Recombinant Mycobacterium bovis BCG as an HIV vaccine vector

Current HIV Research

Volumn 8, Issue 4, 2010, Pages 282-298

  Chapman, Rosamund ^a   Chege, Gerald ^a   Shephard, Enid ^a   Stutz, Helen ^a   Williamson, Anna Lise ^a,b  

^a UNIVERSITY OF CAPE TOWN   (South Africa)

^b UNIVERSITY OF CAPE TOWN   (South Africa)

Author keywords

HIV; Mycobacterium bovis BCG; Recombinant BCG; Vaccine vector

Indexed keywords

ALUMINUM POTASSIUM SULFATE; ASPARAGINYLTHREONYLARGINYLLYSYLSERYLISOLEUCYLHISTIDYLISOLEUCYLGLYCYLPROLYLGLYCYLARGINYLALANYLPHENYLALANYLTYROSYLALANYLTHREONYLGLYCYLSERINE; BCG VACCINE; BETA GALACTOSIDASE; BETA LACTAMASE; GAG PROTEIN; GLYCOPROTEIN GP 110; GLYCOPROTEIN GP 120; GLYCOPROTEIN GP 140; HUMAN IMMUNODEFICIENCY VIRUS VACCINE; LIPOSOME; NEF PROTEIN; NEUTRALIZING ANTIBODY; POL PROTEIN; RECOMBINANT VACCINE; SIMIAN IMMUNODEFICIENCY VIRUS VACCINE; TETANUS TOXIN; UNCLASSIFIED DRUG; VIRUS ENVELOPE PROTEIN; VIRUS GLYCOPROTEIN;

ARTICLE; BACTERIAL STRAIN; CODON USAGE; DRUG EFFECT; DRUG EFFICACY; GENETIC STABILITY; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; HUMORAL IMMUNITY; MUCOSAL IMMUNITY; MYCOBACTERIUM BOVIS; NONHUMAN; PROMOTER REGION; SHUTTLE VECTOR; TRANSGENE; VIRUS LIKE AGENT;

AIDS VACCINES; BCG VACCINE; HIV INFECTIONS; HIV-1; HUMANS;

EID: 77953485289     PISSN: 1570162X     EISSN: None     Source Type: Journal    
DOI: 10.2174/157016210791208686     Document Type: Article

References (182)

1. Hanson MS, Bansal GP, Langermann S, Stover CK, Orme I. Efficacy and safety of live recombinant BCG vaccines. Dev Biol Stand 1995; 84: 229-36.
2. Champlin R, Hunter RL. Studies on the composition of adjuvants which selectively enhance delayed-type hypersensitivity to lipid conjugated protein antigens. J Immunol 1975; 114(1 Pt 1): 76-80.
3. Gheorghiu M, Lagrange PH, Fillastre C. The stability and immunogenicity of a dispersed-grown freeze-dried Pasteur BCG vaccine. J Biol Stand 1988; 16(1): 15-26.
4. Roche PW, Triccas JA, Winter N. BCG vaccination against tuberculosis: past disappointments and future hopes. Trends Microbiol 1995; 3(10): 397-401.
5. Fennelly GJ, Flynn JL, ter MV, Liebert UG, Bloom BR. Recombinant bacille Calmette-Guerin priming against measles. J Infect Dis 1995; 172(3): 698-705.
6. Govan VA, Christensen ND, Berkower C, Jacobs WR, Jr., Williamson AL. Immunisation with recombinant BCG expressing the cottontail rabbit papillomavirus (CRPV) L1 gene provides protection from CRPV challenge. Vaccine 2006; 24(12): 2087-93.
7. Grode L, Seiler P, Baumann S, et al. Increased vaccine efficacy against tuberculosis of recombinant Mycobacterium bovis bacille Calmette-Guerin mutants that secrete listeriolysin. J Clin Invest 2005; 115(9): 2472-9.
8. Langermann S, Palaszynski SR, Burlein JE, et al. Protective humoral response against pneumococcal infection in mice elicited by recombinant bacille Calmette-Guerin vaccines expressing pneumococcal surface protein A. J Exp Med 1994; 180(6): 2277-86.
9. Matsumoto S, Yukitake H, Kanbara H, Yamada T. Recombinant Mycobacterium bovis bacillus Calmette-Guerin secreting merozoite surface protein 1 (MSP1) induces protection against rodent malaria parasite infection depending on MSP1-stimulated interferon gamma and parasite-specific antibodies. J Exp Med 1998; 188(5): 845-54.
10. Nascimento IP, Dias WO, Quintilio W, et al. Neonatal immunization with a single dose of recombinant BCG expressing subunit S1 from pertussis toxin induces complete protection against Bordetella pertussis intracerebral challenge. Microbes Infect 2008; 10(2): 198-202.
11. Stover CK, Bansal GP, Hanson MS, et al. Protective immunity elicited by recombinant Bacille Calmette-Guerin(BCG) expressing Outer Surface Protein A(OspA) lipoprotein: A candidate lyme disease vaccine. J Exp Med 1993; 178: 197-209.
12. Streit JA, Recker TJ, Donelson JE, Wilson ME. BCG expressing LCR1 of Leishmania chagasi induces protective immunity in susceptible mice. Exp Parasitol 2000; 94(1): 33-41.
13. Matthews PC, Prendergast A, Leslie A, et al. Central role of reverting mutations in HLA associations with human immunodeficiency virus set point. J Virol 2008; 82(17): 8548-59.
14. Honeyborne I, Prendergast A, Pereyra F, et al. Control of human immunodeficiency virus type 1 is associated with HLA-B*13 and targeting of multiple gag-specific CD8+ T-cell epitopes. J Virol 2007; 81(7): 3667-72.
