z, Date T, Miyamoto M, Murayama A, Akazawa D, Tanabe J, Sone S, Wakita T (2007) The roles of CD81 and glycosaminoglycans in the adsorption and uptake of infectious HCV particles. J Med Virol 79:714–723
Mota MM, Rodriguez A (2000) Plasmodium yoelii: efficient in vitro invasion and complete development of sporozoites in mouse hepatic cell lines. Exp Parasitol 96:257–259
Mota MM, Pradel G, Vanderberg JP, Hafalla JC, Frevert U, Nussenzweig RS, Nussenzweig V, Rodriguez A (2001) Migration of Plasmodium sporozoites through cells before infection. Science 291:141–144
Mueller AK, Camargo N, Kaiser K, Andorfer C, Frevert U, Matuschewski K, Kappe SH (2005) Plasmodium liver stage developmental arrest by depletion of a protein at the parasite-host interface. Proc Natl Acad Sci USA 102:3022–3027
Nakajima H, Cocquerel L, Kiyokawa N, Fujimoto J, Levy S (2005) Kinetics of HCV envelope proteins’ interaction with CD81 large extracellular loop. Biochem Biophys Res Commun 328:1091–1100
Nakano I, Fukuda Y, Katano Y, Hayakawa T (1999) Conformational epitopes detected by cross-reactive antibodies to envelope 2 glycoprotein of the hepatitis C virus. J Infect Dis 180:1328–1333
Nielsen SU, Bassendine MF, Burt AD, Martin C, Pumeechockchai W, Toms GL (2006) Association between hepatitis C virus and very-low-density lipoprotein (VLDL)/LDL analyzed in iodixanol density gradients. J Virol 80:2418–2428
Op De Beeck A, Montserret R, Duvet S, Cocquerel L, Cacan R, Barberot B, Le Maire M, Penin F, Dubuisson J (2000) The transmembrane domains of hepatitis C virus envelope glycoproteins E1 and E2 play a major role in heterodimerization. J Biol Chem 275:31428–31437
Op De Beeck A, Voisset C, Bartosch B, Ciczora Y, Cocquerel L, Keck Z, Foung S, Cosset FL, Dubuisson J (2004) Characterization of functional hepatitis C virus envelope glycoproteins. J Virol 78:2994–3002
Oren R, Takahashi S, Doss C, Levy R, Levy S (1990) TAPA-1, the target of an antiproliferative antibody, defines a new family of transmembrane proteins. Mol Cell Biol 10:4007–4015
Owen DM, Huang H, Ye J, Gale M Jr (2009) Apolipoprotein E on hepatitis C virion facilitates infection through interaction with low-density lipoprotein receptor. Virology 394:99–108
Owsianka A, Clayton RF, Loomis-Price LD, McKeating JA, Patel AH (2001) Functional analysis of hepatitis C virus E2 glycoproteins and virus-like particles reveals structural dissimilarities between different forms of E2. J Gen Virol 82:1877–1883
Owsianka AM, Timms JM, Tarr AW, Brown RJ, 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 80:8695–8704
Owsianka AM, Tarr AW, Keck ZY, Li TK, Witteveldt J, Adair R, Foung SK, Ball JK, Patel AH (2008) Broadly neutralizing human monoclonal antibodies to the hepatitis C virus E2 glycoprotein. J Gen Virol 89:653–659
Pacheco B, Gomez-Gutierrez J, Yelamos B, Delgado C, Roncal F, Albar JP, Peterson D, Gavilanes F (2006) Membrane-perturbing properties of three peptides corresponding to the ectodomain of hepatitis C virus E2 envelope protein. Biochim Biophys Acta 1758:755–763
Patel AH, Wood J, Penin F, Dubuisson J, McKeating JA (2000) Construction and characterization of chimeric hepatitis C virus E2 glycoproteins: analysis of regions critical for glycoprotein aggregation and CD81 binding. J Gen Virol 81:2873–2883
Patel J, Patel AH, McLauchlan J (2001) The transmembrane domain of the hepatitis C virus E2 glycoprotein is required for correct folding of the E1 glycoprotein and native complex formation. Virology 279:58–68
Perez-Berna AJ, Moreno MR, Guillen J, Bernabeu A, Villalain J (2006) The membrane-active regions of the hepatitis C virus E1 and E2 envelope glycoproteins. Biochemistry 45:3755–3768
