Mycobacterial codon optimization enhances antigen expression and virus-specific immune responses in recombinant Mycobacterium bovis bacille Calmette-Guérin expressing human immunodeficiency virus type 1 Gag

Journal of Virology

Volumn 79, Issue 14, 2005, Pages 8716-8723

  Kanekiyo, Masaru ^a,b   Matsuo, Kazuhiro ^a   Hamatake, Makiko ^a   Hamano, Takaichi ^a   Ohsu, Takeaki ^a   Matsumoto, Sohkichi ^c   Yamada, Takeshi ^d   Yamazaki, Shudo ^a   Hasegawa, Atsuhiko ^b   Yamamoto, Naoki ^a   Honda, Mitsuo ^a  

^a NATIONAL INSTITUTE OF INFECTIOUS DISEASES   (Japan)

^b NIHON UNIVERSITY   (Japan)

^c OSAKA CITY UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^d NAGASAKI UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BCG VACCINE; CD8 ANTIGEN; DNA FRAGMENT; GAG PROTEIN; GAMMA INTERFERON; HUMAN IMMUNODEFICIENCY VIRUS ANTIGEN; IMMUNOGLOBULIN G ANTIBODY; KANAMYCIN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MONOCLONAL ANTIBODY; PENICILLIN DERIVATIVE; RECOMBINANT BCG VACCINE; RECOMBINANT PROTEIN; RECOMBINANT VACCINE; STREPTOMYCIN; UNCLASSIFIED DRUG; VIRUS PROTEIN;

AMINO ACID SEQUENCE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY RESPONSE; ANTIBODY TITER; ANTIGEN EXPRESSION; ARTICLE; BCG VACCINATION; CODON USAGE; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNE RESPONSE; IMMUNIZATION; LOW DRUG DOSE; LYMPHOCYTE PROLIFERATION; MAJOR HISTOCOMPATIBILITY COMPLEX RESTRICTION; MOUSE; MYCOBACTERIUM BOVIS; NONHUMAN; NUCLEOTIDE SEQUENCE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; SPLEEN CELL;

AIDS VACCINES; AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; CD4-POSITIVE T-LYMPHOCYTES; CODON; FEMALE; HIV CORE PROTEIN P24; INTERFERON TYPE II; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED BALB C; MOLECULAR SEQUENCE DATA; MYCOBACTERIUM BOVIS; VACCINES, SYNTHETIC;

ANIMALIA; HIV TYPE 1; HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS 1; MYCOBACTERIUM BOVIS;

EID: 21644444748     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.79.14.8716-8723.2005     Document Type: Article

References (43)

