Long-term persistence of hepatitis B surface antigen and antibody induced by DNA-mediated immunization results in liver and kidney lesions in mice

European Journal of Immunology

Volumn 36, Issue 4, 2006, Pages 875-886

  Zi, Xiao Yuan ^a   Yao, Yu Cheng ^a   Zhu, Hai Ying ^a   Xiong, Jun ^a   Wu, Xiu Ju ^a   Zhang, Nan ^a   Ba, Yue ^a,b   Li, Wen Li ^a   Wang, Xin Ming ^a   Li, Jian Xiu ^a   Yu, Hong Yu ^a   Ye, Xu Ting ^a   Lau, Joseph T Y ^c   Hu, Yi Ping ^a  

^a SECOND MILITARY MEDICAL UNIVERSITY   (China)

^b ZHENGZHOU UNIVERSITY   (China)

^c ROSWELL PARK CANCER INSTITUTE   (United States)

Author keywords

DNA vaccination; Hepatitis B virus; Transgenic mice

Indexed keywords

HEPATITIS B ANTIBODY; HEPATITIS B SURFACE ANTIGEN; PLASMID DNA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DNA REPLICATION; DRUG FORMULATION; DRUG SAFETY; IMMUNE COMPLEX DEPOSITION; IMMUNIZATION; IMMUNOSTIMULATION; KIDNEY DISEASE; LIVER DISEASE; MAMMAL; MOUSE STRAIN; NONHUMAN; PERSISTENT VIRUS INFECTION; PLASMID; PRIORITY JOURNAL; TRANSGENIC MOUSE;

ANIMALS; ANTIBODIES, VIRAL; ANTIGEN-ANTIBODY COMPLEX; ANTIGENS, VIRAL; BLOTTING, WESTERN; HEPATITIS B; HEPATITIS B SURFACE ANTIGENS; IMMUNOHISTOCHEMISTRY; KIDNEY DISEASES; LIVER DISEASES; MICE; MICE, INBRED BALB C; MICE, TRANSGENIC; MICROSCOPY, ELECTRON, TRANSMISSION; PLASMIDS; POLYMERASE CHAIN REACTION; TIME FACTORS; VACCINES, DNA;

EID: 33645910865     PISSN: 00142980     EISSN: None     Source Type: Journal    
DOI: 10.1002/eji.200535468     Document Type: Article

References (61)

