Mechanism of cell infection with hepatitis C virus [HCV] - a new paradigm in virus-cell interaction

• Autorzy: Budkowska A
• Języki publikacji: EN

Abstrakty

EN

Hepatitis C virus (HCV) is an enveloped, single-stranded RNA virus, belonging to the Flaviviridae family. HCV infection is a major cause of chronic hepatitis worldwide, leading to steatosis, liver cirrosis and hepatocellular carcinoma. Significant advances in understanding the mechanisms of HCV infection have been made since the development of a cell culture system reproducing the complete HCV cell cycle in vitro. HCV represents a new paradigm in interactions between the virus and its target cell, the human hepatocyte, due to the central role of lipoproteins in the HCV life cycle. Very low density lipoproteins are required for virus particle assembly and secretion. Upon the release, the infectious virus circulates in the blood as triglyceride-rich particles and infects cells using lipoprotein-receptor dependent mechanisms. HCV cell entry is a multi-step process: heparan sulphate and/or low-density lipoprotein receptor are cell surface factors mediating an initial virus attachment; subsequent virus interaction with tetraspanin CD81 and the human scavenger receptor SR-BI, the main HCV receptors, triggers virus movement to the tight junctions and its uptake via Claudin-1 and occludin. Another originality of HCV is that initiation of productive infection requires dynamic microtubules. Whereas other viruses use kinesin or dynein-dependent transport, HCV exploits mechanisms driven by microtubule polymerization to efficiently infect its target cell, in which virus nucleocapsid protein might play a particular role. An improved of understanding of the cellular-events involved in HCV cell entry and transport, leading to the initiation of productive HCV infection, may reveal novel targets for anti-viral interventions.

Słowa kluczowe

EN

cell infection; chronic liver disease; hepatitis C virus; virus-cell interaction; microtubule; lipoprotein; infection mechanism; cell receptor

• Wydawca: -
• Czasopismo: Polish Journal of Microbiology
• Rocznik: 2009
• Tom: 58
• Numer: 2
• Opis fizyczny: p.93-98,fig.,ref.

Twórcy

autor

Budkowska A

• Pasteur Institute, Hepacivirus and Innate Immunity, 25/28 Rue du Dr.Roux, 75724 Paris, France

