Pre-clinical development of BCG.HIVACAT, an antibiotic-free selection strain, for HIV-TB pediatric vaccine vectored by Lysine Auxotroph of BCG

PLoS ONE

Volumn 7, Issue 8, 2012, Pages

  Saubi, Narcís ^a   Mbewe Mvula, Alice ^b   Gea Mallorqui, Ester ^a   Rosario, Maximillian ^c,d   Gatell, Josep Maria ^a   Hanke, Tomáš ^b,c   Joseph, Joan ^a  

^a UNIVERSITY OF BARCELONA   (Spain)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c UNIVERSITY OF OXFORD   (United Kingdom)

^d UNIVERSITY OF ALBERTA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BCG VACCINE; GAMMA INTERFERON; HUMAN IMMUNODEFICIENCY VIRUS ANTIGEN; INTERLEUKIN 2; LYSINE; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 1; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANTIBIOTIC RESISTANCE; ARTICLE; AUXOTROPHY; BACTERIAL STRAIN; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; DRUG SAFETY; ESCHERICHIA COLI; FEMALE; HUMAN IMMUNODEFICIENCY VIRUS 1; IMMUNE RESPONSE; IMMUNOGENICITY; IN VIVO STUDY; MODIFIED VACCINIA VIRUS ANKARA; MOUSE; MYCOBACTERIUM TUBERCULOSIS; NEWBORN; NONHUMAN; PLASMID; TOXICITY TESTING; VACCINIA VIRUS; WEIGHT REDUCTION;

AIDS VACCINES; ANIMALS; BCG VACCINE; CD8-POSITIVE T-LYMPHOCYTES; CHILD; ESCHERICHIA COLI; FEMALE; GENETIC VECTORS; HIV-1; HUMANS; IMMUNIZATION, SECONDARY; LYSINE; MICE; MYCOBACTERIUM BOVIS; MYCOBACTERIUM TUBERCULOSIS; PHENOTYPE; PLASMIDS; SPECIES SPECIFICITY;

EID: 84865165599     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0042559     Document Type: Article

References (62)

