The use of live attenuated bacteria as a delivery system for heterologous antigens

Journal of Drug Targeting

Volumn 11, Issue 8-10, 2003, Pages 471-479

  Garmory, Helen S ^a   Leary, Sophie E C ^a   Griffin, Kate F ^a   Williamson, E Diane ^a   Brown, Katherine A ^b   Titball, Richard W ^a,c  

^a DEFENCE SCIENCE AND TECHNOLOGY LABORATORY   (United Kingdom)

^b IMPERIAL COLLEGE LONDON   (United Kingdom)

^c LONDON SCHOOL OF HYGIENE AND TROPICAL MEDICINE   (United Kingdom)

Author keywords

Attenuated bacteria; Heterologous antigen; V antigen; Vaccine; Yersinia pestis

Indexed keywords

BACTERIAL ANTIGEN; BACTERIAL VACCINE; BCG VACCINE; PLAGUE VACCINE; TETANUS TOXOID; TYPHOID VACCINE;

ANTIBODY RESPONSE; ANTIGEN EXPRESSION; ANTIGEN PRESENTING CELL; BACTERIAL INFECTION; DRUG DELIVERY SYSTEM; DRUG RESPONSE; DRUG SAFETY; DRUG STABILITY; HUMAN; IMMUNE RESPONSE; IMMUNOGENICITY; NONHUMAN; PLAGUE; PRIORITY JOURNAL; REVIEW; SALMONELLA ENTERICA; TH1 CELL; TH2 CELL; YERSINIA PESTIS;

ANIMALS; ANTIGENS, BACTERIAL; ANTIGENS, HETEROPHILE; BACTERIAL VACCINES; HUMANS; MOUTH MUCOSA; MUCOUS MEMBRANE; PORE FORMING CYTOTOXIC PROTEINS; VACCINES, ATTENUATED; VACCINES, DNA; YERSINIA PESTIS;

EID: 1942443155     PISSN: 1061186X     EISSN: None     Source Type: Journal    
DOI: 10.1080/10611860410001670008     Document Type: Review

References (76)