Bibliografia

• Agnello V., G. Abel, M. Elfahal, G.B. Knight, and Q.X. Zhang. 1999. Hepatitis C virus and other flaviviridae viruses enter cells via low density lipoprotein receptor. Proc. Nat. Acad. Sci. USA 96: 12766-12771.
• André P., F. Komurian-Pradel, S. Deforges, M. Perret, J.L. Berland, M. Sodoyer, S. Pol, C. Brechot, G. Paranhos-Baccala and V. Lotteau. 2002. Characterization of low- and very-low-density hepatitis C virus RNA-containing particles. J. Virol. 76: 6919-6928.
• André P., G. Perlemuter, A. Budkowska, C. Brechot and V. Lotteau. 2005. Hepatitis C virus particles and lipoprotein metabolism. Sem. Liver Dis.25: 93-104.
• Andréo U., P. Maillard, O. Kalinina, M. Walic, E. Meurs, M. Martinot, P. Marcellin and A. Budkowska. 2007. Lipoprotein lipase mediates hepatitis C virus (HCV) cell entry and inhibits HCV infection. Cell Microbiol. 9: 2445-2456.
• Barba G., F. Harper, T. Harada, M. Kohara, S. Goulinet, Y. Matsuura, G. Eder, Z. Schaff, M. J. Chapman, T. Miyamura and C. Brechot. 1997. Hepatitis C virus core protein shows a cytoplasmic localization and associates to cellular lipid storage droplets. Proc. Nat. Acad. Sci. USA 94: 1200-1205.
• Bartenschlager, R., M. Frese and T. Pietschmann. 2004. Novel insights into hepatitis C virus replication and persistence. Adv. Virus Res. 63: 71-180.
• Barth H., C. Schafer, M.I. Adah, F. Zhang, R.J. Linhardt, H. Toyoda, A. Kinoshita-Toyoda, T. Toida, T.H. van Kuppevelt, E. Depla, F. von Weizsacker, H.E. Blum and T.F. Baumert. 2003. Cellular binding of hepatitis C virus envelope glycoprotein E2 requires cell surface heparan sulfate. J. Biol. Chem. 278: 41003-41012.
• Bartosch B., J. Dubuisson and F.L. Cosset. 2003. Infectious hepatitis C virus pseudo-particles containing functional E1-E2 envelope protein complexes. J. Exp. Med. 197: 633-642.
• Bartosch B., G. Verney, M. Dreux, P. Donot, Y. Morice, F. Penin, J.-M. Pawlotsky, D. Lavillette and F.-L. Cosset. 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.
• Blanchard E., S. Belouzard, L. Goueslain, T. Wakita, J. Dubuisson, C. Wychowski and Y. Rouille. 2006. Hepatitis C virus entry depends on clathrin-mediated endocytosis. J. Virol. 80: 6964-6972.
• Boulant S., M.W. Douglas, L. Moody, A. Budkowska, P. Targett-Adams and J. McLauchlan. 2008. Hepatitis C virus core protein induces lipid droplet redistribution in a microtubule-and dynein-dependent manner. Traffic. 9: 1268-1282.
• Boulant S., P. Targett-Adams and J. McLauchlan. 2007. Disrupting the association of hepatitis C virus core protein with lipid droplets correlates with a loss in production of infectious virus. J. Gen. Virol. 88: 2204-2213.
• Bradley D., K. McCaustland, K. Krawczynski, J. Spelbring, C. Humphrey and E.H. Cook. 1991. Hepatitis C virus: buoyant density of the factor VIII-derived isolate in sucrose. J. Med. Virol. 34: 206-208.
• Brass V., D. Moradpour and H.E. Blum. 2006. Molecular virology of hepatitis C virus (HCV): 2006 update. Int. J. Med. Sci. 3: 29-34.
• Brazzoli M., A. Bianchi, S. Filippini, A. Weiner, Q. Zhu, M. Pizza and S. Crotta. 2008. CD81 is a central regulator of cellular events required for hepatitis C virus infection of human hepatocytes. J. Virol. 82: 8316-8329.
• Bukh J. and R.H. Purcell. 2006. A milestone for hepatitis C virus research: A virus generated in cell culture is fully viable in vivo. Proc. Natl. Acad. Sci. USA 103: 3500-3501.
• Burlone M.E. and A. Budkowska. 2009. Hepatitis C virus cell entry: role of lipoproteins and cellular receptors. J. Gen. Virol. 90: 1055-1070.
• Chang K.S., J. Jiang, Z. Cai and G. Luo. 2007. Human apolipo-protein E is required for infectivity and production of hepatitis C virus in cell culture. J. Virol. 81: 13783-13793.