15. Kiepiela P, Ngumbela K, Thobakgale C, et al. CD8+ T-cell responses to different HIV proteins have discordant associations with viral load. Nat Med 2007; 13(1): 46-53.
16. Walker BD, Burton DR. Toward an AIDS vaccine. Science 2008; 320(5877): 760-4.
17. Rerks-Ngarm S, Pitisuttithum P, Nitayaphan S, et al. Vaccination with ALVAC and AIDSVAX to Prevent HIV-1 Infection in Thailand. N Engl J Med 2009; 361(23): 2209-20.
18. Ada G. The importance of vaccination. Front Biosci 2007; 12: 1278-90.
19. Hel Z, Nacsa J, Tryniszewska E, et al. Containment of simian immunodeficiency virus infection in vaccinated macaques: correlation with the magnitude of virus-specific pre- and postchallenge CD4+ and CD8+ T cell responses. J Immunol 2002; 169(9): 4778-87.
20. Johnston MI, Fauci AS. An HIV vaccine--challenges and prospects. N Engl J Med 2008; 359(9): 888-90.
21. Genesca M, McChesney MB, Miller CJ. Antiviral CD8 T cells in the genital tract control viral replication and delay progression to AIDS after vaginal SIV challenge in rhesus macaques immunized with virulence attenuated SHIV 89.6. J Intern Med 2009; 265(1): 67-77.
22. Genesca M, Skinner PJ, Bost KM, et al. Protective attenuated lentivirus immunization induces SIV-specific T cells in the genital tract of rhesus monkeys. Mucosal Immunol 2008; 1(3): 219-28.
23. Vaccari M, Mattapallil J, Song K, et al. Reduced protection from simian immunodeficiency virus SIVmac251 infection afforded by memory CD8+ T cells induced by vaccination during CD4+ T-cell deficiency. J Virol 2008; 82(19): 9629-38.
24. Guadalupe M, Reay E, Sankaran S, et al. Severe CD4+ T-cell depletion in gut lymphoid tissue during primary human immunodeficiency virus type 1 infection and substantial delay in restoration following highly active antiretroviral therapy. J Virol 2003; 77(21): 11708-17.
25. Neutra MR, Kozlowski PA. Mucosal vaccines: the promise and the challenge. Nat Rev Immunol 2006; 6(2): 148-58.
26. Coutsoudis A. Breastfeeding and HIV. Best Pract Res Clin Obstet Gynaecol 2005; 19(2): 185-96.
27. Brenchley JM, Schacker TW, Ruff LE, et al. CD4+ T cell depletion during all stages of HIV disease occurs predominantly in the gastrointestinal tract. J Exp Med 2004; 200(6): 749-59.
28. Veazey RS, DeMaria M, Chalifoux LV, et al. Gastrointestinal tract as a major site of CD4+ T cell depletion and viral replication in SIV infection. Science 1998; 280(5362): 427-31.
29. Belyakov IM, Berzofsky JA. Immunobiology of mucosal HIV infection and the basis for development of a new generation of mucosal AIDS vaccines. Immunity 2004; 20(3): 247-53.
30. Mehandru S, Poles MA, Tenner-Racz K, et al. Mechanisms of gastrointestinal CD4+ T-cell depletion during acute and early human immunodeficiency virus type 1 infection. J Virol 2007; 81(2): 599-612.
31. Belyakov IM, Ahlers JD, Berzofsky JA. Mucosal AIDS vaccines: current status and future directions. Expert Rev Vaccines 2004; 3(4 Suppl): S65-S73.
32. Aldovini A, Young RA. Humural and cell-mediated immune responses to live recombinant BCG-HIV vaccines. Nature 1991; 351: 479-82.
33. Chujoh Y, Matsuo K, Yoshizaki H, et al. Cross-clade neutralizing antibody production against human immunodeficiency virus type 1 clade E and B strains by recombinant Mycobacterium bovis BCG-based candidate vaccine. Vaccine 2001; 20: 797-804.
34. Promkhatkaew D, Pinyosukhee N, Thongdeejaroen W, et al. Enhancement of cell-mediated immune response in mice by whole HIV-1 Gag in Mycobacterium bovis BCG as a live vaccine candidate. Southeast Asian J Trop Med Public Health 2009; 40(1): 113-22.
35. Winter N, Lagranderie M, Rauzier J, et al. Expression of heterologous genes in Mycobacterium bovis BCG: induction of a cellular response against HIV-1 Nef protein. Gene 1991; 109(1): 47-54.
36. Honda M, Matsuo K, Nakasone T, et al. Protective immune responses induced by secretion of a chimeric soluble protein from a recombinant Mycobacterium bovis bacillus Calmette-Guerin vector candidate vaccine for human immunodeficiency virus type 1 in small animals. Proc Natl Acad Sci USA 1995; 92: 10693-7.
37. Kameoka M, Nishino Y, Matsuo K, et al. Cytotoxic T lymphocyte response in mice induced by a recombinant BCG vaccination which produces an extracellular alpha antigen that fused with the human immunodeficiency virus type 1 envelope immunodominant domain in the V3 loop. Vaccine 1994; 12(2): 153-8.
38. Matsuo K, Yamaguchi R, Yamazaki A, et al. Establishment of a foreign antigen secretion system in mycobacteria. Infect Immun 1990; 58(12): 4049-54.
