Viral and cellular determinants of the hepatitis C virus envelope-heparan sulfate interaction

Journal of Virology

Volumn 80, Issue 21, 2006, Pages 10579-10590

  Barth, Heidi ^a   Schnober, Eva K ^a   Zhang, Fuming ^b   Linhardt, Robert J ^b   Depla, Erik ^c   Boson, Bertrand ^d   Cosset, Francois Loic ^d   Patel, Arvind H ^e   Blum, Hubert E ^a   Baumert, Thomas F ^a,f  

^a UNIVERSITY OF FREIBURG   (Germany)

^b RENSSELAER POLYTECHNIC INSTITUTE   (United States)

^c INNOGENETICS   (Belgium)

^d UNIVERSITÉ DE LYON   (France)

^e INSTITUTE OF VIROLOGY   (United Kingdom)

^f INSERM   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CARBOHYDRATE; EPITOPE; GLYCOPROTEIN E2; HEPARAN SULFATE; RECOMBINANT PROTEIN; SULFATE; VIRUS ANTIBODY;

ARTICLE; CONTROLLED STUDY; HEPATITIS C VIRUS; HOST CELL; HUMAN; HUMAN CELL; IMMUNE RESPONSE; NONHUMAN; PRIORITY JOURNAL; TARGET CELL; VIRUS ADSORPTION; VIRUS CELL INTERACTION; VIRUS ENVELOPE; VIRUS INFECTION; VIRUS PARTICLE;

ANIMALS; ANTIBODIES, VIRAL; ANTIGENS, VIRAL; BINDING SITES; CELL LINE; EPITOPE MAPPING; HELA CELLS; HEPACIVIRUS; HEPARITIN SULFATE; HEPATITIS C, CHRONIC; HUMANS; MICE; PROTEIN BINDING; RECOMBINANT PROTEINS; SURFACE PLASMON RESONANCE; VIRAL ENVELOPE PROTEINS; VIRULENCE;

HEPATITIS C VIRUS; HEPATITIS C VIRUS (ISOLATE H);

EID: 33750356630     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.00941-06     Document Type: Article

References (54)