• Coyne C.B., L. Shen, J.R. Turner and J.M. Bergelson. 2007. Coxsackievirus entry across epithelial tight junctions requires occludin and the small GTPases Rab34 and Rab5. Cell. Host. Microb. 2: 181-192.
• Diaz O., F. Delers, M. Maynard, S. Demignot, F. Zoulim, J. Chambaz, C. Trepo, V. Lotteau and P. André. 2006. Preferential association of hepatitis C virus with apolipoprotein B48-containing lipoproteins. J. Gen. Virol. 87: 2983-2991.
• Dreux M., B. Boson, S. Ricard-Blum, J. Molle, D. Lavillette, B. Bartosch, E.I. Pecheur and F.L. Cosset. 2007. The exchangeable apolipoprotein ApoC-I promotes membrane fusion of hepatitis C virus. J. Biol. Chem. 282: 32357-32369.
• Evans M.J., T. von Hahn, D.M. Tscherne, A.J. Syder, M. Panis, B. Wolk, T. Hatziioannou, J.A. McKeating, P.D. Bieniasz and C.M. Rice. 2007. Claudin-1 is a hepatitis C virus co-receptor required for a late step in entry. Nature 446: 801-805.
• Gale M., Jr. and E.M. Foy. 2005. Evasion of intracellular host defence by hepatitis C virus. Nature 436: 939-45.
• Gastaminza P., G. Cheng, S. Wieland, J. Zhong, W. Liao and F.V. Chisari. 2008. Cellular determinants of hepatitis C virus assembly, maturation, degradation, and secretion. J. Virol. 82: 2120-2129.
• Gosert R., D. Egger, V. Lohmann, R. Bartenschlager, H.E. Blum, K. Bienz and D. Moradpour. 2003. Identification of the hepatitis C virus RNA replication complex in Huh-7 cells harbouring subgenomic replicons. J. Virol. 77: 5487-5492.
• Haberstroh A., E.K. Schnober, M.B. Zeisel, P. Carolla, H. Barth, H.E. Blum, F.L. Cosset, G. Koutsoudakis, R. Bartenschlager, A. Union, E. Depla, A. Owsianka, A.H. Patel, C. Schuster, F. Stoll-Keller, M. Doffoel, M. Dreux and T.F. Baumert. 2008. Neutralizing host responses in hepatitis C virus infection target viral entry at postbinding steps and membrane fusion. Gastroenterology 135: 1719-1728.
• Helle F., C. Wychowski, N. Vu-Dac, K.R. Gustafson, C. Voisset and J. Dubuisson. 2006. Cyanovirin-N inhibits hepatitis C virus entry by binding to envelope protein glycans. J. Biol. Chem. 281 : 25177-25183.
• Huang H., F. Sun, D.M. Owen, W. Li, Y. Chen, M. Gale, Jr. and J. Ye. 2007. Hepatitis C virus production by human hepatocytes is dependent on assembly and secretion of very low-density lipoproteins. Proc. Natl. Acad. Sci. USA 104: 5848-5853.
• Jones D.M., S.N. Gretton, J. McLauchlan and P. Targett-Adams. 2007. Mobility analysis of an NS5A-GFP fusion protein in cells actively replicating hepatitis C virus subgenomic RNA. J. Gen. Virol. 88: 470-475.
• Kapadia S.B. and F.V. Chisari. 2005. Hepatitis C virus RNA replication is regulated by host geranylgeranylation and fatty acids. Proc. Natl. Acad. Sci. USA 102: 2561-2566.
• Keam S.J. and R.S. Cvetkovic. 2008. Peginterferon-alpha-2a (40 kD) plus ribavirin: a review of its use in the management of chronic hepatitis C mono-infection. Drugs 68: 1273-1317.
• Koutsoudakis G., A. Kaul, E. Steinmann, S. Kallis, V. Lohmann, T. Pietschmann and R. Bartenschlager. 2006. Characterization of the early steps of hepatitis C virus infection by using luciferase reporter viruses. J. Virol. 80: 5308-5320.
• Lai C.K., K.S. Jeng, K. Machida and M.M. Lai. 2008. Association of hepatitis C virus replication complexes with microtubules and actin filaments is dependent on the interaction of NS3 and NS5A. J. Virol. 82: 8838-8848.
• Lanford R.E., M.J. Evans, V. Lohmann, B. Lindenbach, M. Gale, Jr., B. Rehermann, K.M. Chang and S.M. Lemon. 2009. The accelerating pace of HCV research: a summary of the 15th International Symposium on Hepatitis C Virus And Related Viruses. Gastroenterology 136: 9-16.
• Lavillette D., E.I. Pecheur, P. Donot, J. Fresquet, J. Molle, R. Corbau, M. Dreux, F. Penin and F.L. Cosset. 2007. Characterization of fusion detenninants 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.