Perez-Berna AJ, Bernabeu A, Moreno MR, Guillen J, Villalain J (2008a) The pre-transmembrane region of the HCV E1 envelope glycoprotein: interaction with model membranes. Biochim Biophys Acta 1778:2069–2080
Perez-Berna AJ, Guillen J, Moreno MR, Gomez-Sanchez AI, Pabst G, Laggner P, Villalain J (2008b) Interaction of the most membranotropic region of the HCV E2 envelope glycoprotein with membranes. Biophysical characterization. Biophys J 94:4737–4750
Perez-Berna AJ, Pabst G, Laggner P, Villalain J (2009) Biophysical characterization of the fusogenic region of HCV envelope glycoprotein E1. Biochim Biophys Acta 1788:2183–2193
Petracca R, Falugi F, Galli G, Norais N, Rosa D, Campagnoli S, Burgio V, Di Stasio E, Giardina B, Houghton M, Abrignani S, Grandi G (2000) Structure-function analysis of hepatitis C virus envelope-CD81 binding. J Virol 74:4824–4830
Pileri P, Uematsu Y, Campagnoli S, Galli G, Falugi F, Petracca R, Weiner AJ, Houghton M, Rosa D, Grandi G, Abrignani S (1998) Binding of hepatitis C virus to CD81. Science 282:938–941
Pinzon-Ortiz C, Friedman J, Esko J, Sinnis P (2001) The binding of the circumsporozoite protein to cell surface heparan sulfate proteoglycans is required for plasmodium sporozoite attachment to target cells. J Biol Chem 276:26784–26791
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 457:882–886
Ploss A, Khetani SR, Jones CT, Syder AJ, Trehan K, Gaysinskaya VA, Mu K, Ritola K, Rice CM, Bhatia SN (2010) Persistent hepatitis C virus infection in microscale primary human hepatocyte cultures. Proc Natl Acad Sci USA 107:3141–3145
Podevin P, Carpentier A, Pene V, Aoudjehane L, Carriere M, Zaidi S, Hernandez C, Calle V, Meritet JF, Scatton O, Dreux M, Cosset FL, Wakita T, Bartenschlager R, Demignot S, Conti F, Rosenberg AR, Calmus Y (2010) Production of infectious hepatitis C virus in primary cultures of human adult hepatocytes. Gastroenterology 139:1355–1364
Ponnudurai T, Meuwissen JH, Leeuwenberg AD, Verhave JP, Lensen AH (1982) The production of mature gametocytes of Plasmodium falciparum in continuous cultures of different isolates infective to mosquitoes. Trans R Soc Trop Med Hyg 76:242–250
Popescu CI, Dubuisson J (2009) Role of lipid metabolism in hepatitis C virus assembly and entry. Biol Cell 102:63–74
Potel J, Rassam P, Montpellier C, Kaestner L, Werkmeister E, Tews BA, Couturier C, Popescu CI, Baumert T, Rubinstein E, Dubuisson J, Milhiet P-E, Cocquerel L (2013) EWI-2wint promotes CD81 clustering that abrogates Hepatitis C Virus entry. Cell Microbiol (in press)
Roccasecca R, Ansuini H, Vitelli A, Meola A, Scarselli E, Acali S, Pezzanera M, Ercole BB, McKeating J, Yagnik A, Lahm A, Tramontano A, Cortese R, Nicosia A (2003) Binding of the hepatitis C virus E2 glycoprotein to CD81 is strain specific and is modulated by a complex interplay between hypervariable regions 1 and 2. J Virol 77:1856–1867
Rocha-Perugini V, Montpellier C, Delgrange D, Wychowski C, Helle F, Pillez A, Drobecq H, Le Naour F, Charrin S, Levy S, Rubinstein E, Dubuisson J, Cocquerel L (2008) The CD81 partner EWI-2wint inhibits hepatitis C virus entry. PLoS One 3:e1866
Rocha-Perugini V, Lavie M, Delgrange D, Canton J, Pillez A, Potel J, Lecoeur C, Rubinstein E, Dubuisson J, Wychowski C, Cocquerel L (2009) The association of CD81 with tetraspanin-enriched microdomains is not essential for Hepatitis C virus entry. BMC Microbiol 9:111
Rodrigues CD, Hannus M, Prudencio M, Martin C, Goncalves LA, Portugal S, Epiphanio S, Akinc A, Hadwiger P, Jahn-Hofmann K, Rohl I, van Gemert GJ, Franetich JF, Luty AJ, Sauerwein R, Mazier D, Koteliansky V, Vornlocher HP, Echeverri CJ, Mota MM (2008) Host scavenger receptor SR-BI plays a dual role in the establishment of malaria parasite liver infection. Cell Host Microbe 4:271–282
