Neutralizing monoclonal antibodies against hepatitis C Virus E2 protein bind discontinuous epitopes and inhibit infection at a postattachment step

Journal of Virology

Volumn 85, Issue 14, 2011, Pages 7005-7019

  Sabo, Michelle C ^a   Luca, Vincent C ^a   Prentoe, Jannick ^d   Hopcraft, Sharon E ^f   Blight, Keril J ^a   Yi, MinKyung ^b   Lemon, Stanley M ^c   Ball, Jonathan K ^g   Bukh, Jens ^d,e   Evans, Matthew J ^f   Fremont, Daved H ^a   Diamond, Michael S ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b University of Texas Medical Branch School of Medicine   (United States)

^c UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^d Mental Health Services CPH   (Denmark)

^e UNIVERSITY OF COPENHAGEN   (Denmark)

^f MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^g UNIVERSITY OF NOTTINGHAM   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CD81 ANTIGEN; EPITOPE; HEPATITIS C ANTIBODY; HEPATITIS C VIRUS E2 PROTEIN; MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY H77.16; MONOCLONAL ANTIBODY H77.39; MONOCLONAL ANTIBODY J6.36; NEUTRALIZING ANTIBODY; SCAVENGER RECEPTOR BI; STRUCTURAL PROTEIN; UNCLASSIFIED DRUG; VIRUS PROTEIN;

AMINO ACID SEQUENCE; ANIMAL CELL; ANTIBODY STRUCTURE; ARTICLE; CELL CULTURE; CHIMERA; CONTROLLED STUDY; HEPATITIS C VIRUS; HIGH THROUGHPUT SCREENING; IMMUNOGLOBULIN VARIABLE REGION; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; RECEPTOR BINDING; VIRUS ATTACHMENT; VIRUS NEUTRALIZATION; VIRUS STRAIN;

ANIMALS; ANTIBODIES, MONOCLONAL; ANTIBODIES, NEUTRALIZING; BASE SEQUENCE; CELL LINE; CHO CELLS; CRICETINAE; CRICETULUS; DNA PRIMERS; EPITOPES; HEPACIVIRUS; HUMANS; PROTEIN BINDING; VIRAL ENVELOPE PROTEINS;

HEPATITIS C VIRUS;

EID: 79960485199     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00586-11     Document Type: Article

References (67)