39. Stover CK, de lC V, Fuerst TR, et al. New use of BCG for recombinant vaccines. Nature 1991; 351(6326): 456-60.
40. Wada N, Ohara N, Kameoka M, et al. Long-lasting immune response induced by recombinant bacillus Calmette-Guerin (BCG) secretion system. Scand J Immunol 1996; 43(2): 202-9.
41. Lagranderie M, Balazuc AM, Gicquel B, Gheorghiu M. Oral immunization with recombinant Mycobacterium bovis BCG Simian immunodeficiency virus nef induces local and systemic cytotoxic T-lymphocyte responses in mice. J Virol 1997; 71(3): 2303-9.
42. Winter N, Lagranderie M, Gangloff S, et al. Recombinant BCG strains expressing the SIV(Mac251)Nef gene induce proliferative and CTL responses against Nef synthetic peptides in mice. Vaccine 1995; 13(5): 471-8.
43. Lagranderie M, Winter N, Balazuc AM, Gicquel B, Gheorghiu M. A cocktail of Mycobacterium bovis BCG recombinants expressing the SIV Nef, Env, and Gag antigens induces antibody and cytotoxic responses in mice vaccinated by different mucosal routes. AIDS Res Hum Retroviruses 1998; 14(18): 1625-33.
44. Lagranderie M, Lo-Man R, Deriaud E, et al. Genetic control of antibody responses induced by recombinant Mycobacterium bovis BCG expressing a foreign antigen. Infect Immun 1997; 65(8): 3057-64.
45. Lim EM, Lagranderie M, Le GR, et al. Recombinant Mycobacterium bovis BCG producing the N-terminal half of SIVmac251 Env antigen induces neutralizing antibodies and cytotoxic T lymphocyte responses in mice and guinea pigs. AIDS Res Hum Retroviruses 1997; 13(18): 1573-81.
46. Hiroi T, Goto H, Someya K, et al. 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 2001; 167(10): 5862-7.
47. Kawahara M, Matsuo K, Honda M. Intradermal and oral immunization with recombinant Mycobacterium bovis BCG expressing the simian immunodeficiency virus Gag protein induces long-lasting, antigen-specific immune responses in guinea pigs. Clin Immunol 2006; 119(1): 67-78.
48. Kawahara M. Recombinant Mycobacterium bovis BCG vector system expressing SIV Gag protein stably and persistently induces antigen-specific humoral immune response concomitant with IFN gamma response, even at three years after immunization. Clin Immunol 2008; 129(3): 492-8.
49. Im EJ, Saubi N, Virgili G, et al. Vaccine platform for prevention of tuberculosis and mother-to-child transmission of human immunodeficiency virus type 1 through breastfeeding. J Virol 2007; 81(17): 9408-18.
50. Yu JS, Peacock JW, Jacobs WR, Jr., et al. Recombinant Mycobacterium bovis bacillus Calmette-Guerin elicits human immunodeficiency virus type 1 envelope-specific T lymphocytes at mucosal sites. Clin Vaccine Immunol 2007; 14(7): 886-93.
51. Adams EJ, Parham P. Species-specific evolution of MHC class I genes in the higher primates. Immunol Rev 2001; 183: 41-64.
52. Bontrop RE, Otting N, Slierendregt BL, Lanchburg JS. Evolution of major histocompatibility complex polymorphisms and T-cell receptor diversity in primates. Immunol Rev 1995; 143: 33-62.
53. Bontrop RE, Otting N, de Groot NG, Doxiadis GG. Major histocompatibility complex class II polymorphism in primates. Immunol Rev 1999; 167: 339-50.
54. Bontrop RE, Watkins DI. MHC polymorphism: AIDS susceptibility in non-human primates. Trends Immunol 2005; 26: 227-33.
55. Boyson JE, Shufflebotham C, Cadavid LF, et al. The MHC class I genes of the rhesus monkey. Different evolutionary histories of MHC class I and II genes in primates. J Immunol 1996; 156(12): 4656-65.
56. Damian RT, Greene ND, Katler SS. IgG subclasses of baboon (Papio cynocephalus). J Immunol 1971; 106: 246-57.
57. Doxiadis GG, Otting N, de Groot NG, Bontrop RE. Differential evolutionary MHC-class II strategies in humans and rhesus macaques: relevance for biomedical studies. Immunol Rev 2001; 183: 76-85.
58. Hainsey BM, Hubbard B, Leland MM, Brasky KM. Clinical parameters of the normal baboons (Papio species) and chimpanzes (Pan troglyodytes). Lab Anim Sci 1993; 43: 236-43.
59. Rogers J, Hixson JE. Baboons as an animal model for genetic studies of common human diseases. Am J Hum Genet 1997; 61: 489-93.
60. Behar SM, Dascher CC, Grusby MJ, Wang CR, Brenner MB. Susceptible of mice dificient in CD1D or TAP1 to infection with Mycobacterium tuberculosis. J Exp Med 1999; 189: 1973-80.
61. Geluk A, Elferink DG, Slierendregt BC, et al. Evolutionary conservation of major histocompatibility complex-DR/peptide/T cell interactins in primates. J Exp Med 1993; 177: 979-87.
62. Porcelli S, Morita CT, Brenner MB. CD1b restricts the response of human CD4-8-T lymphocytes to a microbial antigen. Nature 1992; 360: 593-7.
63. Shinkai K, Locksley RM. CDI, tuberculosis, and the evolution of major histocompatibility complex molecules. J Exp Med 2000; 193: 907-14.
64. Carding SR, Egan PJ. The importance of gamma delta T cells in the resolution of pathogen-induced inflammatory immune response. Immunol Rev 2000; 173: 98-108.
65. Constant P, Davodeau F, Peyrat MA, et al. Stimulation of human gamma delta T cells by nonpeptidic mycobacterial ligands. Science 1994; 264: 267-70.
