Broadly neutralizing human monoclonal antibodies to the hepatitis C virus E2 glycoprotein

Journal of General Virology

Volumn 89, Issue 3, 2008, Pages 653-659

  Owsianka, Ania M ^a   Tarr, Alexander W ^b   Keck, Zhen Yong ^c   Li, Ta Kai ^c   Witteveldt, Jeroen ^a   Adair, Richard ^a   Foung, Steven K H ^c   Ball, Jonathan K ^b   Patel, Arvind H ^a  

^a UNIVERSITY OF GLASGOW   (United Kingdom)

^b UNIVERSITY OF NOTTINGHAM   (United Kingdom)

^c STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE; CD81 ANTIGEN; EPITOPE; GLYCOPROTEIN E1; GLYCOPROTEIN E2; HUMAN MONOCLONAL ANTIBODY; HUMAN MONOCLONAL ANTIBODY CBH 2; HUMAN MONOCLONAL ANTIBODY CBH 5; HUMAN MONOCLONAL ANTIBODY CBH 7; MONOCLONAL ANTIBODY; MUTANT PROTEIN; NEUTRALIZING ANTIBODY; VIRUS ENVELOPE PROTEIN; GLYCOPROTEIN E2, HEPATITIS C VIRUS; HEPATITIS C ANTIBODY; LEUKOCYTE ANTIGEN; UNCLASSIFIED DRUG;

AMINO ACID SUBSTITUTION; ARTICLE; BINDING COMPETITION; BINDING SITE; CHIMERA; GENOTYPE; HEPATITIS C VIRUS; MOLECULAR CLONING; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; VIRUS CULTURE; VIRUS ENTRY; VIRUS INHIBITION; VIRUS NEUTRALIZATION; CELL LINE; CHEMISTRY; CLASSIFICATION; GENETICS; HUMAN; IMMUNOLOGY; METABOLISM; PATHOGENICITY; RETROVIRUS; SERODIAGNOSIS; VIRION;

HEPATITIS C VIRUS;

ANTIBODIES, MONOCLONAL; ANTIGENS, CD; CELL LINE; EPITOPES; GENOTYPE; HEPACIVIRUS; HEPATITIS C ANTIBODIES; HUMANS; NEUTRALIZATION TESTS; RETROVIRIDAE; VIRAL ENVELOPE PROTEINS; VIRION;

EID: 42449130231     PISSN: 00221317     EISSN: None     Source Type: Journal    
DOI: 10.1099/vir.0.83386-0     Document Type: Article

References (53)

