DNA-based vaccination against hepatitis C virus (HCV): Effect of expressing different forms of HCV E2 protein and use of CpG-optimized vectors in mice

Vaccine

Volumn 20, Issue 27-28, 2002, Pages 3263-3271

  Ma, Xiaoying ^a   Forns, Xavier ^b   Gutierrez, Robin ^c   Mushahwar, Isa K ^c   Wu, Tong ^a   Payette, Paul J ^a,d   Bukh, Jens ^b   Purcell, Robert H ^b   Davis, Heather L ^a,d  

^a OTTAWA HOSPITAL RESEARCH INSTITUTE   (Canada)

^b NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^c ABBOTT LABORATORIES   (United States)

^d Coley Pharmaceutical Group ^*  (Canada)

Author keywords

Antigen localization; CpG motifs; DNA vaccine; HCV E2; Hepatitis C

Indexed keywords

ANTIBODY; DNA VACCINE; HEPATITIS C VACCINE; IMMUNOGLOBULIN G; VIRUS ENVELOPE PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY RESPONSE; ANTIBODY SPECIFICITY; ARTICLE; CONTROLLED STUDY; CPG ISLAND; FEMALE; HEPATITIS; HEPATITIS C VIRUS; IMMUNIZATION; IMMUNOGENICITY; IMMUNOSTIMULATION; MEMBRANE BINDING; MOUSE; NONHUMAN; PLASMID; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; SEROCONVERSION; T LYMPHOCYTE; TH1 CELL; VACCINATION; VIRUS INFECTION;

ANIMALS; BASE SEQUENCE; CPG ISLANDS; DNA, VIRAL; FEMALE; GENETIC VECTORS; HEPACIVIRUS; HEPATITIS C; HEPATITIS C ANTIBODIES; HEPATITIS C ANTIGENS; HUMANS; MICE; MICE, INBRED BALB C; T-LYMPHOCYTES, CYTOTOXIC; VACCINES, DNA; VIRAL ENVELOPE PROTEINS; VIRAL HEPATITIS VACCINES;

EID: 0037055970     PISSN: 0264410X     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0264-410X(02)00304-3     Document Type: Article

References (82)

