A weak neutralizing antibody response to hepatitis C virus envelope glycoprotein enhances virus infection

PLoS ONE

Volumn 6, Issue 8, 2011, Pages

  Meyer, Keith ^a   Banerjee, Arup ^a   Frey, Sharon E ^a   Belshe, Robert B ^a   Ray, Ranjit ^a  

^a SAINT LOUIS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN; MIFAMURTIDE; NEUTRALIZING ANTIBODY; PLACEBO; PROTEIN ANTIBODY; VIRUS GLYCOPROTEIN; VIRUS VACCINE; E1 PROTEIN, HEPATITIS C VIRUS; GLYCOPROTEIN E2, HEPATITIS C VIRUS; HEPATITIS C ANTIBODY; HEPATITIS VACCINE; MF59 OIL EMULSION; POLYSORBATE; SQUALENE; VIRUS ENVELOPE PROTEIN;

ANTIBODY DEPENDENT ENHANCEMENT; ANTIBODY RESPONSE; ANTIBODY SPECIFICITY; ARTICLE; CELL CULTURE; CELL SURFACE; CONTROLLED STUDY; DOUBLE BLIND PROCEDURE; DRUG RESPONSE; DRUG SAFETY; GENOTYPE; HEPATITIS C; HEPATITIS C VIRUS; HUMAN; HUMAN CELL; IMMUNOGENICITY; IN VITRO STUDY; PSEUDOTYPING; RANDOMIZED CONTROLLED TRIAL; SERUM; VIRUS ENVELOPE; VIRUS INFECTIVITY; CLINICAL TRIAL; HUMORAL IMMUNITY; IMMUNOLOGY; PHASE 1 CLINICAL TRIAL;

HEPATITIS C VIRUS;

ANTIBODIES, NEUTRALIZING; ANTIBODY-DEPENDENT ENHANCEMENT; HEPACIVIRUS; HEPATITIS C; HEPATITIS C ANTIBODIES; HUMANS; IMMUNITY, HUMORAL; POLYSORBATES; SQUALENE; VIRAL ENVELOPE PROTEINS; VIRAL HEPATITIS VACCINES;

EID: 80051923476     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0023699     Document Type: Article

References (44)

