Elicitation of strong immune responses by a DNA vaccine expressing a secreted form of hepatitis C virus envelope protein E2 in murine and porcine animal models

World Journal of Gastroenterology

Volumn 12, Issue 44, 2006, Pages 7126-7135

  Li, Yi Ping ^a,b   Kang, Hye Na ^a,c   Babiuk, Lorne A ^a   Liu, Qiang ^a  

^a UNIVERSITY OF SASKATCHEWAN   (Canada)

^b TECHNICAL UNIVERSITY OF DENMARK   (Denmark)

^c Korea Food and Drug Administration   (South Korea)

Author keywords

DNA vaccine; DNA vaccine prime protein boost; Hepatitis C virus E2

Indexed keywords

DNA VACCINE; HEPATITIS C VACCINE; RECOMBINANT GLYCOPROTEIN E2; RECOMBINANT PROTEIN;

ANIMAL EXPERIMENT; ANTIBODY RESPONSE; ARTICLE; CONTROLLED STUDY; CYTOTOXIC T LYMPHOCYTE; ENZYME LINKED IMMUNOSORBENT ASSAY; ENZYME LINKED IMMUNOSPOT ASSAY; HEPATITIS C VIRUS; HUMORAL IMMUNITY; IMMUNOGENICITY; LYMPHOCYTE PROLIFERATION; MOUSE; NONHUMAN; PROTEIN SECRETION; SWINE; TH1 CELL; TH2 CELL; VIRAL GENE THERAPY;

EID: 33845440918     PISSN: 10079327     EISSN: None     Source Type: Journal    
DOI: 10.3748/wjg.v12.i44.7126     Document Type: Article

References (92)