1. Choo Q.L., Kuo G., Weiner A.J., Overby L.R., Bradley D.W., Houghton M. Isolation of a cDNA clone derived from a blood-borne non-A, non-B viral hepatitis genome. Science. 244:1989;359-362.
2. Clarke B. Molecular virology of hepatitis C virus. J. Gen. Virol. 78:1997;2397-2410.
3. Boyer N., Marcellin P. Pathogenesis, diagnosis and management of hepatitis C. J. Hepatol. 32:2000;98-112.
4. Weiner A.J., Geysens H.M., Christopherson C., Hall E.J., Mason T.J., Saracco G. Evidence of immune selection of hepatitis C virus (HCV) putative envelope glycoprotein variants: potential role in chronic HCV infections. Proc. Natl. Acad. Sci. U.S.A. 89:1992;3468-3472.
5. Tsai S.L., Chen Y.M., Chen M.H., Huang C.Y., Sheen I.S., Yeh C.T.et al. Hepatitis C virus variants circumventing cytotoxic T lymphocyte activity as a mechanism of chronicity. Gastroenterology. 115:1998;954-965.
6. Forns X., Purcell R.H., Bukh J. Quasi species in viral persistence and pathogenesis of hepatitis C virus. Trends Microbiol. 7:1999;402-410.
7. Ferrari C., Valli A., Galati L., Penna A., Scaccaglia P., Giuberti T. T cell response to structural and non-structural hepatitis C virus antigen in persistent and self-limited hepatitis C virus infection. Hepatology. 19:1994;286-295.
8. Diepolder H.M., Zachoval R., Hoffmann R.M., Wierenga E.A., Santantonio T., Jung M.C.et al. Possible mechanism involving T-lymphocyte response to non-structural protein 3 in viral clearance in acute hepatitis C virus infection. Lancet. 346:1995;1006-1007.
9. Lechmann M., Ihlenfeldt H.G., Braunschweiger I., Giers G., Jung G., Matz B.et al. T- and B-cell responses to different hepatitis C virus antigens in patients with chronic hepatitis C infection and in healthy anti-hepatitis C virus - positive blood donors without viremia. Hepatology. 24:1996;790-795.
10. Missale G., Bertoni R., Lamonaca V., Valli A., Massari M., Mori C.et al. Different clinical behaviors of acute hepatitis C virus infection are associated with different vigor of the anti-viral cell-mediated immune response. J. Clin. Invest. 98:1996;706-714.
11. Rehermann B., Chang K.M., McHutchison J.G., Kokka R., Houghton M., Chisari F.V. Quantitative analysis of the peripheral blood cytotoxic T lymphocyte response in patients with chronic hepatitis C virus infection. J. Clin. Invest. 98:1996;1432-1440.
12. Diepolder H.M., Gerlach J.T., Zachoval R., Hoffmann R.M., Jung M.C., Wierenga E.A.et al. Immunodominant CD4+ T-cell epitope within non-structural protein 3 in acute hepatitis C virus infection. J. Virol. 71:1997;6011-6019.
13. Tsai S.L., Liaw Y.F., Chen M.H., Huang C.Y., Kuo G.C. Detection of type 2-like T-helper cells in hepatitis C virus infection: implications for hepatitis C virus chronicity. Hepatology. 25:1997;449-458.
14. Woitas R.P., Lechmann M., Jung G., Kaiser R., Sauerbruch T., Spengler U. CD30 induction and cytokine profiles in hepatitis C virus core-specific peripheral blood T lymphocytes. J. Immunol. 159:1997;1012-1018.
15. Fan X.G., Liu W.E., Li C.Z., Wang Z.C., Luo L.X., Tan D.M.et al. Circulating Th1 and Th2 cytokines in patients with hepatitis C virus infection. Mediators Inflamm. 7:1998;295-297.
16. Schlaak J.F., Pitz T., Lohr H.F., Meyer zum Buschenfelde K.H., Gerken G. Interleukin 12 enhances deficient HCV-antigen-induced Th1-type immune response of peripheral blood mononuclear cells. J. Med. Virol. 56:1998;112-117.
17. Cooper S., Erickson A.L., Adams E.J., Kansopon J., Weiner A.J., Chien D.Y.et al. Analysis of a successful immune response against hepatitis C virus. Immunity. 10:1999;439-449.
18. Cramp M.E., Carucci P., Rossol S., Chokshi S., Maertens G., Williams R.et al. Hepatitis C virus (HCV) specific immune responses in anti-HCV positive patients without hepatitis C viremia. Gut. 44:1999;424-429.
19. Bouffard P., Hayashi P.H., Acevedo R., Levy N., Zeldis J.B. Hepatitis C virus is detected in a monocyte/macrophage subpopulation of peripheral blood mononuclear cells of infected patients. J. Infect. Dis. 166:1992;1276-1280.
20. Hsieh T.T., Yao D.S., Sheen I.S., Liaw Y.F., Pao C.C. Hepatitis C virus in peripheral blood mononuclear cells. Am. J. Clin. Pathol. 98:1992;392-396.
21. Qian C., Camps J., Maluenda M.D., Civeira M.P., Prieto J. Replication of hepatitis C virus in peripheral blood mononuclear cells: effect of alpha-interferon therapy. J. Hepatol. 16:1992;380-383.
