Characterization of antibody-mediated neutralization directed against the hypervariable region 1 of hepatitis C virus E2 glycoprotein

Journal of General Virology

Volumn 92, Issue 3, 2011, Pages 494-506

  Vieyres, Gabrielle ^a,b,c   Dubuisson, Jean ^b,c   Patel, Arvind H ^a  

^a MRC UNIVERSITY OF GLASGOW CENTRE FOR VIRUS RESEARCH   (United Kingdom)

^b INSERM U1019   (France)

^c UNIV LILLE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCOPROTEIN E2; MONOCLONAL ANTIBODY 1020; MONOCLONAL ANTIBODY AP213; MONOCLONAL ANTIBODY R140; NEUTRALIZING ANTIBODY; POLYCLONAL ANTIBODY; UNCLASSIFIED DRUG; VIRUS ENVELOPE PROTEIN;

ANTIGEN ANTIBODY REACTION; ANTIGEN BINDING; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; GENE LOCUS; GENOTYPE; HEPATITIS C; HEPATITIS C VIRUS; HUMAN; HUMAN CELL; HYPERVARIABLE REGION 1; IN VITRO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; RABBIT; VIRION; VIRUS INFECTIVITY; VIRUS NEUTRALIZATION; VIRUS STRAIN;

HEPATITIS C VIRUS; ORYCTOLAGUS CUNICULUS;

EID: 79951803564     PISSN: 00221317     EISSN: 14652099     Source Type: Journal    
DOI: 10.1099/vir.0.028092-0     Document Type: Article

References (71)