1. Alexander, J.E., Andrew, P., Jones, D. and Roberts, I.S. (1993) "Characterization of an aromatic amino acid-dependant Listeria monocytogenes mutant: attenuation, persistence and ability to produce protective immunity in mice", Infect. Immun. 61, 2245-2248.
2. Altboum, Z., Barry, E.M., Losonsky, G., Galen, J.E. and Levine, M.M. (2001) "Attenuated Shigella flexneri 2a Delta guaBA strain CVD 1204 expressing enterotoxigenic Escherichia coli (ETEC) CS2 and CS3 fimbrae as a live mucosal vaccine against Shigella and ETEC infecion", Infect. Immun. 69, 3150-3158.
3. Altboum, Z., Levine, M.M., Galen, J.E. and Barry, E.M. (2003) "Genetic characterization and immunogenicity of coli surface antigen 4 from enterotoxigenic Escherichia coli when it is expressed in a Shigella live-vector strain", Infect. Immun. 71, 1352-1360.
4. Alvarez-Dominguez, C., Roberts, R. and Stahl, P.D. (1997) "Internalized Listeria monocytogenes modulates intracellular trafficking and delays maturation of the phagosome", J. Cell. Sci. 110, 731-743.
5. Anderson, G.W., Jr., Leary, S.E.C., Williamson, E.D., Titball, R.W., Welkos, S.L., Worsham, P.L. and Friedlander, A.M. (1996) "Recombinant V antigen protects mice against pneumonic and bubonic plague caused by F1-capsule-positive and -negative strains of Y. pestis", Infect. Immun. 64, 4580-4585.
6. Barry, E.M., Gomez-Duarte, O., Chatfield, S., Rappuoli, R., Pizza, M., Losonsky, G., Galen, J. and Levine, M.M. (1996) " Expression and immunogenicity of pertussis toxin S1 subunit-tetanus toxin fragment C fusions in Salmonella typhi vaccine strain CVD 908", Infect. Immun. 64, 4172-4181.
7. Bowe, F., O'Gaora, P., Maskell, D., Cafferkey, M. and Dougan, G. (1989) "Virulence, persistence, and immunogenicity of Yersinia enterocolitica O:8 aroA mutants", Infect. Immun. 57, 3234-3236.
8. Buchmeier, N., Blanc-Potard, A., Ehrt, S., Piddington, D., Riley, L. and Groisman, E.A. (2000) "A parallel intraphagosomal survival strategy shared by Mycobacterium tuberculosis and Salmonella enterica", Mol. Microbiol. 35, 1375-1382.
9. + for all three chromosomally located systems of DNA restriction and modification", J. Bacteriol. 156, 471-474.
10. Bullifent, H.L., Griffin, K.F., Jones, S.M., Yates, A., Harrington, L. and Titball, R.W. (2000) "Antibody responses to Yersinia pestis F1-antigen expressed in Salmonella typhimurium aroA from in vivo-inducible promoters", Vaccine 66, 3080-3087.
11. Cersini, A., Salvia, A.M. and Bernardini, M.L. (1998) "Intracellular multiplication and virulence of Shigella flexneri auxotrophic mutants", Infect. Immun. 66, 549-557.
12. Charbit, A., Marineau, P., Ronco, J., Leclerc, C., Lo-Man, R., Michel, V., O'Callaghan, D. and Hofnung, M. (1993) "Expression and immunogenicity of the V3 loop from the envelope of human immunodeficiency virus type 1 in an attenuated aroA strain of Salmonella typhimurium upon genetic coupling of two Escherichia coli carrier proteins", Vaccine 11, 1221-1228.
13. Chatfield, S.N., Charles, I.G., Makoff, A.J., Oxer, M.D., Dougan, G., Pickard, D., Slater, D. and Fairweather, N. (1992) "Use of the nirB promoter to direct stable expression of heterologous antigens in Salmonella oral vaccine strains: development of a single dose oral tetanus vaccine", BioTechnology 10, 888-892.
14. Chen, H. and Schifferli, D.M. (2000) "Mucosal and systemic immune responses to chimeric fimbriae expressed by Salmonella enterica serovar Typhimurium vaccine strains", Infect. Immun. 68, 3129-3139.
15. Chen, I., Finn, T.M., Yanqing, L., Guoming, Q., Rappuoh, R. and Pizza, M. (1998) "A recombinant live attenuated strain of Vibrio cholerae induces immunity against tetanus toxin and Bordatella pertussis tracheal colonization factor", Infect. Immun. 66, 1648-1653.
