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

Journal of Virology

Volumn 77, Issue 3, 2003, Pages 1856-1867

  Roccasecca, RosaMaria ^a   Ansuini, Helenia ^a   Vitelli, Alessandra ^a   Meola, Annalisa ^a   Scarselli, Elisa ^a   Acali, Stefano ^a   Pezzanera, Monica ^a   Bruni Ercole, Bruno ^a   McKeating, Jane ^b   Yagnik, Asutosh ^a   Lahm, Armin ^a   Tramontano, Anna ^a,c   Cortese, Riccardo ^a   Nicosia, Alfredo ^a  

^a IRBM   (Italy)

^b ROCKEFELLER UNIVERSITY   (United States)

^c SAPIENZA UNIVERSITY OF ROME   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

CD81 ANTIGEN; GLYCOPROTEIN E2; MONOCLONAL ANTIBODY; UNCLASSIFIED DRUG; VIRUS GLYCOPROTEIN; VIRUS RECEPTOR;

AMINO TERMINAL SEQUENCE; ARTICLE; COMPUTER MODEL; CONTROLLED STUDY; HEPATITIS C VIRUS; HUMAN; HUMAN CELL; LIVER CELL; MOLECULAR INTERACTION; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN VARIANT; VIRUS ISOLATION;

AMINO ACID SEQUENCE; ANTIGENS, CD; CELL LINE; HUMANS; LIVER; MEMBRANE PROTEINS; MOLECULAR SEQUENCE DATA; SPECIES SPECIFICITY; VIRAL ENVELOPE PROTEINS;

EID: 0037301359     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.77.3.1856-1867.2003     Document Type: Article

References (45)