1. Aldovini, A., and R. A. Young. 1991. Humoral and cell-mediated immune responses to live recombinant BCG-HIV vaccines. Nature 351:479-482.
2. Andersson, S. G. E., and P. M. Sharp. 1996. Codon usage in the Mycobacterium tuberculosis complex. Microbiology 142:915-925.
3. Andre, S., B. Seed, J. Eberle, W. Schraut, A. Bultmann, and J. Haas. 1998. Increased immune response elicited by DNA vaccination with a synthetic gp120 sequence with optimized codon usage. J. Virol. 72:1497-1503.
4. Barouch, D. H., S. Santra, M. J. Kuroda, J. E. Schmitz, R. Plishka, A. Buckler-White, A. E. Gaitan, R. Zin, J. H. Nam, L. S. Wyatt, M. A. Lifton, C. E. Nickerson, B. Moss, D. C. Montefiori, V. M. Hirsch, and N. L. Letvin. 2001. Reduction of simian-human immunodeficiency virus 89.6P viremia in rhesus monkeys by recombinant modified vaccinia virus Ankara vaccination. J. Virol. 75:5151-5158.
5. Benson, J., C. Chougnet, M. Robert-Guroff, D. Montefiori, P. Markham, G. Shearer, R. C. Gallo, M. Cranage, E. Paoletti, K. Limbach, D. Venzon, J. Tartaglia, and G. Franchini. 1998, Recombinant vaccine-induced protection against the highly pathogenic simian immunodeficiency virus SIV(mac251): dependence on route of challenge exposure. J. Virol. 72:4170-4182.
6. Cheynier, R., S. Gratton, M. Halloran, I. Stahmer, N. L. Letvin, and S. Wain-Hobson. 1998. Antigenic stimulation by BCG vaccine as an in vivo driving force for SIV replication and dissemination. Nat. Med. 4:421-427.
7. Fennelly, G. J., W. R. Jacobs, Jr., and B. R. Broom. 1997. BCG as a recombinant vaccine vector, p. 363-377. In M. M. Levine, G. C. Woodrow, J. B. Kaper, and G. S. Cobon (ed.), New generation vaccines, 2nd ed. Marcel Dekker, Inc., New York, N.Y.
8. Girard, M., B. Meignier, F. Barre-Sinoussi, M. P. Kieny, T. Matthews, E. Muchmore, P. L. Nara, Q. Wei, L. Rimsky, and K. Weinhold. 1995. Vaccine-induced protection of chimpanzees against infection by a heterologous human immunodeficiency virus type 1. J. Virol. 69:6239-6248.
9. Hesseling, A, C., H. S. Schaaf, W. A. Haneko, N. Beyers, M. F. Cotton, R. P. Gie, B. J. Marais, P. van Helden, and R. M. Warren. 2003. Danish bacille Calmette-Guérin vaccine-induced disease in human immunodeficiency virus-infected children. Clin. Infect. Dis. 37:1226-1233.
10. Hiroi, T., H. Goto, K. Someya, M. Yanagita, M. Honda, N. Yamanaka, and H, Kiyono. 2001. HIV mucosal vaccine: nasal immunization with rBCG-V3J1 induces a long term V3J1 peptide-specific neutralizing immunity in Th1- and Th2-deficient conditions. J. Immunol. 167:5862-5867.
11. Honda, M., K. Matsuo, T. Nakasone, Y. Okamoto, H. Yoshizaki, K. Kitamura, W. Sugiura, K. Watanabe, Y. Fukushima, S. Haga, H. Tasaka, T. Yamada, A. Yamazaki, and S. Yamazaki. 1995. Protective immune responses induced by secretion of a chimeric soluble protein from a recombinant Mycobacterium bovis bacillus Calmette-Guérin vector candidate vaccine for human immunodeficiency virus type 1 in small animals. Proc. Natl. Acad. Sci. USA 92:10693-10697.
12. Ikemura, T. 1985. Codon usage and tRNA content in unicellular and multicellular organisms. Mol. Biol. Evol. 2:13-34.
13. Jacobs, W. R., Jr., M. Tuckman, and B. R. Bloom. 1987. Introduction of foreign DNA into mycobacteria using a shuttle plasmid. Nature 327:532-535.
14. Kawahara, M., A. Hashimoto, I. Toida, and M. Honda. 2002. Oral recombinant Mycobacterium bovis bacillus Calmette-Guerin expressing HIV-1 antigens as a freeze-dried vaccine induces long-term, HIV-specific mucosal and systemic immunity. Clin. Immunol. 105:326-331.
15. Kawahara, M., K. Matsuo, T. Nakasone, T. Hiroi, H. Kiyono, S. Matsumoto, T. Yamada, N. Yamamoto, and M. Honda. 2002. Combined intrarectal/intradermal inoculation of recombinant Mycobacterium bovis bacillus Calmette-Guérin (BCG) induces enhanced immune responses against the inserted HIV-1 V3 antigen. Vaccine 21:158-166.
