Tetraspanins pp 345-386 | Cite as

The Role of CD81 in HCV and Plasmodium Infection

Chapter
Part of the Proteins and Cell Regulation book series (PROR, volume 9)

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

Primary Human Hepatocyte CD81 Binding Site Plasmodium Sporozoite Sporozoite Invasion 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Abbreviations

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

  1. 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 96:12766–12771PubMedCrossRefGoogle Scholar
  2. 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 81:5036–5045PubMedCrossRefGoogle Scholar
  3. 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 55:998–1007PubMedCrossRefGoogle Scholar
  4. Allander T, Forns X, Emerson SU, Purcell RH, Bukh J (2000) Hepatitis C virus envelope protein E2 binds to CD81 of tamarins. Virology 277:358–367PubMedCrossRefGoogle Scholar
  5. Aly AS, Vaughan AM, Kappe SH (2009) Malaria parasite development in the mosquito and infection of the mammalian host. Annu Rev Microbiol 63:195–221PubMedCrossRefGoogle Scholar
  6. 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 12:220–224PubMedCrossRefGoogle Scholar
  7. 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 76:6919–6928PubMedCrossRefGoogle Scholar
  8. Andre P, Perlemuter G, Budkowska A, Brechot C, Lotteau V (2005) Hepatitis C virus particles and lipoprotein metabolism. Semin Liver Dis 25:93–104PubMedCrossRefGoogle Scholar
  9. 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 9:2445–2456PubMedCrossRefGoogle Scholar
  10. 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 84:5751–5763PubMedCrossRefGoogle Scholar
  11. Bano N, Romano JD, Jayabalasingham B, Coppens I (2007) Cellular interactions of Plasmodium liver stage with its host mammalian cell. Int J Parasitol 37:1329–1341PubMedCrossRefGoogle Scholar
  12. 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 278:41003–41012PubMedCrossRefGoogle Scholar
  13. 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 105:3605–3614PubMedCrossRefGoogle Scholar
  14. Barth H, Liang TJ, Baumert TF (2006) Hepatitis C virus entry: molecular biology and clinical implications. Hepatology 44:527–535PubMedCrossRefGoogle Scholar
  15. Bartosch B, Cosset FL (2006) Cell entry of hepatitis C virus. Virology 348:1–12PubMedCrossRefGoogle Scholar
  16. 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 100:14199–14204PubMedCrossRefGoogle Scholar
  17. Bartosch B, Dubuisson J, Cosset F-L (2003b) Highly infectious hepatitis C pseudo-viruses containing functional E1E2 envelope protein complexes. J Exp Med 197:633–642PubMedCrossRefGoogle Scholar
  18. 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 278:41624–41630PubMedCrossRefGoogle Scholar
  19. 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 79:8217–8229PubMedCrossRefGoogle Scholar
  20. 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 81:3933–3941PubMedCrossRefGoogle Scholar
  21. Baum J, Gilberger TW, Frischknecht F, Meissner M (2008) Host-cell invasion by malaria parasites: insights from Plasmodium and Toxoplasma. Trends Parasitol 24:557–563PubMedCrossRefGoogle Scholar
  22. 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 83:8012–8020PubMedCrossRefGoogle Scholar
  23. 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 51:43–53PubMedCrossRefGoogle Scholar
  24. 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 277:36991–37000PubMedCrossRefGoogle Scholar
  25. Bertaux C, Dragic T (2006) Different domains of CD81 mediate distinct stages of hepatitis C virus pseudoparticle entry. J Virol 80:4940–4948PubMedCrossRefGoogle Scholar
  26. 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 80:6964–6972PubMedCrossRefGoogle Scholar
  27. Bollinger CR, Teichgraber V, Gulbins E (2005) Ceramide-enriched membrane domains. Biochim Biophys Acta 1746:284–294PubMedCrossRefGoogle Scholar
  28. 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):1919–1930PubMedCrossRefGoogle Scholar
  29. 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 443:85–94PubMedCrossRefGoogle Scholar
  30. Boucheix C, Rubinstein E (2001) Tetraspanins. Cell Mol Life Sci 58:1189–1205PubMedCrossRefGoogle Scholar
  31. 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 332:438–453PubMedCrossRefGoogle Scholar
  32. 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 82:8316–8329PubMedCrossRefGoogle Scholar
  33. 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:e2660PubMedCrossRefGoogle Scholar
  34. 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 81:6128–6133PubMedCrossRefGoogle Scholar
  35. 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 79:15331–15341PubMedCrossRefGoogle Scholar
  36. 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 79:362–373PubMedCrossRefGoogle Scholar