1. Aizaki, H., Y. Aoki, T. Harada, K. Ishii, T. Suzuki, S. Nagamori, G. Toda, Y. Matsuura, and T. Miyamura. 1998. Full-length complementary DNA of hepatitis C virus genome from an infectious blood sample. Hepatology 27: 621-627.
2. Allander, T., K. Drakenberg, A. Beyene, D. Rosa, S. Abrignani, M. Houghton, A. Widell, L. Grillner, and M. A. Persson. 2000. Recombinant human monoclonal antibodies against different conformational epitopes of the E2 envelope glycoprotein of hepatitis C virus that inhibit its interaction with CD81. J. Gen. Virol. 10:2451-2459.
3. Bartenschlager, R. 2002. In vitro models for hepatitis C. Virus Res. 82:25-32.
4. Burioni, R., F. Bugli, N. Mancini, D. Rosa, C. Di Campli, G. Moroncini, A. Manzin, S. Abrignani, P. E. Varaldo, M. Clementi, and G. Fadda. 2001. Nonneutralizing human antibody fragments against hepatitis C virus E2 glycoprotein modulate neutralization of binding activity of human recombinant Fabs. Virology 288:29-35.
5. Choo, Q. L., G. Kuo, R. Ralston, A. Weiner, D. Chien, G. Van Nest, J. Han, et al. 1994. Vaccination of chimpanzees against infection by the hepatitis C virus. Proc. Natl. Acad. Sci. USA 91:1294-1298.
6. Crotta, S., A. Stilla, A. Wack, A. D'Andrea, S. Nuti, U. D'Oro, M. Mosca, F. Filliponi, R. M. Brunetto, F. Bonino, S. Abrignani, and N. M. Valiante. 2002. Inhibition of natural killer cells through engagement of CD81 by the major hepatitis C virus envelope protein. J. Exp. Med. 195:35-41.
7. Deleersnyder, V., A. Pillez, C. Wychowski, K. Blight, J. Xu, Y. S. Hahn, C. M. Rice, and J. Dubuisson. 1997. Formation of native hepatitis C virus glycoprotein complexes. J. Virol. 71:697-704.
8. Donnelly, J. J., D. Martinez, K. U. Jansen, R. W. Ellis, D. L. Montgomery, and M. A. Liu. 1996. Protection against papillomavirus with a polynucleotide vaccine. J. Infect. Dis. 173:314-320.
9. Everhart, J. E., M. Stolar, and J. H. Hoofnagle. 1997. Management of hepatitis C: a national survey of gastroenterologists and hepatologists. Hepatology 26:78S-82S.
10. Farci, P., H. J. Alter, D. C. Wong, R. H. Miller, S. Govindarajan, R. Engle, M. Shapiro, and R. H. Purcell. 1994. Prevention of hepatitis C virus infection in chimpanzees after antibody-mediated in vitro neutralization. Proc. Natl. Acad. Sci. USA 16:7792-7796.
11. Farci, P. A., D. Shimoda, T. Wong, D. Cabezon, A. De Gioannis, A. Strazzera, Y. Shimizu, et al. 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 96:15394-15399.
12. Flint, M., J. Dubuisson, C. Maidens, R. Harrop, G. R. Guile, P. Borrow, and J. A. McKeating. 2000. Functional characterization of intracellular and secreted forms of a truncated hepatitis C virus E2 glycoprotein. J. Virol. 74:702-709.
13. Flint, M., C. Maidens, L. D. Loomis-Price, C. Shotton, J. Dubuisson, P. Monk, A. Higginbottom, S. Levy, and J. A. McKeating. 1999. Characterization of hepatitis C virus E2 glycoprotein interaction with a putative cellular receptor, CD81. J. Virol. 73:6235-6244.
14. Fournillier, A., E. Depla, P. Karayiannis, O. Vidalin, G. Maertens, C. Trepo, and G. Inchauspe. 1999. Expression of noncovalent hepatitis C virus envelope E1-E2 complexes is not required for the induction of antibodies with neutralizing properties following DNA immunization. J. Virol. 73:7497-7504.
15. Fried, M. W., and J. H. Hoofnagle. 1995. Therapy of hepatitis C. Semin. Liver Dis. 15:82-91.
16. Hadlock, K. G., R. E. Lanford, S. Perkins, J. Rowe, Q. Yang, S. Levy, P. Pileri, S. Abrignani, and S. K. Foung. 2000. Human monoclonal antibodies that inhibit binding of hepatitis C virus E2 protein to CD81 and recognize conserved conformational epitopes. J. Virol. 74:10407-10416.
17. Higginbottom, A., E. R. Quinn, C. C. Kuo, M. Flint, L. H. Wilson, E. Bianchi, A. Nicosia, P. N. Monk, J. A. McKeating, and S. Levy. 2000. Identification of amino acid residues in CD81 critical for interaction with hepatitis C virus envelope glycoprotein E2. J. Virol. 74:3642-3649.
18. Ishii, K., D. Rosa, Y. Watanabe, T. Katayama, H. Harada, C. Wyatt, K. Kiyosawa, H. Aizaki, Y. Matsuura, M. Houghton, S. Abrignani, and T. Miyamura. 1998. High titers of antibodies inhibiting the binding of envelope to human cells correlate with natural resolution of chronic hepatitis C. Hepatology 28:1117-1120.
19. Jaeckel, E., M. Cornberg, H. Wedemeyer, T. Santantonio, J. Mayer, M. Zankel, G. Pastore, M. Dietrich, C. Trautwein, M. P. Manns, et al. 2001. Treatment of acute hepatitis C with interferon alfa-2b. N. Engl. J. Med. 345:1452-1457.
20. Kato, N., H. Sekiya, Y. Ootsuyama, T. Nakazawa, M. Hijikata, S. Ohkoshi, and K. Shimotohno. 1993. Humoral immune response to hypervariable region 1 of the putative envelope glycoprotein (gp70) of hepatitis C virus. J. Virol. 67:3923-3930.
21. Kitadokoro, K., D. Bordo, G. Galli, R. Petracca, F. Falugi, S. Abrignani, G. Grandi, and M. Bolognesi. 2001. CD81 extracellular domain 3D structure: insight into the tetraspanin superfamily structural motifs. EMBO J. 20:12-18.
22. Kojima, M., T. Osuga, F. Tsuda, T. Tanaka, and H. Okamoto. 1994. Influence of antibodies to the hypervariable region of E2/NS1 glycoprotein on the selective replication of hepatitis C virus in chimpanzees. Virology 204:665-672.