1. UNAIDS World AIDS Day Report 2011 (2011) Joint United Nations Programme on HIV/AIDS (UNAIDS). Available: http://www.unaids.org/en/media/unaids/contentassets/documents/unaidspublication/2011/JC2216_WorldAIDSday_report_2011_en.pdf. Accessed 2012 Aug 1.
2. Cavarelli M, Scarlatti G, (2011) Human immunodeficiency virus type 1 mother-to-child transmission and prevention: successes and controversies. J Intern Med 270: 561-579 doi: 10.1111/j.1365-2796.2011.02458.x.
3. Borkowsky W, Wara D, Fenton T, McNamara J, Kang M, et al. (2000) Lymphoproliferative responses to recombinant HIV-1 envelope antigens in neonates and infants receiving gp120 vaccines. J Infect Dis 181: 890-896 doi: 10.1086/315298.
4. Johnson DC, McFarland EJ, Muresan P, Fenton T, McNamara J, et al. (2005) Safety and immunogenicity of an HIV-1 recombinant canarypox vaccine in newborns and infants of HIV-1-infected women. J Infect Dis 192: 2129-2133 doi: 10.1086/498163.
5. McFarland EJ, Johnson DC, Muresan P, Fenton T, Tomaras GD, et al. (2006) HIV-1 vaccine induced immune responses in newborns of HIV-1 infected mothers. AIDS 20: 1481-1489 doi:10.1097/01.aids.0000237363.33994.45.
6. Nascimento IP, Dias WO, Quintilio W, Hsu T, Jacobs WR Jr, et al. (2009) Construction of an unmarked recombinant BCG expressing a pertussis antigen by auxotrophic complementation: protection against Bordetella pertussis challenge in neonates. Vaccine 27: 7346-7351 doi:10.1016/j.vaccine.2009.09.043.
7. Zhu YD, Fennelly G, Miller C, Tarara R, Saxe I, et al. (1997) Recombinant bacille Calmette-Guérin expressing the measles virus nucleoprotein protects infant rhesus macaques from measles virus pneumonia. J Infect Dis 176: 1445-1453 doi: 10.1086/514140.
8. Bueno SM, González PA, Cautivo KM, Mora JE, Leiva ED, et al. (2008) Protective T cell immunity against respiratory syncytial virus is efficiently induced by recombinant BCG. Proc Natl Acad Sci U S A 105: 20822-20827 doi: 10.1073/pnas.0806244105.
9. Ranganathan UD, Larsen MH, Kim J, Porcelli SA, Jacobs WR Jr, et al. (2009) Recombinant pro-apoptotic Mycobacterium tuberculosis generates CD8+ T-cell responses against human immunodeficiency virus type 1 Env and M. tuberculosis in neonatal mice. Vaccine 28: 152-161 doi: 10.1016/j.vaccine.2009.09.087.
10. Im EJ, Saubi N, Virgili G, Sander C, Teoh D, et al. (2007) Vaccine platform for prevention of tuberculosis and mother-to-child transmission of human immunodeficiency virus type 1 through breastfeeding. J Virol 81 (17): 9408-9418 doi:10.1128%2FJVI.00707-07.
11. Lotte A, Wasz-Hockert O, Poisson N, Dumitrescu N, Verron M, et al. (1984) BCG complications. Estimates of the risks among vaccinated subjects and statistical analysis of their main characteristics. Adv Tuberc Res 21: 107-193.
12. World Health Organization (2007) Revised BCG vaccination guidelines for infants at risk for HIVinfection. Wkly Epidemiol Rec 82: 193-196.
13. Hesseling AC, Cotton MF, Fordham von Reyn C, Graham SM, Gie RP, et al. (2008) Consensus statement on the revised World Health Organization recommendations for BCG vaccination in HIV-infected infants. Int J Tuberc Lung Dis 12: 1376-1379.
14. Joseph J, Saubi N, Pezzat E, Gatell JM, (2006) Progress towards an HIV vaccine based on recombinant Bacillus Calmette-Guérin: failures and challenges. Exp Rev Vac 5: 827-838, 2006 doi: 10.1586/14760584.5.6.827.
15. Matsuo K, Yasutomi Y (2011) Mycobacterium bovis Bacille Calmette-Guérin as a Vaccine Vector for Global Infectious Disease Control. Tuberculosis Research and Treatment. Article ID 574591, 9 pages. doi:10.1155/2011/574591.
16. Gheorghiu M, Lagrange PH, Fillastre C, (1988) The stability and immunogenicity of a dispersed-grown freeze-dried Pasteur BCG vaccine. J Biol Stand 6: 15-26.
17. Koup RA, Safrit JT, Cao Y, Andrews CA, McLeo G, (1994) Temporal association of cellular immune responses with the initial control of viremia in primary human immunodeficiency virus type 1 syndrome. J Virol 68: 4650-4655.
18. Rowland-Jones SL, Dong T, Fowke KR, Kimani J, Krausa P, et al. (1998) Cytotoxic T cell responses to multiple conserved HIV epitopes in HIV-resistant prostitutes in Nairobi. J Clin Invest 102: 1758-1765.
19. Stover CK, de la Cruz VF, Fuerst TR, Burlein JE, Benson LA, et al. (1991) New use of BCG for recombinant vaccines. Nature 351: 456-460.
20. Aldovini A, Young RA, (1991) Humoral and cell-mediated immune responses to live recombinant BCG-HIV vaccines. Nature 351: 479-482.