1. Lagging LM, Meyer K, Owens RJ, Ray R, (1998) Functional role of hepatitis C virus chimeric glycoproteins in the infectivity of pseudotyped virus infectivity. J Virol 72: 3539-3546.
2. Meyer K, Basu A, Ray R, (2000) Functional features of hepatitis C virus glycoproteins for pseudotype virus entry into mammalian cells. Virology 276: 214-226.
3. Meyer K, Beyene A, Bowlin TL, Basu A, Ray R, (2004) Coexpression of hepatitis C virus E1 and E2 chimeric envelope glycoproteins displays separable ligand sensitivity and increases pseudotype infectious titer. J Virol 78: 12838-12847.
4. Kanda T, Basu A, Steele R, Wakita T, Ryerse JS, et al. (2006) Generation of infectious hepatitis C virus in immortalized human hepatocytes. J Virol 80: 4633-4639.
5. Basu A, Kanda T, Beyene A, Saito K, Meyer K, et al. (2007) Sulfated homologues of heparin inhibit hepatitis C virus entry into mammalian cells. J Virol 81: 3933-3941.
6. Takikawa S, Ishii K, Aizaki H, Suzuki T, Asakura H, et al. (2000) Cell fusion activity of hepatitis C virus envelope proteins. J Virol 74: 5066-74.
7. Matsuura Y, Tani H, Suzuki K, Kimura-Someya T, Suzuki R, et al. (2001) Characterization of pseudotype VSV possessing HCV envelope proteins. Virology 286: 263-75.
8. Barth H, Schafer C, Adah MI, Zhang F, Linhardt RJ, et al. (2003) Cellular binding of hepatitis C virus envelope glycoprotein E2 requires cell surface heparan sulfate. J Biol Chem 278: 41003-41012.
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.
10. Pileri P, Uematsu Y, Campagnoli S, Galli G, Falugi F, et al. (1998) Binding of hepatitis C virus to CD81. Science 282: 938-941.
11. Germi R, Crance JM, Garin D, Guimet J, Lortat-Jacob H, et al. (2002) Cellular glycosaminoglycans and low density lipoprotein receptor are involved in hepatitis C virus adsorption. J Med Virol 68: 206-215.
12. Evans, MJ, von Hahn T, Tscherne DM, Syder AJ, Panis M, et al. (2007) Claudin-1 is a hepatitis C virus co-receptor required for a late step in entry. Nature 446: 801-805.
13. Krieger SE, Zeisel MB, Davis C, Thumann C, Harris HJ, et al. (2010) Inhibition of hepatitis C virus infection by anti-claudin-1 antibodies is mediated by neutralization of E2-CD81-claudin-1 associations. Hepatology 51: 1144-1157.
14. Harris, HJ, Davis C, Mullins JG, Hu K, Goodall M, et al. (2010) Claudin association with CD81 defines hepatitis C virus entry. J Biol Chem 285: 21092-21102.
15. Lupberger J, Zeisel MB, Xiao F, Thumann C, Fofana I, et al. (2011) EGFR and EphA2 are host factors for hepatitis C virus entry and possible targets for antiviral therapy. Nat Med 17: 589-95.
16. Tarr AW, Urbanowicz RA, Hamed MR, Albecka A, McClure CP, et al. (2011) Hepatitis C patient-derived glycoproteins exhibit marked differences in susceptibility to serum neutralizing antibodies: genetic subtype defines antigenic but not neutralization serotype. J Virol 85: 4246-57.
17. Lagging LM, Meyer K, Westin J, Wejstal R, Norkrans G, et al. (2002) Neutralization of pseudotyped vesicular stomatitis virus expressing hepatitis C virus envelope glycoprotein 1 or 2 by serum from patients. J Infect.Dis 185: 1165-1169.
18. Rothman AL, Morishima C, Bonkovsky HL, Polyak SJ, Ray R, et al. (2005) Associations among clinical, immunological, and viral quasispecies measurements in advanced chronic hepatitis C. Hepatology 41: 617-625.
19. Morishima C, Polyak SJ, Ray R, Doherty MC, Di Bisceglie AM, et al. (2006) Hepatitis C Antiviral Long-Term Treatment Against Cirrhosis Trial Group. Hepatitis C virus-specific immune responses and quasi-species variability at baseline are associated with nonresponse to antiviral therapy during advanced hepatitis C. J Infect Dis 193: 931-40.
20. Meyer K, Ait-Goughoulte M, Keck ZY, Foung S, Ray R, (2008) Antibody-dependent enhancement of hepatitis C virus infection. J Virol 82: 2140-2149.
21. Ray R, Meyer K, Banerjee A, Basu A, Coates S, et al. (2010) Characterization of antibodies induced by vaccination with hepatitis C virus envelope glycoproteins. J Infect Dis 202: 862-866.
22. Tirado SM, Yoon KJ, (2003) Antibody-dependent enhancement of virus infection and disease. Viral Immunol 16: 69-86.
23. Stoiber H, Soederholm A, Wilflingseder D, Gusenbauer S, Hildgartner A, et al. (2008) Vaccine 26 (Suppl 8): I79-85.
