Hepatitis C virus hypervariable region 1 variants presented on hepatitis B virus capsid-like particles induce cross-neutralizing antibodies

PLoS ONE

Volumn 9, Issue 7, 2014, Pages

  Lange, Milena ^a   Fiedler, Melanie ^a   Bankwitz, Dorothea ^b   Osburn, William ^c   Viazov, Sergei ^a   Brovko, Olena ^a   Zekri, Abdel Rahman ^d   Khudyakov, Yury ^e   Nassal, Michael ^f   Pumpens, Paul ^g   Pietschmann, Thomas ^b   Timm, Jörg ^a   Roggendorf, Michael ^a   Walker, Andreas ^a  

^a UNIVERSITY HOSPITAL ESSEN   (Germany)

^b INSTITUTE OF INFECTION IMMUNOLOGY   (Germany)

^c JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d NATIONAL CANCER INSTITUTE   (Egypt)

^e CENTERS FOR DISEASE CONTROL AND PREVENTION   (United States)

^f UNIVERSITY OF FREIBURG   (Germany)

^g LATVIAN BIOMEDICAL RESEARCH AND STUDY CENTRE   (Latvia)

Author keywords

[No Author keywords available]

Indexed keywords

ARSENIC TRIOXIDE; CORE PROTEIN; HEPATITIS ANTIBODY; HEPATITIS B VIRUS PROTEIN; HYPERVARIABLE REGION 1 CAPSID LIKE PARTICLE; IMMUNOLOGICAL ADJUVANT; NEUTRALIZING ANTIBODY; UNCLASSIFIED DRUG; VIRUS PROTEIN; ALPHA TOCOPHEROL; ASO3B ADJUVANT; CAPSID PROTEIN; DRUG COMBINATION; HEPATITIS VACCINE; HVR1 PROTEIN, HEPATITIS C VIRUS; POLYSORBATE; RECOMBINANT PROTEIN; SQUALENE; VIRUS ANTIBODY; VIRUS ANTIGEN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANTIBODY TITER; ANTIGEN PRESENTATION; ARTICLE; CAPSID LIKE PARTICLE; CONTROLLED STUDY; CROSS REACTION; FEMALE; GENETIC VARIABILITY; HEPATITIS B VIRUS; HEPATITIS C VIRUS; HYPERVARIABLE REGION 1; IMMUNE RESPONSE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN FUNCTION; PROTEIN INDUCTION; SPLITCORE CAPSIDE LIKE PARTICLE; VIRUS CAPSID; VIRUS ISOLATION; VIRUS NEUTRALIZATION; VIRUS PARTICLE; ANIMAL; BIOSYNTHESIS; C57BL MOUSE; CHEMISTRY; CROSS PROTECTION; DRUG COMBINATION; ESCHERICHIA COLI; GENE EXPRESSION; GENETICS; HEPACIVIRUS; HEPATITIS C; HUMAN; HUMORAL IMMUNITY; IMMUNOLOGY; INTRAMUSCULAR DRUG ADMINISTRATION; METABOLISM; SUBCUTANEOUS DRUG ADMINISTRATION; VIROLOGY;

ALPHA-TOCOPHEROL; ANIMALS; ANTIBODIES, NEUTRALIZING; ANTIBODIES, VIRAL; ANTIGEN PRESENTATION; ANTIGENS, VIRAL; CAPSID PROTEINS; CROSS PROTECTION; DRUG COMBINATIONS; ESCHERICHIA COLI; FEMALE; GENE EXPRESSION; HEPACIVIRUS; HEPATITIS B VIRUS; HEPATITIS C; HUMANS; IMMUNITY, HUMORAL; INJECTIONS, INTRAMUSCULAR; INJECTIONS, SUBCUTANEOUS; MICE; MICE, INBRED C57BL; POLYSORBATES; RECOMBINANT PROTEINS; SQUALENE; VIRAL HEPATITIS VACCINES; VIRAL PROTEINS;

EID: 84904177266     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0102235     Document Type: Article

References (78)