66. Poccia F, Malkovsky M, Pollak A, et al. In vivo gamadelta T cell priming to mycobacterial antigens by primary Mycobacterium tuberculosis infection and exposure to nonpeptiditic ligands. Mol Med 1999; 5: 471-6.
67. Chege GK, Williamson AL, Passmore JS, et al. The immune response of the Chacma baboon to Bacille Calmette Guerin: development of a primate model for BCG-based vaccine research. Vaccine 2005; 23(50): 5783-91.
68. Yasutomi Y, Koeing S, Haun SS, et al. Immunization with recombinant BCG-SIV elicits SIV-specific cytotoxic Tlymphocytes in rhesus monkey. J Immunol 1993; 150: 3101-7.
69. Yasutomi Y, Koenig S, Woods RM, et al. A vaccine-elicited, single viral epitope-specific cytotoxic T lymphocyte response does not protect against intravenous, cell-free simian immunodeficiency virus challenge. J Virol 1995; 69(4): 2279-84.
70. Leung NJ, Aldovini A, Young R, et al. The kinetics of specific immune responses in rhesus monkeys inoculated with live recombinant BCG expressing SIV Gag, Pol, Env, and Nef proteins. Virology 2000; 268(1): 94-103.
71. Mederle I, Le GR, Vaslin B, et al. Mucosal administration of three recombinant Mycobacterium bovis BCG-SIVmac251 strains to cynomolgus macaques induces rectal IgAs and boosts systemic cellular immune responses that are primed by intradermal vaccination. Vaccine 2003; 21(27-30): 4153-66.
72. Someya K, Cecilia D, Ami Y, et al. Vaccination of rhesus macaques with recombinant Mycobacterium bovis bacillus Calmette-Guerin Env V3 elicits neutralizing antibody-mediated protection against simian-human immunodeficiency virus with a homologous but not a heterologous V3 motif. J Virol 2005; 79(3): 1452-62.
73. Ami Y, Izumi Y, Matsuo K, et al. Priming-boosting vaccination with recombinant Mycobacterium bovis bacillus Calmette-Guerin and a nonreplicating vaccinia virus recombinant leads to long-lasting and effective immunity. J Virol 2005; 79(20): 12871-9.
74. Cayabyab MJ, Korioth-Schmitz B, Sun Y, et al. Recombinant Mycobacterium bovis BCG prime-recombinant adenovirus boost vaccination in rhesus monkeys elicits robust polyfunctional simian immunodeficiency virus-specific T-cell responses. J Virol 2009; 83(11): 5505-13.
75. Chege GK, Thomas R, Shephard EG, et al. A prime-boost immunisation regimen using recombinant BCG and Pr55(gag) virus-like particle vaccines based on HIV type 1 subtype C successfully elicits Gag-specific responses in baboons. Vaccine 2009; 27(35): 4857-66.
76. Amara R R, Ibegbu C, Villinger F, et al. Studies using a viral challenge and CD8 T cell depletions on the roles of cellular and humoral immunity in the control of an SHIV-89.6P challenge in DNA/MVA-vaccinated macaques. Virology 2005; 343: 246-55.
77. Borrow P, Lewicki H, Hahn BH, Shaw GM, Oldstone MB. Virus-specific CD8+ cytotoxic T-lymphocyte activity associated with control of viremia in primary human immunodeficiency virus type 1 infection. J Virol 1994; 68(6103): 6110.
78. Jin X, Bauer DE, Tuttleton SE, et al. Dramatic rise in plasma viremia after CD8+ T cell depletion in simian immunodeficiecy virus-infected macaques. J Exp Med 1999; 189: 991-8.
79. Koup RA, Safrit JT, Cao Y, et al. Temporal association of cellular immune responses with the initial control of viremia in primary human immunodeficiency virus type 1 syndrome. J Virol 1994; 68: 4650-5.
80. Schmitz JE, Johnson RP, McClure HM, et al. Effect of CD8+lymphocyte depletion on virus containment after simian immunodeficiency virus SIVmac251 challenge of live attenuated SIVmac239delta3-vaccinated rhesus macaques. J Virol 2005; 79: 8131-41.
81. Almeida JR, Price DA, Papagno L, et al. Superior control of HIV-1 replication by CD8+ T cells is reflected by their avidity, polyfunctionality, and clonal turnover. J Exp Med 2007; 204(10): 2473-85.
82. Betts MR, Gray CM, Cox JH, Ferrari G. Antigen-specific T-cell-mediated immunity after HIV-1 infection: implications for vaccine control of HIV development. Expert Rev Vaccines 2006; 5(4): 505-16.
83. Acierno PM, Schmitz JE, Gorgone DA, et al. Preservation of functional virus-specific memory CD8+ T lymphocytes in vaccinated, simian human immunodeficiency virus-infected rhesus monkeys. J Immunol 2006; 176(9): 5338-45.
84. Betts MR, Nason MC, West SM, et al. HIV nonprogressors preferentially maintain highly functional HIV-specific CD8+ T cells. Blood 2006; 107(12): 4781-9.
85. Shankar P, Russo M, Harnisch B, et al. Impaired function of circulating HIV-specific CD8(+) T cells in chronic human immunodeficiency virus infection. Blood 2000; 96(9): 3094-101.
86. McShane H. Prime-boost immunization strategies for infectious diseases. Curr Opin Mol Ther 2002; 4(1): 23-7.
87. Cebere I, Dorrell L, McShane H, et al. Phase I clinical trial safety of DNA- and modified virus Ankara-vectored human immunodeficiency virus type 1 (HIV-1) vaccines administered alone and in a prime-boost regime to healthy HIV-1-uninfected volunteers. Vaccine 2006; 24(4): 417-25.
