Hostname: page-component-78c5997874-s2hrs Total loading time: 0 Render date: 2024-11-15T18:11:58.309Z Has data issue: false hasContentIssue false
  • English
  • Français

The development of oral vaccines against parasitic diseases utilizing live attenuated Salmonella

Published online by Cambridge University Press:  06 April 2009

S. N. Chatfield ,
M. Roberts ,
G. Dougan ,
C. Hormaeche  and
C. M. A. Khan
S. N. Chatfield*
Affiliation:
Medeva Vaccine Research Unit, Imperial College of Science Technology and Medicine, Exhibition Road, London, SW7 2AY, UK
M. Roberts
Affiliation:
Medeva Vaccine Research Unit, Imperial College of Science Technology and Medicine, Exhibition Road, London, SW7 2AY, UK
G. Dougan
Affiliation:
Department of Biochemistry, Imperial College of Science Technology and Medicine, Exhibition Road, London, SW7 2AY, UK
C. Hormaeche
Affiliation:
Department of Microbiology, The Medical School, University of Newcastle, Framlington Place, Newcastle-upon-Tyne, NE2 4HH, UK
C. M. A. Khan
Affiliation:
Department of Microbiology, The Medical School, University of Newcastle, Framlington Place, Newcastle-upon-Tyne, NE2 4HH, UK
*
* Corresponding author.
Get access Rights & Permissions [Opens in a new window]

Summary

Genetically defined, live attenuated Salmonella vaccines are proving useful both as oral vaccines against salmonellosis and for the development of multivalent vaccines based on the expression of heterologous antigens in such strains. Several candidate attenuated S. typhi strains are at present being evaluated as new single dose oral typhoid vaccines in human volunteers. The emergence of such a vaccine will facilitate the development of multivalent vaccines for humans. Many antigens from different infectious organisms have been expressed in attenuated Salmonella. A focus of this work has been on developing vaccines against parasitic diseases. This review will summarize the efforts that have been made in this area.

Keywords

Live attenuated SalmonellaOral vaccinesSchistosomiasis
Type
Research Article
Information
Parasitology , Volume 110 , Supplement S1: Symposia of the British Society for Parasitology Volume 32:Parasite vaccines , March 1995 , pp. S17 - S24
Copyright
Copyright © Cambridge University Press 1995

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Auriault, C., Gras-Masse, H., Wolowczuk, I., Pierce, R. J., Balloul, J. M., Neyrinck, J. L., Drobecq, H., Tartar, A. & Capron, A. (1988). Analysis of T and B cell epitopes of the Schisotoma mansoni P28 antigen in the rat model by using synthetic peptides. Journal of Immunology 141, 1687–94.CrossRefGoogle Scholar
Balloul, J. M., Grzych, J. M., Pierce, R. J. & Capron, A. (1987 a). A purified 28,000 dalton protein from Schistosoma mansoni adult worms protects rats and mice against experimental schisotomiasis. Journal of Immunology 138, 3448–53.CrossRefGoogle Scholar
Balloul, J. M., Sondermyer, P., Dreyer, D., Capron, M., Grzych, J. M., Pierce, R. J., Carvallo, D., Lecocq, J. P. & Capron, A. (1987 b). Molecular cloning of a protective antigen from schistosomes. Nature 326, 149–53.CrossRefGoogle ScholarPubMed
Broekhuijsen, M. P., Van Rijn, J. M. M., Blom, A. J. M., Pouwels, P. H., Enger-Valk, B. E., Brown, F. & Francis, M. (1987). Fusions proteins with multiple copies of the major antigenic determinant of foot-and-mouth disease protect both the natural host and laboratory animals. Journal of General Virology 68, 3137–43.CrossRefGoogle ScholarPubMed