1. Houghton M (2011) Prospects for prophylactic and therapeutic vaccines against the hepatitis C viruses. Immunol Rev 239: 99-108.
2. Kim AY, Kuntzen T, Timm J, Nolan BE, Baca MA, et al. (2011) Spontaneous control of HCV is associated with expression of HLA-B 57 and preservation of targeted epitopes. Gastroenterology 140: 686-696 e681.
3. Bartosch B, Bukh J, Meunier JC, Granier C, Engle RE, et al. (2003) 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. (Pubitemid 37499214)
4. Pestka JM, Zeisel MB, Blaser E, Schurmann P, Bartosch B, et al. (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. (Pubitemid 47175652)
5. Dowd KA, Netski DM, Wang XH, Cox AL, Ray SC (2009) Selection pressure from neutralizing antibodies drives sequence evolution during acute infection with hepatitis C virus. Gastroenterology 136: 2377-2386.
6. Osburn WO, Fisher BE, Dowd KA, Urban G, Liu L, et al. (2010) Spontaneous control of primary hepatitis C virus infection and immunity against persistent reinfection. Gastroenterology 138: 315-324.
7. Page K, Osburn W, Evans J, Hahn JA, Lum P, et al. (2013) Frequent longitudinal sampling of hepatitis C virus infection in injection drug users reveals intermittently detectable viremia and reinfection. Clin Infect Dis 56: 405-413.
8. Mehta SH, Cox A, Hoover DR, Wang XH, Mao Q, et al. (2002) Protection against persistence of hepatitis C. Lancet 359: 1478-1483.
9. von Hahn T, Yoon JC, Alter H, Rice CM, Rehermann B, et al. (2007) Hepatitis C virus continuously escapes from neutralizing antibody and T-cell responses during chronic infection in vivo. Gastroenterology 132: 667-678.
10. Kumar U, Monjardino J, Thomas HC (1994) Hypervariable region of hepatitis C virus envelope glycoprotein (E2/NS1) in an agammaglobulinemic patient. Gastroenterology 106: 1072-1075. (Pubitemid 24109297)
11. Booth JC, Kumar U, Webster D, Monjardino J, Thomas HC (1998) Comparison of the rate of sequence variation in the hypervariable region of E2/NS1 region of hepatitis C virus in normal and hypogammaglobulinemic patients. Hepatology 27: 223-227. (Pubitemid 28041558)
12. Callens N, Ciczora Y, Bartosch B, Vu-Dac N, Cosset FL, et al. (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)
13. Penin F, Combet C, Germanidis G, Frainais PO, Deleage G, et al. (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)
14. Bankwitz D, Steinmann E, Bitzegeio J, Ciesek S, Friesland M, 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.
15. Prentoe J, Jensen TB, Meuleman P, Serre SB, Scheel TK, 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.
16. Vieyres G, Dubuisson J, Patel AH (2010) Characterization of antibody-mediated neutralization directed against the hypervariable region 1 of hepatitis C virus E2 glycoprotein. J Gen Virol 92: 494-506.
17. Hsu M, Zhang J, Flint M, Logvinoff C, Cheng-Mayer C, 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. (Pubitemid 36706428)
18. Mondelli MU, Cerino A, Meola A, Nicosia A (2003) Variability or conservation of hepatitis C virus hypervariable region 1? Implications for immune responses. J Biosci 28: 305-310. (Pubitemid 36512805)
19. Guan M, Wang W, Liu X, Tong Y, Liu Y, et al. (2012) Three different functional microdomains in the hepatitis C virus hypervariable region 1 (HVR1) mediate entry and immune evasion. J Biol Chem 287: 35631-35645.
20. 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.
21. Brimacombe CL, Grove J, Meredith LW, Hu K, Syder AJ, et al. (2011) Neutralizing antibody-resistant hepatitis C virus cell-to-cell transmission. J Virol 85: 596-605.
22. Farci P, Shimoda A, Wong D, Cabezon T, De Gioannis D, 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. (Pubitemid 27009611)
23. 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.