1. Bain, C., A. Fatmi, F. Zoulim, J. P. Zarski, C. Trepo, and G. Inchauspe. 2001. Impaired allostimulatory function of dendritic cells in chronic hepatitis C infection. Gastroenterology 120:512-524.
2. 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.
3. 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.
4. Bartosch, B., A. Vitelli, C. Granier, C. Goujon, J. Dubuisson, S. Pascale, E. Scarselli, R. Cortese, A. Nicosia, and F. L. Cosset. 2003. Cell entry of hepatitis C virus requires a set of co-receptors that include the CD81 tetraspanin and the SR-B1 scavenger receptor. J. Biol. Chem. 278:41624-41630.
5. Baumert, T. F., S. Ito, D. T. Wong, and T. J. Liang. 1998. Hepatitis C virus structural proteins assemble into viruslike particles in insect cells. J. Virol. 72:3827-3836.
6. Baumert, T. F., S. Wellnitz, S. Aono, J. Satoi, D. Herion, J. Tilman Gerlach, G. R. Pape, J. Y. Lau, J. H. Hoofnagle, H. E. Blum, and T. J. Liang. 2000. Antibodies against hepatitis C virus-like particles and viral clearance in acute and chronic hepatitis C. Hepatology 32:610-617.
7. Birkmann, A., K. Mahr, A. Ensser, S. Yaǧuboǧlu, F. Titgemeyer, B. Fleckenstein, and F. Neipel. 2001. Cell surface heparan sulfate is a receptor for human herpesvirus 8 and interacts with envelope glycoprotein K8.1. J. Virol. 75:11583-11593.
8. Callens, N., Y. Ciczora, B. Bartosch, N. Vu-Dac, F. L. Cosset, J.-M. Pawlotsky, F. Penin, and J. Dubuisson. 2005. Basic residues in hypervariable region 1 of hepatitis C virus envelope glycoprotein E2 contribute to virus entry. J. Virol. 79:15331-15341.
9. Chen, Y., T. Maguire, R. E. Hileman, J. R. Fromm, J. D. Esko, R. J. Linhardt, and R. M. Marks. 1997. Dengue virus infectivity depends on envelope protein binding to target cell heparan sulfate. Nat. Med. 3:866-871.
10. Chisari, F. V. 2005. Unscrambling hepatitis C virus-host interactions. Nature 436:930-932.
11. Clayton, R. F., A. Owsianka, J. Aitken, S. Graham, D. Bhella, and A. H. Patel. 2002. Analysis of antigenicity and topology of E2 glycoprotein present on recombinant hepatitis C virus-like particles. J. Virol. 76:7672-7682.
12. Esko, J. D., and U. Lindahl. 2001. Molecular diversity of heparan sulfate. J. Clin. Investig. 108:169-173.
13. Farci, P., A. Shimoda, D. Wong, T. Cabezon, D. De Gioannis, A. Strazzera, Y. Shimizu, M. Shapiro, H. J. Alter, and R. H. Purcell. 1996. Prevention of hepatitis C virus infection in chimpanzees by hyperimmune serum against the hypervariable region 1 of the envelope 2 protein. Proc. Natl. Acad. Sci. USA 93:15394-15399.
14. Feld, J. J., and J. H. Hoofnagle. 2005. Mechanism of action of interferon and ribavirin in treatment of hepatitis C. Nature 436:967-972.
15. Germi, R., J. M. Crance, D. Garin, J. Guimet, H. Lortat-Jacob, R. W. Ruigrok, J. P. Zarski, and E. Drouet. 2002. Cellular glycosaminoglycans and low density lipoprotein receptor are involved in hepatitis C virus adsorption. J. Med. Virol. 68:206-215.
16. Hallak, L. K., D. Spillmann, P. L. Collins, and M. E. Peeples. 2000. Glycosaminoglycan sulfation requirements for respiratory syncytial virus infection. J. Virol. 74:10508-10513.
17. Hsu, M., J. Zhang, M. Flint, C. Logvinoff, C. Cheng-Mayer, C. M. Rice, and J. A. McKeating. 2003. Hepatitis C virus glycoproteins mediate pH-dependent cell entry of pseudotyped retroviral particles. Proc. Natl. Acad. Sci. USA 100:7271-7276.
18. Hulst, M. M., H. G. van Gennip, A. C. Vlot, E. Schooten, A. J. de Smit, and R. J. M. Moormann. 2001. Interaction of classical swine fever virus with membrane-associated heparan sulfate: role for virus replication in vivo and virulence. J. Virol. 75:9585-9595.
19. 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.
20. Lambot, M., S. Fretier, A. Op De Beeck, B. Quatannens, S. Lestavel, V. Clavey, and J. Dubuisson. 2002. Reconstitution of hepatitis C virus envelope glycoproteins into liposomes as a surrogate model to study virus attachment. J. Biol. Chem. 277:20625-20630.