  37. 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 8:31–39PubMedGoogle Scholar
  38. 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 81:8063–8071PubMedCrossRefGoogle Scholar
  39. 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 84:34–43PubMedCrossRefGoogle Scholar
  40. 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 81:13783–13793PubMedCrossRefGoogle Scholar
  41. 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 276:14329–14337PubMedGoogle Scholar
  42. 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 373:409–421PubMedCrossRefGoogle Scholar
  43. 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 33:2479–2489PubMedCrossRefGoogle Scholar
  44. 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 420:133–154PubMedCrossRefGoogle Scholar
  45. 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 284:31572–31578PubMedCrossRefGoogle Scholar
  46. 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 82:2243–2250PubMedGoogle Scholar
  47. 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 86:2793–2798PubMedCrossRefGoogle Scholar
  48. 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 167:5115–5121PubMedGoogle Scholar
  49. 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 72:2183–2191PubMedGoogle Scholar
  50. 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 73:2641–2649PubMedGoogle Scholar
  51. 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 74:3623–3633PubMedCrossRefGoogle Scholar
  52. 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 82:1629–1635PubMedGoogle Scholar
  53. 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 21:2893–2902PubMedCrossRefGoogle Scholar
  54. Cocquerel L, Kuo CC, Dubuisson J, Levy S (2003a) CD81-dependent binding of hepatitis C virus E1E2 heterodimers. J Virol 77:10677–10683PubMedCrossRefGoogle Scholar
  55. 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 77:1604–1609PubMedCrossRefGoogle Scholar
  56. Cocquerel L, Voisset C, Dubuisson J (2006) Hepatitis C virus entry: potential receptors and their biological functions. J Gen Virol 87:1075–1084PubMedCrossRefGoogle Scholar
  57. 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:e1000702PubMedCrossRefGoogle Scholar
  58. Connelly MA, Williams DL (2004) Scavenger receptor BI: a scavenger receptor with a mission to transport high density lipoprotein lipids. Curr Opin Lipidol 15:287–295PubMedCrossRefGoogle Scholar
  59. Coppi A, Pinzon-Ortiz C, Hutter C, Sinnis P (2005) The Plasmodium circumsporozoite protein is proteolytically processed during cell invasion. J Exp Med 201:27–33PubMedCrossRefGoogle Scholar
  60. 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 2:316–327PubMedCrossRefGoogle Scholar
  61. 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 101:7270–7274PubMedCrossRefGoogle Scholar
  62. Coyne CB, Bergelson JM (2006) Virus-induced Abl and Fyn kinase signals permit coxsackie virus entry through epithelial tight junctions. Cell 124:119–131PubMedCrossRefGoogle Scholar
  63. 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 195:35–41PubMedCrossRefGoogle Scholar
  64. 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 36:919–929PubMedCrossRefGoogle Scholar
  65. 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 84:5494–5507PubMedCrossRefGoogle Scholar
  66. 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 474:208–211PubMedCrossRefGoogle Scholar
  67. 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 282:32357–32369PubMedCrossRefGoogle Scholar
  68. 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:e1000310PubMedCrossRefGoogle Scholar
  69. 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 76:11143–11147PubMedCrossRefGoogle Scholar
  70. Drummer HE, Maerz A, Poumbourios P (2003) Cell surface expression of functional hepatitis C virus E1 and E2 glycoproteins. FEBS Lett 546:385–390PubMedCrossRefGoogle Scholar
  71. Drummer HE, Wilson KA, Poumbourios P (2005) Determinants of CD81 dimerization and interaction with hepatitis C virus glycoprotein E2. Biochem Biophys Res Commun 328:251–257PubMedCrossRefGoogle Scholar
  72. 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 80:7844–7853PubMedCrossRefGoogle Scholar
  73. 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 88:1144–1148PubMedCrossRefGoogle Scholar
  74. Dubuisson J, Rice CM (1996) Hepatitis C virus glycoprotein folding: disulfide bond formation and association with calnexin. J Virol 70:778–786PubMedGoogle Scholar
  75. 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 273:32088–32095PubMedCrossRefGoogle Scholar
  76. 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 446:801–805PubMedCrossRefGoogle Scholar
  77. 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 81:8072–8079PubMedCrossRefGoogle Scholar