1. Allander, T., Drakenberg, K., Beyene, A., Rosa, D., Abrignani, S., Houghton, M., Widell, A., Grillner, L. & Persson, M. A. (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 81, 2451-2459.
2. Anonymous (1999). Global surveillance and control of hepatitis C. Report of a WHO Consultation organized in collaboration with the Viral Hepatitis Prevention Board, Antwerp, Belgium. J Viral Hepat 6, 35-47.
3. 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.
4. 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.
5. 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-BI scavenger receptor. J Biol Chem 278, 41624-41630.
6. Bowen, D. G. &, Walker, C. M. (2005). Adaptive immune responses in acute and chronic hepatitis C virus infection. Nature 436, 946-952.
7. Brown, R.J., Juttla, V. S., Tarr, A.W., Finnis, R., Irving, W. L., Hemsley, S., Flower, D. R., Borrow, P. & Ball, J. K. (2005). Evolutionary dynamics of hepatitis C virus envelope genes during chronic infection. J Gen Virol 86, 1931-1942.
8. Bugli, F., Mancini, N., Kang, C. Y., Di Campli, C., Grieco, A., Manzin, A., Gabrielli, A., Gasbarrini, A., Fadda, G. & other authors (2001). Mapping B-cell epitopes of hepatitis C virus E2 glycoprotein using human monoclonal antibodies from phage display libraries. J Virol 75, 9986-9990.
9. Bukh, J., Miller, R. H. & Purcell, R. H. (1995). Genetic heterogeneity of hepatitis C virus: quasispecies and genotypes. Semin Liver Dis 15, 41-63.
10. 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.
11. Cocquerel, L., Voisset, C. & Dubuisson, J. (2006). Hepatitis C virus entry: potential receptors and their biological functions. J Gen Virol 87, 1075-1084.
12. Conrad, M. E. & Lemon.. S. M. (1987). Prevention of endemic icteric viral hepatitis by administration of immune serum gamma globulin. J Infect Dis 156, 56-63.
13. Drummer, H. E., Boo, I., Maerz, A. L. & Poumbourios, P. (2006). A conserved Gly436-Trp-Leu-Ala-Gly-Leu-Phe-Tyr motif in hepatitis C virus glycoprotein E2 is a determinant of CD81 binding and viral entry. J Virol 80, 7844-7853.
14. Eren, R., Landstein, D., Terkieltaub, D., Nussbaum, O., Zauberman, A., Ben-Porath, J., Gopher, J., Buchnick, R., Koviazin, R. & other authors (2006). Preclinical evaluation of two neutralizing human monoclonal antibodies against hepatitis C virus (HCV): a potential treatment to prevent HCV reinfection in liver transplant patients. J Virol 80, 2654-2664.
15. Farci, P., Alter, H. J., Wong, D. C., Miller, R. H., Govindarajan, S., Engle, R., Shapiro, M. & Purcell, R. H. (1994). Prevention of hepatitis C virus infection in chimpanzees after antibody-mediated in vitro neutralization. Proc Natl Acad Sci U S A 91, 7792-7796.
16. 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.
17. Flint M., Maidens, C, Loomis-Price, L. D., Shotton, C., Dubuisson, J., Monk, P., Higginbottom, A., Levy, S. & McKeating, J. A. (1999). Characterization of hepatitis C virus E2 glycoprotein interaction with a putative cellular receptor, CD81. J Virol 73, 6235-6244.
18. Gale, M., Jr & Foy, E. M. (2005). Evasion of intracellular host defence by hepatitis C virus. Nature 436, 939-945.
19. Goffard, A, Callens, N., Bartosch, B., Wychowski, C., Cosset, F. L., Montpellier, C. & Dubuisson, J. (2005). Role of N-linked glycans in the functions of hepatitis C virus envelope glycoproteins. J Virol 79, 8400-8409.
20. Habersetzer, F., Fournillier, A., Dubuisson, J., Rosa, D., Abrignani, S., Wychowski, C., Nakano, I., Trepo, C, Desgranges, C. & Inchauspe, G., (1998). Characterization of human monoclonal antibodies specific to the hepatitis C virus glycoprotein E2 with in vitro binding neutralization properties. Virology 249, 32-41.
21. Hadlock, K. G., Lanford, R. E., Perkins, S., Rowe, J., Yang, O., Levy, S., Piled, P., Abrignani, S. & Foung, S. K. (2000). Human monoclonal antibodies that inhibit binding of hepatitis C virus E2 protein to CD81 and recognize conserved conformational epitopes. J Virol 74,
22. Helle, F., Goffard, A., Morel, V., Duverlie, G., McKeating, J., Keck, Z. Y., Foung, S., Penin, F., Dubuisson, J. & Voisset, C. (2007). The neutralizing activity of anti-HCV antibodies is modulated by specific glycans on the E2 envelope protein. J Virol 81, 8101-8111.
23. 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.
24. 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.
25. Kapadia, S. B., Barth, H., Baumert, T., McKeating, J. A. & Chisari, F. V. (2007). Initiation of hepatitis C virus infection is dependent on cholesterol and cooperativity between CD81 and scavenger receptor B type I. J Virol 81, 374-383.
26. Keck, Z. Y., Op De Beeck, A., Hadlock, K. G., Xia, J., Li, T. K., Dubuisson, J. & Foung, S. K. (2004). Hepatitis C virus E2 has three immunogenic domains containing conformational epitopes with distinct properties and biological functions. J Virol 78, 9224-9232.