Rothwangl KB, Manicassamy B, Uprichard SL, Rong L (2008) Dissecting the role of putative CD81 binding regions of E2 in mediating HCV entry: putative CD81 binding region 1 is not involved in CD81 binding. Virol J 5:46
Rubinstein E, Le Naour F, Lagaudriere-Gesbert C, Billard M, Conjeaud H, Boucheix C (1996) CD9, CD63, CD81, and CD82 are components of a surface tetraspan network connected to HLA-DR and VLA integrins. Eur J Immunol 26:2657–2665
Rumin S, Berthillon P, Tanaka E, Kiyosawa K, Trabaud MA, Bizollon T, Gouillat C, Gripon P, Guguen-Guillouzo C, Inchauspe G, Trepo C (1999) Dynamic analysis of hepatitis C virus replication and quasispecies selection in long-term cultures of adult human hepatocytes infected in vitro. J Gen Virol 80(Pt 11):3007–3018
Russell RS, Kawaguchi K, Meunier JC, Takikawa S, Faulk K, Bukh J, Purcell RH, Emerson SU (2009) Mutational analysis of the hepatitis C virus E1 glycoprotein in retroviral pseudoparticles and cell-culture-derived H77/JFH1 chimeric infectious virus particles. J Viral Hepat 16:621–632
Sala-Valdes M, Ursa A, Charrin S, Rubinstein E, Hemler ME, Sanchez-Madrid F, Yanez-Mo M (2006) EWI-2 and EWI-F link the tetraspanin web to the actin cytoskeleton through their direct association with ezrin-radixin-moesin proteins. J Biol Chem 281:19665–19675
Santos JM, Lebrun M, Daher W, Soldati D, Dubremetz JF (2009) Apicomplexan cytoskeleton and motors: key regulators in morphogenesis, cell division, transport and motility. Int J Parasitol 39:153–162
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 21:5017–5025
Schwarz AK, Grove J, Hu K, Mee CJ, Balfe P, McKeating JA (2009) Hepatoma cell density promotes claudin-1 and scavenger receptor BI expression and hepatitis C virus internalization. J Virol 83:12407–12414
Seigneuret M (2006) Complete predicted three-dimensional structure of the facilitator transmembrane protein and hepatitis C virus receptor CD81: conserved and variable structural domains in the tetraspanin superfamily. Biophys J 90:212–227
Selby MJ, Glazer E, Masiarz F, Houghton M (1994) Complex processing and protein: protein interactions in the E2:NS2 region of HCV. Virology 204:114–122
Sharma NR, Mateu G, Dreux M, Grakoui A, Cosset FL, Melikyan GB (2011) Hepatitis C virus is primed by CD81 protein for low pH-dependent fusion. J Biol Chem 286:30361–30376
Shaw ML, McLauchlan J, Mills PR, Patel AH, McCruden EA (2003) Characterisation of the differences between hepatitis C virus genotype 3 and 1 glycoproteins. J Med Virol 70:361–372
Silver DL, Wang N, Xiao X, Tall AR (2001) High density lipoprotein (HDL) particle uptake mediated by scavenger receptor class B type 1 results in selective sorting of HDL cholesterol from protein and polarized cholesterol secretion. J Biol Chem 276:25287–25293
Silvie O, Rubinstein E, Franetich JF, Prenant M, Belnoue E, Renia L, Hannoun L, Eling W, Levy S, Boucheix C, Mazier D (2003) Hepatocyte CD81 is required for Plasmodium falciparum and Plasmodium yoelii sporozoite infectivity. Nat Med 9:93–96
Silvie O, Franetich JF, Charrin S, Mueller MS, Siau A, Bodescot M, Rubinstein E, Hannoun L, Charoenvit Y, Kocken CH, Thomas AW, Van Gemert GJ, Sauerwein RW, Blackman MJ, Anders RF, Pluschke G, Mazier D (2004) A role for apical membrane antigen 1 during invasion of hepatocytes by Plasmodium falciparum sporozoites. J Biol Chem 279:9490–9496
Silvie O, Charrin S, Billard M, Franetich JF, Clark KL, van Gemert GJ, Sauerwein RW, Dautry F, Boucheix C, Mazier D, Rubinstein E (2006a) Cholesterol contributes to the organization of tetraspanin-enriched microdomains and to CD81-dependent infection by malaria sporozoites. J Cell Sci 119:1992–2002
Silvie O, Greco C, Franetich JF, Dubart-Kupperschmitt A, Hannoun L, van Gemert GJ, Sauerwein RW, Levy S, Boucheix C, Rubinstein E, Mazier D (2006b) Expression of human CD81 differently affects host cell susceptibility to malaria sporozoites depending on the Plasmodium species. Cell Microbiol 8:1134–1146