23. Lescar, J., A. Roussel, M. W. Wien, J. Navaza, S. D. Fuller, G. Wengler, G. Wengler, and F. A. Rey. 2001. The fusion glycoprotein shell of Semliki Forest virus: an icosahedral assembly primed for fusogenic activation at endosomal pH. Cell 105:137-148.
24. Levy, S., S. C. Todd, and H. T. Maecker. 1998. CD81 (TAPA-1): a molecule involved in signal transduction and cell adhesion in the immune system. Annu. Rev. Immunol. 16:89-109.
25. Li, C., D. Candotti, and J. P. Allain. 2001. Production and characterization of monoclonal antibodies specific for a conserved epitope within hepatitis C virus hypervariable region 1. J. Virol. 75:12412-12420.
26. McHutchison, J. G., S. C. Gordon, E. R. Schiff, M. L. Shiffman, W. M. Lee, V. K. Rustgi, Z. D. Goodman, et al. 1998. Interferon alfa-2b alone or in combination with ribavirin as initial treatment for chronic hepatitis C. N. Engl. J. Med. 339:1485-1492.
27. Meola, A., A. Sbardellati, B. Bruni Ercole, M. Cerretani, M. Pezzanera, A. Ceccacci, A. Vitelli, S. Levy, A. Nicosia, C. Traboni, J. McKeating, and E. Scarselli. 2000. Binding of hepatitis C virus E2 glycoprotein to CD81 does not correlate with species permissiveness to infection. J. Virol. 74:5933-5938.
28. Michalak, J. P., C. Wychowski, A. Choukhi, J. C. Meunier, S. Ung, C. M. Rice, and J. Dubuisson. 1997. Characterization of truncated forms of hepatitis C virus glycoproteins. J. Gen. Virol. 78:2299-2306.
29. Owsianka, A., R. F. Clayton, L. D. Loomis-Price, J. A. McKeating, and A. H. Patel. 2001. Functional analysis of hepatitis C virus E2 glycoproteins and virus-like particles reveals structural dissimilarities between different forms of E2. J. Gen. Virol. 82:1877-1883.
30. Patel, A. H., J. Wood, F. Penin, J. Dubuisson, and J. A. McKeating. 2000. Construction and characterization of chimeric hepatitis C virus E2 glycoproteins: analysis of regions critical for glycoprotein aggregation and CD81 binding. J. Gen. Virol. 12:2873-2883.
31. Penin, F., C. Combet, G. Germanidis, P. O. Frainais, G. Deleage, 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.
32. 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 human CD81. Science 282:938-941.
33. Puntoriero, G., A. Meola, A. Lahm, S. Zucchelli, B. Bruni Ercole, R. Tafi, M. Pezzanera, M. U. Mondelli, R. Cortese, A. Tramontano, G. Galfrè, and A. Nicosia. 1998. Towards a solution for hepatitis C virus hypervariability: mimotopes of the hypervariable region 1 can induce antibodies cross-reacting with a large number of viral variants. EMBO J. 17:3521-3533.
34. Rey, F. A., F. X. Heinz, C. Mandl, C. Kunz, and S. C. Harrison. 1995. The envelope glycoprotein from tick-borne encephalitis virus at 2 Å resolution. Nature 375:291-298.
35. Rosa, D., S. Campagnoli, C. Moretto, E. Guenzi, L. Cousens, M. Chin, C. Dong, A. J. Weiner, J. Y. 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.
36. Scarselli, E., H. Ansuini, R. Cerino, R. 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.
37. Shimizu, Y. K., M. Hijikata, A. Iwamoto, H. J. Alter, R. H. Purcell, and H. Yoshikura. 1994. Neutralizing antibodies against hepatitis C virus and the emergence of neutralization escape mutant viruses. J. Virol. 65:1494-1500.
38. Sobolev, B. N., V. V. Poroikov, L. V. Olenina, E. F. Kolesanova, and A. L. Archakov. 2000. Comparative analysis of amino acid sequences from envelope proteins isolated from different hepatitis C virus variants: possible role of conservative and variable regions. J. Viral. Hepatol. 7:368-374.
39. Tseng, C. T., and G. R. Klimpel. 2002. Binding of the hepatitis C virus envelope protein E2 to CD81 inhibits natural killer cell functions. J. Exp. Med. 195:43-49.
40. Van Doorn, L. J., I. Capriles, G. Maertens, R. DeLeys, K. Murray, T. Kos, H. Schellekens, and W. Quint. 1995. Sequence evolution of the hypervariable region in the putative envelope region E2/NS1 of hepatitis C virus is correlated with specific humoral immune responses. J. Virol. 69:773-778.
41. Wack, A., E. Soldaini, C. Tseng, S. Nuti, G. Klimpel, and S. Abrignani. 2001. Binding of the hepatitis C virus envelope protein E2 to CD81 provides a co-stimulatory signal for human T cells. Eur. J. Immunol. 31:166-175.
42. Wasley, A., and M. J. Alter. 2000. Epidemiology of hepatitis C: geographic differences and temporal trends. Semin. Liver Dis. 20:1-16.
43. Weiner, A. J., H. M. Geysen, C. Christopherson, J. E. Hall, T. J. Mason, G. Saracco, F. Bonino, et al. 1992. Evidence for immune selection of hepatitis C virus (HCV) putative envelope glycoprotein variants: potential role in chronic HCV infections. Proc. Natl. Acad. Sci. USA 89:3468-3472.
44. Yagnik, A. T., A. Lahm, A. Meola, R. M. Roccasecca, B. Bruni Ercole, A. Nicosia, and A. Tramontano. 2000. A model for the hepatitis C virus envelope glycoprotein E2. Proteins 40:355-366.
45. Zucchelli, S., R. Roccasecca, A. Meola, B. Bruni Ercole, R. Tafi, J. Duboisson, G. Galfrè, R. Cortese, and A. Nicosia. 2001. Mimotopes of the hepatitis C virus hypervariable region 1, but not the natural sequences, induce cross-reactive antibody response by genetic immunization. Hepatology 33:692-703.