16. Kent, S. J., A. Zhao, S. J. Best, J. D. Chandler, D. B. Boyle, and I. A. Ramshaw. 1998. Enhanced T-cell immunogenicity and protective efficacy of a human immunodeficiency virus type 1 vaccine regimen consisting of consecutive priming with DNA and boosting with recombinant fowlpox virus. J. Virol. 72:10180-10188.
17. Langermann, S., S. R. Paraszynski, J. E. Burlein, S. Koenig, M. S. Hanson, D. E. Briles, and C. K. Stover. 1994. Protective humoral response against pneumococcal infection in mice elicited by recombinant bacille Calmette-Guérin vaccines expressing pneumococcal surface protein A. J. Exp. Med. 180:2277-2286.
18. Leder, C., J. A. Kleinschmidt, C. Wiethe, and M. Muller. 2001. Enhancement of capsid gene expression: preparing the human papillomavirus type 16 major structural gene L1 for DNA vaccination purposes. J. Virol. 75:9201-9209.
19. Matsumoto, S., M. Tamaki, H. Yukitake, T. Matsuo, M. Naito, H. Teraoka, and T. Yamada. 1996. A stable Escherichia coli-mycobacteria shuttle vector pSO246′ in Mycobacterium bovis BCG. FEMS Microbiol. Lett. 135:237-243.
20. Matsuo, K., Y. Nishino, T. Kimura, R. Yamaguchi, A. Yamazaki, T. Mikami, and K. Ikuta. 1992. Highly conserved epitope domain in major core protein p24 is structurally similar among human, simian and feline immunodeficiency viruses. J. Gen. Virol. 73:2445-2450.
21. McMichael, A., M. Mwau, and T. Hanke. 2002. Design and tests of an HIV vaccine. Br. Med. Bull. 62:87-92.
22. Méderlé, I., I. Bourguin, D. Ensergueix, E. Badell, J. Moniz-Peireira, B. Gicquel, and N. Winter. 2002. Plasmidic versus insertional cloning of heterologous genes in Mycobacterium bovis BCG: impact on in vivo antigen persistence and immune responses. Infect. Immun. 70:303-314.
23. Mothe, B. R., H. Horton, D. K. Carter, T. M. Allen, M. E. Liebl, P. Skinner, T. U. Vogel, S. Fuenger, K. Vielhuber, W. Rehrauer, N. Wilson, G. Franchini, J. D. Altman, A. Haase, L. J. Picker, D. B. Allison, and D. I. Watkins. 2002. Dominance of CD8 responses specific for epitopes bound by a single major histocompatibility complex class I molecule during the acute phase of viral infection. J. Virol. 76:875-884.
24. Nakamura, Y., T. Gojobori, and T. Ikemura. 2000. Codon usage tabulated from the international DNA sequence databases: status for the year 2000. Nucleic Acids Res. 28:292.
25. Narum, D. L., S. Kumar, W. O. Rogers, S. R. Fuhrmann, H. Liang, M. Oakley, A. Taye, B. K. Sim, and S. L. Hoffman. 2001. Codon optimization of gene fragments encoding Plasmodium falciparum merozoite proteins enhances DNA vaccine protein expression and immunogenicity in mice. Infect. Immun. 69:7250-7253.
26. Pym, A. S., P. Brodin, L. Majlessi, R. Brosch, C. Demangel, A. Williams, K. E. Griffiths, G. Marchai, C. Leclecc, and S. T. Cole. 2003. Recombinant BCG exporting ESAT-6 confers enhanced protection against tuberculosis. Nat. Med. 9:533-539.
27. Qiu, J. T., R. Song, M. Dettenhofer, C. Tian, T. August, B. K. Felber, G. N. Pavlakis, and X. F. Yu. 1999. Evaluation of novel human immunodeficiency virus type 1 Gag DNA vaccines for protein expression in mammalian cells and induction of immune responses. J. Virol. 73:9145-9152.
28. Salk, J., and P. A. e. a. Bretcher. 1993. A strategy for prophylactic vaccination against HIV. Science 260:1270-1272.
29. Shiver, J. W., T. M. Fu, L. Chen, D. R. Casimiro, M. E. Davies, R. K. Evans, Z. Q. Zhang, A. J. Simon, W. L. Trigona, S. A. Dubey, L. Huang, V. A. Harris, R. S. Long, X. Liang, L. Handt, W. A. Schleif, L. Zhu, D. C. Freed, N. V. Persaud, L. Guan, K. S. Punt, A. Tang, M. Chen, K. A. Wilson, K. B. Collins. G. J. Heidecker, V. R. Fernandez, H. C. Perry, J. G. Joyce, K. M. Grimm, J. C. Cook, P. M. Keller, D. S. Kresock, H. Mach, R. D. Troutman, L. A. Isopi, D. M. Williams, Z. Xu, K. E. Bohannon, D. B. Volkin, D. C. Montefieri, A. Miura, G. R. Krìvulka, M. A. Lìfton, M. J. Kuroda, J. E. Schmitz, N. L. Letvin, M. J. Caulfield, A. J. Bett, R. Youil, D. C. Kaslow, and E. A. Emini. 2002. Replication-incompetent adenoviral vaccine vector elicits effective anti-immunodeficiency-virus immunity. Nature 415:331-335.