1. Agnello, V., Abel, G., Elfahal, M., Knight, G. B. & Zhang, Q. X. (1999). Hepatitis C virus and other Flaviviridae viruses enter cells via low density lipoprotein receptor. Proc Natl Acad Sci U S A 96, 12766-12771. (Pubitemid 29513577)
2. Bankwitz, D., Steinmann, E., Bitzegeio, J., Ciesek, S., Friesland, M., Herrmann, E., Zeisel, M. B., Baumert, T. F., Keck, Z. Y. & other authors (2010). Hepatitis C virus hypervariable region 1 modulates receptor interactions, conceals the CD81 binding site, and protects conserved neutralizing epitopes. J Virol 84, 5751-5763.
3. Barth, H., Schafer, C., Adah, M. I., Zhang, F., Linhardt, R. J., Toyoda, H., Kinoshita-Toyoda, A., Toida, T., Van Kuppevelt, T. H. & other authors (2003). Cellular binding of hepatitis C virus envelope glycoprotein E2 requires cell surface heparan sulfate. J Biol Chem 278, 41003-41012.
4. Barth, H., Schnober, E. K., Zhang, F., Linhardt, R. J., Depla, E., Boson, B., Cosset, F. L., Patel, A. H., Blum, H. E. &Baumert, T. F. (2006). Viral and cellular determinants of the hepatitis C virus envelope-heparan sulfate interaction. J Virol 80, 10579-10590.
5. Bartosch, B., Bukh, J., Meunier, J. C., Granier, C., Engle, R. E., Blackwelder, W. C., Emerson, S. U., Cosset, F. L. & Purcell, R. H. (2003a). In vitro assay for neutralizing antibody to hepatitis C virus: evidence for broadly conserved neutralization epitopes. Proc Natl Acad Sci U S A 100, 14199-14204.
6. Bartosch, B., Dubuisson, J. & Cosset, F. L. (2003b). Infectious hepatitis C virus pseudo-particles containing functional E1-E2 envelope protein complexes. J Exp Med 197, 633-642. (Pubitemid 36314658)
7. Bartosch, B., Vitelli, A., Granier, C., Goujon, C., Dubuisson, J., Pascale, S., Scarselli, E., Cortese, R., Nicosia, A. & Cosset, F. L. (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, 41624-41630. (Pubitemid 37310418)
8. Bartosch, B., Verney, G., Dreux, M., Donot, P., Morice, Y., Penin, F., Pawlotsky, J. M., Lavillette, D. & Cosset, F. L. (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. (Pubitemid 40853525)
9. Basu, A., Beyene, A., Meyer, K. & Ray, R. (2004). The hypervariable region 1 of the E2 glycoprotein of hepatitis C virus binds to glycosaminoglycans, but this binding does not lead to infection in a pseudotype system. J Virol 78, 4478-4486. (Pubitemid 38501067)
10. Bukh, J., Miller, R. H. & Purcell, R. H. (1995). Genetic heterogeneity of hepatitis C virus: quasispecies and genotypes. Semin Liver Dis 15, 41-63.
11. Callens, N., Ciczora, Y., Bartosch, B., Vu-Dac, N., Cosset, F. L., Pawlotsky, J. M., 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, 15331-15341. (Pubitemid 43032315)
12. Chang, K. S., 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, 13783-13793. (Pubitemid 350247871)
13. Clackson, T. & Wells, J. A. (1995). A hot spot of binding energy in a hormone-receptor interface. Science 267, 383-386.
14. Clayton, R. F., Owsianka, A., Aitken, J., Graham, S., Bhella, D. & Patel, A. H. (2002). Analysis of antigenicity and topology of E2 glycoprotein present on recombinant hepatitis C virus-like particles. J Virol 76, 7672-7682. (Pubitemid 34760991)
15. Cocquerel, L., Meunier, J. C., 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, 2183-2191. (Pubitemid 28100775)
16. Dhillon, S., Witteveldt, J., Gatherer, D., Owsianka, A. M., Zeisel, M. B., Zahid, M. N., Rychlowska, M., Foung, S. K., Baumert, T. F. & other authors (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, 5494-5507.
17. Dreux, M., Pietschmann, T., Granier, C., Voisset, C., Ricard-Blum, S., Mangeot, P. E., Keck, Z., Foung, S., Vu-Dac, N. & other authors (2006). High density lipoprotein inhibits hepatitis C virus-neutralizing antibodies by stimulating cell entry via activation of the scavenger receptor BI. J Biol Chem 281, 18285-18295.