1. Allander, T., et al. 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. Balsitis, S. J., et al. 2010. Lethal antibody enhancement of dengue disease in mice is prevented by Fc modification. PLoS Pathog. 6:e1000790.
3. Bankwitz, D., et al. 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.
4. Bartenschlager, R., M. Frese, and T. Pietschmann. 2004. Novel insights into hepatitis C virus replication and persistence. Adv. Virus Res. 63:71-180.
5. Bartosch, B., et al. 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.
6. Bertaux, C., and T. Dragic. 2006. Different domains of CD81 mediate distinct stages of hepatitis C virus pseudoparticle entry. J. Virol. 80:4940-4948.
7. Bowen, D. G., and C. M. Walker. 2005. Adaptive immune responses in acute and chronic hepatitis C virus infection. Nature 436:946-952.
8. Brien, J. D., et al. 2010. Genotype-specific neutralization and protection by antibodies against dengue virus type 3. J. Virol. 84:10630-10643.
9. Broering, T. J., et al. 2009. Identification and characterization of broadly neutralizing human monoclonal antibodies directed against the E2 envelope glycoprotein of hepatitis C virus. J. Virol. 83:12473-12482.
10. Choo, Q. L., et al. 1994. Vaccination of chimpanzees against infection by the hepatitis C virus. Proc. Natl. Acad. Sci. U. S. A. 91:1294-1298.
11. Dhillon, S., et al. 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.
12. Diamond, M. S., J. Garcia-Aguilar, J. K. Bickford, A. L. Corbi, and T. A. Springer. 1993. The I domain is a major recognition site on the leukocyte integrin Mac-1 (CD11b/CD18) for four distinct adhesion ligands. J. Cell Biol. 120:1031-1043.
13. Drummer, H. E., K. A. Wilson, and P. Poumbourios. 2002. Identification of the hepatitis C virus E2 glycoprotein binding site on the large extracellular loop of CD81. J. Virol. 76:11143-11147.
14. Evans, M. J., et al. 2007. Claudin-1 is a hepatitis C virus co-receptor required for a late step in entry. Nature 446:801-805.
15. Farci, P., 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. U. S. A. 93:15394-15399.
16. Feld, J. J., and J. H. Hoofnagle. 2005. Mechanism of action of interferon and ribavirin in treatment of hepatitis C. Nature 436:967-972.
17. Feldhaus, M. J., et al. 2003. Flow-cytometric isolation of human antibodies from a nonimmune Saccharomyces cerevisiae surface display library. Nat. Biotechnol. 21:163-170.
18. Flint, M., et al. 1999. Characterization of hepatitis C virus E2 glycoprotein interaction with a putative cellular receptor, CD81. J. Virol. 73:6235-6244.
19. Gal-Tanamy, M., et al. 2008. In vitro selection of a neutralization-resistant hepatitis C virus escape mutant. Proc. Natl. Acad. Sci. U. S. A. 105:19450-19455.
20. Goffard, A., et al. 2005. Role of N-linked glycans in the functions of hepatitis C virus envelope glycoproteins. J. Virol. 79:8400-8409.
21. Goffard, A., and J. Dubuisson. 2003. Glycosylation of hepatitis C virus envelope proteins. Biochimie 85:295-301.
22. Gottwein, J. M., et al. 2010. Novel infectious cDNA clones of hepatitis C virus genotype 3a (strain S52) and 4a (strain ED43): genetic analyses and in vivo pathogenesis studies. J. Virol. 84:5277-5293.
23. Gottwein, J. M., et al. 2007. Robust hepatitis C genotype 3a cell culture releasing adapted intergenotypic 3a/2a (S52/JFH1) viruses. Gastroenterology 133:1614-1626.
24. Gottwein, J. M., et al. 2009. Development and characterization of hepatitis C virus genotype 1-7 cell culture systems: role of CD81 and scavenger receptor class B type I and effect of antiviral drugs. Hepatology 49:364-377.
25. Haberstroh, A., et al. 2008. Neutralizing host responses in hepatitis C virus infection target viral entry at postbinding steps and membrane fusion. Gastroenterology 135:1719-1728.
26. Hadlock, K. G., et al. 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.
27. Helle, F., et al. 2010. Role of N-linked glycans in the functions of hepatitis C virus envelope proteins incorporated into infectious virions. J. Virol. 84: 11905-11915.
28. Higginbottom, A., et al. 2000. Identification of amino acid residues in CD81 critical for interaction with hepatitis C virus envelope glycoprotein E2. J. Virol. 74:3642-3649.
29. Houghton, M., and S. Abrignani. 2005. Prospects for a vaccine against the hepatitis C virus. Nature 436:961-966.
30. Hsu, M., et al. 2003. Hepatitis C virus glycoproteins mediate pH-dependent cell entry of pseudotyped retroviral particles. Proc. Natl. Acad. Sci. U. S. A. 100:7271-7276.
31. Hüssy, P., G. Schmid, J. Mous, and H. Jacobsen. 1996. Purification and in vitro-phospholabeling of secretory envelope proteins E1 and E2 of hepatitis C virus expressed in insect cells. Virus Res. 45:45-57.
32. Jensen, T. B., et al. 2008. Highly efficient JFH1-based cell-culture system for hepatitis C virus genotype 5a: failure of homologous neutralizing-antibody treatment to control infection. J. Infect. Dis. 198:1756-1765.
33. Johansson, D. X., et al. 2007. Human combinatorial libraries yield rare antibodies that broadly neutralize hepatitis C virus. Proc. Natl. Acad. Sci. U. S. A. 104:16269-16274.