Brown, A., Hormaeche, C. E., Demarco de Hormaeche, R., Winther, M., Dougan, G., Maskell, D. J. & Stocker, B. A. D. (1987). An attenuated aroA Salmonella typhimurium vaccine elicits humoral and cellular immunity to cloned b-galactosidase in mice. Journal of Infectious Diseases 155, 86–92.CrossRefGoogle Scholar
Bushara, H. O., Bashir, M. E. N., Malik, K. H. E., Mukhtar, M. M., Trottein, F., Capron, A. & Taylor, M. G. (1993). Suppression of Schistosoma bovis egg production in cattle by vaccination with either glutathione S-transferase or keyhole limpet haemocyanin. Journal of Parasite Immunology 15, 383–90.CrossRefGoogle ScholarPubMed
Chatfield, S., Li, J. L., Sydenham, M., Douce, G. & Dougan, G. (1992 c). Salmonella genetics and vaccine development. In Molecular Biology of Bacterial Infection: Current Status and Future Perspectives (ed. Hormaeche, C., Penn, C. & Smythe, C.), pp. 299–312. Society for General Microbiology Symposium, Cambridge, Cambridge University Press.Google Scholar
Chatfield, S., Roberts, M., Londono, P., Cropley, I., Douce, C. & Dougan, G. (1993). The development of oral vaccines based on live attenuated Salmonella strains. FEMS Immunology and Medical Microbiology 7, 1–8.CrossRefGoogle ScholarPubMed
Chatfield, S. N., Charles, I. G., Makoff, A. J., Oxer, M. D., Dougan, G., Pickard, D., Slater, D. & Fairweather, N. F. (1992 d). Use of the nirB promoter to direct the stable expression of heterologous antigens in Salmonella oral vaccine strains: development of a single-dose oral tetanus vaccine. BioTechnology 10, 888–92.Google ScholarPubMed
Chatfield, S. N., Dorman, C. J., Hayward, C. & Dougan, G. (1991). Role of ompR-dependent genes in Salmonella typhimurium virulence: mutants deficient in both ompC and ompF are attenuated in vivo. Infection and Immunity 59, 449–52.CrossRefGoogle ScholarPubMed
Chatfield, S. N., Fairweather, N. F., Charles, I., Pickard, D., Levine, M., Hone, D., Posada, M., Strugnell, R. A. & Dougan, G. (1992 a). Construction of a genetically defined Salmonella typhi Ty2 aroA, aroC mutant for the engineering of a candidate oral typhoid-tetanus vaccine. Infection and Immunity 10, 53–60.Google ScholarPubMed
Chatfield, S. N., Strahan, K., Pickard, D., Charles, I. G., Hormaeche, C. E. & Dougan, G. (1992 b). Evaluation of Salmonella typhimurium strains harbouring defined mutations in htrA and aroA in the murine salmonellosis model. Microbial Pathogenesis 12, 145–51.CrossRefGoogle ScholarPubMed
Chatfield, S. N., Strugnell, R. A. & Dougan, G. (1989). Live Salmonella as vaccines and carriers of foreign antigenic determinants. Vaccine 7, 495–8.CrossRefGoogle ScholarPubMed
Collins, F. M. (1974). Vaccines and cell-mediated immunity. Bacterial Reviews 38, 371–402.CrossRefGoogle ScholarPubMed
Cooper, G. L., Venables, L. M., Nicholas, R. A., Cullen, G. A. & Hormaeche, C. E. (1992). Vaccination of chickens with chicken-derived Salmonella enteritidis phage type 4 aroA live oral Salmonella vaccines. Vaccine 10, 247–54.CrossRefGoogle ScholarPubMed
Curtiss, R. III., & Kelly, S. M. (1987). Salmonella typhimurium deletion mutants lacking adenylate cyclase and cyclic AMP receptor protein are avirulent and immunogenic. Infection and Immunity 55, 3035–43.CrossRefGoogle ScholarPubMed
Dorman, C. J., Chatfield, S., Higgins, C. F., Hayward, C. & Dougan, G. (1989). Characterisation of porin and ompR mutants of a virulent strain of Salmonella typhimurium: ompR mutants are attenuated in vivo. Infection and Immunity 57, 2136–40.CrossRefGoogle ScholarPubMed