  78. 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 80:1943–1947PubMedGoogle Scholar
  79. 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 73:6235–6244PubMedGoogle Scholar
  80. 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 73:6782–6790PubMedGoogle Scholar
  81. 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 80:11331–11342PubMedCrossRefGoogle Scholar
  82. 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 e951-954PubMedCrossRefGoogle Scholar
  83. Forns X, Allander T, Rohwer-Nutter P, Bukh J (2000a) Characterization of modified hepatitis C virus E2 proteins expressed on the cell surface. Virology 274:75–85PubMedCrossRefGoogle Scholar
  84. 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 97:13318–13323PubMedCrossRefGoogle Scholar
  85. 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 79:2367–2374PubMedGoogle Scholar
  86. 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 177:1287–1298PubMedCrossRefGoogle Scholar
  87. 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 76:257–266PubMedCrossRefGoogle Scholar
  88. 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:e192PubMedCrossRefGoogle Scholar
  89. 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 68:3667–3673PubMedCrossRefGoogle Scholar
  90. 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 307:255–265PubMedCrossRefGoogle Scholar
  91. 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 82:2120–2129PubMedCrossRefGoogle Scholar
  92. 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 68:206–215PubMedCrossRefGoogle Scholar
  93. 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 79:8400–8409PubMedCrossRefGoogle Scholar
  94. 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 49:364–377PubMedCrossRefGoogle Scholar
  95. 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 81:3162–3169PubMedCrossRefGoogle Scholar
  96. 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 284:17657–17667PubMedCrossRefGoogle Scholar
  97. 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 82:5007–5020PubMedCrossRefGoogle Scholar
  98. 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 285:21092–21102PubMedCrossRefGoogle Scholar
  99. Hartsock A, Nelson WJ (2008) Adherens and tight junctions: structure, function and connections to the actin cytoskeleton. Biochim Biophys Acta 1778:660–669PubMedCrossRefGoogle Scholar
  100. 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 15:7–16PubMedCrossRefGoogle Scholar
  101. Heiskala M, Peterson PA, Yang Y (2001) The roles of claudin superfamily proteins in paracellular transport. Traffic 2:93–98PubMedCrossRefGoogle Scholar
  102. 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 81:8101–8111PubMedCrossRefGoogle Scholar
  103. 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 84:11905–11915PubMedCrossRefGoogle Scholar
  104. 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 74:3642–3649PubMedCrossRefGoogle Scholar
  105. 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 32:682–684PubMedGoogle Scholar
  106. 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 132:909–913PubMedGoogle Scholar
  107. 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 100:7271–7276PubMedCrossRefGoogle Scholar
  108. 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 104:5848–5853PubMedCrossRefGoogle Scholar
  109. 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 144:275–279PubMedCrossRefGoogle Scholar
  110. 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 151:6470–6481PubMedGoogle Scholar
  111. 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 58:1264–1275PubMedCrossRefGoogle Scholar
  112. 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 1:346–356PubMedCrossRefGoogle Scholar
  113. Jiang J, Luo G (2009) Apolipoprotein E but not B is required for the formation of infectious hepatitis C virus particles. J Virol 83:12680–12691PubMedCrossRefGoogle Scholar
  114. 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 28:167–171PubMedCrossRefGoogle Scholar
  115. 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 81:374–383PubMedCrossRefGoogle Scholar
  116. 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 147:937–944PubMedCrossRefGoogle Scholar
  117. 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 85:10451–10463PubMedCrossRefGoogle Scholar
  118. 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 20:12–18PubMedCrossRefGoogle Scholar
  119. 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 80:5308–5320PubMedCrossRefGoogle Scholar
  120. 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 81:588–598PubMedCrossRefGoogle Scholar
  121. 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:e1000762PubMedCrossRefGoogle Scholar