1. Arbuthnot, P. and Kew, M., Hepatitis B virus and hepatocellular carcinoma. Int. J. Exp. Pathol. 2001. 82: 77-100.
2. Ganem, D. and Prince, A. M., Hepatitis B virus infection-natural history and clinical consequences. N. Engl. J. Med. 2004. 350: 1118-1129.
3. Lai, C. L., Ratziu, V., Yuen, M. F. and Poynard, T., Viral hepatitis B. Lancet 2003. 362: 2089-2094.
4. Shouval, D., Hepatitis B vaccines. J. Hepatol. 2003. 39 (Suppl 1): S70-S76.
5. Tang, D. C., DeVit, M. and Johnston, S. A., Genetic immunization is a simple method for eliciting an immune response. Nature 1992. 356: 152-154.
6. Maloy, K. J., Erdmann, I., Basch, V., Sierro, S., Kramps, T. A., Zinkernagel, R. M., Oehen, S. and Kundig, T. M., Intralymphatic immunization enhances DNA vaccination. Proc. Natl. Acad. Sci. USA 2001. 13: 3299-3303.
7. Estcourt, M. J., McMichael, A. J. and Hanke T., DNA vaccines against human immunodeficiency virus type 1. Immunol. Rev. 2004. 199: 144-155.
8. Autran, B., Carcelain, G., Combadiere, B. and Debre, P., Therapeutic vaccines for chronic infections. Science 2004. 305: 205-208.
9. Beckebaum, S., Cicinnati, V. R. and Gerken, G., DNA-based immunotherapy: potential for treatment of chronic viral hepatitis? Rev. Med. Virol. 2002. 12: 297-319.
10. Yang, Z. Y., Kong, W. P., Huang, Y., Roberts, A., Murphy, B. R., Subbarao, K. and Nabel, G. J., A DNA vaccine induces SARS coronavirus neutralization and protective immunity in mice. Nature 2004. 428: 561-564.
11. Whalen, R. G. and Davis, H. L., DNA-mediated immunization and the energetic immune response to hepatitis B surface antigen. Clin. Immunol. Immunopathol. 1995. 75: 1-12.
12. Michel, M. L. and Loirat, D.DNA vaccines for prophylactic or therapeutic immunization against hepatitis B. Intervirology 2001. 44: 78-87.
13. Davis, H. L., Mancini, M., Michel, M. L. and Whalen, R. G., DNA-mediated immunization to hepatitis B surface antigen: longevity of primary response and effect of boost. Vaccine 1996. 14: 910-915.
14. Michel, M. L., Davis, H. L., Schleef, M., Mancini, M., Tiollais, P. and 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. USA 1995. 92: 5307-5311.
15. Davis, H. L., Michel, M. L. and Whalen, R. G., DNA-based immunization induces continuous secretion of hepatitis B surface antigen and high levels of circulating antibody. Hum. Mol. Genet. 1993. 2: 1847-1851.
16. Davis, H. L., Michel, M. L., Mancini, M., Schleef, M. and Whalen, R. G., Direct gene transfer in skeletal muscle: plasmid DNA-based immunization against the hepatitis B virus surface antigen. Vaccine 1994. 12: 1503-1509.
17. Pisetsky, D. S., Immunostimulatory DNA: a clear and present danger? Nat. Med. 1997. 3: 829-831.
18. Davis, H. L., Demeneix, B. A., Quantin, B., Coulombe, J. and Whalen, R. G., Plasmid DNA is superior to viral vectors for direct gene transfer into adult mouse skeletal muscle. Hum. Gene Ther. 1993. 4: 733-740.
19. Lee, W. M., Hepatitis B virus infection. N. Engl. J. Med. 1997. 337: 1733-1745.
20. Tsai, J. F., Margolis, H. S., Jeng, J. E., Ho, M. S., Chang, W. Y., Hsieh, M. Y., Lin, Z. Y. and Tsai, J. H., Immunoglobulin- and hepatitis B surface antigen-specific circulating immune complexes in chronic hepatitis B virus infection. Clin. Immunol. Immunopathol. 1998. 86: 246-251.
21. Bhimma, R. and Coovadia, H. M., Hepatitis B virus-associated nephropathy. Am. J. Nephrol. 2004. 24: 198-211.
22. Hu, Y. P., Hu, W. J., Zheng, W. C., Li, J. X., Dai, D. S., Wang, X. M., Zhang, S. Z. et al., Establishment of transgenic mouse harboring hepatitis B virus (adr subtype) genomes. World J. Gastroenterol. 2001. 7: 111-114.
23. Kowalczyk, D. W. and Ertl, H. C., Immune responses to DNA vaccines. Cell Mol. Life Sci. 1999. 55: 751-770.
24. Wolff, J. A., Ludtke, J. J., Acsadi, G., Williams, P. and Jani, A., Long-term persistence of plasmid DNA and foreign gene expression in mouse muscle. Hum. Mol. Genet. 1992. 1: 363-369.
