The ins and outs of hepatitis C virus entry and assembly

Hepatitis C virus, a major human pathogen, produces infectious virus particles with several unique features, such as an ability to interact with serum lipoproteins, a dizzyingly complicated process of virus entry, and a pathway of virus assembly and release that is closely linked to lipoprotein secretion. Here, we review these unique features, with an emphasis on recent discoveries concerning virus particle structure, virus entry and virus particle assembly and release.

[1]  Raymond T Chung,et al.  Apolipoprotein B–dependent hepatitis C virus secretion is inhibited by the grapefruit flavonoid naringenin , 2008, Hepatology.

[2]  D. Lavanchy,et al.  The global burden of hepatitis C , 2009, Liver international : official journal of the International Association for the Study of the Liver.

[3]  Christopher T. Jones,et al.  Hepatitis C Virus p7 and NS2 Proteins Are Essential for Production of Infectious Virus , 2007, Journal of Virology.

[4]  Thomas F. Baumert,et al.  Neutralizing Antibody-Resistant Hepatitis C Virus Cell-to-Cell Transmission , 2010, Journal of Virology.

[5]  F. Penin,et al.  NS2 Protein of Hepatitis C Virus Interacts with Structural and Non-Structural Proteins towards Virus Assembly , 2011, PLoS pathogens.

[6]  C. Englert,et al.  Characterization of cell lines allowing tightly regulated expression of hepatitis C virus core protein. , 1996, Virology.

[7]  Toshiaki Maruyama,et al.  Complete Replication of Hepatitis C Virus in Cell Culture , 2005, Science.

[8]  F. Rey,et al.  Virus membrane-fusion proteins: more than one way to make a hairpin , 2006, Nature Reviews Microbiology.

[9]  Robert V Farese,et al.  Efficient Hepatitis C Virus Particle Formation Requires Diacylglycerol Acyltransferase 1 (DGAT1) , 2010, Nature Medicine.

[10]  M. Hiet,et al.  Mouse hepatic cells support assembly of infectious hepatitis C virus particles. , 2011, Gastroenterology.

[11]  R. Purcell,et al.  Equilibrium centrifugation studies of hepatitis C virus: evidence for circulating immune complexes , 1993, Journal of virology.

[12]  D. Stuart,et al.  Structure of a Pestivirus Envelope Glycoprotein E2 Clarifies Its Role in Cell Entry , 2013, Cell reports.

[13]  M. Niepmann Hepatitis C virus RNA translation. , 2013, Current topics in microbiology and immunology.

[14]  S. V. van IJzendoorn,et al.  Protein Kinase A-Dependent Step(s) in Hepatitis C Virus Entry and Infectivity , 2008, Journal of Virology.

[15]  M. Houghton,et al.  Binding of hepatitis C virus to CD81. , 1998, Science.

[16]  J. McKeating,et al.  Hepatitis C virus cell‐cell transmission in hepatoma cells in the presence of neutralizing antibodies , 2007, Hepatology.

[17]  William J. Rice,et al.  Ultrastructural analysis of hepatitis C virus particles , 2013, Proceedings of the National Academy of Sciences.

[18]  L. Kaderali,et al.  MAP-Kinase Regulated Cytosolic Phospholipase A2 Activity Is Essential for Production of Infectious Hepatitis C Virus Particles , 2012, PLoS pathogens.

[19]  C. Rice,et al.  Genetic and Functional Characterization of the N-Terminal Region of the Hepatitis C Virus NS2 Protein , 2013, Journal of Virology.

[20]  H. Kräusslich,et al.  More than one door – Budding of enveloped viruses through cellular membranes , 2007, FEBS Letters.

[21]  P. Borrow,et al.  Functional Characterization of Intracellular and Secreted Forms of a Truncated Hepatitis C Virus E2 Glycoprotein , 2000, Journal of Virology.

[22]  G. Reynolds,et al.  Hepatitis C virus receptor expression in normal and diseased liver tissue , 2007, Hepatology.