1. Shepard CW, Finelli L, Alter MJ. Global epidemiology of hepatitis C virus infection. Lancet Infect Dis 2005; 5: 558-567
2. Choo QL, Kuo G, Weiner AJ, Overby LR, Bradley DW, Houghton M. Isolation of a cDNA done derived from a blood-borne non-A, non-B viral hepatitis genome. Science 1989; 244: 359-362
3. Hoofnagle JH. Course and outcome of hepatitis C. Hepatology 2002; 36: S21-S29
4. Feld JJ, Hoofnagle JH. Mechanism of action of interferon and ribavirin in treatment of hepatitis C. Nature 2005; 436: 967-972
5. Houghton M, Abrignani S. Prospects for a vaccine against the hepatitis C virus. Nature 2005; 436: 961-966
6. Lindenbach BD, Rice CM. Flaviviridae: The Viruses and Their Replication. In: Knipe DM, Howley PM, editors. Fields Virology. 4th ed. Philadelphia: Lippincott Williams & Wilkins, 2001: 991-1041
7. Major ME, Rehermann B, Feinstone SM. Hepatitis C Viruses. In: Knipe DM, Howley PM, editors. Fields Virology. 4th ed. Philadelphia: Lippincott Williams & Wilkins, 2001: 1127-1161
8. Penin F, Dubuisson J, Rey FA, Moradpour D, Pawlotsky JM. Structural biology of hepatitis C virus. Hepatology 2004, 39: 5-19
9. Petit MA, Lievre M, Peyrol S, De Sequeira S, Berthillon P, Ruigrok RW, Trepo C. Enveloped particles in the serum of chronic hepatitis C patients. Virology 2005; 336: 144-153
10. Schofield DJ, Bartosch B, Shimizu YK, Allander T, Alter HJ, Emerson SU, Cosset FL, Purcell RH. Human monoclonal antibodies that react with the E2 glycoprotein of hepatitis C virus and possess neutralizing activity. Hepatology 2005; 42: 1055-1062
11. Yuki N, Hayashi N, Kasahara A, Hagiwara H, Mita E, Ohkawa K, Katayama K, Fusamoto H, Kamada T. Quantitative analysis of antibody to hepatitis C virus envelope 2 glycoprotein in patients with chronic hepatitis C virus infection. Hepatology 1996; 23: 947-952
12. Netski DM, Mosbruger T, Depla E, Maertens G, Ray SC, Hamilton RG, Roundtree S, Thomas DL, McKeating J, Cox A. Humoral immune response in acute hepatitis C virus infection. Clin Infect Dis 2005; 41: 667-675
13. Chen M, Sallberg M, Sonnerborg A, Weiland O, Mattsson L, Jin L, Birkett A, Peterson D, Milich DR. Limited humoral immunity in hepatitis C virus infection. Gastroenterology 1999; 116: 135-143
14. Farci P, Alter HJ, Wong DC, Miller RH, Govindarajan S, Engle R, Shapiro M, Purcell RH. Prevention of hepatitis C virus infection in chimpanzees after antibody-mediated in vitro neutralization. Proc Natl Acad Sci USA 1994; 91: 7792-7796
15. Farci P, Shimoda A, Wong D, Cabezon T, De Gioannis D, Strazzera A, Shimizu Y, Shapiro M, Alter HJ, Purcell RH. 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 USA 1996; 93: 15394-15399
16. Shimizu YK, Igarashi H, Kiyohara T, Cabezon T, Farci P, Purcell RH, Yoshikura H. A hyperimmune serum against a synthetic peptide corresponding to the hypervariable region 1 of hepatitis C virus can prevent viral infection in cell cultures. Virology 1996, 223: 409-412
17. Ishii K, Rosa D, Watanabe Y, Katayama T, Harada H, Wyatt C, Kiyosawa K, Aizaki H, Matsuura Y, Houghton M, Abrignani S, Miyamura T. High titers of antibodies inhibiting the binding of envelope to human cells correlate with natural resolution of chronic hepatitis C. Hepatology 1998; 28: 1117-1120
18. Shoukry NH, Cawthon AG, Walker CM. Cell-mediated immunity and the outcome of hepatitis C virus infection. Annu Rev Microbiol 2004; 58: 391-424
19. Bowen DG, Walker CM. Adaptive immune responses in acute and chronic hepatitis C virus infection. Nature 2005; 436: 946-952
20. Neumann-Haefelin C, Blum HE, Chisari FV, Thimme R. T cell response in hepatitis C virus infection. J Clin Virol 2005; 32: 75-85
21. Koziel MJ. Cellular immune responses against hepatitis C virus. Clin Infect Dis 2005; 41 Suppl 1: S25-S31
22. Rehermann B, Nascimbeni M. Immunology of hepatitis B virus and hepatitis C virus infection. Nat Rev Immunol 2005; 5: 215-229