88. Girard MP, Osmanov SK, Kieny MP. A review of vaccine research and development: The human immunodeficiency virus (HIV). Vaccine 2006; 24(19): 4062-81.
89. McShane H, Pathan AA, Sander CR, et al. Recombinant modified vaccinia virus Ankara expressing antigen 85A boosts BCG-primed and naturally acquired antimycobacterial immunity in humans. Nat Med 2004; 10(11): 1240-4.
90. Vordermeier HM, Rhodes SG, Dean G, et al. Cellular immune responses induced in cattle by heterologous prime-boost vaccination using recombinant viruses and bacille Calmette-Guerin. Immunology 2004; 112(3): 461-70.
91. Im EJ, Saubi N, Virgili G, et al. Vaccine platform for prevention of tuberculosis and mother-to-child transmission of human immunodeficiency virus type 1 through breastfeeding. J Virol 2007; 81(17): 9408-18.
92. Snapper SB, Lugosi L, Jekkel A, et al. Lysogeny and transformation in mycobacteria: stable expression of foreign genes. Proc Natl Acad Sci USA 1988; 85(18): 6987-91.
93. Bourn WR, Jansen Y, Stutz H, et al. Creation and characterisation of a high-copy-number version of the pAL5000 mycobacterial replicon. Tuberculosis (Edinb) 2007; 87(6): 481-8.
94. Mo Y, Quanquin NM, Vecino WH, et al. Genetic alteration of Mycobacterium smegmatis to improve mycobacterial bactofection and DNA immunisation. Infect Immun 2007; 75(10): 4804-16.
95. Anes E, Portugal I, Moniz-Pereira J. Insertion into the Mycobacterium smegmatis genome of the aph gene through lysogenization with the temperate mycobacteriophage Ms6. FEMS Microbiol Lett 1992; 74(1): 21-5.
96. Lee MH, Pascopella L, Jacobs WR, Jr., Hatfull GF. Site-specific integration of mycobacteriophage L5: integration-proficient vectors for Mycobacterium smegmatis, Mycobacterium tuberculosis, and bacille Calmette-Guerin. Proc Natl Acad Sci USA 1991; 88(8): 3111-5.
97. Marklund BI, Speert DP, Stokes RW. Gene replacement through homologous recombination in Mycobacterium intracellulare. J Bacteriol 1995; 177(21): 6100-5.
98. Mederle I, Bourguin I, Ensergueix D, et al. Plasmidic versus insertional cloning of heterologous genes in Mycobacterium bovis BCG: impact on in vivo antigen persistence and immune responses. Infect Immun 2002; 70(1): 303-14.
99. Dennehy M, Bourn W, Steele D, Williamson AL. Evaluation of recombinant BCG expressing rotavirus VP6 as an anti-rotavirus vaccine. Vaccine 2007; 25(18): 3646-57.
100. Dellagostin OA, Wall S, Norman E, et al. Construction and use of integrative vectors to express foreign genes in mycobacteria. Mol Microbiol 1993; 10(5): 983-93.
101. Dellagostin OA, Esposito G, Eales LJ, Dale JW, McFadden J. Activity of mycobacterial promoters during intracellular and extracellular growth. Microbiology 1995; 141(Pt 8): 1785-92.
102. Murray A, Winter N, Lagranderie M, et al. Expression of Escherichia coli beta-galactosidase in Mycobacterium bovis BCG using an expression system isolated from Mycobacterium paratuberculosis which induced humoral and cellular immune responses. Mol Microbiol 1992; 6(22): 3331-42.
103. Himmelrich H, Lo-Man R, Winter N, et al. Immune responses induced by recombinant BCG strains according to level of production of a foreign antigen: malE. Vaccine 2000; 18(24): 2636-47.
104. Parish T, Mahenthiralingam E, Draper P, Davis EO, Colston MJ. Regulation of the inducible acetamidase gene of Mycobacterium smegmatis. Microbiology 1997; 143(Pt 7): 2267-76.
105. Bukau B, Horwich AL. The Hsp70 and Hsp60 chaperone machines. Cell 1998; 92(3): 351-66.
106. da Cruz FW, McBride AJ, Conceicao FR, et al. Expression of the B-cell and T-cell epitopes of the rabies virus nucleoprotein in Mycobacterium bovis BCG and induction of an humoral response in mice. Vaccine 2001; 20(5-6): 731-6.
107. Dhandayuthapani S, Via LE, Thomas CA, et al. Green fluorescent protein as a marker for gene expression and cell biology of mycobacterial interactions with macrophages. Mol Microbiol 1995; 17(5): 901-12.
108. Kumar D, Srivastava BS, Srivastava R. Genetic rearrangements leading to disruption of heterologous gene expression in mycobacteria: an observation with Escherichia coli beta-galactosidase in Mycobacterium smegmatis and its implication in vaccine development. Vaccine 1998; 16(11-12): 1212-5.
109. Al Zarouni M, Dale JW. Expression of foreign genes in Mycobacterium bovis BCG strains using different promoters reveals instability of the hsp60 promoter for expression of foreign genes in Mycobacterium bovis BCG strains. Tuberculosis 2002; 82(6): 283-91.
110. Haeseleer F. Structural instability of recombinant plasmids in mycobacteria. Res Microbiol 1994; 145(9): 683-7.
111. Via LE, Curcic R, Mudd MH, et al. Elements of signal transduction in Mycobacterium tuberculosis: in vitro phosphorylation and in vivo expression of the response regulator MtrA. J Bacteriol 1996; 178(11): 3314-21.