22. Wang J.T., Sheu J.C., Lin J.T., Wang T.H., Chen D.S. Detection of replicative form of hepatitis C virus RNA in peripheral blood mononuclear cells. J. Infect. Dis. 166:1992;1167-1169.
23. Zignego A.L., Macchia D., Monti M., Thiers V., Mazzetti M., Foschi M.et al. Infection of peripheral mononuclear blood cells by hepatitis C virus. J. Hepatol. 15:1992;382-386.
24. Muller H.M., Pfaff E., Goeser T., Kallinowski B., Solbach C., Theilmann L. Peripheral blood leukocytes serve as a possible extrahepatic site for hepatitis C virus replication. J. Gen. Virol. 74:1993;669-676.
25. Moldvay J., Deny P., Pol S., Brechot C., Lamas E. Detection of hepatitis C virus RNA in peripheral blood mononuclear cells of infected patients by in situ hybridization. Blood. 83:1994;269-273.
26. Navas S., Castillo I., Bartolome J., Marriott E., Herrero M., Carreno V. Positive and negative hepatitis C virus RNA strands in serum, liver and peripheral blood mononuclear cells in anti-HCV patients: relation with the liver lesion. J. Hepatol. 21:1994;182-186.
27. Willems M., Peerlinck K., Moshage H., Deleu I., Van den Eynde C., Vermylen J.et al. Hepatitis C virus-RNAs in plasma and in peripheral blood mononuclear cells of hemophiliacs with chronic hepatitis C: evidence for viral replication in peripheral blood mononuclear cells. J. Med. Virol. 42:1994;272-278.
28. Yun Z.B., Sonnerborg A., Weiland O. Hepatitis C virus replication in liver and peripheral blood mononuclear cells of interferon-alpha-treated and untreated patients with chronic hepatitis C. Scand. J. Gastroenterol. 29:1994;82-86.
29. Zignego A.L., De Carli M., Monti M., Careccia G., La Villa G., Giannini C.et al. Hepatitis C virus infection of mononuclear cells from peripheral blood and liver infiltrates in chronically infected patients. J. Med. Virol. 47:1995;58-64.
30. Lerat H., Berby F., Trabaud M.A., Vidalin O., Major M., Trepo C.et al. Specific detection of hepatitis C virus minus strand RNA in hematopoietic cells. J. Clin. Invest. 97:1996;845-851.
31. Mihm S., Hartmann H., Ramadori G. A reevaluation of the association of hepatitis C virus replicative intermediates with peripheral blood cells including granulocytes by a tagged reverse transcription/polymerase chain reaction technique. J. Hepatol. 24:1996;491-497.
32. Lerat H., Rumin S., Habersetzer F., Berby F., Trabaud M.A., Trepo C.et al. In vivo tropism of hepatitis C virus genomic sequences in hematopoietic cells: influence of viral load, viral genotype, and cell phenotype. Blood. 91:1998;3841-3849.
33. Fugier-Vivier I., Servet-Delprat C., Rivailler P., Rissoan M.C., Liu Y.J., Rabourdin-Combe C. Measles virus suppresses cell-mediated immunity by interfering with the survival and functions of dendritic and T cells. J. Exp. Med. 186:1997;813-823.
34. Grosjean I., Caux C., Bella C., Berger I., Wild F., Banchereau J.et al. Measles virus infects human dendritic cells and blocks their allostimulatory properties for CD4+ T cells. J. Exp. Med. 186:1997;801-812.
35. Schnorr J.J., Xanthakos S., Keikavoussi P., Kampgen E., ter Meulen V., Schneider-Schaulies S. Induction of maturation of human blood dendritic cell precursors by measles virus is associated with immunosuppression. Proc. Natl. Acad. Sci. U.S.A. 94:1997;5326-5331.
36. Salio M., Cella M., Suter M., Lanzavecchia A. Inhibition of dendritic cell maturation by herpes simplex virus. Eur. J. Immunol. 29:1999;3245-3253.
37. Kruse M., Rosorius O., Kratzer F., Stelz G., Kuhnt C., Schuler G.et al. Mature dendritic cells infected with herpes simplex virus type 1 exhibit inhibited T-cell stimulatory capacity. J. Virol. 74:2000;7127-7136.
38. Servet-Delprat C., Vidalain P.O., Bausinger H., Manie S., Le Deist F., Azocar O.et al. Measles virus induces abnormal differentiation of CD40 ligand-activated human dendritic cells. J. Immunol. 164:2000;1753-1760.
39. Vidalain P.O., Azocar O., Rabourdin-Combe C., Servet-Delprat C. Measle virus-infected dendritic cells develop immunosuppressive and cytotoxic activities. Immunobiology. 204:2001;629-638.
40. Inchauspe G. Gene vaccination for hepatitis C. Springer Semin. Immunopathol. 19:1997;211-221.
41. Choo Q.L., Kuo G., Ralston R., Weiner A., Chien D., Van Nest G.et al. Vaccination of chimpanzees against infection by the hepatitis C virus. Proc. Natl. Acad. Sci. U.S.A. 91:1994;1294-1298.