[23]  F. Chisari,et al.  Ultrastructural and Biophysical Characterization of Hepatitis C Virus Particles Produced in Cell Culture , 2010, Journal of Virology.

[24]  L. Komuves,et al.  Hepatitis C Virus Induces Epidermal Growth Factor Receptor Activation via CD81 Binding for Viral Internalization and Entry , 2012, Journal of Virology.

[25]  S. Ciesek,et al.  Hepatitis C Virus Hypervariable Region 1 Modulates Receptor Interactions, Conceals the CD81 Binding Site, and Protects Conserved Neutralizing Epitopes , 2010, Journal of Virology.

[26]  A. Shavinskaya,et al.  The Lipid Droplet Binding Domain of Hepatitis C Virus Core Protein Is a Major Determinant for Efficient Virus Assembly* , 2007, Journal of Biological Chemistry.

[27]  M. Imamura,et al.  Identification of the Niemann-Pick C1-like 1 cholesterol absorption receptor as a new hepatitis C virus entry factor , 2011, Nature Medicine.

[28]  R. Cortese,et al.  The human scavenger receptor class B type I is a novel candidate receptor for the hepatitis C virus , 2002, The EMBO journal.

[29]  P. Rebers,et al.  The purification and concentration of hog cholera virus. , 1968, Canadian journal of comparative medicine : Revue canadienne de medecine comparee.

[30]  F. Penin,et al.  Structural Determinants That Target the Hepatitis C Virus Core Protein to Lipid Droplets* , 2006, Journal of Biological Chemistry.

[31]  C. Rice,et al.  Characterization of truncated forms of hepatitis C virus glycoproteins. , 1997, The Journal of general virology.

[32]  F. Penin,et al.  Hepatitis C Virus Core Protein Is a Dimeric Alpha-Helical Protein Exhibiting Membrane Protein Features , 2005, Journal of Virology.

[33]  S. Boulant,et al.  Disrupting the association of hepatitis C virus core protein with lipid droplets correlates with a loss in production of infectious virus. , 2007, The Journal of general virology.

[34]  Céline Hernandez,et al.  Production of infectious hepatitis C virus in primary cultures of human adult hepatocytes. , 2010, Gastroenterology.

[35]  R. Thomssen,et al.  Association of hepatitis C virus in human sera with β-lipoprotein , 2004, Medical Microbiology and Immunology.

[36]  A. Helenius,et al.  Folding and dimerization of hepatitis C virus E1 and E2 glycoproteins in stably transfected CHO cells. , 2005, Virology.

[37]  J. Navaza,et al.  The Fusion Glycoprotein Shell of Semliki Forest Virus An Icosahedral Assembly Primed for Fusogenic Activation at Endosomal pH , 2001, Cell.

[38]  J. M. Acosta,et al.  Purification and partial characterization of maize mosaic virus. , 1979, Intervirology.

[39]  M. Shapiro,et al.  Determining the size of non-A, non-B hepatitis virus by filtration. , 1987, The Journal of infectious diseases.

[40]  Robert V Farese,et al.  Diacylglycerol Acyltransferase-1 Localizes Hepatitis C Virus NS5A Protein to Lipid Droplets and Enhances NS5A Interaction with the Viral Capsid Core* , 2013, The Journal of Biological Chemistry.

[41]  V. Lohmann Hepatitis C Virus RNA Replication , 2013, Current topics in microbiology and immunology.

[42]  S. Pfeffer,et al.  Reconstitution of the Entire Hepatitis C Virus Life Cycle in Nonhepatic Cells , 2012, Journal of Virology.

[43]  F. Penin,et al.  Hepatitis C virus proteins: from structure to function. , 2013, Current topics in microbiology and immunology.

[44]  Yuqiong Liang,et al.  NS3 Helicase Domains Involved in Infectious Intracellular Hepatitis C Virus Particle Assembly , 2008, Journal of Virology.

[45]  J. Chou,et al.  Unusual architecture of the p7 channel from hepatitis C virus , 2013, Nature.

[46]  P. Stillemark-Billton,et al.  Intracellular assembly of VLDL: two major steps in separate cell compartments. , 2000, Trends in cardiovascular medicine.