Silvie O, Franetich JF, Boucheix C, Rubinstein E, Mazier D (2007) Alternative invasion pathways for Plasmodium berghei sporozoites. Int J Parasitol 37:173–182
Slater-Handshy T, Droll DA, Fan X, Di Bisceglie AM, Chambers TJ (2004) HCV E2 glycoprotein: mutagenesis of N-linked glycosylation sites and its effects on E2 expression and processing. Virology 319:36–48
Snounou G, Gruner AC, Muller-Graf CD, Mazier D, Renia L (2005) The Plasmodium sporozoite survives RTS, S vaccination. Trends Parasitol 21:456–461
Stipp CS, Kolesnikova TV, Hemler ME (2001a) EWI-2 is a major CD9 and CD81 partner and member of a novel Ig protein subfamily. J Biol Chem 276:40545–40554
Stipp CS, Orlicky D, Hemler ME (2001b) FPRP, a major, highly stoichiometric, highly specific CD81- and CD9- associated protein. J Biol Chem 276:4853–4862
Strebel K, Luban J, Jeang KT (2009) Human cellular restriction factors that target HIV-1 replication. BMC Med 7:48
Tham TN, Gouin E, Rubinstein E, Boucheix C, Cossart P, Pizarro-Cerda J (2009) Tetraspanin CD81 is required for Listeria monocytogenes invasion. Infect Immun 78:204–209
Timpe JM, Stamataki Z, Jennings A, Hu K, Farquhar MJ, Harris HJ, Schwarz A, Desombere I, Roels GL, Balfe P, McKeating JA (2008) Hepatitis C virus cell-cell transmission in hepatoma cells in the presence of neutralizing antibodies. Hepatology 47:17–24
Trager W, Jensen JB (1976) Human malaria parasites in continuous culture. Science 193:673–675
Troesch M, Meunier I, Lapierre P, Lapointe N, Alvarez F, Boucher M, Soudeyns H (2006) Study of a novel hypervariable region in hepatitis C virus (HCV) E2 envelope glycoprotein. Virology 352:357–367
Tscherne DM, Jones CT, Evans MJ, Lindenbach BD, McKeating JA, Rice CM (2006) Time- and temperature-dependent activation of hepatitis C virus for low-pH-triggered entry. J Virol 80:1734–1741
van Dijk MR, Douradinha B, Franke-Fayard B, Heussler V, van Dooren MW, van Schaijk B, van Gemert GJ, Sauerwein RW, Mota MM, Waters AP, Janse CJ (2005) Genetically attenuated, P36p-deficient malarial sporozoites induce protective immunity and apoptosis of infected liver cells. Proc Natl Acad Sci USA 102:12194–12199
van Schaijk BC, Janse CJ, van Gemert GJ, van Dijk MR, Gego A, Franetich JF, van de Vegte-Bolmer M, Yalaoui S, Silvie O, Hoffman SL, Waters AP, Mazier D, Sauerwein RW, Khan SM (2008) Gene disruption of Plasmodium falciparum p52 results in attenuation of malaria liver stage development in cultured primary human hepatocytes. PLoS One 3:e3549
Vieyres G, Thomas X, Descamps V, Duverlie G, Patel AH, Dubuisson J (2010) Characterization of the envelope glycoproteins associated with infectious hepatitis C virus. J Virol 84:10159–10168
Voisset C, Callens N, Blanchard E, Op De Beeck A, Dubuisson J, Vu-Dac N (2005) High density lipoproteins facilitate hepatitis C virus entry through the scavenger receptor class B type I. J Biol Chem 280:7793–7799
Voisset C, Lavie M, Helle F, Op De Beeck A, Bilheu A, Bertrand-Michel J, Terce F, Cocquerel L, Wychowski C, Vu-Dac N, Dubuisson J (2008) Ceramide enrichment of the plasma membrane induces CD81 internalization and inhibits hepatitis C virus entry. Cell Microbiol 10:606–617
von Hahn T, Lindenbach BD, Boullier A, Quehenberger O, Paulson M, Rice CM, McKeating JA (2006) Oxidized low-density lipoprotein inhibits hepatitis C virus cell entry in human hepatoma cells. Hepatology 43:932–942
Wack A, Soldaini E, Tseng C, Nuti S, Klimpel G, Abrignani S (2001) Binding of the hepatitis C virus envelope protein E2 to CD81 provides a co-stimulatory signal for human T cells. Eur J Immunol 31:166–175