21. Lee, E., M. Pavy, N. Young, C. Freeman, and M. Lobigs. 2006. Antiviral effect of the heparan sulfate mimetic, PI-88, against dengue and encephalitic flaviviruses. Antivir. Res. 69:31-38.
22. 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 C. M. Rice. 2005. Complete replication of hepatitis C virus in cell culture. Science 309:623-626.
23. Lindenbach, B. D., and C. M. Rice. 2005. Unravelling hepatitis C virus replication from genome to function. Nature 436:933-938.
24. Liu, J., Z. Shriver, M. Pope, S. C. Thorp, M. B. Duncan, R. J. Copeland, C. S. Raska, K. Yoshida, R. J. Eisenberg, G. Cohen, R. J. Linhardt, and R. Sasisekharan. 2002. Characterization of a heparan sulfate octasaccharide that binds to herpes simplex viral type 1 glycoprotein D. J. Biol. Chem. 277:33456-33467.
25. Lozach, P. Y., A. Amara, B. Bartosch, J. L. Virelizier, F. Arenzana-Seisdedos, F. L. Cosset, and R. Altmeyer. 2004. C-type lectins L-SIGN and DC-SIGN capture and transmit infectious hepatitis C virus pseudotype particles. J. Biol. Chem. 279:32035-32045.
26. Ludwig, I. S., A. N. Lekkerkerker, E. Depla, F. Bosman, R. J. P. Musters, S. Depraetere, Y. van Kooyk, and T. B. Geijtenbeek. 2004. Hepatitis C virus targets DC-SIGN and L-SIGN to escape lysosomal degradation. J. Virol. 78:8322-8332.
27. Mahoney, D. J., J. D. Whittle, C. M. Milner, S. J. Clark, B. Mulloy, D. J. Buttle, G. C. Jones, A. J. Day, and R. D. Short. 2004. A method for the non-covalent immobilization of heparin to surfaces. Anal. Biochem. 330:123-129.
28. Mandl, C. W., H. Kroschewski, S. L. Allison, R. Kofler, H. Holzmann, T. Meixner, and F. X. Heinz. 2001. Adaptation of tick-borne encephalitis virus to BHK-21 cells results in the formation of multiple heparan sulfate binding sites in the envelope protein and attenuation in vivo. J. Virol. 75:5627-5637.
29. Margalit, H., N. Fischer, and S. A. Ben-Sasson. 1993. Comparative analysis of structurally defined heparin binding sequences reveals a distinct spatial distribution of basic residues. J. Biol. Chem. 268:19228-19231.
30. Marks, R. M., H. Lu, R. Sundaresan, T. Toida, A. Suzuki, T. Imanari, M. J. Hernaiz, and R. J. Linhardt. 2001. Probing the interaction of dengue virus envelope protein with heparin: assessment of glycosaminoglycan-derived inhibitors. J. Med. Chem. 44:2178-2187.
31. Munoz, E. M., and R. J. Linhardt. 2004. Heparin-binding domains in vascular biology. Arterioscler. Thromb. Vasc. Biol. 24:1549-1557.
32. Opitz, O. G., Y. Suliman, W. C. Hahn, H. Harada, H. E. Blum, and A. K. Rustgi. 2001. Cyclin D1 overexpression and p53 inactivation immortalize primary oral keratinocytes by a telomerase-independent mechanism. J. Clin. Investig. 108:725-732.
33. Penin, F., C. Combet, G. Germanidis, P.-O. Frainais, G. Deléage, and J.-M. Pawlotsky. 2001. Conservation of the conformation and positive charges of hepatitis C virus E2 envelope glycoprotein hypervariable region 1 points to a role in cell attachment. J. Virol. 75:5703-5710.
34. Pervin, A., C. Gallo, K. A. Jandik, X. J. Han, and R. J. Linhardt. 1995. Preparation and structural characterization of large heparin-derived oligosaccharides. Glycobiology 5:83-95.
35. 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.
36. Rabenstein, D. L. 2002. Heparin and heparan sulfate: structure and function. Nat. Prod. Rep. 19:312-331.
37. Rosa, D., S. Campagnoli, C. Moretto, E. Guenzi, L. Cousens, M. Chin, C. Dong, A. Weiner, J. Y. N. Lau, Q.-L. Choo, D. Chien, P. Pileri, M. Houghton, and S. Abrignani. 1996. A quantitative test to estimate neutralizing antibodies to the hepatitis C virus: cytofluorimetric assessment of envelope glycoprotein 2 binding to target cells. Proc. Natl. Acad. Sci. USA 93:1759-1763.