[47]  T. Krey,et al.  Acid-Resistant Bovine Pestivirus Requires Activation for pH-Triggered Fusion during Entry , 2005, Journal of Virology.

[48]  J. Dubuisson,et al.  Characterization of Hepatitis C Virus E2 Glycoprotein Interaction with a Putative Cellular Receptor, CD81 , 1999, Journal of Virology.

[49]  K. Ishii,et al.  Interaction of Hepatitis C Virus Nonstructural Protein 5A with Core Protein Is Critical for the Production of Infectious Virus Particles , 2008, Journal of Virology.

[50]  Jieyun Jiang,et al.  Human Apolipoprotein E Is Required for Infectivity and Production of Hepatitis C Virus in Cell Culture , 2007, Journal of Virology.

[51]  J. Dubuisson,et al.  Virus‐neutralizing antibodies to hepatitis C virus , 2013, Journal of viral hepatitis.

[52]  Y. Modis,et al.  Crystal structure of glycoprotein C from Rift Valley fever virus , 2013 .

[53]  R. Garry,et al.  Proteomics computational analyses suggest that hepatitis C virus E1 and pestivirus E2 envelope glycoproteins are truncated class II fusion proteins. , 2003, Virology.

[54]  L. Jia,et al.  Niemann-pick C1-like 1 (NPC1L1) protein in intestinal and hepatic cholesterol transport. , 2011, Annual review of physiology.

[55]  Wei Zhang,et al.  Structure of the Immature Dengue Virus at Low pH Primes Proteolytic Maturation , 2008, Science.

[56]  H. Laude Nonarbo-togaviridae: Comparative hydrodynamic properties of the pestivirus genus , 2005, Archives of Virology.

[57]  F. Cosset,et al.  Hepatitis C Virus Is Primed by CD81 Protein for Low pH-dependent Fusion* , 2011, The Journal of Biological Chemistry.

[58]  Sangeeta N. Bhatia,et al.  Persistent hepatitis C virus infection in microscale primary human hepatocyte cultures , 2010, Proceedings of the National Academy of Sciences.

[59]  M. Rossmann,et al.  A structural perspective of the flavivirus life cycle , 2005, Nature Reviews Microbiology.

[60]  D. Wong,et al.  Hepatitis C Virus Structural Proteins Assemble into Viruslike Particles in Insect Cells , 1998, Journal of Virology.

[61]  Charles M. Rice,et al.  Human occludin is a hepatitis C virus entry factor required for infection of mouse cells , 2009, Nature.

[62]  M. Lai,et al.  Hepatitis C Virus Egress and Release Depend on Endosomal Trafficking of Core Protein , 2010, Journal of Virology.

[63]  S. Uprichard,et al.  Identification of transferrin receptor 1 as a hepatitis C virus entry factor , 2013, Proceedings of the National Academy of Sciences.

[64]  N. Kato,et al.  The ESCRT System Is Required for Hepatitis C Virus Production , 2011, PloS one.

[65]  S. Evans,et al.  The p7 protein of hepatitis C virus forms an ion channel that is blocked by the antiviral drug, Amantadine , 2003, FEBS letters.

[66]  D. Stuart,et al.  The postfusion structure of baculovirus gp64 supports a unified view of viral fusion machines , 2008, Nature Structural &Molecular Biology.

[67]  M. Hulst,et al.  Inhibition of pestivirus infection in cell culture by envelope proteins E(rns) and E2 of classical swine fever virus: E(rns) and E2 interact with different receptors. , 1997, The Journal of general virology.

[68]  L. Kaderali,et al.  Hepatitis C Virus p7 is Critical for Capsid Assembly and Envelopment , 2013, PLoS pathogens.

[69]  S. Levy,et al.  Functional Analysis of Cell Surface-Expressed Hepatitis C Virus E2 Glycoprotein , 1999, Journal of Virology.

[70]  T. Tellinghuisen,et al.  Regulation of Hepatitis C Virion Production via Phosphorylation of the NS5A Protein , 2008, PLoS pathogens.