24. Roccasecca R, Folgori A, Ercole BB, Puntoriero G, Lahm A, et al. (2001) Induction of cross-reactive humoral immune response by immunization with mimotopes of the hypervariable region 1 of the hepatitis C virus. Int Rev Immunol 20: 289-300. (Pubitemid 33119082)
25. Roccasecca R, Folgori A, Ercole BB, Puntoriero G, Lahm A, et al. (2001) Mimotopes of the hyper variable region 1 of the hepatitis C virus induce cross-reactive antibodies directed against discontinuous epitopes. Mol Immunol 38: 485-492. (Pubitemid 34008478)
26. Zucchelli S, Roccasecca R, Meola A, Ercole BB, Tafi R, et al. (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. (Pubitemid 32185232)
27. Campo DS, Dimitrova Z, Yokosawa J, Hoang D, Perez NO, et al. (2012) Hepatitis C virus antigenic convergence. Sci Rep 2: 267.
28. Douglas T, Young M (2006) Viruses: making friends with old foes. Science 312: 873-875. (Pubitemid 43727311)
29. Manolova V, Flace A, Bauer M, Schwarz K, Saudan P, et al. (2008) Nanoparticles target distinct dendritic cell populations according to their size. Eur J Immunol 38: 1404-1413.
30. Conway JF, Watts NR, Belnap DM, Cheng N, Stahl SJ, et al. (2003) Characterization of a conformational epitope on hepatitis B virus core antigen and quasiequivalent variations in antibody binding. J Virol 77: 6466-6473. (Pubitemid 36588416)
31. Birnbaum F, Nassal M (1990) Hepatitis B virus nucleocapsid assembly: primary structure requirements in the core protein. J Virol 64: 3319-3330. (Pubitemid 20219537)
32. Milich DR, McLachlan A (1986) The nucleocapsid of hepatitis B virus is both a T-cell-independent and a T-cell-dependent antigen. Science 234: 1398-1401. (Pubitemid 17210220)
33. Fehr T, Skrastina D, Pumpens P, Zinkernagel RM (1998) T cell-independent type I antibody response against B cell epitopes expressed repetitively on recombinant virus particles. Proc Natl Acad Sci U S A 95: 9477-9481. (Pubitemid 28506256)
34. Keller SA, Schwarz K, Manolova V, von Allmen CE, Kinzler MG, et al. (2010) Innate signaling regulates cross-priming at the level of DC licensing and not antigen presentation. Eur J Immunol 40: 103-112.
35. Lee BO, Tucker A, Frelin L, Sallberg M, Jones J, et al. (2009) Interaction of the hepatitis B core antigen and the innate immune system. J Immunol 182: 6670-6681.
36. Pumpens P, Grens E (2001) HBV core particles as a carrier for B cell/T cell epitopes. Intervirology 44: 98-114. (Pubitemid 32757388)
37. Ulrich R, Nassal M, Meisel H, Kruger DH (1998) Core particles of hepatitis B virus as carrier for foreign epitopes. Adv Virus Res 50: 141-182.
38. Gregson AL, Oliveira G, Othoro C, Calvo-Calle JM, Thorton GB, et al. (2008) Phase I trial of an alhydrogel adjuvanted hepatitis B core virus-like particle containing epitopes of Plasmodium falciparum circumsporozoite protein. PLoS One 3: e1556.
39. Oliveira GA, Wetzel K, Calvo-Calle JM, Nussenzweig R, Schmidt A, et al. (2005) Safety and enhanced immunogenicity of a hepatitis B core particle Plasmodium falciparum malaria vaccine formulated in adjuvant Montanide ISA 720 in a phase I trial. Infect Immun 73: 3587-3597. (Pubitemid 40745903)
40. Nassal M, Skamel C, Vogel M, Kratz PA, Stehle T, et al. (2008) Development of hepatitis B virus capsids into a whole-chain protein antigen display platform: new particulate Lyme disease vaccines. Int J Med Microbiol 298: 135-142. (Pubitemid 350216556)
41. Kratz PA, Bottcher B, Nassal M (1999) Native display of complete foreign protein domains on the surface of hepatitis B virus capsids. Proc Natl Acad Sci U S A 96: 1915-1920. (Pubitemid 29117842)