27. Keck Z. Y., Li, T. K., Xia, J., Bartosch, B., Cosset, F. L., Dubuisson, J. & Foung, S. K. (2005). Analysis of a highly flexible conformational immunogenic domain A in hepatitis C virus E2. J Virol 79, 13199-13208.
28. Keck, Z. Y., Xia, J., Cai, Z., Li, T. K., Owslanka, 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.
29. Knodell, R. G., Conrad, M. E., Ginsberg, A. L. & Bell, C. J. (1976). Efficacy of prophylactic gamma-globulin in preventing non-A, non-B post-transfusion hepatitis. Lancet 1, 557-561.
30. Koutsoudakis, G., Herrmann, E., Kallis, S., Bartenschlager, R. & Pletschmann, T. (2007). The level of CD81 cell surface expression is a key determinant for productive entry of hepatitis C virus into host cells. J Virol 81, 588-598.
31. Lavillette, D., Morice, Y., Germanidis, G., Donot, P., Soulier, A., Pagkalos, E., Sakellariou, G., Intrator, L., Bartosch, B. & other authors (2005a). Human serum facilitates hepatitis C virus infection, and neutralizing responses inversely correlate with viral replication kinetics at the acute phase of hepatitis C virus infection. J Virol 79, 6023-6034.
32. Lavillette, D., Tarr, A. W., Voisset C., Donot P., Bartosch, B., Bain, C., Patel, A. H., Dubuisson, J., Ball, J. K. & Cosset F. L. (2005b). Characterization of host-range and cell entry properties of the major genotypes and subtypes of hepatitis C virus. Hepatology 41, 265-274.
33. 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.
34. Meylan, E & Tschopp, J. (2006). Toll-like receptors and RNA helicases: two parallel ways to trigger antiviral responses. Mol Cell 22, 561-569.
35. Nakabayashi, H., Taketa, K., Miyano, K., Yamane, T. & Sato, J. (1962). Growth of human hepatoma cells lines with differentiated functions in chemically defined medium. Cancer Res 42, 3858-3863.
36. Op De Beeck, A., Voisset, C., Bartosch, B., Ciczora, Y., Cocquerel, L., Keck, Z., Foung, S., Cosset, F. L. & Dubuisson, J. (2004). Characterization of functional hepatitis C virus envelope glycoproteins. J Virol 78, 2994-3002.
37. Owsianka, X., Clayton, R. F., Loomis-Price, L. D., McKeating, J. A. & Patel, A. H. (2001). Functional analysis of hepatitis C virus E2 glycoproteins and virus-Re particles reveals structural dissimilarities between different forms of E2. J Gen Virol 82, 1877-1883.
38. 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.
39. Owsianka, A. M., Timms, J. M., Tarr, A. W., Brown, R. J., Hickling, T. P., Szwelk, A., Bienkowska-Szewczyk, K., Thomson, B. J., Patel, A. H. & Ball, J. K. (2006). Identification of conserved residues in the E2 envelope glycoprotein of the hepatitis C virus that are critical for CD81 binding. J Virol 80, 8695-8704.
40. 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 HCV\E2 protein. J Virol (in press). doi:10.1128/IVI.01986-07
41. Pestka, J. M., Zelsel, M. B., Blaser, E., Schurmann, P., Bartosch, B., Cosset, F. L., Patel, A. H., Meisel, H., Baumert, J. & other authors (2007). Rapid induction of virus-neutralizing antibodies and viral clearance in a single-source outbreak of hepatitis'C. Proc Natl Acad Sci U S A 104, 6025-6030.
42. 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.
43. 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.
44. Sandrin, V., Boulanger, P., Penin, F., Granier, C., Cosset, F. L. & Bartosch, B. (2005). Assembly of functional hepatitis C virus glycoproteins on infectious pseudoparticles occurs intracellularly and requires concomitant incorporation of E1 and E2 glycoproteins. J Gen Virol 86, 3189-3199.
45. 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.
46. 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.
47. Shoukry, N. H., Cawthon, A. G. & Walker, C. M. (2004). Cell-mediated immunity and the outcome of hepatitis C virus infection. Annu Rev Microbiol 58, 391-424.
48. Simmonds, P., Bukh, J., Combet C., Deleage, G., Enomoto, N., Feinstone, S., Halfon, P., Inchauspe, G., Kuiken, C. & other authors (2005). Consensus proposals for a unified system of nomenclature of hepatitis C virus genotypes. Hepatology 42, 962-973.
49. 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.
50. Thimme, R., Lohmann, V. & Weber, F. (2006). A target on the move: innate and adaptive immune'escape strategies of hepatitis C virus. Antiviral Res 69, 129-141.
51. 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.
52. Yu, M. Y., Bartosch, B., Zhang, P., Guo, Z. P., Renzi, P. M., Shen, L. M., Granier, C., Feinstone, S. M., Cosset F. L. & Purcell, R. H. (2004). Neutralizing antibodies to hepatitis C virus (HCV) in immune globulins derived from anti-HCV-positive plasma. Proc Natl Acad Sci U S A 101, 7705-7710.
53. 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.