25. Kessler, P. D., Podsakoff, G. M., Chen, X., McQuiston, S. A., Colosi, P. C., Matelis, L. A., Kurtzman, G. J. and Byrne, B. J., Gene delivery to skeletal muscle results in sustained expression and systemic delivery of a therapeutic protein. Proc. Natl. Acad. Sci. USA 1996. 93: 14082-14087.
26. Mir, L. M., Bureau, M. F., Gehl, J., Rangara, R., Rouy, D., Caillaud, J. M., Delaere, P. et al., High-efficiency gene transfer into skeletal muscle mediated by electric pulses. Proc. Natl. Acad. Sci. USA 1999. 96: 4262-4267.
27. Herzog, R. W., Hagstrom, J. N., Kung, S. H., Tai, S. J., Wilson, J. M., Fisher, K. J. and High, K. A., Stable gene transfer and expression of human blood coagulation factor IX after intramuscular injection of recombinant adeno-associated virus. Proc. Natl. Acad. Sci. USA 1997. 94: 5804-5809.
28. Arruda, V. R., Schuettrumpf, J., Herzog, R. W., Nichols, T. C., Robinson, N., Lotfi, Y., Mingozzi, F. et al., Safety and efficacy of factor IX gene transfer to skeletal muscle in murine and canine hemophilia B models by adeno-associated viral vector serotype 1. Blood 2004. 103: 85-92.
29. Bettan, M., Emmanuel, F., Darteil, R., Caillaud, J. M., Soubrier, F., Delaere, P., Branelec, D. et al., High-level protein secretion into blood circulation after electric pulse-mediated gene, transfer into skeletal muscle. Mol. Ther. 2000. 2: 204-210.
30. Wolff, J. A., Malone, R. W., Williams, P., Chong, W., Acsadi, G., Jani, A. and Felgner, P. L., Direct gene transfer into mouse muscle in vivo. Science 1990. 247: 1465-1468.
31. Doh, S. G., Vahlsing, H. L., Hartikka, J., Liang, X. and Manthorpe, M, Spatial-temporal patterns of gene expression in mouse skeletal muscle after injection of lacZ plasmid DNA. Gene Ther. 1997. 4: 648-663.
32. Davis, H. L., Millan, C. L. and Watkins, S. C., Immune-mediated destruction of transfected muscle fibers after direct gene transfer with antigen-expressing plasmid DNA. Gene Ther. 1997. 4: 181-188.
33. Wang, L., Dobrzynski, E., Schlachterman, A., Cao, O. and Herzog, R. W., Systemic protein delivery by muscle-gene transfer is limited by a local immune response. Blood 2005. 105: 4226-4234.
34. Manthorpe, M., Cornefert-Jensen, F., Hartikka, J., Felgner, J., Rundell, A., Margalith, M. and Dwarki, V., Gene therapy by intramuscular injection of plasmid DNA: Studies on firefly luciferase gene expression in mice. Hum. Gene. Ther. 1993. 4: 419-431.
35. Goebels, N., Michaelis, D., Wekerle, H. and Hohlfeld, R., Human myoblasts as antigen-presenting cells. J. Immunol. 1992. 149: 661-667.
36. Wu, Y. Z., Zhao, J. P., Wan, Y., Jia, Z. C., Zhou, W., Bian, J., Ni, B. et al., Mimovirus: a novel form of vaccine that induces hepatitis B virus-specific cytotoxic T-lymphocyte responses in vivo. J. Virol. 2002. 76: 10264-10269.
37. Bocher, W. O., Dekel, B., Schwerin, W., Geissler, M., Hoffmann, S., Rohwer, A., Arditti, F. et al., Induction of strong hepatitis B virus (HBV) specific T helper cell and cytotoxic T lymphocyte responses by therapeutic vaccination in the trimera mouse model of chronic HBV infection. Eur. J. Immunol. 2001. 31: 2071-2079.
38. + T cells, T helper cells, and protective levels of antibody in humans by particle-mediated administration of a hepatitis B virus DNA vaccine. Vaccine 2000. 19: 764-778.
39. Rottinghaus, S. T., Poland, G. A., Jacobson, R. M., Barr, L. J. and Roy, M. J., Hepatitis B DNA vaccine induces protective antibody responses in human non-responders to conventional vaccination. Vaccine 2003. 21: 4604-4608.
40. Mwau, M., Cebere, I., Sutton, J., Chikoti, P., Winstone, N., Wee, EG., Beattie, T. et al., A human immunodeficiency virus 1 (HIV-1) clade A vaccine in clinical trials: stimulation of HIV-specific T-cell responses by DNA and recombinant modified vaccinia virus Ankara (MVA) vaccines in humans. J. Gen. Virol. 2004. 85: 911-919.
41. Wang, R., Doolan, DL., Le, T. P., Hedstrom, R. C., Coonan, K. M., Charoenvit, Y., Jones, T. R. et al., Induction of antigen-specific cytotoxic T lymphocytes in humans by a malaria DNA vaccine. Science 1998. 282: 476-480.