18. Evans, M. J., von Hahn, T., Tscherne, D. M., Syder, A. J., Panis, M., Wolk, B., Hatziioannou, T., McKeating, J. A., Bieniasz, P. D. & Rice, C. M. (2007). Claudin-1 is a hepatitis C virus co-receptor required for a late step in entry. Nature 446, 801-805. (Pubitemid 46582027)
19. Farci, P., Shimoda, A., Wong, D., Cabezon, T., De Gioannis, D., Strazzera, A., Shimizu, Y., Shapiro, M., Alter, H. J. & Purcell, R. H. (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 U S A 93, 15394-15399. (Pubitemid 27009611)
20. Farci, P., Shimoda, A., Coiana, A., Diaz, G., Peddis, G., Melpolder, J. C., Strazzera, A., Chien, D. Y., Munoz, S. J. & other authors (2000). The outcome of acute hepatitis C predicted by the evolution of the viral quasispecies. Science 288, 339-344. (Pubitemid 30226196)
21. Flint,M., Dubuisson, J., Maidens, C., Harrop, R., Guile, G. R., Borrow, P. & McKeating, J. A. (2000). Functional characterization of intracellular and secreted forms of a truncated hepatitis C virus E2 glycoprotein. J Virol 74, 702-709. (Pubitemid 30036206)
22. 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, 75-85. (Pubitemid 30650684)
23. Forns, X., Thimme, R., Govindarajan, S., Emerson, S. U., Purcell, R. H., Chisari, F. V. & 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 U S A 97, 13318-13323.
24. Haberstroh, A., Schnober, E. K., Zeisel, M. B., Carolla, P., Barth, H., Blum, H. E., Cosset, F. L., Koutsoudakis, G., Bartenschlager, R. & other authors (2008). Neutralizing host responses in hepatitis C virus infection target viral entry at postbinding steps and membrane fusion. Gastroenterology 135, 1719-1728.
25. Hijikata, M., Kato, N., Ootsuyama, Y., Nakagawa, M., Ohkoshi, S. & Shimotohno, K. (1991). Hypervariable regions in the putative glycoprotein of hepatitis C virus. Biochem Biophys Res Commun 175, 220-228.
26. Hsu, M., Zhang, J., Flint, M., Logvinoff, C., Cheng-Mayer, C., Rice, C. M. & McKeating, J. A. (2003). Hepatitis C virus glycoproteins mediate pH-dependent cell entry of pseudotyped retroviral particles. Proc Natl Acad Sci U S A 100, 7271-7276. (Pubitemid 36706428)
27. Iro, M., Witteveldt, J., Angus, A. G., Woerz, I., Kaul, A., Bartenschlager, R. & Patel, A. H. (2009). A reporter cell line for rapid and sensitive evaluation of hepatitis C virus infectivity and replication. Antiviral Res 83, 148-155.
28. Johansson, D. X., Voisset, C., Tarr, A. W., Aung, M., Ball, J. K., Dubuisson, J. & Persson, M. A. (2007). Human combinatorial libraries yield rare antibodies that broadly neutralize hepatitis C virus. Proc Natl Acad Sci U S A 104, 16269-16274. (Pubitemid 350099395)
29. Kato, T., Date, T.,Murayama, A., Morikawa, K., Akazawa, D. &Wakita, T. (2006). Cell culture and infection system for hepatitis C virus. Nat Protoc 1, 2334-2339.
30. Keck, Z. Y., Xia, J., Cai, Z., Li, T. K., Owsianka, A. M., Patel, A. H., Luo, G. & Foung, S. K. (2007). Immunogenic and functional organization of hepatitis C virus (HCV) glycoprotein E2 on infectious HCV virions. J Virol 81, 1043-1047. (Pubitemid 46067930)
31. 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, 5308-5320.
32. Kurosaki, M., Enomoto, N., Marumo, F. & Sato, C. (1993). Rapid sequence variation of the hypervariable region of hepatitis C virus during the course of chronic infection. Hepatology 18, 1293-1299. (Pubitemid 23348412)
33. Lavillette, D., Tarr, A. W., Voisset, C., Donot, P., Bartosch, B., Bain, C., Patel, A. H., Dubuisson, J., Ball, J. K. & Cosset, F. L. (2005). Characterization of host-range and cell entry properties of the major genotypes and subtypes of hepatitis C virus. Hepatology 41, 265-274. (Pubitemid 40173981)
34. Law, M., Maruyama, T., Lewis, J., Giang, E., Tarr, A. W., Stamataki, Z., Gastaminza, P., Chisari, F. V., Jones, I. M. & other authors (2008). Broadly neutralizing antibodies protect against hepatitis C virus quasispecies challenge. Nat Med 14, 25-27.
35. Li, C. & Allain, J. P. (2005). Chimeric monoclonal antibodies to hypervariable region 1 of hepatitis C virus. J Gen Virol 86, 1709-1716. (Pubitemid 40766883)