• Lindenbach B.D., M.J. Evans, A.J. Syder, B. Wolk, T.L. Tellinghuisen, C.C. Liu, T. Maruyama, R.O. Hynes, D.R. Burton, J.A. McKeating and CM. Rice. 2005. Complete replication of hepatitis C virus in cell culture. Science 309: 623-626.
• Lindenbach B.D., P. Meuleman, A. Ploss, T. Vanwolleghem, A.J. Syder, J.A. McKeating, R.E. Lanford, S.M. Feinstone, M.E. Major, G. Leroux-Roels and CM. Rice. 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.
• Liu S., W. Yang, L. Shen, J.R. Turner, C.B. Coyne and T. Wang. 2008. Tight junction proteins Claudin-1 and occludin control hepatitis C virus entry and are down-regulated during infection to prevent superinfection. J. Virol. 83: 2011-2014.
• Maillard P., T. Huby, U. Andréo, M. Moreau, J. Chapman and A. Budkowska. 2006. The interaction of natural hepatitis C vims with human scavenger receptor SR-BI/Cla 1 is mediated by ApoB-containing lipoproteins. FASEB J. 20: 735-737.
• Maillard P., K. Krawczynski, J. Nitkiewicz, C. Bronnert, M. Sidorkicwicz, P. Gounon, J. Dubuisson, G. Faure, R. Crainte and A. Budkowska. 2001. Nonenveloped nucleocapsids of hepatitis C vims in the serum of infected patients. J. Virol. 75: 8240-8250.
• Maillard P., J.P. Lavergne, S. Siberil, G. Faure, F. Roohvand, S. Petres, J.L. Teillaud and A. Budkowska. 2004. Fcgamma receptor-like activity of hepatitis C vims core protein. J. Biol. Chem. 279: 2430-2437.
• Masciopinto R, C. Giovani, S. Campagnoli, L. Galli-Stampino, P. Colombatto, M. Brunetto, T.S. Yen, M. Houghton, P. Pileri and S. Abrignani. 2004. Association of hepatitis C virus envelope proteins with exosomes. Eur. J. Immunol. 34: 2834-2842.
• Meertens L., C. Bertaux and T. Dragic. 2006. Hepatitis C virus entry requires a critical postinternalization step and delivery to early endosomes via clathrin-coated vesicles. J. Virol. 80: 11571-11578.
• Meunier J.-C., R.E. Engle, K. Faulk, M. Zhao, B. Bartosch, H. Alter, S.U. Emerson, F.-L. Cosset, R.H. Purcell and J. Bukh. 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.
• Meurs E.F. and A. Breiman. 2007. The interferon inducing pathways and the hepatitis C virus. World J. Gastroenterol. 7: 2446-2454.
• Miyanari Y., K. Atsuzawa, N. Usuda, K. Watashi, T. Hishiki, M. Zayas, R. Bartenschlager, T. Wakita, M. Hijikata and K. Shimotohno. 2007. The lipid droplet is an important organelle for hepatitis C virus production. Nature Cell. Biol. 9: 1089-1097.
• Molina S., D. Missé, S. Roche, S. Badiou, J.P. Cristol, C. Bonfils, J.F. Dierick, F. Veas, T. Levayer, D. Bonnefont-Rousselot, P. Maurel, J. Coste and C. Fournier-With. 2008. Identification of ApoC-III as a potential plasmatic biomarker associated with the resolution of HCV infection. Proteomics Clin. Appl. 2: 751-761.
• Monazahian M., I. Bohme, S. Bonk, A. Koch, C. Scholz, S. Grethe and R. Thomssen. 1999. Low density lipoprotein receptor as a candidate receptor for hepatitis C virus. J. Med. Virol. 57: 223-229.
• Nielsen S.U., M.F. Bassendine, A.D. Burt, C. Martin, W. Pumeechockchai and G.L. Toms. 2006. Association between hepatitis C virus and very-low-density lipoprotein (VLDL)/LDL analyzed in iodixanol density gradients. J. Virol. 80: 2418-2428.
• Pawlotsky J.M. 2006. Therapy of hepatitis C: from empiricism to eradication. Hepatology 43: S207-220.
• Penin R, J. Dubuisson, F.A. Rey, D. Moradpour and J.M. Pawlotsky. 2004. Structural biology of hepatitis C virus. Hepatology 39: 5-19.
• Petit J.M., M. Benichou, L. Duvillard, V. Jooste, J.B. Bour, A. Minello, B. Verges, J.M. Brun, P. Gambert and P. Hillon. 2003. Hepatitis C virus-associated hypobetalipoproteinemia is correlated with plasma viral load, steatosis, and liver fibrosis. Am. J. Gastroenterol. 98: 1150-1154.