34. Keck, Z. Y., et al. 2008. Definition of a conserved immunodominant domain on hepatitis C virus E2 glycoprotein by neutralizing human monoclonal antibodies. J. Virol. 82:6061-6066.
35. Kolykhalov, A. A., et al. 1997. Transmission of hepatitis C by intrahepatic inoculation with transcribed RNA. Science 277:570-574.
36. Krey, T., et al. 2010. The disulfide bonds in glycoprotein E2 of hepatitis C virus reveal the tertiary organization of the molecule. PLoS Pathog. 6:e1000762.
37. Law, M., et al. 2008. Broadly neutralizing antibodies protect against hepatitis C virus quasispecies challenge. Nat. Med. 14:25-27.
38. Lindenbach, B. D., et al. 2005. Complete replication of hepatitis C virus in cell culture. Science 309:623-626.
39. Lindenbach, B. D., and C. M. Rice. 2005. Unravelling hepatitis C virus replication from genome to function. Nature 436:933-938.
40. Ma, Y., J. Yates, Y. Liang, S. M. Lemon, and M. Yi. 2008. NS3 helicase domains involved in infectious intracellular hepatitis C virus particle assembly. J. Virol. 82:7624-7639.
41. Martinez-Donato, G., et al. 2006. Expression and processing of hepatitis C virus structural proteins in Pichia pastoris yeast. Biochem. Biophys. Res. Commun. 342:625-631.
42. Nybakken, G. E., et al. 2005. Structural basis of West Nile virus neutralization by a therapeutic antibody. Nature 437:764-769.
43. Oliphant, T., et al. 2005. Development of a humanized monoclonal antibody with therapeutic potential against West Nile virus. Nat. Med. 11:522-530.
44. Oliphant, T., et al. 2006. Antibody recognition and neutralization determinants on domains I and II of West Nile Virus envelope protein. J. Virol. 80:12149-12159.
45. 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.
46. Owsianka, A., et al. 2005. Monoclonal antibody AP33 defines a broadly neutralizing epitope on the hepatitis C virus E2 envelope glycoprotein. J. Virol. 79:11095-11104.
47. Owsianka, A. M., et al. 2008. Broadly neutralizing human monoclonal antibodies to the hepatitis C virus E2 glycoprotein. J. Gen. Virol. 89:653-659.
48. Owsianka, A. M., et al. 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.
49. Perotti, M., et al. 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.
50. Petracca, R., et al. 2000. Structure-function analysis of hepatitis C virus envelope-CD81 binding. J. Virol. 74:4824-4830.
51. Pierson, T. C., and M. S. Diamond. 2008. Molecular mechanisms of antibody-mediated neutralisation of flavivirus infection. Expert Rev. Mol. Med. 10:e12.
52. Pierson, T. C., et al. 2007. The stoichiometry of antibody-mediated neutralization and enhancement of West Nile virus infection. Cell Host Microbe 1:135-145.
53. Pileri, P., et al. 1998. Binding of hepatitis C virus to CD81. Science 282:938-941.
54. Ploss, A., et al. 2009. Human occludin is a hepatitis C virus entry factor required for infection of mouse cells. Nature 457:882-886.
55. Prentoe, J., et al. 2011. Hypervariable region 1 differentially impacts viability of hepatitis C virus strains of genotypes 1 to 6 and impairs virus neutralization. J. Virol. 85:2224-2234.
56. Scarselli, E., et al. 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. Scheel, T. K., et al. 2008. Development of JFH1-based cell culture systems for hepatitis C virus genotype 4a and evidence for cross-genotype neutralization. Proc. Natl. Acad. Sci. U. S. A. 105:997-1002.
58. Scheller, N., et al. 2009. Translation and replication of hepatitis C virus genomic RNA depends on ancient cellular proteins that control mRNA fates. Proc. Natl. Acad. Sci. U. S. A. 106:13517-13522.
59. Shrestha, B., et al. 2010. The development of therapeutic antibodies that neutralize homologous and heterologous genotypes of dengue virus type 1. PLoS Pathog. 6:e1000823.
60. Sukupolvi-Petty, S., et al. 2010. Structure and function analysis of therapeutic monoclonal antibodies against dengue virus type 2. J. Virol. 84:9227-9239.
61. Sukupolvi-Petty, S., et al. 2007. Typeand subcomplex-specific neutralizing antibodies against domain III of dengue virus type 2 envelope protein recognize adjacent epitopes. J. Virol. 81:12816-12826.
62. Tarr, A. W., et al. 2006. Characterization of the hepatitis C virus E2 epitope defined by the broadly neutralizing monoclonal antibody AP33. Hepatology 43:592-601.
63. Thompson, B. S., et al. 2009. A therapeutic antibody against West Nile virus neutralizes infection by blocking fusion within endosomes. PLoS Pathog. 5:e1000453.
64. Vanwolleghem, T., et al. 2008. Polyclonal immunoglobulins from a chronic hepatitis C virus patient protect human liver-chimeric mice from infection with a homologous hepatitis C virus strain. Hepatology 47:1846-1855.
65. Vieyres, G., J. Dubuisson, and A. H. Patel. 2011. Characterization of antibody-mediated neutralization directed against the hypervariable region 1 of hepatitis C virus E2 glycoprotein. J. Gen. Virol. 92:494-506.
66. Vogt, M. R., et al. 2009. Human monoclonal antibodies against West Nile virus induced by natural infection neutralize at a postattachment step. J. Virol. 83:6494-6507.
67. Yi, M., Y. Ma, J. Yates, and S. M. Lemon. 2007. Compensatory mutations in E1, p7, NS2, and NS3 enhance yields of cell culture-infectious intergenotypic chimeric hepatitis C virus. J. Virol. 81:629-638.