36. Li, C., Candotti, D. & Allain, J. P. (2001). Production and characterization of monoclonal antibodies specific for a conserved epitope within hepatitis C virus hypervariable region 1. J Virol 75, 12412-12420. (Pubitemid 33115913)
37. Lindenbach, B. D., Evans, M. J., Syder, A. J., Wolk, B., Tellinghuisen, T. L., Liu, C. C., Maruyama, T., Hynes, R. O., Burton, D. R. & other authors (2005). Complete replication of hepatitis C virus in cell culture. Science 309, 623-626. (Pubitemid 41033648)
38. Liu, S., Yang, W., Shen, L., Turner, J. R., Coyne, C. B. & 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, 2011-2014.
39. Macdonald, A., Crowder, K., Street, A., McCormick, C., Saksela, K. & Harris, M. (2003). The hepatitis C virus non-structural NS5A protein inhibits activating protein-1 function by perturbing ras - ERK pathway signaling. J Biol Chem 278, 17775-17784. (Pubitemid 36799381)
40. Mancini, N., Diotti, R. A., Perotti, M., Sautto, G., Clementi, N., Nitti, G., Patel, A. H., Ball, J. K., Clementi, M. & Burioni, R. (2009). Hepatitis C virus (HCV) infection may elicit neutralizing antibodies targeting epitopes conserved in all viral genotypes. PLoS ONE 4, e8254.
41. McCaffrey, K., Boo, I., Poumbourios, P. & Drummer, H. E. (2007). Expression and characterization of a minimal hepatitis C virus glycoprotein E2 core domain that retains CD81 binding. J Virol 81, 9584-9590. (Pubitemid 47311505)
42. Meertens, L., Bertaux, C., Cukierman, L., Cormier, E., Lavillette, D., Cosset, F. L. & Dragic, T. (2008). The tight junction proteins claudin-1, -6, and -9 are entry cofactors for hepatitis C virus. J Virol 82, 3555-3560. (Pubitemid 351429931)
43. Moradpour, D., Penin, F. & Rice, C. M. (2007). Replication of hepatitis C virus. Nat Rev Microbiol 5, 453-463. (Pubitemid 46780082)
44. Nakabayashi, H., Taketa, K., Miyano, K., Yamane, T. & Sato, J. (1982). Growth of human hepatoma cells lines with differentiated functions in chemically defined medium. Cancer Res 42, 3858-3863. (Pubitemid 12054507)
45. Owsianka, A., Clayton, R. F., Loomis-Price, L. D., McKeating, J. A. & Patel, A. H. (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. (Pubitemid 32707551)
46. Owsianka, A., Tarr, A. W., Juttla, V. S., Lavillette, D., Bartosch, B., Cosset, F. L., Ball, J. K. & Patel, A. H. (2005). Monoclonal antibody AP33 defines a broadly neutralizing epitope on the hepatitis C virus E2 envelope glycoprotein. J Virol 79, 11095-11104. (Pubitemid 41170650)
47. Owsianka, A. M., Tarr, A. W., Keck, Z. Y., Li, T. K., Witteveldt, J., Adair, R., Foung, S. K., Ball, J. K. & Patel, A. H. (2008). Broadly neutralizing human monoclonal antibodies to the hepatitis C virus E2 glycoprotein. J Gen Virol 89, 653-659.
48. Patel, A. H., Wood, J., Penin, F., Dubuisson, J. & McKeating, J. A. (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, 2873-2883. (Pubitemid 32000634)
49. Pawlotsky, J. M. (2003). Hepatitis C virus genetic variability: pathogenic and clinical implications. Clin Liver Dis 7, 45-66.
50. Penin, F., Combet, C., Germanidis, G., Frainais, P. O., Deleage, G. & Pawlotsky, J. M. (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. (Pubitemid 32488166)
51. Perotti, M., Mancini, N., Diotti, R. A., Tarr, A. W., Ball, J. K., Owsianka, A., Adair, R., Patel, A. H., Clementi, M. & Burioni, R. (2008). Identification of a broadly cross-reacting and neutralizing human monoclonal antibody directed against the hepatitis C virus E2 protein. J Virol 82, 1047-1052.
52. Pileri, P., Uematsu, Y., Campagnoli, S., Galli, G., Falugi, F., Petracca, R., Weiner, A. J., Houghton, M., Rosa, D. & other authors (1998). Binding of hepatitis C virus to CD81. Science 282, 938-941. (Pubitemid 28507525)
53. Ploss, A., Evans, M. J., Gaysinskaya, V. A., Panis, M., You, H., de Jong, Y. P. & Rice, C. M. (2009). Human occludin is a hepatitis C virus entry factor required for infection of mouse cells. Nature 457, 882-886.