42. Skamel C, Ploss M, Bottcher B, Stehle T, Wallich R, et al. (2006) Hepatitis B virus capsid-like particles can display the complete, dimeric outer surface protein C and stimulate production of protective antibody responses against Borrelia burgdorferi infection. J Biol Chem 281: 17474-17481.
43. Walker A, Skamel C, Nassal M (2011) SplitCore: An exceptionally versatile viral nanoparticle for native whole protein display regardless of 3D structure. Sci Rep 1: 5.
44. Puntoriero G, Meola A, Lahm A, Zucchelli S, Ercole BB, et al. (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. (Pubitemid 28327371)
45. Vieyres G, Dubuisson J, Patel AH (2011) Characterization of antibody-mediated neutralization directed against the hypervariable region 1 of hepatitis C virus E2 glycoprotein. J Gen Virol 92: 494-506.
46. Zibert A, Kraas W, Meisel H, Jung G, Roggendorf M (1997) Epitope mapping of antibodies directed against hypervariable region 1 in acute self-limiting and chronic infections due to hepatitis C virus. J Virol 71: 4123-4127. (Pubitemid 27172432)
47. Pietschmann T, Kaul A, Koutsoudakis G, Shavinskaya A, Kallis S, et al. (2006) Construction and characterization of infectious intragenotypic and intergenotypic hepatitis C virus chimeras. Proc Natl Acad Sci U S A 103: 7408-7413. (Pubitemid 43727846)
48. Nassal M, Skamel C, Kratz PA, Wallich R, Stehle T, et al. (2005) A fusion product of the complete Borrelia burgdorferi outer surface protein A (OspA) and the hepatitis B virus capsid protein is highly immunogenic and induces protective immunity similar to that seen with an effective lipidated OspA vaccine formula. Eur J Immunol 35: 655-665. (Pubitemid 40331342)
49. Geldmacher A, Skrastina D, Borisova G, Petrovskis I, Kruger DH, et al. (2005) A hantavirus nucleocapsid protein segment exposed on hepatitis B virus core particles is highly immunogenic in mice when applied without adjuvants or in the presence of pre-existing anti-core antibodies. Vaccine 23: 3973-3983. (Pubitemid 40726191)
50. Ameiss K, Ashraf S, Kong W, Pekosz A, Wu WH, et al. (2010) Delivery of woodchuck hepatitis virus-like particle presented influenza M2e by recombinant attenuated Salmonella displaying a delayed lysis phenotype. Vaccine 28: 6704-6713.
51. Sallberg M, Hughes J, Jones J, Phillips TR, Milich DR (2002) A malaria vaccine candidate based on a hepatitis B virus core platform. Intervirology 45: 350-361. (Pubitemid 36173445)
52. Walker A, Skamel C, Nassal A (2011) SplitCore: An exceptionally versatile viral nanoparticle for native whole protein display regardless of 3D structure. Nature Scientific Reports 1.
53. Singh S, Zlotnick A (2003) Observed hysteresis of virus capsid disassembly is implicit in kinetic models of assembly. J Biol Chem 278: 18249-18255. (Pubitemid 36799443)
54. Jegerlehner A, Wiesel M, Dietmeier K, Zabel F, Gatto D, et al. (2010) Carrier induced epitopic suppression of antibody responses induced by virus-like particles is a dynamic phenomenon caused by carrier-specific antibodies. Vaccine 28: 5503-5512.
55. Billaud JN, Peterson D, Lee BO, Maruyama T, Chen A, et al. (2007) Advantages to the use of rodent hepadnavirus core proteins as vaccine platforms. Vaccine 25: 1593-1606. (Pubitemid 46108210)
56. Herzenberg LA, Tokuhisa T (1980) Carrier-priming leads to hapten-specific suppression. Nature 285: 664-667. (Pubitemid 10058188)
57. Whitacre DC, Lee BO, Milich DR (2009) Use of hepadnavirus core proteins as vaccine platforms. Expert Rev Vaccines 8: 1565-1573.
58. Billaud JN, Peterson D, Barr M, Chen A, Sallberg M, et al. (2005) Combinatorial approach to hepadnavirus-like particle vaccine design. J Virol 79: 13656-13666. (Pubitemid 41508177)
59. Guy B (2007) The perfect mix: recent progress in adjuvant research. Nature Reviews Microbiology 5: 505-517.