  122. 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 51:1144–1157PubMedCrossRefGoogle Scholar
  123. 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 75:3758–3768PubMedCrossRefGoogle Scholar
  124. 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 50:17–24PubMedCrossRefGoogle Scholar
  125. 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 44:1626–1634PubMedCrossRefGoogle Scholar
  126. Lavie M, Goffard A, Dubuisson J (2007) Assembly of a functional HCV glycoprotein heterodimer. Curr Issues Mol Biol 9:71–86PubMedGoogle Scholar
  127. 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 41:265–274PubMedCrossRefGoogle Scholar
  128. 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 281:3909–3917PubMedCrossRefGoogle Scholar
  129. 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 81:8752–8765PubMedCrossRefGoogle Scholar
  130. 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 170:478–489PubMedCrossRefGoogle Scholar
  131. 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 1253–1304Google Scholar
  132. Levy S, Shoham T (2005a) Protein-protein interactions in the tetraspanin web. Physiology (Bethesda) 20:218–224CrossRefGoogle Scholar
  133. Levy S, Shoham T (2005b) The tetraspanin web modulates immune-signalling complexes. Nat Rev Immunol 5:136–148PubMedCrossRefGoogle Scholar
  134. 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 16:89PubMedCrossRefGoogle Scholar
  135. 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 309:623–626PubMedCrossRefGoogle Scholar
  136. 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 103:3805–3809PubMedCrossRefGoogle Scholar
  137. Lindenbach BD, Thiel HJ, Rice CM (2007) Flaviviridae: the viruses and their replication. Lippincott Williams & Wilkins, PhiladelphiaGoogle Scholar
  138. 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 83:2011–2014PubMedCrossRefGoogle Scholar
  139. Lopez D (2008) PCSK9: an enigmatic protease. Biochim Biophys Acta 1781:184–191PubMedCrossRefGoogle Scholar
  140. Maecker HT, Levy S (1997) Normal lymphocyte development but delayed humoral immune response in CD81-null mice. J Exp Med 185:1505–1510PubMedCrossRefGoogle Scholar
  141. 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 20:735–737PubMedGoogle Scholar
  142. Manns MP, Wedemeyer H, Cornberg M (2006) Treating viral hepatitis C: efficacy, side effects, and complications. Gut 55:1350–1359PubMedCrossRefGoogle Scholar
  143. 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 304:187–196PubMedCrossRefGoogle Scholar
  144. 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 307:367–369PubMedCrossRefGoogle Scholar
  145. 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 227:440–442PubMedCrossRefGoogle Scholar
  146. 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 78:8496–8505PubMedCrossRefGoogle Scholar
  147. Mee CJ, Grove J, Harris HJ, Hu K, Balfe P, McKeating JA (2008) Effect of cell polarization on hepatitis C virus entry. J Virol 82:461–470PubMedCrossRefGoogle Scholar
  148. 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 83:6211–6221PubMedCrossRefGoogle Scholar
  149. 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 80:11571–11578PubMedCrossRefGoogle Scholar
  150. 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 82:3555–3560PubMedCrossRefGoogle Scholar
  151. Menard R, Janse C (1997) Gene targeting in malaria parasites. Methods (San Diego, Calif) 13:148–157CrossRefGoogle Scholar
  152. 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 74:5933–5938PubMedCrossRefGoogle Scholar
  153. 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 48:1761–1768PubMedCrossRefGoogle Scholar
  154. 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 80:887–896PubMedGoogle Scholar
  155. 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 102:4560–4565PubMedCrossRefGoogle Scholar
  156. Meunier JC, Russell RS, Engle RE, Faulk KN, Purcell RH, Emerson SU (2008) Apolipoprotein c1 association with hepatitis C virus. J Virol 82:9647–9656PubMedCrossRefGoogle Scholar
  157. 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 78:2299–2306PubMedGoogle Scholar
  158. 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 46:411–419PubMedCrossRefGoogle Scholar
  159. 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 82:569–574PubMedCrossRefGoogle Scholar
  160. 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 57:223–229PubMedCrossRefGoogle Scholar
  161. 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 286:13954–13965PubMedCrossRefGoogle Scholar
  162. 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 79:714–723PubMedCrossRefGoogle Scholar
  163. Mota MM, Rodriguez A (2000) Plasmodium yoelii: efficient in vitro invasion and complete development of sporozoites in mouse hepatic cell lines. Exp Parasitol 96:257–259PubMedCrossRefGoogle Scholar