23. Ward S, Lauer G, Isba R, Walker B, Klenerman P. Cellular immune responses against hepatitis C virus: the evidence base 2002. Clin Exp Immunol 2002; 128: 195-203
24. Leroux-Roels G, Esquivel CA, DeLeys R, Stuyver L, Elewaut A, Philippe J, Desombere I, Paradijs J, Maertens G. Lymphoproliferative responses to hepatitis C virus core, E1, E2, and NS3 in patients with chronic hepatitis C infection treated with interferon alfa. Hepatology 1996; 23: 8-16
25. Sarobe P, Lasarte JJ, Garcia N, Civeira MP, Borras-Cuesta F, Prieto J. Characterization of T-cell responses against immunodominant epitopes from hepatitis C virus E2 and NS4a proteins. J Viral Hepat 2006; 13: 47-55
26. Gurunathan S, Klinman DM, Seder RA. DNA vaccines: immunology, application, and optimization. Annu Rev Immunol 2000; 18: 927-974
27. Berzofsky JA, Ahlers JD, Belyakov IM. Strategies for designing and optimizing new generation vaccines. Nat Rev Immunol 2001; 1: 209-219
28. Sharma AK, Khuller GK DNA vaccines: future strategies and relevance to intracellular pathogens. Immunol Cell Biol 2001; 79: 537-546
29. Lemieux P. Technological advances to increase immuno-genicity of DNA vaccines. Expert Rev Vaccines 2002; 1: 85-93
30. Doria-Rose NA, Haigwood NL. DNA vaccine strategies: candidates for immune modulation and immunization regimens. Methods 2003; 31: 207-216
31. Manoj S, Babiuk LA, van Drunen Littel-van den Hurk S. Approaches to enhance the efficacy of DNA vaccines. Crit Rev Clin Lab Sci 2004; 41: 1-39
32. Rath A, Choudhury S, Batra D, Kapre SV, Rupprecht CE, Gupta SK. DNA vaccine for rabies: relevance of the transmembrane domain of the glycoprotein in generating an antibody response. Virus Res 2005; 113: 143-152
33. Barnett SW, Rajasekar S, Legg H, Doe B, Fuller DH, Haynes JR, Walker CM, Steimer KS. Vaccination with HIV-1 gp120 DNA induces immune responses that are boosted by a recombinant gp120 protein subunit. Vaccine 1997; 15: 869-873
34. Letvin NL, Montefiori DC, Yasutomi Y, Perry HC, Davies ME, Lekutis C, Alroy M, Freed DC, Lord CI, Handt LK, Liu MA, Shiver JW. Potent, protective anti-HIV immune responses generated by bimodal HIV envelope DNA plus protein vaccination. Proc Natl Acad Sci USA 1997; 94: 9378-9383
35. Leung L, Srivastava IK, Kan E, Legg H, Sun Y, Greer C, Montefiori DC, zur Megede J, Barnett SW. Immunogenicity of HIV-1 Env and Gag in baboons using a DNA prime/protein boost regimen. AIDS 2004; 18: 991-1001
36. Song MK, Lee SW, Suh YS, Lee KJ, Sung YC. Enhancement of immunoglobulin G2a and cytotoxic T-lymphocyte responses by a booster immunization with recombinant hepatitis C virus E2 protein in E2 DNA-primed mice. J Virol 2000; 74: 2920-2925
37. Manabe S, Fuke I, Tanishita O, Kaji C, Gomi Y, Yoshida S, Mori C, Takamizawa A, Yosida I, Okayama H. Production of nonstructural proteins of hepatitis C virus requires a putative viral protease encoded by NS3. Virology 1994; 198: 636-644
38. van Drimen Littel-van den Hurk S, Braun RP, Karvonen BC, King T, Yoo D, Babiuk LA. Immune responses and protection induced by DNA vaccines encoding bovine parainfluenza virus type 3 glycoproteins. Virology 1999; 260: 35-46
39. Yu H, Babiuk LA, van Drunen Littel-van den Hurk S. Priming with CpG-enriched plasmid and boosting with protein formulated with CpG oligodeoxynucleotides and Quil A induces strong cellular and humoral immune responses to hepatitis C virus NS3. J Gen Virol 2004; 85: 1533-1543
40. Graham FL, van der Eb AJ. A new technique for the assay of infectivity of human adenovirus 5 DNA. Virology 1973; 52: 456-467
41. Ioannou XP, Gomis SM, Karvonen B, Hecker R, Babiuk LA, van Drunen Littel-van den Hurk S. CpG-containing oligodeoxynucleotides, in combination with conventional adjuvants, enhance the magnitude and change the bias of the immune responses to a herpesvirus glycoprotein. Vaccine 2002; 21: 127-137