112. Zahrt TC, Deretic V. An essential two-component signal transduction system in Mycobacterium tuberculosis. J Bacteriol 2000; 182(13): 3832-8.
113. Mahenthiralingam E, Draper P, Davis EO, Colston MJ. Cloning and sequencing of the gene which encodes the highly inducible acetamidase of Mycobacterium smegmatis. J Gen Microbiol 1993; 139(3): 575-83.
114. Roberts G, Muttucumaru DG, Parish T. Control of the acetamidase gene of Mycobacterium smegmatis by multiple regulators. FEMS Microbiol Lett 2003; 221(1): 131-6.
115. Ehrt S, Guo XV, Hickey CM, et al. Controlling gene expression in mycobacteria with anhydrotetracycline and Tet repressor. Nucleic Acids Res 2005; 33(2): e21.
116. Scholz O, Henssler EM, Bail J, et al. Activity reversal of Tet repressor caused by single amino acid exchanges. Mol Microbiol 2004; 53(3): 777-89.
117. Kamionka A, Bertram R, Hillen W. Tetracycline-dependent conditional gene knockout in Bacillus subtilis. Appl Environ Microbiol 2005; 71(2): 728-33.
118. Gandotra S, Schnappinger D, Monteleone M, Hillen W, Ehrt S. In vivo gene silencing identifies the Mycobacterium tuberculosis proteasome as essential for the bacteria to persist in mice. Nat Med 2007; 13(12): 1515-20.
119. Guo XV, Monteleone M, Klotzsche M, et al. Silencing essential protein secretion in Mycobacterium smegmatis by using tetracycline repressors. J Bacteriol 2007; 189(13): 4614-23.
120. Klotzsche M, Ehrt S, Schnappinger D. Improved tetracycline repressors for gene silencing in mycobacteria. Nucleic Acids Res 2009; 37(6): 1778-88.
121. Andersson GE, Sharp PM. Codon usage in the Mycobacterium tuberculosis complex. Microbiology 1996; 142(Pt 4): 915-25.
122. Kanekiyo M, Matsuo K, Hamatake M, et al. Mycobacterial codon optimization enhances antigen expression and virus-specific immune responses in recombinant Mycobacterium bovis bacille Calmette-Guerin expressing human immunodeficiency virus type 1 Gag. J Virol 2005; 79(14): 8716-23.
123. Hanson MS, Lapcevich CV, Haun SL. Progress on development of the live BCG recombinant vaccine vehicle for combined vaccine delivery. Ann N Y Acad Sci 1995; 754: 214-21.
124. Supply P, Sutton P, Coughlan SN, et al. Immunogenicity of recombinant BCG producing the GRA1 antigen from Toxoplasma gondii. Vaccine 1999; 17(7-8): 705-14.
125. Abomoelak B, Huygen K, Kremer L, Turneer M, Locht C. Humoral and cellular immune responses in mice immunized with recombinant Mycobacterium bovis Bacillus Calmette-Guerin producing a pertussis toxin-tetanus toxin hybrid protein. Infect Immun 1999; 67(10): 5100-5.
126. Karnasuta C, Paris RM, Cox JH, et al. Antibody-dependent cell-mediated cytotoxic responses in participants enrolled in a phase I/II ALVAC-HIV/AIDSVAX B/E prime-boost HIV-1 vaccine trial in Thailand. Vaccine 2005; 23(19): 2522-9.
127. Bastos RG, Dellagostin OA, Barletta RG, et al. Construction and immunogenicity of recombinant Mycobacterium bovis BCG expressing GP5 and M protein of porcine reproductive respiratory syndrome virus. Vaccine 2002; 21(1-2): 21-9.
128. Himmelrich H, Lo-Man R, Winter N, et al. Immune responses induced by recombinant BCG strains according to level of production of a foreign antigen: malE. Vaccine 2000; 18(24): 2636-47.
129. Grode L, Kursar M, Fensterle J, Kaufmann SH, Hess J. Cell-mediated immunity induced by recombinant Mycobacterium bovis bacille Calmette-Guerin strains against an intracellular bacterial pathogen: importance of antigen secretion or membrane-targeted antigen display as lipoprotein for vaccine efficacy. J Immunol 2002; 168(4): 1869-76.
130. Haynes BF, Shattock RJ. Critical issues in mucosal immunity for HIV-1 vaccine development. J Allergy Clin Immunol 2008; 122(1): 3-9.
131. Power CA, Wei G, Bretscher PA. Mycobacterial dose defines the Th1/Th2 nature of the immune response independently of whether immunization is administered by the intravenous, subcutaneous, or intradermal route. Infect Immun 1998; 66(12): 5743-50.
132. Horwitz MA, Harth G, Dillon BJ, Maslesa-Galic S. A novel live recombinant mycobacterial vaccine against bovine tuberculosis more potent than BCG. Vaccine 2006; 24(10): 1593-600.
133. Rao V, Dhar N, Tyagi AK. Modulation of host immune responses by overexpression of immunodominant antigens of Mycobacterium tuberculosis in bacille Calmette-Guerin. Scand J Immunol 2003; 58(4): 449-61.
134. Dhar N, Rao V, Tyagi AK. Skewing of the Th1/Th2 responses in mice due to variation in the level of expression of an antigen in a recombinant BCG system. Immunol Lett 2003; 88(3): 175-84.
135. Mehandru S, Poles MA, Tenner-Racz K, et al. Lack of mucosal immune reconstitution during prolonged treatment of acute and early HIV-1 infection. PLoS Med 2006; 3(12): e484.