21. Lagranderie M, Murray A, Gicquel B, Leclerc C, Gheorghiu M, (1993) Oral immunization with recombinant BCG induces cellular and humoral immune responses against the foreign antigen. Vaccine 11: 1283-1290.
22. Hanke T, McMichael AJ, (2000) Design and construction of an experimental HIV-1 vaccine for a year-2000 clinical trial in Kenya. Nat Med 6: 951-955.
23. Joseph J, Fernández-Lloris R, Pezzat E, Saubi N, Cardona PJ, et al. (2010) Molecular characterization of heterologous HIV-1gp120 gene expression disruption in Mycobacterium bovis BCG host strain: a critical issue for engineering mycobacterial based-vaccine vectors. J Biomed Biotechnol pp. 357370 doi: 10.1155/2010/357370.
24. Saubi N, Im EJ, Fernandez-Lloris R, Gil O, Cardona PJ, et al. (2011) Newborn mice vaccination with rBCG:HIVA+MVA:HIVA enhances HIV-1-specific immune responses. Influence of age and immunization routes. Clinical and Developmental Immunology 516219 doi: 10.1155/2011/516219.
25. Hopkins R, Bridgeman A, Joseph J, Gilbert S, McShane H, et al. (2011) Dual neonate vaccine platform against HIV-1 and tuberculosis. PLOs ONE 6: e20067 doi: 10.1371/journal.pone.0020067.
26. Andre S, Seed B, Eberle J, Schraut W, Bultmann A, et al. (1998) Increased immune response elicited by DNA vaccination with a synthetic gp120 sequence with optimized codon usage. J Virol 72: 1497-1503.
27. Andersson GE, Sharp PM, (1996) Codon usage in the Mycobacterium tuberculosis complex. Microbiology 142: 915-925.
28. Takahashi H, Cohen J, Hosmalin A, Cease KB, Houghten R, et al. (1988) An immunodominant epitope of the human immunodeficiency virus envelope glycoprotein gp160 recognized by class I major histocompatibility molecule-restricted murine cytotoxic T lymphocytes. Proc Natl Acad Sci USA 85: 3105-3109.
29. Stover CK, Bansal GP, Hanson MS, Burlein JE, Palaszynski SR, et al. (1993) Protective immunity elicited by recombinant bacille Calmette-Guerin (BCG) expressing outer surface protein A (OspA) lipoprotein: a candidate Lyme disease vaccine. J Exp Med 178: 197-209.
30. Williams SG, Cranenburgh RM, Weiss AME, Wrighton CJ, Sherratt DJ, et al. (1998) Repressor titration: A novel system for selection and maintenance of recombinant plasmids. Nucleic Acids Res 26: 2120-2124.
31. Cranenburgh RM, Hanak JAJ, Williams SG, Sherratt DJ, (2001) Escherichia coli strains that allow antibiotic-free plasmid selection and maintenance by repressor titration. Nucleic Acids Res 29: e26.
32. Cranenburgh RM, Lewis KS, Hanak JAJ, (2004) Effect of Plasmid Copy Number and lac Operator Sequence on Antibiotic-Free Plasmid Selection by Operator-Repressor Titration in Escherichia coli. J Mol Microbiol Biotechnol 7: 197-203 DOI: 10.1159/000079828.
33. Pavelka MS Jr, Jacobs WR Jr, (1999) Comparison of the construction of unmarked deletion mutations in Mycobacterium smegmatis, Mycobacterium bovis bacillus Calmette-Guerin, and Mycobacterium tuberculosis H37Rv by allelic exchange. J Bacteriol 181: 4780-4789.
34. Behr MA, Small PM, (1999) A historical and molecular phylogeny of BCG strains. Vaccine 17: 915-922.
35. Pan Y, Yang X, Duan J, Lu N, Leung AS, et al. (2011) Whole-genome sequences of four Mycobacterium bovis BCG vaccine strains. J Bacteriol 193: 3152-3153 doi: 10.1128/JB.00405-11.
36. Trovero A, Argüelles C, Cataldi A, (2010) Preparation of a working seed lot of BCG and quality control by PCR genotyping. Rev Argent Microbiol 42: 4-10.
37. Castillo-Rodal AI, Castañón-Arreola M, Hernández-Pando R, Calva JJ, Sada-Díaz E, (2006) Mycobacterium bovis BCG substrains confer different levels of protection against Mycobacterium tuberculosis infection in a BALB/c model of progressive pulmonary tuberculosis. Infect Immun 74: 1718-1724 doi: 10.1128/IAI.74.3.1718-1724.2006.
38. Bedwell J, Kairo SK, Behr MA, Bygraves JA, (2001) Identification of substrains of BCG vaccine using multiplex PCR. Vaccine 19: 2146-2151.
39. Section 5.2.6, European Pharmacopoeia, 7th Edition (2010) Online Version, Published by the Council of Europe, 2010.
40. van Soolingen D, Hoogenboezem T, de Haas PE, Hermans PW, Koedam MA, (1997) A novel pathogenic taxon of the Mycobacterium tuberculosis complex, Canetti: characterization of an exceptional isolate from Africa. Int J Syst Bacteriol 147: 1236-1245.
41. Kasai H, Watanabe K, Gasteiger E, Bairoch A, Isono K, (1998) Construction of the gyrB Database for the Identification and Classification of Bacteria. Genome Inform Ser Workshop Genome Inform 9: 13-21.