  164. 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 291:141–144PubMedCrossRefGoogle Scholar
  165. 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 102:3022–3027PubMedCrossRefGoogle Scholar
  166. 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 328:1091–1100PubMedCrossRefGoogle Scholar
  167. 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 180:1328–1333PubMedCrossRefGoogle Scholar
  168. 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 80:2418–2428PubMedCrossRefGoogle Scholar
  169. 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 275:31428–31437PubMedCrossRefGoogle Scholar
  170. 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 78:2994–3002PubMedCrossRefGoogle Scholar
  171. 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 10:4007–4015PubMedGoogle Scholar
  172. 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 394:99–108PubMedCrossRefGoogle Scholar
  173. 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 82:1877–1883PubMedGoogle Scholar
  174. 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 80:8695–8704PubMedCrossRefGoogle Scholar
  175. 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 89:653–659PubMedCrossRefGoogle Scholar
  176. 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 1758:755–763PubMedCrossRefGoogle Scholar
  177. 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 81:2873–2883PubMedGoogle Scholar
  178. 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 279:58–68PubMedCrossRefGoogle Scholar
  179. 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 45:3755–3768PubMedCrossRefGoogle Scholar
  180. 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 1778:2069–2080PubMedCrossRefGoogle Scholar
  181. 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 94:4737–4750PubMedCrossRefGoogle Scholar
  182. Perez-Berna AJ, Pabst G, Laggner P, Villalain J (2009) Biophysical characterization of the fusogenic region of HCV envelope glycoprotein E1. Biochim Biophys Acta 1788:2183–2193PubMedCrossRefGoogle Scholar
  183. 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 74:4824–4830PubMedCrossRefGoogle Scholar
  184. 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 282:938–941PubMedCrossRefGoogle Scholar
  185. 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 276:26784–26791PubMedCrossRefGoogle Scholar
  186. 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 457:882–886PubMedCrossRefGoogle Scholar
  187. 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 107:3141–3145PubMedCrossRefGoogle Scholar
  188. 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 139:1355–1364PubMedCrossRefGoogle Scholar
  189. 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 76:242–250PubMedCrossRefGoogle Scholar
  190. Popescu CI, Dubuisson J (2009) Role of lipid metabolism in hepatitis C virus assembly and entry. Biol Cell 102:63–74PubMedCrossRefGoogle Scholar
  191. 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)Google Scholar
  192. 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 77:1856–1867PubMedCrossRefGoogle Scholar
  193. 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:e1866PubMedCrossRefGoogle Scholar
  194. 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 9:111PubMedCrossRefGoogle Scholar
  195. 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 4:271–282PubMedCrossRefGoogle Scholar
  196. 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 5:46PubMedCrossRefGoogle Scholar
  197. 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 26:2657–2665PubMedCrossRefGoogle Scholar
  198. 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):3007–3018PubMedGoogle Scholar
  199. 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 16:621–632PubMedCrossRefGoogle Scholar
  200. 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 281:19665–19675PubMedCrossRefGoogle Scholar
  201. 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 39:153–162PubMedCrossRefGoogle Scholar
  202. 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 21:5017–5025PubMedCrossRefGoogle Scholar
  203. 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 83:12407–12414PubMedCrossRefGoogle Scholar
  204. 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 90:212–227PubMedCrossRefGoogle Scholar
  205. Selby MJ, Glazer E, Masiarz F, Houghton M (1994) Complex processing and protein: protein interactions in the E2:NS2 region of HCV. Virology 204:114–122PubMedCrossRefGoogle Scholar
  206. 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 286:30361–30376PubMedCrossRefGoogle Scholar
  207. 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 70:361–372PubMedCrossRefGoogle Scholar
