Salmonella vaccines for use in humans: Present and future perspectives

FEMS Microbiology Reviews

Volumn 26, Issue 4, 2002, Pages 339-353

  Garmory, Helen S ^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 live carrier; Salmonella vaccine; Typhoid vaccine

Indexed keywords

4 AMINOBENZOIC ACID; ANTIMALARIAL AGENT; CHOLERA VACCINE; DNA VACCINE; LIVE VACCINE; SALMONELLOSIS VACCINE; TETANUS TOXIN; TYPHOID VACCINE; UNCLASSIFIED DRUG; VI POLYSACCHARIDE PROTEIN CONJUGATE;

ANTIBODY RESPONSE; ANTIBODY TITER; ANTIGEN EXPRESSION; ANTIGEN PRESENTING CELL; BACTEREMIA; BACTERIAL STRAIN; BACTERIAL VIRULENCE; CLINICAL TRIAL; COLONY FORMING UNIT; COMMON COLD; DIARRHEA; DOSE RESPONSE; DRUG DELIVERY SYSTEM; DRUG EFFECT; DRUG EFFICACY; DRUG SAFETY; DRUG TOLERABILITY; FEVER; HUMAN; IMMUNE RESPONSE; IMMUNITY; IMMUNIZATION; IMMUNOGENICITY; NONHUMAN; PROTEIN EXPRESSION; REVIEW; SALMONELLA ENTERICA; SEROTYPE; SIDE EFFECT; TREATMENT OUTCOME; TYPHOID FEVER; VACCINAEMIA; VACCINE PRODUCTION; VERNER MORRISON SYNDROME; VOMITING;

ANTIGENS, HETEROPHILE; CLINICAL TRIALS; HUMANS; SALMONELLA ENTERICA; SALMONELLA INFECTIONS; SALMONELLA VACCINES; VACCINES, DNA; VACCINES, SYNTHETIC;

SALMONELLA; SALMONELLA ENTERICA; SALMONELLA ENTERICA SUBSP. ENTERICA SEROVAR TYPHI;

EID: 0036842164     PISSN: 01686445     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0168-6445(02)00113-4     Document Type: Review

References (173)