42. Rosa D., Campagnoli S., Moretto C., Cuenzi E., Cousens L., Chin M. A quantitative test to estimate neutralizing antibodies to hepatitis C virus: cytoflourimetric assessment of envelope glycoprotein 2 binding to target cells. Proc. Natl. Acad. Sci. U.S.A. 93:1996;1759-1763.
43. Farci P., Alter H.J., Wong D.C., Miller R.H., Govindarajan S., Engle R.et al. Prevention of hepatitis C virus infection in chimpanzees after antibody-mediated in vitro neutralization. Proc. Natl. Acad. Sci. U.S.A. 91:1994;7792-7796.
44. Farci P., Shimoda A., Wong D., Cabezon T., De Gioannis D., Strazzera A.et al. 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. 93:1996;15394-15399.
45. Krieg A.M., Wu T., Weeratna R., Efler S.M., Love-Homan L., Yang L.et al. Sequence motifs in adenoviral DNA block immune activation by stimulatory CpG motifs. Proc. Natl. Acad. Sci. U.S.A. 95:1998;12631-12636.
46. Davis H.L., Weeratna R., Waldschmidt T.J., Schorr J., Krieg A.M. CpG DNA is a potent enhancer of specific immunity in mice immunized with recombinant hepatitis B surface antigen. J. Immunol. 160:1998a;870-876.
47. Davis H.L., McCluskie M.J. DNA vaccines for viral diseases. Microbes. Infect. 1:1999;7-21.
48. Davis H.L. Use of CpG DNA for enhancing specific immune responses. Curr. Top. Microbiol. Immunol. 247:2000;171-183.
49. Krieg A.M. The role of CpG motifs in innate immunity. Curr. Opin. Immunol. 12:2000;35-43.
50. Nakano I., Maertens G., Major M.E., Vitvitski L., Dubuisson J., Fournillier A.et al. Immunization with plasmid DNA encoding hepatitis C virus envelope E2 antigenic domains induces antibodies whose immune reactivity is linked to the injection mode. J. Virol. 71:1997;7101-7109.
51. Tedeschi V., Akatsuka T., Shih J.W., Battegay M., Feinstone S.M. A specific antibody response to HCV E2 elicited in mice by intramuscular inoculation of plasmid DNA containing coding sequences for E2. Hepatology. 25:1997;459-462.
52. Fournillier A., Nakano I., Vitvitski L., Depla E., Vidalin O., Maertens G.et al. Modulation of immune responses to hepatitis C virus envelope E2 protein following injection of plasmid DNA using single or combined delivery routes. Hepatology. 28:1998;237-244.
53. MacGregor R.R., Boyer J.D., Ugen K.E., Lacy K.E., Gluckman S.J., Bagarazzi M.L.et al. First human trial of a DNA-based vaccine for treatment of human immunodeficiency virus type 1 infection: safety and host response. J. Infect. Dis. 178:1998;92-100.
54. Ugen K.E., Nyland S.B., Boyer J.D., Vidal C., Lera L., Rasheid S.et al. DNA vaccination with HIV-1 expressing constructs elicits immune responses in humans. Vaccine. 16:1998;1818-1821.
55. Wang R., Doolan D.L., Le T.P., Hedstrom R.C., Coonan K.M., Charoenvit Y.et al. Induction of antigen-specific cytotoxic T lymphocytes in humans by a malaria DNA vaccine. Science. 282:1998;476-480.
56. Boyer J.D., Chattergoon M.A., Ugen K.E., Shah A., Bennett M., Cohen A.et al. Enhancement of cellular immune response in HIV-1 seropositive individuals: a DNA-based trial. Clin. Immunol. 90:1999;100-107.
57. Tacket C.O., Roy M.J., Widera G., Swain W.F., Broome S., Edelman R. Phase 1 safety and immune response studies of a DNA vaccine encoding hepatitis B surface antigen delivered by a gene delivery device. Vaccine. 17:1999;2826-2829.
58. Boyer J.D., Cohen A.D., Vogt S., Schumann K., Nath B., Ahn L.et al. Vaccination of seronegative volunteers with a human immunodeficiency virus type 1 env/rev DNA vaccine induces antigen-specific proliferation and lymphocyte production of beta-chemokines. J. Infect. Dis. 181:2000;476-483.
59. Swain W.E., Heydenburg Fuller D., Wu M.S., Barr L.J., Fuller J.T., Culp J.et al. Tolerability and immune responses in humans to a PowderJect DNA vaccine for hepatitis B. Dev. Biol. Basel. 104:2000;115-119.
60. Wang R., Epstein J., Baraceros F.M., Gorak E.J., Charoenvit Y., Carucci D.J.et al. Induction of CD4(+) T cell-dependent CD8(+) type 1 responses in humans by a malaria DNA vaccine. Proc. Natl. Acad. Sci. U.S.A. 98:2001;10817-10822.
61. Yanagi M., Purcell R.H., Emerson S.U., Bukh J. 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. 94:1997;8738-8743.
62. Schubert M., Joshi B., Blondel D., Harmison G.G. Insertion of the human immunodeficiency virus CD4 receptor into the envelope of vesicular stomatitis virus particles. J. Virol. 66:1992;1579-1589.