42. Liébana E, Aranaz A, Francis B, Cousins D, (1996) Assessment of genetic markers for species differentiation within the Mycobacterium tuberculosis complex. J Clin Microbiol 34: 933-938.
43. Niemann S, Kubica T, Bange FC, Adjei O, Browne EN, et al. (2004) The species Mycobacterium africanum in the light of new molecular markers. J Clin Microbiol 42: 3958-3962.
44. Talbot EA, Williams DL, Frothingham R, (1997) PCR identification of Mycobacterium bovis BCG. J Clin Microbiol 35: 566-569.
45. Niemann S, Harmsen D, Rüsch-Gerdes S, Richter E, (2000) Differentiation of clinical Mycobacterium tuberculosis complex isolates by gyrB DNA sequence polymorphism analysis. J Clin Microbiol 38: 3231-3234.
46. Richter E, Weizenegger M, Rüsch-Gerdes S, Niemann S, (2003) Evaluation of genotype MTBC assay for differentiation of clinical Mycobacterium tuberculosis complex isolates. J Clin Microbiol 41: 2672-2675.
47. Cole ST, Brosch R, Parkhill J, Garnier T, Churcher C, et al. (1998) Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature. 393: 537-544. Erratum (1998) Nature 396: 190.
48. Behr MA, Wilson MA, Gill WP, Salamon H, Schoolnik GK, et al. (1999) Comparative genomics of BCG vaccines by whole-genome DNA microarray. Science 284: 1520-1523.
49. Magdalena J, Supply P, Locht C, (1998) Specific differentiation between Mycobacterium bovis BCG and virulent strains of the Mycobacterium tuberculosis complex. J Clin Microbiol 36: 2471-2476.
50. Chege GK, Thomas R, Shephard EG, Meyers A, Bourn W, et al. (2009) 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 27: 4857-4866 doi: 10.1016/j.vaccine.2009.05.064.
51. Cayabyab MJ, Hovav AH, Hsu T, Krivulka GR, Lifton MA, et al. (2006) Generation of CD8+ T-cell responses by a recombinant nonpathogenic Mycobacterium smegmatis vaccine vector expressing human immunodeficiency virus type 1 Env. J Virol 80: 1645-1652 doi: 10.1128/JVI.80.4.1645-1652.2006.
52. Honda M, Matsuo K, Nakasone T, Okamoto Y, Yoshizaki H, et al. (1995) 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 92: 10693-10697.
53. Ami Y, Izumi Y, Matsuo K, Someya K, Kanekiyo M, (2005) 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 79: 12871-12879 doi: 10.1128/JVI.79.20.12871-12879.2005.
54. Cayabyab MJ, Korioth-Schmitz B, Sun Y, Carville A, Balachandran H, et al. (2009) Recombinant Mycobacterium bovis BCG prime-recombinant adenovirus boost vaccination in rhesus monkeys elicits robust polyfunctional simian immunodeficiency virus-specific T-cell responses. J Virol 83: 5505-5513, 2009 doi: 10.1128/JVI.02544-08.
55. Vordermeier HM, Villarreal-Ramos B, Cockle PJ, McAulay M, Rhodes SG, et al. (2009) "Viral booster vaccines improve Mycobacterium bovis BCG-induced protection against bovine tuberculosis. Infect Immun 77: 3364-3373 doi: 10.1128/IAI.00287-09.
56. McShane H, Pathan AA, Sander CR, Keating SM, Gilbert SC, et al. (2004) Recombinant modified vaccinia virus Ankara expressing antigen 85A boosts BCG-primed and naturally acquired antimycobacterial immunity in humans. Nat Med 10: 1240-1244 doi:10.1038/nm1128.
57. Hovav AH, Panas MW, Osuna CE, Cayabyab MJ, Autissier P, et al. (2007) The impact of a boosting immunogen on the differentiation of secondary memory CD8+ T cells. J Virol 81: 12793-12802 doi: 10.1128/JVI.01519-07.
58. Hopkins R, Bridgeman A, Bourne C, Mbewe-Mvula A, Sadoff JC, et al. (2011) Optimizing HIV-1-specific CD8+ T-cell induction by recombinant BCG in prime-boost regimens with heterologous viral vectors. Eur J Immunol 41: 3542-3552 doi: 10.1002/eji.201141962.
59. Rosario M, Fulkerson J, Soneji S, Parker J, Im EJ, et al. (2010) Safety and immunogenicity of novel recombinant BCG and modified vaccinia virus Ankara vaccines in neonate rhesus macaques. J Virol 84: 7815-7821 doi: 10.1128/JVI.00726-10.
60. Ota MO, Vekemans J, Schlegel-Haueter SE, Fielding K, Sanneh M, et al. (2002) Influence of Mycobacterium bovis bacillus Calmette-Guérin on antibody and cytokine responses to human neonatal vaccination. J Immunol 168: 919-925.
61. Marchant A, Goetghebuer T, Ota MO, Wolfe I, Ceesay SJ, et al. (1999) Newborns develop a Th1-type Immune response to Mycobacterium bovis bacillus Calmette-Guérin vaccination. J Immunol 163: 2249-2255.
62. Létourneau S, Im EJ, Mashishi T, Brereton C, Bridgeman A, et al. (2007) Design and pre-clinical evaluation of a universal HIV-1 vaccine. PLoS One 2: e984 doi: 10.1371/journal.pone.0000984.