38. Scarselli, E., H. Ansuini, R. Cerino, R. M. Roccasecca, 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.
39. Shafti-Keramat, S., A. Handisurya, E. Kriehuber, G. Meneguzzi, K. Slupetzky, and R. Kirnbauer. 2003. Different heparan sulfate proteoglycans serve as cellular receptors for human papillomaviruses. J. Virol. 77:13125-13135.
40. Shukla, D., J. Liu, P. Blaiklock, N. W. Shworak, X. Bai, J. D. Esko, G. H. Cohen, R. J. Eisenberg, R. D. Rosenberg, and P. G. Spear. 1999. A novel role for 3-O-sulfated heparan sulfate in herpes simplex virus 1 entry. Cell 99:13-22.
41. Steinmann, D., H. Barth, B. Gissler, P. Schürmann, M. I. Adah, J. T. Gerlach, G. R. Pape, E. Depla, D. Jacobs, G. Maertens, A. H. Patel, G. Inchauspé, T. J. Liang, H. E. Blum, and T. F. Baumert. 2004. Inhibition of hepatitis C virus-like particle binding to target cells by antiviral antibodies in acute and chronic hepatitis C. J. Virol. 78:9030-9040.
42. Tarr, A. W., A. M. Owsianka, J. M. Timms, C. P. McClure, R. J. Brown, T. P. Hickling, T. Pietschmann, R. Bartenschlager, A. H. Patel, J. K. Ball, A. Owsianka, V. S. Juttla, D. Lavillette, B. Bartosch, and F. L. Cosset. 2006. Characterization of the hepatitis C virus E2 epitope defined by the broadly neutralizing monoclonal antibody AP33. Hepatology 43:592-601.
43. Toida, T., R. E. Hileman, A. E. Smith, P. I. Vlahova, and R. J. Linhardt. 1996. Enzymatic preparation of heparin oligosaccharides containing antithrombin III binding sites. J. Biol. Chem. 271:32040-32047.
44. Toida, T., H. Yoshida, H. Toyoda, I. Koshiishi, T. Imanari, R. E. Hileman, J. R. Fromm, and R. J. Linhardt. 1997. Structural differences and the presence of unsubstituted amino groups in heparan sulphates from different tissues and species. Biochem. J. 322:499-506.
45. van Doorn, L. J., K. van Hoek, G. de Martinoff, F. Bosman, L. Stuyver, T. Kos, I. Frantzen, P. Sillekens, G. Maertens, and W. Quint. 1997. Serological and molecular analysis of hepatitis C virus envelope regions 1 and 2 during acute and chronic infections in chimpanzees. J. Med. Virol. 52:441-450.
46. Vives, R. R., A. Imberty, Q. J. Sattentau, and H. Lortat-Jacob. 2005. Heparan sulfate targets the HIV-1 envelope glycoprotein gp120 coreceptor binding site. J. Biol. Chem. 280:21353-21357.
47. Vongchan, P., M. Warda, H. Toyoda, T. Toida, R. M. Marks, and R. J. Linhardt. 2005. Structural characterization of human liver heparan sulfate. Biochim. Biophys. Acta 1721:1-3.
48. 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. Nat. Med. 11:791-796.
49. Wellnitz, S., B. Klumpp, H. Barth, S. Ito, E. Depla, J. Dubuisson, H. E. Blum, and T. F. Baumert. 2002. Binding of hepatitis C virus-like particles derived from infectious clone H77C to defined human cell lines. J. Virol. 76:1181-1193.
50. Yagnik, A. T., A. Lahm, A. Meola, R. M. Roccasecca, B. B. Ercole, A. Nicosia, and A. Tramontano. 2000. A model for the hepatitis C virus envelope glycoprotein E2. Proteins 40:355-366.
51. Yanagi, M., M. St. Claire, M. Shapiro, S. U. Emerson, R. H. Purcell, and J. Bukh. 1998. Transcripts of a chimeric cDNA clone of hepatitis C virus genotype 1b are infectious in vivo. Virology 244:161-172.
52. Yu, G., N. S. Gunay, R. J. Linhardt, T. Toida, J. Fareed, D. A. Hoppensteadt, H. Shadid, V. Ferro, C. Li, K. Fewings, M. C. Palermo, and D. Podger. 2002. Preparation and anticoagulant activity of the phosphosulfomannan PI-88. Eur. J. Med. Chem. 37:783-791.
53. Zahn, A., and J. P. Allain. 2005. Hepatitis C virus and hepatitis B virus bind to heparin: purification of largely IgG-free virions from infected plasma by heparin chromatography. J. Gen. Virol. 86:677-685.
54. Zhong, J., P. Gastaminza, G. Cheng, S. Kapadia, T. Kato, D. R. Burton, S. F. Wieland, S. L. Uprichard, T. Wakita, and F. V. Chisari. 2005. Robust hepatitis C virus infection in vitro. Proc. Natl. Acad. Sci. USA 102:9294-9299.