42. Rankin R, Pontarollo R, Ioannou X, Krieg AM, Hecker R, Babiuk LA, van Drunen Littel-van den Hurk S. CpG motif identification for veterinary and laboratory species demonstrates that sequence recognition is highly conserved. Antisense Nucleic Acid Drug Dev 2001; 11: 333-340
43. Van Pel A, De Plaen E, Boon T. Selection of highly transfectable variant from mouse mastocytoma P815. Somat Cell Mol Genet 1985; 11: 467-475
44. Liu Q, Tikoo SK, Babiuk LA. Nuclear localization of the ORF2 protein encoded by porcine circovirus type 2. Virology 2001; 285: 91-99
45. Liu Q, Zaiss AK, Colarusso P, Patel K, Haljan G, Wickham TJ, Muruve DA. The role of capsid-endothelial interactions in the innate immune response to adenovirus vectors. Hum Gene Ther 2003; 14: 627-643
46. Abbas AK, Murphy KM, Sher A. Functional diversity of helper T lymphocytes. Nature 1996; 383: 787-793
47. Braun R, Babiuk LA, van Drunen Littel-van den Hurk. Compatibility of plasmids expressing different antigens in a single DNA vaccine formulation. J Gen Virol 1998; 79 (Pt 12): 2965-2970
48. Rothschild MF. Porcine genomics delivers new tools and results: this little piggy did more than just go to market. Genet Res 2004; 83: 1-6
49. Fournillier A, Nakano I, Vitvitski L, Depla E, Vidalin O, Maertens G, Trepo C, Inchauspe G. Modulation of immune responses to hepatitis C virus envelope E2 protein following injection of plasmid DNA using single or combined delivery routes. Hepatology 1998; 28: 237-244
50. Pancholi P, Liu Q, Tricoche N, Zhang P, Perkus ME, Prince AM. DNA prime-canarypox boost with polycistronic hepatitis C virus (HCV) genes generates potent immune responses to HCV structural and nonstructural proteins. J Infect Dis 2000; 182:18-27
51. Pancholi P, Perkus M, Tricoche N, Liu Q, Prince AM. DNA immunization with hepatitis C virus (HCV) polycistronic genes or immunization by HCV DNA priming-recombinant canarypox virus boosting induces immune responses and protection from recombinant HCV-vaccinia virus infection in HLA-A2.1-transgenic mice. J Virol 2003; 77: 382-390
52. Tedeschi. V, Akatsuka T, Shih JW, Battegay M, Feinstone SM. A specific antibody response to HCV E2 elicited in mice by intramuscular inoculation of plasmid DNA containing coding sequences for E2. Hepatology 1997; 25: 459-462
53. Ha SJ, Chang J, Song MK, Suh YS, Jin HT, Lee CH, Nam GH, Choi G, Choi KY, Lee SH, Kim WB, Sung YC. Engineering N-glycosylation mutations in IL-12 enhances sustained cytotoxic T lymphocyte responses for DNA immunization. Nat Biotechnol 2002; 20: 381-386
54. Ha SJ, Kim DJ, Baek KH, Yun YD, Sung YC. IL-23 induces stronger sustained CTL and Th1 immune responses than IL-12 in hepatitis C virus envelope protein 2 DNA immunization. J Immunol 2004; 172: 525-531
55. Puig M, Major ME, Mihalik K, Feinstone SM. Immunization of chimpanzees with an envelope protein-based vaccine enhances specific humoral and cellular immune responses that delay hepatitis C virus infection. Vaccine 2004; 22: 991-1000
56. Vidalin O, Fournillier A, Renard N, Chen M, Depla E, Boucreux D, Brinster C, Baumert T, Nakano I, Fukuda Y, Liljestrom P, Trepo C, Inchauspe G. Use of conventional or replicating nucleic acid-based vaccines and recombinant Semliki forest virus-derived particles for the induction of immune responses against hepatitis C virus core and E2 antigens. Virology 2000; 276: 259-270
57. Saito T, Sherman GJ, Kurokohchi K, Guo ZP, Donets M, Yu MY, Berzofsky JA, Akatsuka T, Feinstone SM. Plasmid DNA-based immunization for hepatitis C virus structural proteins: immune responses in mice. Gastroenterology 1997; 112: 1321-1330
58. Lee SW, Cho JH, Lee KJ, Sung YC. Hepatitis C virus envelope DNA-based immunization elicits humoral and cellular immune responses. Mol Cells 1998; 8: 444-451