• Petit M.A., M. Lievre, S. Peyrol, S. Dc Sequeira, P. Berthillon, R. W. Ruigrok and C. Trepo. 2005. Enveloped particles in the serum of chronic hepatitis C patients. Virology 336: 144-153.
• Pietschmann T. 2009. Virology: Final entry key for hepatitis C. Nature 457: 797-798.
• Pileri P., Y. Uematsu, S. Campagnoli, G. Galli, F. Falugi, R. Petracca, A.J. Weiner, M. Houghton, D. Rosa, G. Grandi and S. Abrignani. 1998. Binding of hepatitis C virus to CD81. Science 282: 938-941.
• Ploss A., M.J. Evans, V.A. Gaysinskaya, M. Panis, H. You, Y.P. de Jong and C.M. Rice. 2009. Human occludin is a hepatitis C virus entry factor required for infection of mouse cells. Nature 457: 882-886.
• Radtke K., K. Dohner and B. Sodeik. 2006. Viral interactions with the cytoskeleton: a hitchhiker's guide to the cell. Cell. Microbiol. 8: 387-400.
• Rehermann B. and M. Nascimbeni. 2005. Immunology of hepatitis B virus and hepatitis C virus infection. Nat. Rev. Immunol. 5: 215-229.
• Rocha-Perugini V., C. Montpellier, D. Delgrange, C. Wychowski, F. Helle, A. Pillez, H. Drobecq, F. Le Naour, S. Charrin, S. Levy, E. Rubinstein, J. Dubuisson and L. Cocquercl. 2008. The CD81 partner EWI-2wint inhibits hepatitis C virus entry. PLoS ONE 3: e1866.
• Rodinov V.I. and G.G. Borisy. 1997. Microtubules treadmilling in vivo. Science 275: 215-218.
• Roohvand R, P. Maillard, J.P. Lavergne, S. Boulant, M. Walic, U. Andréo, L. Goueslain, F. Helle, A. Mallet, J. McLauchlan and A. Budkowska. 2009. Initiation of hepatitis C virus infection requires the dynamic microtubule network: Role of the viral nucleocapsid protein. J. Biol. Chem. 284: 13778-13791.
• Scarselli E., H. Ansuini, R. Cerino, R.M. Roccasccca, S. Acali, G. Filocamo, C. Traboni, A. Nicosia, R. Cortese and A. Vitelli. 2002. The human scavenger receptor class B type I is a novel candidate receptor for the hepatitis C virus. EMBO J. 21:5017-5025.
• Shepard C.W., L. Finelli and M.J. Alter. 2005. Global epidemiology of hepatitis C virus infection. Lancet Infect. Dis. 5: 558-567.
• Shin K., V.C. Fogg and B. Margolis. 2006. Tight junctions and cell polarity.Mnn. Rev. Cell Dev. Biol. 22: 207-235.
• Simmonds P., J. Bukh, C. Combet, G. Deleage, N. Enomoto, S. Feinstone, P. Halfon, G. Inchauspe, C. Kuiken, G. Maertens, etal. 2005. Consensus proposals for a unified system of nomenclature of hepatitis C virus genotypes. Hepatology 42: 962-73.
• Thomssen R., S. Bonk, C. Propfe, K.H. Heermann, H.G. Kochel and A. Uy. 1992. Association of hepatitis C virus in human sera with beta-lipoprotein. Med. Microbiol. Immunol. 181: 293-300.
• Voisset C, N. Callens, E. Blanchard, A. Op De Beeck, J. Dubuisson and N. Vu-Dac. 2005. High density lipoproteins facilitate hepatitis C virus entry through the scavenger receptor class B type I. J. Biol. Chem. 280: 7793-7799.
• von Hahn T., B.D. Lindenbach, A. Boullier, O. Quehenberger, M. Paulson, C.M. Rice and J.A. McKeating. 2006. Oxidized low-density lipoprotein inhibits hepatitis C virus cell entry in human hepatoma cells. Hepatology 43: 932-942.
• Wakita T., T. Pietschmann, T. Kato, T. Date, M. Miyamoto, Z. Zhao, K. Murthy, A. Habermann, H. G. Krausslich, M. Mizokami, R. Bartenschlager and T.J. Liang. 2005. Production of infectious hepatitis C virus in tissue culture from a cloned viral genome. Nature Med. 11: 791-796.
• Wolk B., B. Buchele, D. Moradpour and C.M. Rice. 2008. A dynamic view of hepatitis C virus replication complexes. J. Virol. 82: 10519-10531.
• Ye J. 2007. Reliance of host cholesterol metabolic pathways for the life cycle of hepatitis C virus. PLoS Pathogen 3: e108.
• Zheng A., F. Yuan, Y. Li, F. Zhu, P. Hou, J. Li, X. Song, M. Ding and H. Deng. 2007. Claudin-6 and Claudin-9 function as additional coreceptors for hepatitis C virus. J. Virol. 81: 12465-12471.