[71]  C. Cheng‐Mayer,et al.  Hepatitis C virus glycoproteins mediate pH-dependent cell entry of pseudotyped retroviral particles , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[72]  Q. Sattentau,et al.  Avoiding the void: cell-to-cell spread of human viruses , 2008, Nature Reviews Microbiology.

[73]  F. Penin,et al.  Structural and Functional Characterization of Nonstructural Protein 2 for Its Role in Hepatitis C Virus Assembly* , 2008, Journal of Biological Chemistry.

[74]  S. Lemon,et al.  Intracellular Proton Conductance of the Hepatitis C Virus p7 Protein and Its Contribution to Infectious Virus Production , 2010, PLoS pathogens.

[75]  B. Lindenbach Virion assembly and release. , 2013, Current topics in microbiology and immunology.

[76]  J. McKeating,et al.  Hepatitis C Virus Induces CD81 and Claudin-1 Endocytosis , 2012, Journal of Virology.

[77]  J. d'Alayer,et al.  The Disulfide Bonds in Glycoprotein E2 of Hepatitis C Virus Reveal the Tertiary Organization of the Molecule , 2010, PLoS pathogens.

[78]  M. Harada,et al.  High‐density lipoprotein binding rate differs greatly between genotypes 1b and 2a/2b of hepatitis C virus , 2003, Journal of medical virology.

[79]  D. Bradley,et al.  Posttransfusion non-A, non-B hepatitis in chimpanzees: Physicochemical evidence that the tubule-forming agent is a small, enveloped virus , 1985 .

[80]  M. Yanagi,et al.  Transcripts from a single full-length cDNA clone of hepatitis C virus are infectious when directly transfected into the liver of a chimpanzee. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[81]  M. Houghton,et al.  Isolation of a cDNA clone derived from a blood-borne non-A, non-B viral hepatitis genome. , 1989, Science.

[82]  M. J. Evans,et al.  Temporal Analysis of Hepatitis C Virus Cell Entry with Occludin Directed Blocking Antibodies , 2013, PLoS pathogens.

[83]  Ralf Bartenschlager,et al.  Characterization of Hepatitis C Virus Particle Subpopulations Reveals Multiple Usage of the Scavenger Receptor BI for Entry Steps* , 2012, The Journal of Biological Chemistry.

[84]  Y. Moriwaki,et al.  A newly discovered apolipoprotein B-containing high-density lipoprotein produced by human hepatoma cells. , 1987, Biochimica et biophysica acta.

[85]  R. DuBois,et al.  Functional and evolutionary insight from the crystal structure of rubella virus protein E1 , 2013, Nature.

[86]  S. Burgess,et al.  Evidence for the Formation of a Heptameric Ion Channel Complex by the Hepatitis C Virus P7 Protein in Vitro* , 2006, Journal of Biological Chemistry.

[87]  M. Hiet,et al.  Biochemical and Morphological Properties of Hepatitis C Virus Particles and Determination of Their Lipidome* , 2010, The Journal of Biological Chemistry.

[88]  C. Rice,et al.  Transmission of hepatitis C by intrahepatic inoculation with transcribed RNA. , 1997, Science.

[89]  Y. Modis,et al.  Crystal structure of glycoprotein E2 from bovine viral diarrhea virus , 2013, Proceedings of the National Academy of Sciences.

[90]  J. Dubuisson,et al.  Role of low‐density lipoprotein receptor in the hepatitis C virus life cycle , 2012, Hepatology.

[91]  B. Lindenbach,et al.  The NS4A Protein of Hepatitis C Virus Promotes RNA-Coupled ATP Hydrolysis by the NS3 Helicase , 2009, Journal of Virology.

[92]  T. Dragic,et al.  Different Domains of CD81 Mediate Distinct Stages of Hepatitis C Virus Pseudoparticle Entry , 2006, Journal of Virology.

[93]  Cynthia L. de la Fuente,et al.  Animal models for hepatitis C. , 2013, Current topics in microbiology and immunology.