30. Someya, K., D. Cecilia, T. Nakasone, Y. Ami, K. Matsuo, S. Burda, H. Yamamoto, N. Yoshino, M. Kaizu, S. Ando, S. Zolla-Pazner, N. Yamamoto, and M. Honda. 2005. Vaccination with recombinant Mycobacterium bovis bacillus Calmette-Guérin (BCG)-Env V3 elicits neutralizing antibody-mediated protection in rhesus macaques against simian-human immunodeficiency virus 10with a homologous but not a heterologous V3 motif. J. Virol. 79:1452-1462.
31. Someya, K., K. Q. Xin, K. Matsuo, K. Okuda, N. Yamamoto, and M. Honda. 2004. A consecutive priming-boosting vaccination of mice with simian immunodeficiency virus (SIV) gag/pol DNA and recombinant vaccinia virus strain DIs elicits effective anti-SIV immunity. J. Virol. 78:9842-9853.
32. Stover, C. K., G. P. Bansal, M. S. Hanson, J. E. Burlein, S. R. Palaszynski, J. F. Young, S. Koeoig, D. B. Young, A. Sadziene, and A. G. Barbour. 1993. Protective immunity elicited by recombinant bacille Calmette-Guérin (BCG) expressing outer surface protein A (OspA) lipoprotein; a candidate Lyme disease vaccine. J. Exp. Med. 178:197-209.
33. Stover, C. K., V. F. de la Cruz, T. R. Fuerst, J. E. Burlein, L. A. Benson, L. T. Bennett, G. P. Bansal, J. F. Young, M. H. Lee, G. F. Hatfull, S. B. Snapper, R. G. Barletta, W. R. Jacobs, and B. R. Bloom. 1991. New use of BCG for recombinant vaccines. Nature 351:456-460.
34. Stratford, R., G. Douce, L. Zhang-Barber, N. Fairweather, J. Eskola, and G. Dougan. 2000. Influence of codon usage on the immunogenicity of a DNA vaccine against tetanus. Vaccine 19:810-815.
35. a-positive activated T cells in primary response to Mycobacterium bovis bacillus Calmette-Guérin (BCG) in guinea pigs. Cytometry Res. 10:37-45.
36. Thole, J. E., W. J. Keulen, J. De Bruyn, A. H. Kolk, D. G. Groothuis, L. G. Berwald, R. H. Tiesjema, and J. D. van Embden. 1987. Characterization, sequence determination, and immunogenicity of a 64-kilodalton protein of Mycobacterium bovis BCG expressed in Escherichia coli K-12. Infect. Immun. 55:1466-1475.
37. Uchijima, M., A. Yoshida, T. Nagata, and Y. Koide. 1998. Optimization of codon usage of plasmid DNA vaccine is required for the effective MHC class I-restricted T-cell responses against an intracellular bacterium. J. Immunol. 161:5594-5599.
38. Wild, J., A. Bojak, L. Demi, and R. Wagner. 2004. Influence of polypeptide size and intracellular sorting on the induction of epitope-specific CTL responses by DNA vaccines in a mouse model. Vaccine 22:1732-1743.
39. Williams, P. D., D. Regier, D, Akiyoshi, F. Genbauffe, and J. R. Murphy. 1988. Design, synthesis, and expression of a human interleukin-2 gene incorporating the codon usage bias found in highly expressed Escherichia coli genes. Nucleic Acids Res. 16:10453-10467.
40. Winter, N., M. Lagranderie, J. Rauzier, J. Timm, C. Leclerc, B. Guy, M. P. Kieny, M. Gheorghiu, and B. Gicquel. 1991. Expression of heterologous genes in Mycobacterium bovis BCG: induction of a cellular response against HIV-1 Nef protein. Gene 109:47-51.
41. Zhou, D., Y. Shen, L. Chalifoux, D. Lee-Parritz, M. Simon, P. K. Sehgal, L. Zheng, M. Halloran, and Z. W. Chen. 1999. Mycobacterium bovis bacille Calmette-Guérin enhances pathogenicity of simian immunodeficiency virus infection and accelerates progression to AIDS in macaques: a role of persistent T-cell activation in AIDS pathogenesis. J. Immunol. 162:2204-2216.
42. Zolotukhin, S., M. Potter, W. W. Hauswirth, J. Guy, and N. Muzyczka. 1996. A "humanized" green fluorescent protein cDNA adapted for high-level expression in mammalian cells. J. Virol. 70:4646-4654.
43. zur Megede, J., M. C. Chen, B. Doe, M. Schaefer, C. E. Greer, M. Selby, G. R. Otten, and S. W. Barnett. 2000. Increased expression and immunogenicity of sequence-modified human immunodeficiency virus type 1 gag gene. J. Virol. 74:2628-2635.