Dougan, G., Chatfield, S., Pickard, D., Bester, J., O'Callaghan, D. & Maskell, D. (1988). Construction and characterisation of vaccine strains of salmonella harbouring mutations in two different aro genes. Journal of Infectious Diseases 158, 1329–35.CrossRefGoogle ScholarPubMed
Dougan, G., Smith, L. & Heffron, F. (1989). Live bacterial vaccines and their application as carriers for foreign antigens. In Advances in Veterinary Science and Comparative Medicine, pp. 271–300. Orlando, Florida: Academic Press.Google Scholar
Flynn, J. L., Weiss, W. R., Norris, K. A., Seifert, H. S., Kumar, S. & So, M. (1990). Generation of cytotoxin T-lymphocyte response using a Salmonella antigen-delivery system. Molecular Microbiology 4, 2111–18.CrossRefGoogle Scholar
Galan, J. E. & Curtiss, R. I. (1989). Virulence and vaccine potential of phoP mutants of Salmonella typhimurium. Microbial Pathogenesis 6, 433–43.CrossRefGoogle ScholarPubMed
Gonzalez, C., Hone, D., Noriega, F. R., Tacket, C. O., Davis, J. R., Losonsky, G., Nataro, J. P., Hoffman, S., Malik, A., Nardin, E., Sztein, M. B., Heppner, G., Fouts, T. R., Isibasi, A. & Levine, M. M. (1994). Salmonella typhi vaccine strain CVD908 expressing the circumsporozoite protein of Plasmodium falciparum: strain construction and safety and immunogenicity in humans. Journal of Infectious Diseases 169, 927–31.CrossRefGoogle Scholar
Herrington, D. A., Clyde, D. F., Losonsky, G., Cortesia, M., Murphy, J. R., Davis, J., Baqar, S., Feli, A. M., Heimer, E. P., Gillessen, D., Nardin, E., Nussenzweig, R. S., Nussensweig, V., Hollingdale, M. R. & Levine, M. (1987). Safety and immunogenicity in man of a synthetic peptide malaria vaccine against Plasmodium falciparum sporozoites. Nature 328, 257–9.CrossRefGoogle ScholarPubMed
Hoiseth, S. K. & Stocker, B. A. D. (1981). Aromatic-dependent Salmonella typhimurium are non-virulent and effective as live vaccines. Nature 291, 238–40.CrossRefGoogle ScholarPubMed
Hone, D., Attridge, S., Van Den Bosch, L. & Hackett, J. (1988). A chromosomal integration system for stabilisation of heterologous genes in Salmonella based vaccine strains. Microbial Pathogenesis 5, 407–18.CrossRefGoogle ScholarPubMed
Hone, D. M., Harris, A. M., Chatfield, S., Dougan, G. & Levine, M. M. (1991). Construction of genetically defined double aro mutants of Salmonella typhi. Vaccine 9, 810–16.CrossRefGoogle ScholarPubMed
Hormaeche, C. E. (1979). Natural resistance to Salmonella typhimurium in different inbred mouse strains. Immunology 37, 311–18.Google ScholarPubMed
Hormaeche, C. E., Joysey, H. S., Desilva, L., Izhar, M. & Stocker, B. A. (1990). Immunity induced by live attenuated Salmonella vaccines. Research in Microbiology 141, 757–64.CrossRefGoogle ScholarPubMed
Hormaeche, C. E., Khan, C. M. A., Mastroeni, P., Villarreal, B., Roberts, M., Dougan, G. & Chatfield, S. N. (1994). Salmonella vaccines: mechanisms of immunity and their use as carriers of recombinant antigens. In Molecular and Clinical Aspects of Vaccine Development (ed. Ala'Aldeen, D. & Hormaeche, C.), Chichester: John Wiley.Google Scholar
Izhar, M., Desilva, L., Joysey, H. S. & Hormaeche, C. E. (1990). Moderate immune suppression does not increase susceptibility to aroA salmonella vaccine strains. Infection and Immunity 58, 2258–61.CrossRefGoogle Scholar
Johnson, K., Charles, I., Dougan, G., Pickard, D., O'Gaora, P., Costa, G., Ali, T., Miller, I. & Hormaeche, C. (1991). The role of a stress-response protein in Salmonella typhimurium virulence. Molecular Microbiology 5, 401–7.CrossRefGoogle ScholarPubMed