16. Corchero, J.L. and Villaverde, A. (1998) "Plasmid maintenance in Escherichia coli recombinant cultures is dramatically, steadily, and specifically influenced by features of the encoded proteins", Biotechnol. Bioeng. 58, 625-632.
17. Covone, M.G., Brocchi, M., Palla, M., Dias Da Silveira, E., Rappuoli, W. and Galeotti, C.L. (1998) "Levels of expression and immunogenicity of attenuated Salmonella enterica serovar Typhimurium strains expressing Escherichia coli mutant heat-labile enterotoxin", Infect. Immun. 66, 2Z4-231.
18. Dorrell, N., Li, S.-R., Everest, P., Dougan, G. and Wren, B.W. (1998) "Construction and characterisation of a Yersinia enterocolitica O:8 ompR mutant", FEMS Microbiol. Lett. 165, 145-151.
19. Dougan, G., Maskell, D., Pickard, D. and Hormaeche, C.E. (1997) "Isolation of stable aroA mutants of Salmonella typhi Ty2: properties and preliminary characterization in mice", Mol. Gen. Genet. 207, 402-407.
20. Dunstan, S.J., Simmons, C.P. and Strugnell, R.A. (1999) "Use of in vivo-regulated promoters to deliver antigens from attenuated Salmonella enterica var. Typhimurium", Infect. Immun. 67, 5133-5141.
21. Everest, P., Frankel, G., Li, J., Lund, P., Chatfield, S. and Dougan, G. (1995) "Expression of LacZ from the htrA, nirB and groE promoters in a Salmonella vaccine strain: influence of growth in mammalian cells", FEMS Microbiol. Lett. 126, 97-102.
22. Fontana, M.R., Monaci, E., Yanqing, L., Guoming, Q., Duan, G., Rappuoli, R. and Pizza, M. (2000) "IEM101, a naturally attenuated Vibrio cholerae strain as carrier for genetically detoxified derivatives of cholera toxin", Vaccine 19, 75-85.
23. Fouts, T.R., Tuskan, R.G., Chada, S., Hone, D.M. and Lewis, G.K. (1995a) "Construction and immunogenicity of Salmonella typhimurium vaccine vectors that express HIV-1 gp120", Vaccine 13, 1697-1705.
24. Fouts, T.R., Lewis, G.K. and Hone, D.M. (1995b) "Construction and characterization of a Salmonella typhi-based human immunodeficiency virus type 1 vector vaccine", Vaccine 13, 561-569.
25. c fragment", Vaccine 21, 1052-1059.
26. Francis, M.J., Hastings, G.Z., Syred, A.D., McGinn, B., Brown, F. and Rowlands, D.J. (1987) "Nonresponsiveness to a foot-and-mouth disease virus peptide overcome by addition of foreign helper T cell determinants", Nature 330, 168-170.
27. Galen, J.E. and Levine, M.M. (2001) "Can a "flawless" live vector vaccine strain be engineered?", Trends Microbiol. 9, 372-376.
28. Galen, J.E., Nair, J., Wang, J.Y., Wasserman, S.S., Tanner, M.K., Sztein, M.B. and Levine, M.M. (1999) "Optimization of plasmid maintenance in the attenuated live vaccine vector strain Salmonella typhi CVD 908-htrA", Infect. Immun. 67, 6424-6433.
29. Garmory, H.S., Brown, K.A. and Titball, R.W. (2002) "Salmonella vaccines for use in humans: present and future perspectives", FEMS Microbiol. Rev. 26, 339-353.
30. Garmory, H.S., Griffin, K.F., Brown, K.A. and Titball, R.W. (2003) "Oral immunisation with live aroA attenuated Salmonella enteica serovar Typhimurium expressing the Yersinia pestis V antigen protects mice against plague", Vaccine 21, 3051-3057.
31. Gentschev, I., Dietrich, G., Mollenkopf, H.-J., Sokolovic, Z., Hess, J., Kaufmann, S.H.E. and Goebel, W. (1997) "The Escherichia coli hemolysin secretion apparatus - a versatile antigen delivery system in attenuated Salmonella", Behring Inst. Mitt. 98, 103-113.
32. Gentschev, I., Glaser, I., Goebel, W., McKeever, D.J., Musoke, A. and Heussler, V.T. (1998) "Delivery of the p67 sporozoite antigen of Theileria parva by using recombinant Salmonella Dublin: secretion of the product enhances specific antibody responses in cattle", Infect. Immun. 66, 2060-2064.