54. Roccasecca, R., Ansuini, H., Vitelli, A., Meola, A., Scarselli, E., Acali, S., Pezzanera, M., Ercole, B. B., McKeating, J. & other authors (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, 1856-1867.
55. Rosa, D., Campagnoli, S., Moretto, C., Guenzi, E., Cousens, L., Chin,M., Dong, C., Weiner, A. J., Lau, J. Y. & other authors (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 U S A 93, 1759-1763. (Pubitemid 26079830)
56. Scarselli, E., Ansuini, H., Cerino, R., Roccasecca, R. M., 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, 5017-5025.
57. Schofield, D. J., Bartosch, B., Shimizu, Y. K., Allander, T., Alter, H. J., Emerson, S. U., Cosset, F. L. & Purcell, R. H. (2005). Human monoclonal antibodies that react with the E2 glycoprotein of hepatitis C virus and possess neutralizing activity. Hepatology 42, 1055-1062. (Pubitemid 43112672)
58. Shimizu, Y. K., Hijikata, M., Iwamoto, A., Alter, H. J., Purcell, R. H. & Yoshikura, H. (1994). Neutralizing antibodies against hepatitis C virus and the emergence of neutralization escape mutant viruses. J Virol 68, 1494-1500. (Pubitemid 24065713)
59. Simmonds, P. (1995). Variability of hepatitis C virus. Hepatology 21, 570-583.
60. Tarr, A. W., Owsianka, A. M., Timms, J. M., McClure, C. P., Brown, R. J., Hickling, T. P., Pietschmann, T., Bartenschlager, R., Patel, A. H. & Ball, J. K. (2006). Characterization of the hepatitis C virus E2 epitope defined by the broadly neutralizing monoclonal antibody AP33. Hepatology 43, 592-601.
61. 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, 357-367. (Pubitemid 44216011)
62. Vieyres, G., Angus, A. G., Haberstroh, A., Baumert, T. F., Dubuisson, J. & Patel, A. H. (2009). Rapid synchronization of hepatitis C virus infection by magnetic adsorption. J Virol Methods 157, 69-79.
63. 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, 7793-7799. (Pubitemid 40349673)
64. Wakita, T., Pietschmann, T., Kato, T., Date, T., Miyamoto, M., Zhao, Z., Murthy, K., Habermann, A., Krausslich, H. G. & other authors (2005). Production of infectious hepatitis C virus in tissue culture from a cloned viral genome. Nat Med 11, 791-796. (Pubitemid 41021213)
65. Weiner, A. J., Brauer, M. J., Rosenblatt, J., Richman, K. H., Tung, J., Crawford, K., Bonino, F., Saracco, G., Choo, Q. L. & other authors (1991). Variable and hypervariable domains are found in the regions of HCV corresponding to the flavivirus envelope and NS1 proteins and the pestivirus envelope glycoproteins. Virology 180, 842-848.
66. Weiner, A. J., Geysen, H. M., Christopherson, C., Hall, J. E., Mason, T. J., Saracco, G., Bonino, F., Crawford, K., Marion, C. D. & other authors (1992). Evidence for immune selection of hepatitis C virus (HCV) putative envelope glycoprotein variants: potential role in chronic HCV infections. Proc Natl Acad Sci U S A 89, 3468-3472.
67. Yanagi, M., Purcell, R. H., Emerson, S. U. & Bukh, J. (1997). Transcripts from a single full-length cDNA clone of hepatitis C virus are infectious when directly transfected into the liver of a chimpanzee. Proc Natl Acad Sci U S A 94, 8738-8743. (Pubitemid 27335109)
68. Zeisel, M. B., Koutsoudakis, G., Schnober, E. K., Haberstroh, A., Blum, H. E., Cosset, F. L., Wakita, T., Jaeck, D., Doffoel, M. & other authors (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, 1722-1731.
69. 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, 12465-12471.
70. Zhong, J., Gastaminza, P., Cheng, G., Kapadia, S., Kato, T., Burton, D. R., Wieland, S. F., Uprichard, S. L., Wakita, T. & Chisari, F. V. (2005). Robust hepatitis C virus infection in vitro. Proc Natl Acad Sci U S A 102, 9294-9299. (Pubitemid 40923557)
71. Zibert, A., Schreier, E. & Roggendorf, M. (1995). Antibodies in human sera specific to hypervariable region 1 of hepatitis C virus can block viral attachment. Virology 208, 653-661.