  208. 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 276:25287–25293PubMedCrossRefGoogle Scholar
  209. 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 9:93–96PubMedCrossRefGoogle Scholar
  210. 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 279:9490–9496PubMedCrossRefGoogle Scholar
  211. 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 119:1992–2002PubMedCrossRefGoogle Scholar
  212. 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 8:1134–1146PubMedCrossRefGoogle Scholar
  213. Silvie O, Franetich JF, Boucheix C, Rubinstein E, Mazier D (2007) Alternative invasion pathways for Plasmodium berghei sporozoites. Int J Parasitol 37:173–182PubMedCrossRefGoogle Scholar
  214. 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 319:36–48PubMedCrossRefGoogle Scholar
  215. Snounou G, Gruner AC, Muller-Graf CD, Mazier D, Renia L (2005) The Plasmodium sporozoite survives RTS, S vaccination. Trends Parasitol 21:456–461PubMedCrossRefGoogle Scholar
  216. 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 276:40545–40554PubMedCrossRefGoogle Scholar
  217. Stipp CS, Orlicky D, Hemler ME (2001b) FPRP, a major, highly stoichiometric, highly specific CD81- and CD9- associated protein. J Biol Chem 276:4853–4862PubMedCrossRefGoogle Scholar
  218. Strebel K, Luban J, Jeang KT (2009) Human cellular restriction factors that target HIV-1 replication. BMC Med 7:48PubMedCrossRefGoogle Scholar
  219. Tham TN, Gouin E, Rubinstein E, Boucheix C, Cossart P, Pizarro-Cerda J (2009) Tetraspanin CD81 is required for Listeria monocytogenes invasion. Infect Immun 78:204–209PubMedCrossRefGoogle Scholar
  220. 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 47:17–24PubMedCrossRefGoogle Scholar
  221. Trager W, Jensen JB (1976) Human malaria parasites in continuous culture. Science 193:673–675PubMedCrossRefGoogle Scholar
  222. 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 352:357–367PubMedCrossRefGoogle Scholar
  223. 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 80:1734–1741PubMedCrossRefGoogle Scholar
  224. 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 102:12194–12199PubMedCrossRefGoogle Scholar
  225. 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:e3549PubMedCrossRefGoogle Scholar
  226. 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 84:10159–10168PubMedCrossRefGoogle Scholar
  227. 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 280:7793–7799PubMedCrossRefGoogle Scholar
  228. 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 10:606–617PubMedCrossRefGoogle Scholar
  229. 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 43:932–942CrossRefGoogle Scholar
  230. 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 31:166–175PubMedCrossRefGoogle Scholar
  231. 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 11:791–796PubMedCrossRefGoogle Scholar
  232. 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 140:1334–1344PubMedCrossRefGoogle Scholar
  233. 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 180:842–848PubMedCrossRefGoogle Scholar
  234. 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 90:48–58PubMedCrossRefGoogle Scholar
  235. World Health Organization, Geneva (2009) Malaria Report 2009Google Scholar
  236. 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 20:3840–3848PubMedCrossRefGoogle Scholar
  237. 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 40:355–366PubMedCrossRefGoogle Scholar
  238. 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 4:283–292PubMedCrossRefGoogle Scholar
  239. 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:e1000010PubMedCrossRefGoogle Scholar
  240. Yamauchi LM, Coppi A, Snounou G, Sinnis P (2007) Plasmodium sporozoites trickle out of the injection site. Cell Microbiol 9:2093CrossRefGoogle Scholar
  241. 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):8643–8653PubMedCrossRefGoogle Scholar
  242. 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 46:1722–1731PubMedCrossRefGoogle Scholar
  243. 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 78:1448–1455PubMedCrossRefGoogle Scholar
  244. Zhang YY, Zhang BH, Ishii K, Liang TJ (2010) Novel function of CD81 in controlling hepatitis C virus replication. J Virol 84:3396–3407PubMedCrossRefGoogle Scholar
  245. 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 81:12465–12471PubMedCrossRefGoogle Scholar
  246. 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 102:9294–9299PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  1. 1.Center for Infection and Immunity of LilleInserm U1019 – CNRS UMR8204, Pasteur Institute of Lille, University Lille North of FranceLille CedexFrance
  2. 2.INSERM, UMR S 945ParisFrance
  3. 3.Université Pierre et Marie Curie-Paris 6, UMR S 945ParisFrance

Personalised recommendations