59. Esumi M, Rikihisa T, Nishimura S, Goto J, Mizuno K, Zhou YH, Shikata T. Experimental vaccine activities of recombinant E1 and E2 glycoproteins and hypervariable region 1 peptides of hepatitis C virus in chimpanzees. Arch Virol 1999; 144: 973-980
60. Abraham JD, Himoudi N, Kien F, Berland JL, Codran A, Bartosch, B, Baumert T, Paranhos-Baccala G, Schuster C, Inchauspe G, Kieny MP. Comparative immunogenicity analysis of modified vaccinia Ankara vectors expressing native or modified forms of hepatitis C virus E1 and E2 glycoproteins. Vaccine 2004; 22: 3917-3928
61. Forns X Payette PJ, Ma X, Satterfield W, Eder G, Mushahwar IK, Govindarajan S, Davis HL, Emerson SU, Purcell RH, Bukh J. Vaccination of chimpanzees with plasmid DNA encoding the hepatitis C virus (HCV) envelope E2 protein modified the infection after challenge with homologous monoclonal HCV. Hepatology 2000; 32: 618-625
62. Youn JW, Park SH, Lavillette D, Cosset FL, Yang SH, Lee CG, Jin HT, Kim CK Shata MT, Lee DH, Pfahler W, Prince AM, Sung YC. Sustained E2 antibody response correlates with reduced peak viremia after hepatitis C virus infection in the chimpanzee. Hepatology 2005; 42: 1429-1436
63. Forns X, Emerson SU, Tobin GJ, Mushahwar IK, Purcell RH, 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 1999, 17: 1992-2002
64. Rollier C, Depla E, Drexhage JA, Verschoor EJ, Verstrepen BE, Fatmi A, Brinster C, Fournillier A, Whelan JA, Whelan M, Jacobs D, Maertens G, Inchauspe G, Heeney JL. Control of heterologous hepatitis C virus infection in chimpanzees is associated with the quality of vaccine-induced peripheral T-helper immune response. J Virol 2004; 78: 187-196
65. Inchauspe G, Major ME, Nakano I, Vitvitski L, Trepo C. DNA vaccination for the induction of immune responses against hepatitis C virus proteins. Vaccine 1997; 15: 853-856
66. Zhu LX, Liu J, Ye Y, Xie YH, Kong YY, Li GD, Wang Y. A candidate DNA vaccine elicits HCV specific humoral and cellular immune responses. World J Gastroenterol 2004; 10: 2488-2492
67. Ma X, Forns X, Gutierrez R, Mushahwar IK, Wu T, Payette PJ, Bukh J, Purcell RH, Davis HL. 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 2002; 20: 3263-3271
68. Zucchelli S, Capone S, Fattori E, Folgori A, Di Marco A, Casimiro D, Simon AJ, Laufer R, La Monica N, Cortese R, Nicosia A. Enhancing B- and T-cell immune response to a hepatitis C virus E2 DNA vaccine by intramuscular electrical gene transfer. J Virol 2000; 74: 11598-11607
69. Youn JW, Park SH, Cho JH, Sung YC. Optimal induction of T-cell responses against hepatitis C virus E2 by antigen engineering in DNA immunization. J Virol 2003; 77: 11596-11602
70. Park SH, Yang SH, Lee CG, Youn JW, Chang J, Sung YC. Efficient induction of T helper 1 CD4+ T-cell responses to hepatitis C virus core and E2 by a DNA prime-adenovirus boost. Vaccine 2003; 21: 4555-4564
71. Jin J, Yang JY, Liu J, Kong YY, Wang Y, Li GD. DNA immunization with fusion genes encoding different regions of hepatitis C virus E2 fused to the gene for hepatitis B surface antigen elicits immune responses to both HCV and HBV. World J Gastroenterol 2002; 8: 505-510
72. Heile JM, Fong YL, Rosa D, Berger K, Saletti G, Campagnoli S, Bensi G, Capo S, Coates S, Crawford K, Dong C, Wininger M, Baker G, Cousens L, Chien D, Ng P, Archangel P, Grandi G, Houghton M, Abrignani S. Evaluation of hepatitis C virus glycoprotein E2 for vaccine design: an endoplasmic reticulum-retained recombinant protein is superior to secreted recombinant protein and DNA-based vaccine candidates. J Virol 2000; 74: 6885-6892
73. Lee AY, Polakos NK, Otten GR, Ulmer JB, Houghton M, Paliard X. Quantification of the number of cytotoxic T cells specific for an immunodominant HCV-specific CTL epitope primed by DNA immunization. Vaccine 2000; 18: 1962-1968