Wakita T, Pietschmann T, Kato T, Date T, Miyamoto M, Zhao Z, Murthy K, Habermann A, Krausslich HG, Mizokami M, Bartenschlager R, Liang TJ (2005) Production of infectious hepatitis C virus in tissue culture from a cloned viral genome. Nat Med 11:791–796
Washburn ML, Bility MT, Zhang L, Kovalev GI, Buntzman A, Frelinger JA, Barry W, Ploss A, Rice CM, Su L (2011) A humanized mouse model to study hepatitis C virus infection, immune response, and liver disease. Gastroenterology 140:1334–1344
Weiner AJ, Brauer R, Rosenblatt J, Richman KH, Tung J, Crawford K, Bonino F, Saracco G, Choo Q-L, Houghton M, Han JH (1991) Variable and hypervariable domains are found in the regions of HCV corresponding to the flavivirus envelope and NS1 proteins and the pestivirus envelop glycoproteins. Virology 180:842–848
Witteveldt J, Evans MJ, Bitzegeio J, Koutsoudakis G, Owsianka AM, Angus AG, Keck ZY, Foung SK, Pietschmann T, Rice CM, Patel AH (2009) CD81 is dispensable for hepatitis C virus cell-to-cell transmission in hepatoma cells. J Gen Virol 90:48–58
World Health Organization, Geneva (2009) Malaria Report 2009
Xu Z, Choi J, Yen TS, Lu W, Strohecker A, Govindarajan S, Chien D, Selby MJ, Ou J (2001) Synthesis of a novel hepatitis C virus protein by ribosomal frameshift. EMBO J 20:3840–3848
Yagnik AT, Lahm A, Meola A, Roccasecca RM, Ercole BB, Nicosia A, Tramontano A (2000) A model for the hepatitis C virus envelope glycoprotein E2. Proteins 40:355–366
Yalaoui S, Huby T, Franetich JF, Gego A, Rametti A, Moreau M, Collet X, Siau A, van Gemert GJ, Sauerwein RW, Luty AJ, Vaillant JC, Hannoun L, Chapman J, Mazier D, Froissard P (2008a) Scavenger receptor BI boosts hepatocyte permissiveness to Plasmodium infection. Cell Host Microbe 4:283–292
Yalaoui S, Zougbede S, Charrin S, Silvie O, Arduise C, Farhati K, Boucheix C, Mazier D, Rubinstein E, Froissard P (2008b) Hepatocyte permissiveness to Plasmodium infection is conveyed by a short and structurally conserved region of the CD81 large extracellular domain. PLoS Pathog 4:e1000010
Yamauchi LM, Coppi A, Snounou G, Sinnis P (2007) Plasmodium sporozoites trickle out of the injection site. Cell Microbiol 9:2093
Yang W, Qiu C, Biswas N, Jin J, Watkins SC, Montelaro RC, Coyne CB, Wang T (2008) Correlation of the tight junction-like distribution of claudin-1 to the cellular tropism of HCV. J Biol Chem 283(13):8643–8653
Zeisel MB, Koutsoudakis G, Schnober EK, Haberstroh A, Blum HE, Cosset FL, Wakita T, Jaeck D, Doffoel M, Royer C, Soulier E, Schvoerer E, Schuster C, Stoll-Keller F, Bartenschlager R, Pietschmann T, Barth H, Baumert TF (2007) Scavenger receptor class B type I is a key host factor for hepatitis C virus infection required for an entry step closely linked to CD81. Hepatology 46:1722–1731
Zhang J, Randall G, Higginbottom A, Monk P, Rice CM, McKeating JA (2004) CD81 is required for hepatitis C virus glycoprotein-mediated viral infection. J Virol 78:1448–1455
Zhang YY, Zhang BH, Ishii K, Liang TJ (2010) Novel function of CD81 in controlling hepatitis C virus replication. J Virol 84:3396–3407
Zheng A, Yuan F, Li Y, Zhu F, Hou P, Li J, Song X, Ding M, Deng H (2007) Claudin-6 and claudin-9 function as additional coreceptors for hepatitis C virus. J Virol 81:12465–12471
Zhong J, Gastaminza P, Cheng G, Kapadia S, Kato T, Burton DR, Wieland SF, Uprichard SL, Wakita T, Chisari FV (2005) Robust hepatitis C virus infection in vitro. Proc Natl Acad Sci USA 102:9294–9299
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Cocquerel, L., Silvie, O. (2013). The Role of CD81 in HCV and Plasmodium Infection. In: Berditchevski, F., Rubinstein, E. (eds) Tetraspanins. Proteins and Cell Regulation, vol 9. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-6070-7_14
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