Jones, P. W., Dougan, G., Hayward, C., Mackensie, N., Collins, P. & Chatfield, S. N. (1990). Oral vaccination of calves against experimental salmonellosis using a double aro mutant of Salmonella typhimurium. Vaccine 9, 29–36.CrossRefGoogle Scholar
Khan, C. M. A., Villarreal-Ramos, B., Pierce, R. J., Demarco de Hormaeche, R., McNeill, H., Ali, T., Chatfield, S., Capron, A., Dougan, G. & Hormaeche, C. E. (1994 a). The construction, expression and immunogenicity of multiple tandem copies of Schistosoma mansoni peptide comprising of amino acids 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. Journal of Immunology 153, 5632–42.Google Scholar
Khan, C. M. A., Villarreal-Ramos, B., Pierce, R. J., Demarco De Hormaeche, R., McNeill, H., Ali, T., Chatfield, S., Capron, A., Dougan, G. & Hormaeche, C. E. (1994 b). The construction, expression and immunogenicity of the Schistosoma mansoni P28 glutathione S-transferase as a genetic fusion to tetanus toxin fragment C in a live aro attenuated vaccine strain of Salmonella. Proceedings of the National Academy of Sciences USA 91, 11261–5.CrossRefGoogle Scholar
Killar, L. M. & Eisenstein, T. K. (1985). Immunity of Salmonella typhimurium infection in C3H/HeJ and C3H/HeNCrlBR mice: studies with an aromatic-dependent live S. typhimurium as a vaccine. Infection and Immunity 47, 605–12.CrossRefGoogle ScholarPubMed
Lipscombe, M., Charles, I. G., Roberts, M., Dougan, G., Tite, J. & Fairweather, N. F. (1991). Intranasal immunisation using the B subunit of the Escherichia coli heat labile toxin fused to an epitope of the Bordetella pertussis P.69 antigen. Molecular Microbiology 5, 1385–92.CrossRefGoogle Scholar
Mackaness, G. B. (1971). Resistance to intracellular infection. Journal of Infectious Diseases 123, 439–45.CrossRefGoogle ScholarPubMed
Miller, I., Maskell, D., Hormaeche, C., Pickard, D. & Dougan, G. (1989 a). The isolation of orally attenuated Salmonella typhimurium following TnphoA mutagenesis. Infection and Immunity 57, 2758–63.CrossRefGoogle ScholarPubMed
Miller, I. A., Chatfield, S., Dougan, G., Desilva, L., Joysey, H. S. & Hormaeche, C. (1989 b). Bacteriophage P22 as a vehicle for transducing cosmic gene banks between smooth strains of Salmonella typhimurium: use in identifying a role for aroD in attenuating virulent Salmonella strains. Molecular and General Genetics 215, 312–16.CrossRefGoogle Scholar
Mukkur, T. K., Walker, K. H. & Stocker, B. A. (1991). Generation of aromatic-dependent Salmonella havana and evaluation of its immunogenic potential in mice and sheep. Veterinary Microbiology 29, 181–94.CrossRefGoogle ScholarPubMed
Nakayama, K., Kelly, S. M. & Curtiss, R. (1988). Construction of an Asd expression-cloning vector: stable maintenance and high level expression of cloned genes in a Salmonella vaccine strain. BioTechnology 6, 693–7.Google Scholar
Nikaido, H. & Vaara, M. (1985). Molecular basis of bacterial outer membrane permeability. Microbiology Reviews 49, 1–32.CrossRefGoogle ScholarPubMed
Peakman, T., Crouzet, J., Jayaux, J. F., Busby, S., Mohan, S., Harborne, N., Wooton, J., Nicholson, R. & Cole, J. (1990). Nucleotide sequence, organisation and structural analysis of the products of genes in the nirB–cysB region of the Escherichia coli K–12 chromosome. European Journal of Biochemistry 191, 315–23.CrossRefGoogle ScholarPubMed
Pickard, D., Li, J.-L., Roberts, M., Maskell, D., Hone, D., Levine, M., Dougan, G. & Chatfield, S. (1994). Characterization of defined ompR mutants of Salmonella typhi: ompR is involved in the regulation of Vi polysaccharide expression. Infection and Immunity 62, 3984–93.CrossRefGoogle ScholarPubMed