74. Choo QL, Kuo G, Ralston R, Weiner A, Chien D, Van Nest G, Han J, Berger K, Thudium K, Kuo C. Vaccination of chimpanzees against infection by the hepatitis C virus. Proc Natl Acad Sci USA 1994; 91: 1294-1298
75. Dubuisson J, Hsu HH, Cheung RC, Greenberg HB, Russell DG, Rice CM. Formation and intracellular localization of hepatitis C virus envelope glycoprotein complexes expressed by recombinant vaccinia and Sindbis viruses. J Virol 1994; 68: 6147-6160
76. Dubuisson J. Folding, assembly and subcellular localization of hepatitis C virus glycoproteins. Curr Top Microbiol Immunol 2000; 242: 135-148
77. Goffard A, Dubuisson J. Glycosylation of hepatitis C virus envelope proteins. Biochimie 2003; 85: 295-301
78. Inudoh M, Nyunoya H, Tanaka T, Hijikata M, Kato N, Shimotohno K. Antigenicity of hepatitis C virus envelope proteins expressed in Chinese hamster ovary cells. Vaccine 1996; 14: 1590-1596
79. Sato K, Okamoto H, Aihara S, Hoshi Y, Tanaka T, Mishiro S. Demonstration of sugar moiety on the surface of hepatitis C virions recovered from the circulation of infected humans. Virology 1993; 196: 354-357
80. Cocquerel L, Meunier JC, Pillez A, Wychowski C, Dubuisson J. A retention signal necessary and sufficient for endoplasmic reticulum localization maps to the transmembrane domain of hepatitis C virus glycoprotein E2. J Virol 1998; 72: 2183-2191
81. Cocquerel L, Op de Beeck A, Lambot M, Roussel J, Delgrange D, Pillez A, Wychowski C, Penin F, Dubuisson J. Topological changes in the transmembrane domains of hepatitis C virus envelope glycoproteins. EMBO J 2002; 21: 2893-2902
82. Spaete RR, Alexander D, Rugroden ME, Choo QL, Berger K, Crawford K, Kuo C, Leng S, Lee C, Ralston R. Characterization of the hepatitis C virus E2/NS1 gene product expressed in mammalin cells. Virology 1992; 188: 819-830
83. Michalak JP, Wychowski C, Choukhi A, Meunier JC, Ung S, Rice CM, Dubuisson J. Characterization of truncated forms of hepatitis C virus glycoproteins. J Gen Virol 1997; 78 (Pt 9): 2299-2306
84. Simmonds P. Genetic diversity and evolution of hepatitis C virus-15 years on. J Gen Virol 2004; 85: 3173-3188
85. Kato N, Sekiya H, Ootsuyama Y, Nakazawa T, Hijikata M, Ohkoshi S, Shimotohno K. Humoral immune response to hypervariable region 1 of the putative envelope glycoprotein (gp70) of hepatitis C virus. J Virol 1993; 67:3923-3930
86. Weiner AJ, Brauer MJ, Rosenblatt J, Richman KH, Tung J, Crawford K, Bonino F, Saracco G, Choo QL, Houghton M. Variable and hypervariable domains are found in the regions of HCV corresponding to the flavivirus envelope and NS1 proteins and the pestivirus envelope glycoproteins. Virology 1991; 180: 842-848
87. Scotta C, Tuosto L, Masci AM, Racioppi L, Piccolella E, Frasca L. Hypervariable region 1 variant acting as TCR antagonist affects hepatitis C virus-specific CD4+ T cell repertoire by favoring CD95-mediated apoptosis. J Leukoc Biol 2005; 78: 372-382
88. Pennica D, Holmes WE, Kohr WJ, Harkins RN, Vehar GA, Ward CA, Bennett WF, Yelverton E, Seeburg PH, Heyneker HL, Goeddel DV, Collen D. Cloning and expression of human tissue-type plasminogen activator cDNA in E. coli. Nature 1983; 301: 214-221
89. Brazolot Millan CL, Weeratna R, Krieg AM, Siegrist CA, Davis HL. CpG DNA can induce strong Th1 humoral and cell-mediated immune responses against hepatitis B surface antigen in young mice. Proc Natl Acad Sci USA 1998; 95: 15553-15558
90. Weeratna RD, Brazolot Millan CL, McCluskie MJ, Davis HL. CpG ODN can re-direct the Th bias of established Th2 immune responses in adult and young mice. FEMS Immunol Med Microbiol 2001; 32: 65-71
91. Davis HL, Weeratna R, Waldschmidt TJ, Tygrett L, Schorr J, Krieg AM. CpG DNA is a potent enhancer of specific immunity in mice immunized with recombinant hepatitis B surface antigen. J Immunol 1998; 160: 870-876
92. Donnelly JJ, Wahren B, Liu MA. DNA vaccines: progress and challenges. J Immunol 2005; 175: 633-639