33. Germanier, R. and Fuer, E. (1975) "Isolation and characterization of Gal E mutant Ty21a of Salmonella typhi: a candidate strain for a live, oral typhoid vaccine", J. Infect. Dis. 18, 609-620.
34. Gomez-Duarte, O.G., Galen, J., Chattfield, S.N., Rappuoli, R., Eidels, L. and Levine, M.M. (1995) "Expression of fragment C of tetanus toxin fused to a carboxyl-terminal fragment of diptheria toxin in Salmonella typhi CVD908 vaccine strain", Vaccine 13, 1596-1602.
35. Guérin, C. (1957) The History of BCG. BCG Vaccination Against Tuberculosis (Little, Brown and Company, Boston, MA), pp 48-53.
36. Gupta, R.K., Chang, A.-C. and Siber, G.R. (1998) "Biodegradable polymer microspheres as vaccine adjuvants and delivery systems", Dev. Biol. Stand. 92, 63-78.
37. Hess, J., Gentschev, I., Gentschev, I., Miko, D., Welzel, M., Ladel, C., Goebel, W. and Kaufmann, S.H.E. (1996) "Superior efficacy of secreted over somatic antigen display in recombinant Salmonella vaccine induced protection against listeriosis", Proc. Natl Acad. Sci. USA 93, 1458-1463.
38. Hess, J., Dietrich, G., Genschev, I., Miko, D., Goebel, W. and Kaufmann, S.H.E. (1997) "Protection against murine listeriosis by an attenuated recombinant Salmonella vaccine strain that secretes the naturally somatic antigen superoxide dismutase", Infect. Immun. 65, 1286-1292.
39. Hess, J., Grode, L., Hellwig, P., Conradt, I., Gentschev, I., Goebel, W., Ladel, C. and Kaufmann, S.H.E. (2000) "Protection against murine tuberculosis by an attenuated recombinant Salmonella typhimurium vaccine strain that secretes the 30-kDa antigen of Mycobacterium bovis BCG", FEMS Immunol. Med. Microbiol. 27, 283-289.
40. Hill, J., Leary, S.E.C., Griffin, K.F., Williamson, E.D. and Titball, R.W. (1997) "Regions of Yersinia pestis V antigen that contribute to protection against plague identified by passive and active immunization", Infect. Immun. 65, 4476-4482.
41. Hohmann, E.L., Oletta, C.A., Loomis, W.P. and Miller, S.I. (1995) "Macrophage-inducible expression of a model antigen in Salmonella typhimurium enhances immunogenicity", Proc. Natl Acad. Sci. USA 92, 2904-2908.
42. Hohmann, E.L., Oletta, C.A., Killeen, K.P. and Miller, S.I. (1996) "phoP/phoQ-deleted Salmonella typhi (Ty800) is a safe and immunogenic sungle-dose typhoid fever vaccine in volunteers", J. Infect. Dis. 173, 1408-1414.
43. Hone, D.M., Shata, M.T., Pascual, D.W. and Lewis, G.K. (1999) "Mucosal vaccination with Salmonella vaccine vectors. Intracellular bacterial vaccine vectors: immunology, cell biology and genetics", (John Wiley and Sons, London), pp 122-171.
44. Hosieth, S.K. and Stocker, B.A.D. (1981) "Aromatic-dependant Salmonella typhimurium are non-virulent and effective as live vaccines", Nature 291, 238-239.
45. Johnson, K., Charles, I., Dougan, G., O'Gaora, P., Costa, G., Ali, T., Miller, I. and Hormaeche, C. (1991) "The role of a stress-response protein in Salmonella typhimurium virulence", Mol. Microbiol. 5, 401-407.
46. Khan, C.M., Villarreal-Ramos, B., Pierce, R.J., Demarco de Hormaeche, R., MvNeill, H., Chatfield, S., Capron, A., Dougan, G. and Hormeache, C.E. (1994) "Construction, expression and immunogenicity of multiple tandem copies of the Schistosoma mansoni peptide 115-131 of the P28 glutathione S-transferase expressed as C-terminal fusions to tetanus toxin fragment C in a live Aro attenuated vaccine strain of Salmonella", J. Immunol. 153, 5634-5642.