24. Fust G, Toth FD, Kiss J, Ujhelyi J, Nagy I, et al. (1994) Neutralizing and enhancing antibodies measured in complement-restored serum samples from HIV-1-infected individuals correlate with immunosuppression and disease. AIDS 8: 603-609.
25. Homsy J, Meyer M, Levy JA, (1990) Serum enhancement of human immunodeficiency virus (HIV) infection correlates with disease in HIV-infected individuals. J Virol 64: 1437-1440.
26. Tremblay M, Meloche S, Sekaly RP, Wainberg MA, (1990) Complement receptor 2 mediates enhancement of human immunodeficiency virus 1 infection in Epstein-Barr virus-carrying B cells. J Exp Med 171: 1791-1796.
27. Takeda A, Robinson JE, Ho DD, Debouck C, Haigwood NL, et al. (1992) Distinction of human immunodeficiency virus type 1 neutralization and infection enhancement by human monoclonal antibodies to glycoprotein 120. J Clin Investig 89: 1952-1957.
28. Thieblemont N, Haeffner-Cavaillon N, Ledur A, L'Age-Stehr J, Ziegler-Heitbrock HW, et al. (1993) CR1 (CD35) and CR3 (CD11b/CD18) mediate infection of human monocytes and monocytic cell lines with complement-opsonized HIV independently of CD4. Clin Exp Immunol 92: 106-113.
29. Szabo J, Prohaszka Z, Toth FD, Gyuris A, Segesdi J, et al. (1999) Strong correlation between the complement-mediated antibody-dependent enhancement of HIV-1 infection and plasma viral load. AIDS 13: 1841-1849.
30. Montefiori DC, Reimann KA, Letvin NL, Zhou J, Hu SL, (1995) Studies of complement-activating antibodies in the SIV/macaque model of acute primary infection and vaccine protection. AIDS Res. Hum.Retrovir 11: 963-970.
31. Halstead SB, (1979) In vivo enhancement of dengue virus infection in rhesus monkeys by passively transferred antibody. J Infect.Dis 140: 527-533.
32. Porterfield JS, (1986) Antibody-dependent enhancement of viral infectivity. Adv Virus Res 31: 335-355.
33. Frey, SE, Houghton M, Coates S, Abrignani S, Chien D, et al. (2010) Safety and Immunogenicity of HCV E1E2 Vaccine Adjuvanted with MF59 Administered to Healthy Adults. Vaccine 28: 6367-6373.
34. Engle RE, Russell RS, Purcell RH, Bukh J, (2008) Development of a TaqMan assay for the six major genotypes of hepatitis C virus: comparison with commercial assays. J Med Virol 80: 72-79.
35. Simister P, Schmitt M, Geitmann M, Wicht O, Danielson UH, et al. (2009) Structural and functional analysis of hepatitis C virus strain JFH1 polymerase. J Virol 83: 11926-39.
36. Morens DM, Halstead SB, Marchette NJ, (1987) Profiles of antibody-dependent enhancement of dengue virus type 2 infection. Microb. Pathog 3: 231-237.
37. Munakata Y, Kato I, Saito T, Kodera T, Ishii KK, et al. (2006) Human parvovirus B19 infection of monocytic cell line U937 and antibody-dependent enhancement. Virology 345: 251-257.
38. Halstead SB, O'Rourke EJ, (1977) Dengue viruses and mononuclear phagocytes. I. Infection enhancement by non-neutralizing antibody. J Exp.Med 146: 201-217.
39. Zeira M, Byrn RA, Groopman JE, (1990) Inhibition of serum-enhanced HIV-1 infection of U937 monocytoid cells by recombinant soluble CD4 and anti-CD4 monoclonal antibody. AIDS Res Hum Retroviruses 6: 629-39.
40. Chen RF, Yeh WT, Yang MY, Yang KD, (2001) A model of the real-time correlation of viral titers with immune reactions in antibody-dependent enhancement of dengue-2 infections. FEMS Immunol Med Microbiol 30: 1-7.
41. Libraty DH, Endy TP, Houng HS, Green S, Kalayanarooj S, et al. (2002) Differing influences of virus burden and immune activation on disease severity in secondary dengue-3 virus infections. J Infect Dis 185: 1213-21.
42. Goncalvez, AP, Engle RE, Claire M St, Purcell RH, Lai CJ, (2007) Monoclonal antibody-mediated enhancement of dengue virus infection in vitro and in vivo and strategies for prevention. Proc. Natl. Acad. Sci. USA 104: 9422-9427.
43. Balsitis SJ, Williams KL, Lachica R, Flores D, Kyle JL, et al. (2010) Lethal antibody enhancement of dengue disease in mice is prevented by Fc modification. PLoS Pathog 6: e10000790.
44. Dejnirattisai W, Jumnainsong A, Onsirisakul N, Fitton P, Vasanawathana S, et al. (2010) Cross-reacting antibodies enhance dengue virus infection in humans. Science 328: 745-8.