60. Wynne SA, Crowther RA, Leslie AG (1999) The crystal structure of the human hepatitis B virus capsid. Mol Cell 3: 771-780. (Pubitemid 29323055)
61. Meunier JC, Gottwein JM, Houghton M, Russell RS, Emerson SU, et al. (2011) Vaccine-induced cross-genotype reactive neutralizing antibodies against hepatitis C virus. J Infect Dis 204: 1186-1190.
62. Conaty S, Watson L, Dinnes J, Waugh N (2004) The effectiveness of pneumococcal polysaccharide vaccines in adults: a systematic review of observational studies and comparison with results from randomised controlled trials. Vaccine 22: 3214-3224. (Pubitemid 39037227)
63. Law M, Maruyama T, Lewis J, Giang E, Tarr AW, et al. (2008) Broadly neutralizing antibodies protect against hepatitis C virus quasispecies challenge. Nat Med 14: 25-27.
64. Logvinoff C, Major ME, Oldach D, Heyward S, Talal A, et al. (2004) Neutralizing antibody response during acute and chronic hepatitis C virus infection. Proc Natl Acad Sci U S A 101: 10149-10154. (Pubitemid 38891210)
65. Law JL, Chen C, Wong J, Hockman D, Santer DM, et al. (2013) A Hepatitis C Virus (HCV) Vaccine Comprising Envelope Glycoproteins gpE1/gpE2 Derived from a Single Isolate Elicits Broad Cross-Genotype Neutralizing Antibodies in Humans. PLoS ONE 8: e59776.
66. Burton DR (2002) Antibodies, viruses and vaccines. Nat Rev Immunol 2: 706- 713.
67. Fournillier A, Frelin L, Jacquier E, Ahlen G, Brass A, et al. (2013) A heterologous prime/boost vaccination strategy enhances the immunogenicity of therapeutic vaccines for hepatitis C virus. J Infect Dis 208: 1008-1019.
68. Barnes E, Folgori A, Capone S, Swadling L, Aston S, et al. Novel adenovirus-based vaccines induce broad and sustained T cell responses to HCV in man. Sci Transl Med 4: 115ra111.
69. Barouch DH, Liu J, Li H, Maxfield LF, Abbink P, et al. Vaccine protection against acquisition of neutralization-resistant SIV challenges in rhesus monkeys. Nature.
70. Nassal M (1988) Total chemical synthesis of a gene for hepatitis B virus core protein and its functional characterization. Gene 66: 279-294.
71. Vogel M, Vorreiter J, Nassal M (2005) Quaternary structure is critical for protein display on capsid-like particles (CLPs): efficient generation of hepatitis B virus CLPs presenting monomeric but not dimeric and tetrameric fluorescent proteins. Proteins 58: 478-488. (Pubitemid 40076061)
72. Walker A, Skamel C, Vorreiter J, Nassal M (2008) Internal core protein cleavage leaves the hepatitis B virus capsid intact and enhances its capacity for surface display of heterologous whole chain proteins. J Biol Chem 283: 33508-33515.
73. Bichko V, Schodel F, Nassal M, Gren E, Berzinsh I, et al. (1993) Epitopes recognized by antibodies to denatured core protein of hepatitis B virus. Mol Immunol 30: 221-231.
74. Bottcher B, Vogel M, Ploss M, Nassal M (2006) High plasticity of the hepatitis B virus capsid revealed by conformational stress. J Mol Biol 356: 812-822. (Pubitemid 43139340)
75. Connor RI, Chen BK, Choe S, Landau NR (1995) Vpr is required for efficient replication of human immunodeficiency virus type-1 in mononuclear phagocytes. Virology 206: 935-944.
76. Bartosch B, Vitelli A, Granier C, Goujon C, Dubuisson J, 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. Journal of Biological Chemistry 278: 41624-41630. (Pubitemid 37310418)
77. Vogel M, Diez M, Eisfeld J, Nassal M (2005) In vitro assembly of mosaic hepatitis B virus capsid-like particles (CLPs): rescue into CLPs of assembly-deficient core protein fusions and FRET-suited CLPs. FEBS Lett 579: 5211-5216. (Pubitemid 41318093)
78. Belnap DM, Watts NR, Conway JF, Cheng N, Stahl SJ, et al. (2003) Diversity of core antigen epitopes of hepatitis B virus. Proc Natl Acad Sci U S A 100: 10884-10889. (Pubitemid 37140122)