47. Lawton, D.G., Longstaff, C., Wallace, B.M., Hill, J., Leary, S.E.C., Titball, R.W. and Brown, K.A. (2002) "Interactions of the type III secretory pathway proteins LcrV and LcrG from Yersinia pestis are mediated by coiled-coil domains", J. Biol. Chem. 277, 38714-38722.
48. Leary, S.E.C., Williamson, E.D., Griffin, K.F., Russell, P., Eley, S.M. and Titball, R.W. (1995) "Active immunization with recombinant V antigen from Yersinia pestis protects mice against plague", Infect. Immun. 63, 2854-2858.
49. Leclerc, C., Charbit, A., Martineau, P., Deriaud, E. and Hofnung, M. (1991) "The cellular location of a foreign B cell epitope expressed by recombinant bacteria determines its T cell-dependant or T cell-independent characteristics", J. Immunol. 147, 3545-3552.
50. Lee, J.J., Sinha, K.A., Harrison, J.A., Demarco de Hormaeche, R., Riveau, G., Pierce, R.J., Capron, A., Wilson, R.A. and Khan, C.M.A. (2000) "Tetanus toxin fragment C expressed in live Salmonella vaccines enhances antibody responses to its fusion partner Schistosoma haematobium glutathione S-transferase", Infect. Immun. 68, 2503-2512.
51. Lee, E., Platt, R., Kang, S., Roth, J.A. and Phillips, G.J. (2001) "Chromosomal integration and expression of the Escherichia coli K88 gene cluster in Salmonella enterica ser. Cholerasuis strain 54 (SC54)", Vet. Microbiol. 83, 177-183.
52. Londono-Arcila, P., Freeman, D., Kleanthous, H., O'Dowd, A.M., Lewis, S., Turner, A.K., Rees, E.L., Tibbitts, T.J., Greenwood, J., Monath, T.P. and Darsley, M.J. (2002) "Attenuated Salmonella enterica serovar Typhi expressing urease effectively immunizes mice against Helicobacter pylori challenge as part of a heterologous mucosal priming-parenteral boosting vaccination regimen", Infect. Immun. 70, 5096-5106.
53. McNeill, H.V., Sinha, K.A., Hormaeche, C.E., Lee, J.J. and Khan, C.M.A. (2000) "Development of a nonantibiotic marker for positively selecting expression plasmids in multivalent Salmonella vaccines", Appl. Environ. Microbiol. 66, 1216-1219.
54. McSorely, S.J., Xu, D. and Liew, F.Y. (1997) "Vaccine efficacy of Salmonella strains expressing glycoprotein 63 with different promoters", Infect. Immun. 65, 171-178.
55. Medina, S.I. and Guzman, C.A. (2000) "Modulation of immune responses following antigen administration by mucosal route", FEMS Immunol. Med. Microbiol. 22, 305-311.
56. Mielcarek, N., Alonso, S. and Locht, C. (2001) "Nasal vaccination using live bacterial vectors", Adv. Drug Deliv. Rev. 51, 55-69.
57. Molina, N.C. and Parker, C.D. (1990) "Murine antibody responses to oral infection with live aroA recombinant Salmonella dublin vaccine strains expressing filamentous hemagglutinin antigen from Bordatella pertussis", Infect. Immun. 58, 2523-2528.
58. Mollenkopf, H., Dietrich, G. and Kaufmann, S.H.E. (2001) "Intracellular bacteria as targets and carriers for vaccination", Biol. Chem. 382, 521-532.
59. + expression cloning vector: stable maintenance and high level expression of cloned genes in a Salmonella vaccine strain", BioTechnology 6, 693-697.
60. O'Gaora, P., Roberts, M., Bowe, F., Hormaeche, C., Demarco de Hormaeche, R., Cafferkey, M., Tite, J. and Dougan, G. (1989) " Cloning and characterisation of the serC and aroA genes of Yersinia enterocolitica, and construction of an aroA mutant", Gene 84, 23-30.
61. Parish, T. and Stoker, N.G. (2002) "The common aromatic amino acid biosynthesis pathway is essential in Mycobacterium tuberculosis", Microbiology 148, 1077-3069.
62. Roberts, M., Maskell, D., Novotny, P. and Dougan, G. (1990) "Construction and characterization in vivo of Bordatella pertussis aroA mutants", Infect. Immun. 58, 732-739.
63. Roberts, M., Li, J., Bacon, M. and Chatfield, S. (1998) "Oral vaccination against tetanus: comparison of the immunogenicities of Salmonella strains expressing fragment C from the nirB and htrA promoters", Infect. Immun. 66, 3080-3087.