[94]  V. Agnello,et al.  Hepatitis C virus and other flaviviridae viruses enter cells via low density lipoprotein receptor. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[95]  Andrew S. Kohlway,et al.  The Acidic Domain of Hepatitis C Virus NS4A Contributes to RNA Replication and Virus Particle Assembly , 2010, Journal of Virology.

[96]  J. Maniloff,et al.  Virus taxonomy : eighth report of the International Committee on Taxonomy of Viruses , 2005 .

[97]  N. Tanaka,et al.  Regulation of hepatitis C virus secretion by the Hrs-dependent exosomal pathway. , 2012, Virology.

[98]  M. Tremblay,et al.  Palmitoylation of Hepatitis C Virus Core Protein Is Important for Virion Production* , 2009, The Journal of Biological Chemistry.

[99]  Christopher T. Jones,et al.  Different Requirements for Scavenger Receptor Class B Type I in Hepatitis C Virus Cell-Free versus Cell-to-Cell Transmission , 2013, Journal of Virology.

[100]  R. Bartenschlager,et al.  Production of Infectious Genotype 1b Virus Particles in Cell Culture and Impairment by Replication Enhancing Mutations , 2009, PLoS pathogens.

[101]  H. Lortat-Jacob,et al.  Cellular glycosaminoglycans and low density lipoprotein receptor are involved in hepatitis C virus adsorption , 2002, Journal of medical virology.

[102]  N. Heaton,et al.  Molecular Determinants and Dynamics of Hepatitis C Virus Secretion , 2012, PLoS pathogens.

[103]  J. Dubuisson,et al.  Characterization of the Envelope Glycoproteins Associated with Infectious Hepatitis C Virus , 2010, Journal of Virology.

[104]  Mark Harris,et al.  Vps4 and the ESCRT-III complex are required for the release of infectious hepatitis C virus particles. , 2010, The Journal of general virology.

[105]  Helen H. Hobbs,et al.  Identification of Scavenger Receptor SR-BI as a High Density Lipoprotein Receptor , 1996, Science.

[106]  D. Bradley,et al.  Posttransfusion non-A, non-B hepatitis in chimpanzees. Physicochemical evidence that the tubule-forming agent is a small, enveloped virus. , 1985, Gastroenterology.

[107]  R. Purcell,et al.  Transfusion‐associated hepatitis not due to viral hepatitis type A or B † , 1975, The New England journal of medicine.

[108]  R. Norberg,et al.  Evidence for circulating immune complexes in sarcoidosis. , 1974, Clinical and experimental immunology.

[109]  C. Rice,et al.  Phosphorylation of hepatitis C virus nonstructural protein 5A modulates its protein interactions and viral RNA replication. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[110]  M. Phillips,et al.  High density lipoprotein structure-function and role in reverse cholesterol transport. , 2010, Sub-cellular biochemistry.

[111]  T. Baumert,et al.  Epidermal growth factor receptor signaling impairs the antiviral activity of interferon‐alpha , 2013, Hepatology.

[112]  Charles M. Rice,et al.  Completion of the entire hepatitis C virus life-cycle in genetically humanized mice , 2013, Nature.

[113]  Olivier Poch,et al.  EGFR and EphA2 are host factors for hepatitis C virus entry and possible targets for antiviral therapy , 2011, Nature Medicine.

[114]  P. André,et al.  Preferential association of Hepatitis C virus with apolipoprotein B48-containing lipoproteins. , 2006, The Journal of general virology.

[115]  V. Lohmann HCV replicons: overview and basic protocols. , 2009, Methods in molecular biology.

[116]  V. Hsu,et al.  Getting active: protein sorting in endocytic recycling , 2012, Nature Reviews Molecular Cell Biology.

[117]  Ralf Bartenschlager,et al.  Essential Role of Domain III of Nonstructural Protein 5A for Hepatitis C Virus Infectious Particle Assembly , 2008, PLoS pathogens.