42. Huygen, K., Plasmid DNA vaccination. Microbes Infect 2005. 7: 932-938.
43. Timmerman, J. M., Singh, G., Hermanson, G., Hobart, P., Czerwinski, DK., Taidi, B., Rajapaksa, R. et al., Immunogenicity of a plasmid DNA vaccine encoding chimeric idiotype in patients with B-cell lymphoma. Cancer Res. 2002. 62: 5845-5852.
44. Chisari, F. V., Rous-Whipple Award Lecture: viruses, immunity, and cancer: lessons from hepatitis B. Am. J. Pathol. 2000. 156: 1117-1132.
45. Chattopodhyay, D. and Sen, M. R., Circulating immune complex in murine autoimmune hepatitis. Indian J. Exp. Biol. 1999. 37: 308-310.
46. Kim, S. A., Lee, S. I., Choi, I. H., Shin, J. S., Uhm, J. R., Kim, S. J. and Choi, H. J., Circulating immune complexes and cell-mediated immunity in patients with hepatitis B virus associated liver diseases. Yonsei Med. J. 1990. 31: 347-358.
47. Madalinski, K., Burczynska, B., Heermann, K. H., Uy, A. and Gerlich, W. H., Analysis of viral proteins in circulating immune complexes from chronic carriers of hepatitis B virus. Clin. Exp. Immunol. 1991. 84: 493-500.
48. di Belgiojoso, G. B., Ferrario, F. and Landriani, N., Virus-related glomerular diseases: histological and clinical aspects. J. Nephrol. 2002. 15: 469-479.
49. Gonzalo, A., Mampaso, F., Barcena, R., Gallego, N. and Ortuno, J., Membranous nephropathy associated with hepatitis B virus infection: long-term clinical and histological outcome. Nephrol. Dial. Transplant. 1999. 14: 416-418.
50. Oka, Y., Akber, S. M., Horiike, N., Joko, K. and Onji, M., Mechanism and therapeutic potential of DNA-based immunization against the envelope proteins of hepatitis B virus in normal and transgenic mice. Immunology 2001. 103: 90-97.
51. Wells, D. J., Improved gene transfer by direct plasmid injection associated with regeneration in mouse skeletal muscle. FEBS Lett. 1993. 332: 179-182.
52. Danko, I., Fritz, J. D., Jiao, S., Hogan, K., Latendresse, J. S. and Wolff, J. A., Pharmacological enhancement of in vivo foreign gene expression in muscle. Gene Ther. 1994. 1: 114-121.
53. Vitadello, M., Schiaffino, M. V., Picard, A., Scarpa, M. and Schiaffino, S., Gene transfer in regenerating muscle. Hum. Gene Ther. 1994. 5: 11-18.
54. Hanke, T. and McMichael, A. J., Design and construction of an experimental HIV-1 vaccine for a year-2000 clinical trial in Kenya. Nat. Med. 2000. 6: 951-955.
55. Tacket, C. O., Roy, M. J., Widera, G., Swain, W. F., Broome, S. and 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 1999. 17: 2826-2829.
56. Hanke, T., McMichael, A. J., Samuel, R. V., Powell, L. A., McLoughlin, L., Crome, S. J. and Edlin, A., Lack of toxicity and persistence in the mouse associated with administration of candidate DNA- and modified vaccinia virus Ankara (MVA)-based HIV vaccines for Kenya. Vaccine 2002. 21: 108-114.
57. Tuomela, M., Malm, M., Wallen, M., Stanescu, I., Krohn, K. and Peterson P., Biodistribution and general safety of a naked DNA plasmid, GTU®-MultiHIV, in a rat, using a quantitative PCR method. Vaccine 2005. 23: 890-896.
58. Parker, S. E., Borellini, F., Wenk, M. L., Hobart, P., Hoffman, S. L., Hedstrom, R., Le, T. and Norman, J.A., Plasmid DNA malaria vaccine: tissue distribution and safety studies in mice and rabbits. Hum. Gene Ther. 1999. 10: 741-758.
59. Epstein, J. E., Charoenvit, Y., Kester, K. E., Wang, R., Newcomer, R., Fitzpatrick, S., Richie, T. L. et al., Safety, tolerability, and antibody responses in humans after sequential immunization with a PfCSP DNA vaccine followed by the recombinant protein vaccine RTS,S/AS02A. Vaccine 2004. 22: 1592-603.
60. Gan, R. B., Chu, M. J., Shen, L. P., Qian, S. W. and Li, Z. P., The complete nucleotide sequence of the cloned DNA of hepatitis B virus subtype adr in pADR-1. Sci. Sin. [B] 1987. 30: 507-521.
61. Xiong, J., Yao, Y. C., Zi, X. Y., Li, J. X., Wang, X. M., Ye, X. T., Zhao, S. M. et al., Expression of hepatitis B virus X protein in transgenic mice. World J. Gastroenterol. 2003. 9: 112-116.