64. Russmann, H., Shams, H., Poblete, F., Fu, Y., Galan, J.E. and Donis, R.O. (1998) "Delivery of epitopes by the Salmonella type III secretion system for vaccine development", Science 281, 565-568.
65. Ryan, E.T., Butterton, J.R., Zhang, T., Baker, M.A., Stanley, S.L.J. and Calderwood, S.B. (1997) "Oral immunization with attenuated vaccine strains of Vibrio cholerae expressing a dodecapeptide repeat of the serine-rich Entamoeba histolytica protein fused to the choler toxin B subunit induces systemic and mucosal antiamebic and anti-V. cholerae antibody responses in mice", Infect. Immun. 65, 3118-3125.
66. Ryan, E.T., Crean, T.I., Kochi, S.M., John, M., Luciano, A., Killeen, K.P., Klose, K.E. and Balderwood, S.B. (2000) "Development of a ΔglnA balance lethal plasmid system for expression of heterologous antigens by attenuated vaccine vector strains of Vibrio cholerae", Infect. Immun. 68, 221-226.
67. Schodel, F., Kelly, S.M., Peterson, D.L., Milich, D.R. and Curtiss, R. III, (1994) "Hybrid hepatitis B virus core-pre-S proteins synthesized in avirulent Salmonella typhimurium and Salmonella typhi for oral vaccination", Infect. Immun. 62, 1669-1676.
68. Stevenson, A. and Roberts, M. (2002) "Use of a rationally attenuated Bordatella bronchiseptica as a live mucosal vaccine and vector for heterologous antigens", Vaccine 20, 2325-2335.
69. Strugnell, R., Dougan, G., Chatfield, S., Charles, I., Fairweather, N., Tite, J., Li, J., Beesley, J. and Roberts, M. (1992) "Characterization of a Salmonella typhimurium aro vaccine strain expressing the P.69 antigen of Bordatella pertussis", Infect. Immun. 60, 3994-4002.
70. Tacket, C.O., Sztein, M.B., Losonsky, G.A., Wasserman, S.S., Nataro, P., Edelman, R., Pickard, D., Dougan, G., Chatfield, S.N. and Levine, M.M. (1997a) "Safety of live oral Salmonella typhi vaccine strains with deletions in htrA and aroC aroD and immune response in humans", Infect. Immun. 65, 452-456.
71. Tacket, C.O., Kelly, S.M., Schödel, F., Losonsky, G., Nataro, J.P., Edelman, R., Levine, M.M. and Curtiss, R. III (1997b) "Safety and immunogenicity in humans of an attenuated Salmonella typhi vaccine vector strain expressing plasmid-encoded hepatitis B antigens stabilized by the asd-balanced lethal vector system", Infect. Immun. 65, 3381-3385.
72. Tacket, C.O., Sztein, M.B., Wasserman, S.S., Losonsky, G., Kotloff, K.L., Wyant, T.L., Nataro, J.P., Edelman, R., Perry, J., Bergman, P., Brown, D., Chatfield, S., Dougan, G. and Levine, M.M. (2000) "Phase 2 clinical trial of attenuated Salmonella enterica serovar Typhi oral live vector vaccine CVD 908-htrA in U.S. volunteers", Infect. Immun. 68, 1196-1201.
73. Thole, J.E.R., van Dalen, P.J., Havenith, C.E.G., Pouwels, P.H., Seegers, J.F.M.L., Tielen, F.D., van der Zee, M.D., Zegers, N.D. and Shaw, M. (2000) "Live bacterial delivery systems for development of mucosal vaccines", Curr. Opin. Mol. Ther. 2, 94-99.
74. Wassef, N.M., Alving, C.R. and Richards, R.L. (1994) "Liposomes as carriers for vaccines", Immunomethods 4, 217-222.
75. Whittle, B.L., Lee, E., Weir, R.C. and Verma, N.K. (1997) "Immune response to a Murray Valley encephalitis virus epitope expressed in the flagellin of an attenuated strain of Salmonella", J. Med. Microbiol. 46, 129-138.
76. Williamson, E.D., Eley, S.M., Griffin, K.F., Green, M., Russell, P., Leary, S.E.C., Oyston, P.C.F., Easterbrook, T., Reddin, K.F., Robinson, A. and Titball, R.W. (1995) "A new improved sub-unit vaccine for plague: the basis of protection", FEMS Immunol. Med. Microbiol. 12, 223-230.