[118]  M. Houghton,et al.  Evaluation of Hepatitis C Virus Glycoprotein E2 for Vaccine Design: an Endoplasmic Reticulum-Retained Recombinant Protein Is Superior to Secreted Recombinant Protein and DNA-Based Vaccine Candidates , 2000, Journal of Virology.

[119]  Jieyun Jiang,et al.  Apolipoprotein E but Not B Is Required for the Formation of Infectious Hepatitis C Virus Particles , 2009, Journal of Virology.

[120]  M. Houghton,et al.  Structure-Function Analysis of Hepatitis C Virus Envelope-CD81 Binding , 2000, Journal of virology.

[121]  J. McKeating,et al.  Claudin Association with CD81 Defines Hepatitis C Virus Entry , 2010, The Journal of Biological Chemistry.

[122]  B. Bartosch,et al.  Infectious Hepatitis C Virus Pseudo-particles Containing Functional E1–E2 Envelope Protein Complexes , 2003, The Journal of experimental medicine.

[123]  Anna Tramontano,et al.  A model for the hepatitis C virus envelope glycoprotein E2 , 2000, Proteins.

[124]  J. Marcotrigiano,et al.  Blocking Hepatitis C Virus Infection with Recombinant Form of Envelope Protein 2 Ectodomain , 2009, Journal of Virology.

[125]  T. Pietschmann,et al.  Cell culture systems for hepatitis C virus. , 2013, Current topics in microbiology and immunology.

[126]  R. Bartenschlager,et al.  Production of infectious hepatitis C virus in tissue culture from a cloned viral genome , 2005, Nature Medicine.

[127]  C. Rice,et al.  Formation and intracellular localization of hepatitis C virus envelope glycoprotein complexes expressed by recombinant vaccinia and Sindbis viruses , 1994, Journal of virology.

[128]  Ariel D. Quiroga,et al.  Lumenal lipid metabolism: implications for lipoprotein assembly. , 2012, Arteriosclerosis, thrombosis, and vascular biology.

[129]  C. Rice,et al.  Innate immune responses to hepatitis C virus. , 2013, Current topics in microbiology and immunology.

[130]  Y. Jacob,et al.  Identification and Targeting of an Interaction between a Tyrosine Motif within Hepatitis C Virus Core Protein and AP2M1 Essential for Viral Assembly , 2012, PLoS pathogens.

[131]  Christopher T. Jones,et al.  University of Birmingham Time-and Temperature-Dependent Activation of Hepatitis C Virus for Low-pH-Triggered Entry , 2006 .

[132]  B. Lindenbach,et al.  Trafficking of Hepatitis C Virus Core Protein during Virus Particle Assembly , 2011, PLoS pathogens.

[133]  S. Kottilil,et al.  A Genetic Interaction between the Core and NS3 Proteins of Hepatitis C Virus Is Essential for Production of Infectious Virus , 2011, Journal of Virology.

[134]  S. Emerson,et al.  Apolipoprotein C1 Association with Hepatitis C Virus , 2008, Journal of Virology.

[135]  Johan Neyts,et al.  The postbinding activity of scavenger receptor class B type I mediates initiation of hepatitis C virus infection and viral dissemination , 2013, Hepatology.

[136]  F. Chisari,et al.  Cellular Determinants of Hepatitis C Virus Assembly, Maturation, Degradation, and Secretion , 2007, Journal of Virology.

[137]  H. Drummer,et al.  Mutagenesis of a conserved fusion peptide-like motif and membrane-proximal heptad-repeat region of hepatitis C virus glycoprotein E1. , 2007, The Journal of general virology.

[138]  S. Lemon,et al.  Regulation of the Production of Infectious Genotype 1a Hepatitis C Virus by NS5A Domain III , 2011, Journal of Virology.

[139]  F. Penin,et al.  Structural and Functional Studies of Nonstructural Protein 2 of the Hepatitis C Virus Reveal Its Key Role as Organizer of Virion Assembly , 2010, PLoS pathogens.

[140]  Charles M. Rice,et al.  A genetically humanized mouse model for hepatitis C virus infection , 2011, Nature.