63. Forns X., Bukh J., Purcell R.H., Emerson S.U. How Escherichia coli can bias the results of molecular cloning: preferential selection of defective genomes of hepatitis C virus during the cloning procedure. Proc. Natl. Acad. Sci. U.S.A. 94:1997;13909-13914.
64. Forns X., Allander T., Rohwer-Nutter P., Bukh J. Characterization of modified hepatitis C virus E2 proteins expressed on the cell surface. Virology. 274:2000;75-85.
65. Davis H.L., Michel M.-L., Whalen R.G. DNA-based immunization induces continuous secretion of hepatitis B surface antigen and high levels of circulating antibody. Hum. Mol. Genet. 2:1993;1847-1851.
66. Lesniewski R., Okasinski G., Carrick R., Van Sant C., Desai S., Johnson R.et al. Antibody to hepatitis C virus second envelope (HCV-E2) glycoprotein: a new marker of HCV infection closely associated with viremia. J. Med. Virol. 45:1995;415-422.
67. Davis H.L., Schirmbeck R., Reimann J., Whalen R.G. DNA-mediated immunization in mice induces a potent MHC class I-restricted cytotoxic T lymphocyte response to the hepatitis B envelope protein. Hum. Gene. Ther. 6:1995;1447-1456.
68. Infante-Duarte C., Kamradt T. Th1/Th2 balance in infection. Springer. Semin. Immunopathol. 21:1999;317-338.
69. Snapper C.M., Paul W.E. Interferon-gamma and B cell stimulatory factor-1 reciprocally regulate Ig isotype production. Science. 236:1987;944-947.
70. Gurunathan S., Klinman D.M., Seder R.A. DNA vaccines: immunology, application and optimization. Annu. Rev. Immunol. 18:2000;927-974.
71. Boyle J.S., Koniaras C., Lew A.M. Influence of cellular location of expressed antigen on the efficacy of DNA vaccination: cytotoxic T lymphocyte and antibody responses are suboptimal when antigen is cytoplasmic after intramuscular DNA immunization. Int. Immunol. 9:1997;1897-1906.
72. Milich D.R., Schodel F., Hughes J.L., Jones J.E., Peterson D.L. The hepatitis B virus core and e antigens elicit different Th cell subsets: antigen structure can affect Th cell phenotype. J. Virol. 71:1997;2192-2201.
73. Lewis P.J., van Drunen Littel-van den H., Babiuk L.A. Altering the cellular location of an antigen expressed by a DNA-based vaccine modulates the immune response. J. Virol. 73:1999;10214-10223.
74. Prange R., Werr M. DNA-mediated immunization to hepatitis B virus envelope proteins: preS antigen secretion enhances the humoral response. Vaccine. 17:1999;617-623.
75. Svanholm C., Bandholtz L., Lobell A., Wigzell H. Enhancement of antibody responses by DNA immunization using expression vectors mediating efficient antigen secretion. J. Immunol. Methods. 228:1999;121-130.
76. Torres C.A., Yang K., Mustafa F., Robinson H.L. DNA immunization: effect of secretion of DNA-expressed hemagglutinins on antibody responses. Vaccine. 18:1999;805-814.
77. Forns X., Emerson S.U., Tobin G.J., Mushahwar I.K., Purcell R.H., Bukh J. DNA immunization of mice and macaques with plasmids encoding hepatitis C virus envelope E2 protein expressed intracellularly and on the cell surface. Vaccine. 17:1999;1992-2002.
78. Inchauspé G., Vitvitski L., Major M.E., Jung G., Spengler U., Maisonnas M.et al. Plasmid DNA expressing a secreted or a non-secreted form of hepatitis C virus nucleocapsid: comparative studies of antibody and T-helper responses following genetic immunization. DNA Cell Biol. 16:1997;185-195.
79. Mahon B.P., Katrak K., Nomoto A., Macadam A.J., Minor P.D., Mills K.H. Poliovirus-specific CD4+ Th1 clones with both cytotoxic and helper activity mediate protective humoral immunity against a lethal poliovirus infection in transgenic mice expressing the human poliovirus receptor. J. Exp. Med. 181:1995;1285-1292.
80. Michel M.L., Davis H.L., Schleef M., Mancini M., Tiollais P., Whalen R.G. DNA-mediated immunization to the hepatitis B surface antigen in mice: aspects of the humoral response mimic hepatitis B viral infection in humans. Proc. Natl. Acad. Sci. U.S.A. 92:1995;5307-5311.
81. Davis H.L., Brazolot Millan C.L., Watkins S.C. Immune-mediated destruction of transfected muscle fibers after direct gene transfer with antigen-expressing plasmid DNA. Gene Ther. 4:1997a;181-188.
82. Gordon E.J., Bhat R., Liu Q., Wang Y.F., Tackney C., Prince A.M. Immune responses to hepatitis C virus structural and non-structural proteins induced by plasmid DNA immunizations. J. Infect. Dis. 181:2000;42-50.