136. Belyakov IM, Hel Z, Kelsall B, et al. Mucosal AIDS vaccine reduces disease and viral load in gut reservoir and blood after mucosal infection of macaques. Nat Med 2001; 7(12): 1320-6.
137. Benevolo-de-Andrade TC, Monteiro-Maia R, Cosgrove C, Castello-Branco LR. BCG Moreau Rio de Janeiro: an oral vaccine against tuberculosis--review. Mem Inst Oswaldo Cruz 2005; 100(5): 459-65.
138. Aldwell FE, Keen DL, Stent VC, et al. Route of BCG administration in possums affects protection against bovine tuberculosis. N Z Vet J 1995; 43(7): 356-9.
139. Aldwell FE, Keen DL, Parlane NA, et al. Oral vaccination with Mycobacterium bovis BCG in a lipid formulation induces resistance to pulmonary tuberculosis in brushtail possums. Vaccine 2003; 22(1): 70-6.
140. Badell E, Nicolle F, Clark S, et al. Protection against tuberculosis induced by oral prime with Mycobacterium bovis BCG and intranasal subunit boost based on the vaccine candidate Ag85B-ESAT-6 does not correlate with circulating IFN-gamma producing T-cells. Vaccine 2009; 27(1): 28-37.
141. Buddle BM, Denis M, Aldwell FE, et al. Vaccination of cattle with Mycobacterium bovis BCG by a combination of systemic and oral routes. Tuberculosis (Edinb) 2008; 88(6): 595-600.
142. Clark S, Cross ML, Smith A, et al. Assessment of different formulations of oral Mycobacterium bovis bacille Calmette-Guerin (BCG) vaccine in rodent models for immunogenicity and protection against aerosol challenge with M. bovis. Vaccine 2008; 26(46): 5791-7.
143. Ajdary S, Dobakhti F, Taghikhani M, et al. Oral administration of BCG encapsulated in alginate microspheres induces strong Th1 response in BALB/c mice. Vaccine 2007; 25(23): 4595-601.
144. Clark S, Cross ML, Nadian A, et al. Oral vaccination of guinea pigs with a Mycobacterium bovis bacillus Calmette-Guerin vaccine in a lipid matrix protects against aerosol infection with virulent M. bovis. Infect Immun 2008; 76(8): 3771-6.
145. Cross ML, Lambeth MR, Coughlan Y, Aldwell FE. Oral vaccination of mice with lipid-encapsulated Mycobacterium bovis BCG: Effect of reducing or eliminating BCG load on cell-mediated immunity. Vaccine 2007; 25(7): 1297-303.
146. Vipond J, Cross ML, Lambeth MR, et al. Immunogenicity of orally-delivered lipid-formulated BCG vaccines and protection against Mycobacterium tuberculosis infection. Microbes Infect 2008; 10(14-15): 1577-81.
147. Kawahara M, Matsuo K, Nakasone T, et al. Combined intrarectal/intradermal inoculation of recombinant Mycobacterium bovis bacillus Calmette-Guerin (BCG) induces enhanced immune responses against the inserted HIV-1 V3 antigen. Vaccine 2002; 21(3-4): 158-66.
148. Langermann S, Palaszynski SR, Sadziene A, Stover CK, Koenig S.Systemic and mucosal immunity induced by BCG vector expressing outer-surface protein A of Borrelia burgdorferi. Nature 1994; 372: 552-5.
149. Lagranderie M, Balazuc AM, Abolhassani M, et al. Development of mixed Th1/Th2 type immune response and protection against Mycobacterium tuberculosis after rectal or subcutaneous immunization of newborn and adult mice with Mycobacterium bovis BCG. Scand J Immunol 2002; 55(3): 293-303.
150. Wu B, Huang C, Garcia L, et al. Unique gene expression profiles in infants vaccinated with different strains of Mycobacterium bovis bacille Calmette-Guerin. Infect Immun 2007; 75(7): 3658-64.
151. Horwitz MA, Harth G, Dillon BJ, Maslesa-Galic S. Commonly administered BCG strains including an evolutionarily early strain and evolutionarily late strains of disparate genealogy induce comparable protective immunity against tuberculosis. Vaccine 2009; 27(3): 441-5.
152. Bloom B. Tuberculosis: Pathogenesis, Protection, and Control. ASM; 1994.
153. Lotte A, Wasz-Hockert O, Poisson N, et al. A bibliography of the complications of BCG vaccination. A comprehensive list of the world literature since the introduction of BCG up to July 1982, supplemented by over 100 personal communications. Adv Tuberc Res 1984; 21: 194-245.
154. Chen ZW, Shen Y, Zhou D, et al. In vivo T-lymphocyte activation and transient reduction of viral replication in macaques infected with simian immunodeficiency virus. J Virol 2001; 75(10): 4713-20.
155. Tullius MV, Harth G, Maslesa-Galic S, Dillon BJ, Horwitz MA. A replication-limited recombinant Mycobacterium bovis BCG vaccine against tuberculosis designed for human immunodeficiency virus-positive persons is safer and more efficacious than BCG. Infect Immun 2008; 76(11): 5200-14.
156. Magalhaes I, Sizemore DR, Ahmed RK, et al. rBCG induces strong antigen-specific T cell responses in rhesus macaques in a prime-boost setting with an adenovirus 35 tuberculosis vaccine vector. PLoS ONE 2008; 3(11): e3790.
157. Dennehy M, Williamson AL. Factors influencing the immune response to foreign antigen expressed in recombinant BCG vaccines. Vaccine 2005; 23(10): 1209-24.