[141]  E. Hildt,et al.  Apolipoprotein E interacts with hepatitis C virus nonstructural protein 5A and determines assembly of infectious particles , 2010, Hepatology.

[142]  Gregory Taylor,et al.  Current and future , 1998 .

[143]  M. Binder,et al.  Role of Annexin A2 in the Production of Infectious Hepatitis C Virus Particles , 2010, Journal of Virology.

[144]  R. Dwek,et al.  The 3-dimensional structure of a hepatitis C virus p7 ion channel by electron microscopy , 2009, Proceedings of the National Academy of Sciences.

[145]  F. Chisari,et al.  Differential Biophysical Properties of Infectious Intracellular and Secreted Hepatitis C Virus Particles , 2006, Journal of Virology.

[146]  G. Schonfeld,et al.  Determination of kinetic parameters of apolipoprotein B metabolism using amino acids labeled with stable isotopes. , 1991, Journal of lipid research.

[147]  Mariagrazia Pizza,et al.  CD81 Is a Central Regulator of Cellular Events Required for Hepatitis C Virus Infection of Human Hepatocytes , 2008, Journal of Virology.

[148]  F. Penin,et al.  Nonstructural protein 3‐4A: the Swiss army knife of hepatitis C virus , 2011, Journal of viral hepatitis.

[149]  M. Gale,et al.  Hepatitis C virus production by human hepatocytes dependent on assembly and secretion of very low-density lipoproteins , 2007, Proceedings of the National Academy of Sciences.

[150]  R. Thomssen,et al.  Low density lipoprotein receptor as a candidate receptor for hepatitis C virus , 1999, Journal of medical virology.

[151]  C. Rice,et al.  CD81 is dispensable for hepatitis C virus cell-to-cell transmission in hepatoma cells , 2009, The Journal of general virology.

[152]  C. Packard,et al.  Intravascular transfer contributes to postprandial increase in numbers of very-low-density hepatitis C virus particles. , 2010, Gastroenterology.

[153]  Y. Modis,et al.  Structure of the dengue virus envelope protein after membrane fusion , 2004, Nature.

[154]  B. Lindenbach,et al.  Hepatitis C Virus NS2 Protein Contributes to Virus Particle Assembly via Opposing Epistatic Interactions with the E1-E2 Glycoprotein and NS3-NS4A Enzyme Complexes , 2009, Journal of Virology.

[155]  R. Bartenschlager,et al.  The lipid droplet is an important organelle for hepatitis C virus production , 2007, Nature Cell Biology.

[156]  Ding‐Shinn Chen,et al.  Hepatitis C virus NS3 RNA helicase activity is modulated by the two domains of NS3 and NS4A. , 2004, Biochemical and biophysical research communications.

[157]  N. Heaton,et al.  RNA Interference and Single Particle Tracking Analysis of Hepatitis C Virus Endocytosis , 2009, PLoS pathogens.

[158]  A. Maerz,et al.  Cell surface expression of functional hepatitis C virus E1 and E2 glycoproteins , 2003, FEBS letters.

[159]  Charles M. Rice,et al.  Claudin-1 is a hepatitis C virus co-receptor required for a late step in entry , 2007, Nature.

[160]  M. Kohara,et al.  Hepatitis C virus core protein shows a cytoplasmic localization and associates to cellular lipid storage droplets. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[161]  H. Koprowski,et al.  Density Gradient Centrifugation Studies on Rabies Virus , 1966, Journal of bacteriology.

[162]  J. Pawlotsky Treatment of chronic hepatitis C: current and future. , 2013, Current topics in microbiology and immunology.

[163]  C. Rice,et al.  Cell culture-grown hepatitis C virus is infectious in vivo and can be recultured in vitro. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[164]  François-Loïc Cosset,et al.  HRas signal transduction promotes hepatitis C virus cell entry by triggering assembly of the host tetraspanin receptor complex. , 2013, Cell host & microbe.

[165]  D. Burton,et al.  Robust hepatitis C virus infection in vitro. , 2005, Proceedings of the National Academy of Sciences of the United States of America.