Pulkkinen, W. S. & Miller, S. I. (1991). A Salmonella typhimurium virulence protein is similar to a Yersinia entercolitica invasion protein and a bacteriophage lambda outer membrane protein. Journal of Bacteriology 173, 86–93.CrossRefGoogle Scholar
Roberts, M., Chatfield, S. N. & Dougan, G. (1994). Salmonella as carriers of heterologous antigens. In Novel Delivery Systems for Oral Vaccines (ed. O'Hagan, D. T.), pp. 27–48. New York: CRC Press.Google Scholar
Roberts, M., Dougan, G., Li, J. L., Chatfield, S. & Strugnell, R. (1993). Immunisation against Bordetella pertussis infection of mice using a Salmonella typhimurium aro vaccine strain expressing the Bordetella pertussis P.69 antigen. Biologicals 21, 4–5.CrossRefGoogle Scholar
Sadoff, J. C., Ballou, W. R., Baron, L. S., Majarian, W. R., Brey, R. N., Hockmeyer, W. T., Young, J. F., Cryz, J. J., Ou, J., Lowell, G. H. & Chulay, J. D. (1988). Oral Salmonella typhimurium vaccine expressing cirumsporozoite protein protects against malaria. Science 240, 236–8.CrossRefGoogle Scholar
Stocker, B. A. (1990). Aromatic-dependent Salmonella as live vaccine presenters of foreign epitopes as inserts in flagellin. Research in Microbiology 1990, 787–96.CrossRefGoogle Scholar
Tacket, C. O., Hone, D. M., Curtiss, R. III., Kelly, S. M., Losonsky, G., Guers, L., Harris, A. M., Edelman, R. & Levine, M. M. (1992 a). Comparison of the safety and immunogenicity of delta aroC delta aroD and delta cya delta crp Salmonella typhi strains in adult volunteers. Infection and Immunity 60, 536–41.CrossRefGoogle ScholarPubMed
Tacket, C. O., Hone, D. M., Losonsky, G. A., Guers, L., Edelman, R. & Levine, M. M. (1992 b). Clinical acceptability and immunogenicity of CVD908 Salmonella typhi vaccine strain. Vaccine 10, 443–6.CrossRefGoogle Scholar
Tite, J. P., Dougan, G. & Chatfield, S. N. (1991). The involvement of tumor necrosis factor in immunity to Salmonella infection. Journal of Immunology 147, 3161–4.CrossRefGoogle ScholarPubMed
Wolowczuk, I., Auriault, C., Bossus, M., Boulanger, D., Gras-Masse, H., Mazingue, C., Pierce, R. J., Grezel, D., Reid, G. D., Tartar, A. & Capron, M. (1991). Antigenicity and immunogenicity of a multiple peptidic construction of the Schistosoma mansoni SM28 GST antigen in rat, mouse and monkey. 1. Partial protection of Fischer rats after active immunisation. Journal of Immunology 146, 1987–95.CrossRefGoogle Scholar
Wolowczuk, I., Auriault, C., Gras-Masse, H., Mazingue, C., Vendeville, C., Tartar, A. & Capron, A. (1990). T-cell responsiveness towards various synthetic peptides of the P28 antigen in rat and mouse models during Schistosoma mansoni infection. International Archives of Applied Immunology 93, 350–8.CrossRefGoogle ScholarPubMed
Xu, D., McSorley, S. J., Chatfield, S. N., Dougan, G. & Liew, F. Y. (1994). Potentiation of protection against Leishmania major by cytokines delivered orally by recombinant Salmonella typhimurium: IFN-Y, IL-2 and TNFa enhance the immunity induced by gp63 in BALB/c mice. Journal of Immunology (in press).Google Scholar
Yang, D. M., Fairweather, N., Button, L. L., McMaster, W. R., Kahl, L. p. & Liew, F. Y. (1990). Oral Salmonella typhimurium (AroaA-) vaccine expressing a major leishmanial surface protein (gp63) preferentially induces T helper 1 cells and protective immunity against leishmaniasis. Journal of Immunology 145, 2281–5.CrossRefGoogle Scholar