158. Medeiros MA, Dellagostin OA, Armoa GR, et al. Comparative evaluation of Mycobacterium vaccae as a surrogate cloning host for use in the study of mycobacterial genetics. Microbiology 2002; 148(Pt 7): 1999-2009.
159. Becker J, Craig EA. Heat-shock proteins as molecular chaperones. Eur J Biochem 1994; 219(1-2): 11-23.
160. Fuerst TR, de lC V, Bansal GP, Stover CK. Development and analysis of recombinant BCG vector systems. AIDS Res Hum Retroviruses 1992; 8(8): 1451-5.
161. Kumar D, Srivastava BS, Srivastava R. Genetic rearrangements leading to disruption of heterologous gene expression in mycobacteria: an observation with Escherichia coli beta-galactosidase in Mycobacterium smegmatis and its implication in vaccine development. Vaccine 1998; 16(11-12): 1212-5.
162. Borsuk S, Mendum TA, Fagundes MQ, et al. Auxotrophic complementation as a selectable marker for stable expression of foreign antigens in Mycobacterium bovis BCG. Tuberculosis (Edinb) 2007; 87(6): 474-80.
163. Nascimento IP, Dias WO, Quintilio W, et al. Construction of an unmarked recombinant BCG expressing a pertussis antigen by auxotrophic complementation: protection against Bordetella pertussis challenge in neonates. Vaccine 2009; 27(52): 7346-51.
164. Trunz BB, Fine P, Dye C. Effect of BCG vaccination on childhood tuberculous meningitis and miliary tuberculosis worldwide: a metaanalysis and assessment of cost-effectiveness. Lancet 2006; 367(9517): 1173-80.
165. Fine PE. Variation in protection by BCG: implications of and for heterologous immunity. Lancet 1995; 346(8986): 1339-45.
166. de Lisle GW, Wards BJ, Buddle BM, Collins DM. The efficacy of livetuberculosisvaccinesafterpresensitizationwith Mycobacterium avium. Tuberculosis (Edinb) 2005; 85(1-2): 73-9.
167. Young SL, Slobbe L, Wilson R, et al. Environmental strains of Mycobacterium avium interfere with immune responses associated with Mycobacterium bovis BCG vaccination. Infect Immun 2007; 75(6): 2833-40.
168. Brandt L, Feino CJ, Weinreich OA, et al. Failure of the Mycobacterium bovis BCG vaccine: some species of environmental mycobacteria block multiplication of BCG and induction of protective immunity to tuberculosis. Infect Immun 2002; 70(2): 672-8.
169. Orme IM, Roberts AR, Collins FM. Lack of evidence for a reduction in the efficacy of subcutaneous BCG vaccination in mice infected with nontuberculous mycobacteria. Tubercle 1986; 67(1): 41-6.
170. Smith D, Reeser P, Musa S. Does infection with environmental mycobacteria suppress the protective response to subsequent vaccination with BCG? Tubercle 1985; 66(1): 17-23.
171. Demangel C, Garnier T, Rosenkrands I, Cole ST. Differential effects of prior exposure to environmental mycobacteria on vaccination with Mycobacterium bovis BCG or a recombinant BCG strain expressing RD1 antigens. Infect Immun 2005; 73(4): 2190-6.
172. Dharmapuri S, Peruzzi D, Aurisicchio L. Engineered adenovirus serotypes for overcoming anti-vector immunity. Expert Opin Biol Ther 2009; 9(10): 1279-87.
173. Gudmundsdotter L, Nilsson C, Brave A, et al. Recombinant Modified Vaccinia Ankara (MVA) effectively boosts DNA-primed HIV-specific immune responses in humans despite pre-existing vaccinia immunity. Vaccine 2009; 27(33): 4468-74.
174. Buddle BM, Wedlock DN, Parlane NA, et al. Revaccination of neonatal calves with Mycobacterium bovis BCG reduces the level of protection against bovine tuberculosis induced by a single vaccination. Infect Immun 2003; 71(11): 6411-9.
175. Barreto ML, Pereira SM, Ferreira AA. BCG vaccine: efficacy and indications for vaccination and revaccination. J Pediatr (Rio J) 2006; 82(3 Suppl): S45-S54.
176. Crampin AC, Glynn JR, Fine PE. What has Karonga taught us? Tuberculosis studied over three decades. Int J Tuberc Lung Dis 2009; 13(2): 153-64.
177. Elias D, Mengistu G, Akuffo H, Britton S. Are intestinal helminths risk factors for developing active tuberculosis? Trop Med Int Health 2006; 11(4): 551-8.
178. Diniz LM, Zandonade E, Dietze R, Pereira FE, Ribeiro-Rodrigues R. Short report: do intestinal nematodes increase the risk for multibacillary leprosy? Am J Trop Med Hyg 2001; 65(6): 852-4.
179. Tristao-Sa R, Ribeiro-Rodrigues R, Johnson LT, Pereira FE, Dietze R. Intestinal nematodes and pulmonary tuberculosis. Rev Soc Bras Med Trop 2002; 35(5): 533-5.
180. Elias D, Akuffo H, Thors C, Pawlowski A, Britton S. Low dose chronic Schistosoma mansoni infection increases susceptibility to Mycobacterium bovis BCG infection in mice. Clin Exp Immunol 2005; 139(3): 398-404.
181. Malhotra I, Mungai P, Wamachi A, et al. Helminth- and Bacillus Calmette-Guerin-induced immunity in children sensitized in utero to filariasis and schistosomiasis. J Immunol 1999; 162(11): 6843-8.
182. Kawahara M, Hashimoto A, Toida I, Honda M. 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 2002; 105(3): 326-31.