1. Levine, M.M. (1999) Typhoid fever vaccines. In: Vaccines (Plotkin, S.A. and Orenstein, W.A., Eds.), pp. 781-814. W.B. Saunders, London.
2. Hessel L., Debois H., Fletcher M., Dumas R. Experience with Salmonella typhi Vi capsular polysaccharide vaccine. Eur. J. Clin. Microbiol. Infect. Dis. 18:1999;609-620.
3. Germanier R., Fuer E. Isolation and characterization of Gal E mutant Ty21a of Salmonella typhi: a candidate strain for a live, oral typhoid vaccine. J. Infect. Dis. 131:1975;553-558.
4. Felix A., Pitt RM. A new antigen of B. typhosus its relation to virulence and to active and passive immunization. Lancet. 2:1934;186-191.
5. Robbins J.D., Robbins J.B. Re-examination of the protective role of the capsular polysaccharide (Vi antigen) of Salmonella typhi. J. Infect. Dis. 150:1984;436-449.
6. Looney J.R., Steigbigel R.T. Role of the Vi antigen of Salmonella typhi in resistance to host defense in vitro. J. Lab. Clin. Med. 108:1986;506-516.
7. World Health Organisation (2000) Weekly Epidemiol. Rec. 32, 257-264.
8. Merican I. Typhoid fever: Present and future. Med. J. Malaysia. 52:1997;299-308.
9. Gherardi M.M., Garcia V.E., Brizzio V., Sordelli D.O., Cerquetti M.C. Differential persistence, immunogenicity and protective capacity of temperature-sensitive mutants of Salmonella enteritidis after oral or intragastric administration to mice. FEMS Immunol. Med. Microbiol. 7:1993;161-168.
10. Lantier F., Pardon P., Marly J. Vaccinal properties of Salmonella abortus ovis mutants for streptomycin: screening with a murine model. Infect. Immun. 34:1981;492-497.
11. Hone D.M., Attridge S.R., Forrest B., Morona R., Daniels D., LaBrooy J.T., Bartholomeusz R.C., Shearman D.J., Hackett J. A galE via (Vi antigen-negative) mutant of Salmonella typhi Ty2 retains virulence in humans. Infect. Immun. 56:1988;1326-1333.
12. Hone D., Morona R., Attridge S., Hackett J. Construction of defined galE mutants of Salmonella for use as vaccines. J. Infect. Dis. 156:1987;167-174.
13. McKenna A.J., Bygraves J.A., Maiden M.C., Feavers I.M. Attenuated typhoid vaccine Salmonella typhi Ty21a: fingerprinting and quality control. Microbiology. 141:1995;1993-2002.
14. Wahdan M.H., Serie C., Cerisier Y., Sallam S., Germanier R. A controlled field trial of live Salmonella typhi strain Ty21a oral vaccine against typhoid: three-year results. J. Infect. Dis. 145:1982;292-295.
15. Cryz S.J. Jr., Vanprapar N., Thisyakorn U., Olanratmanee T., Losonsky G., Levine M.M., Chearskul S. Safety and immunogenicity of Salmonella typhi Ty21a vaccine in young Thai children. Infect. Immun. 61:1993;1149-1151.
16. Levine M.M., Ferreccio C., Black R.E., Germanier R. Large-scale field trial of Ty21a live oral typhoid vaccine in enteric-coated capsule formulation. Lancet. 1:1987;1049-1052.
17. Black R.E., Levine M.M., Ferreccio C., Clements M.L., Lanata C., Rooney J., Germanier R. Efficacy of one or two doses of Ty21a Salmonella typhi vaccine in enteric-coated capsules in a controlled field trial. Chilean Typhoid Comm. Vaccine. 8:1990;81-84.
18. Murphy J.R., Grez L., Schlesinger L., Ferreccio C., Baqar S., Munoz C., Wasserman S.S., Losonsky G., Olson J.G., Levine M.M. Immunogenicity of Salmonella typhi Ty21a vaccine for young children. Infect. Immun. 59:1991;4291-4293.
19. Levine M.M., Ferrecio C., Cryz S., Ortiz E. Comparison of enteric-coated capsules and liquid formulation of Ty21a typhoid vaccine in randomised controlled field trial. Lancet. 336:1990;891-894.
20. Levine M.M., Ferreccio C., Abrego P., San Martin O., Ortiz E., Cryz S. Duration of efficacy of Ty21a, attenuated Salmonella typhi live oral vaccine. Vaccine. 17:1999;S22-S27.
21. Kollaritsch H., Fürer E., Herzog C., Wiedermann G., Que J.U., Cryz S.J. Jr. Randomized, double-blind placebo-controlled trial to evaluate the safety and immunogenicity of combined Salmonella typhi Ty21a and Vibrio cholerae CVD103-HgR live oral vaccines. Infect. Immun. 64:1996;1454-1457.
22. Kollaritsch H., Que J.U., Kunz C., Wiedermann G., Herzog C., Cryz S.J. Jr. Safety and immunogenicity of live oral cholera and typhoid vaccines administered alone or in combination with antimalarial drugs, oral polio vaccine, or yellow fever vaccine. J. Infect. Dis. 175:1997;871-875.
23. Mastroeni P., Chabalgoity J.A., Dunstan S.J., Maskell D.J., Dougan G. Salmonella: immune responses and vaccines. Vet. J. 161:2000;132-164.
24. Bacon G.A., Burrows T.W., Yates M. The effect of biochemical mutation on the virulence of Bacterium typhosum: the loss of virulence of certain mutants. Br. J. Exp. Pathol. 31:1950;714-724.
25. Pittard, A.J. (1987) Biosynthesis of the aromatic amino acids. In: Escherichia coli and Salmonella typhimurium: Cellular and Molecular Biology (Neidhardt, F.C., Ingraham, J.L., Magasanik, B., Low, K.B., Schaechter, M. and Umbarger, H.E., Eds.), pp. 368-369. American Society for Microbiology, Washington, DC.
26. Hosieth S.K., Stocker B.A.D. Aromatic-dependant Salmonella typhimurium are non-virulent and effective as live vaccines. Nature. 291:1981;238-239.
27. Dougan G., Maskell D., Pickard D., Hormaeche C.E. Isolation of stable aroA mutants of Salmonella typhi Ty2: Properties and preliminary characterization in mice. Mol. Gen. Genet. 207:1987;402-407.
28. Miller S.I., Mekalanos J.J. Effect of a purA mutation on efficacy of Salmonella live-vaccine vectors. Infect. Immun. 57:1989;1858-1861.
29. O'Callaghan D., Maskell D., Liew F.Y., Easmon C.S., Dougan G. Characterization of aromatic- and purine-dependant Salmonella typhimurium: attenuation, persistence, and ability to induce protective immunity in BALB/c mice. Infect. Immun. 56:1988;419-423.
30. O'Callaghan D., Maskell D., Tite J., Dougan G. Immune responses in BALB/c mice following immunization with aromatic compound or purine-dependent Salmonella typhimurium strains. Immunology. 69:1990;184-189.
31. Levine M.M., Herrington D., Murphy J.R., Morris J.G., Losonsky G., Tall B., Lindberg A.A., Svenson S., Baqar S., Edwards M.F., Stocker B. Safety, infectivity, immunogenicity, and in vivo stability of two attenuated auxotrophic mutant strains of Salmonella typhi, 541Ty and 543Ty, as live oral vaccines in humans. J. Clin. Invest. 79:1987;888-902.
32. Dougan G., Chatfield S., Pickard D., Bester J., O'Callaghan D., Maskell D. Construction and characterization of vaccine strains of Salmonella harbouring mutations in two different aro genes. J. Infect. Dis. 158:1988;1329-1335.
33. Chatfield S.N., Fairweather N., Charles I., Pickard D., Levine M., Hone D., Posada M., Strugnell R.A., Dougan G. Construction of a genetically defined Salmonella typhi Ty2 aroA, aroC mutant for the engineering of a candidate oral typhoid-tetanus vaccine. Vaccine. 10:1992;53-60.
34. Hone D.M., Harris A.M., Chatfield S., Dougan G., Levine M.M. Construction of genetically defined double aro mutants of Salmonella typhi. Vaccine. 9:1991;810-816.
35. Chatfield S.N., Strahan K., Pickard D., Charles I.G., Hormaeche C.E., Dougan G. Evaluation of Salmonella typhimurium strains harbouring defined mutations in htrA and aroA in the murine salmonellosis model. Microb. Pathogen. 12:1992;145-151.
36. Tacket C.O., Sztein M.B., Losonsky G.A., Wasserman S.S., Nataro P., Edelman R., Pickard D., Dougan G., Chatfield S.N., Levine M.M. Safety of live oral Salmonella typhi vaccine strains with deletions in htrA and aroC aroD and immune response in humans. Infect. Immun. 65:1997;452-456.
37. Johnson K., Charles I., Dougan G., Pickard D., O'Goara P., Costa G., Ali T., Miller I., Hormaeche C. The role of a stress-response protein in Salmonella typhimurium virulence. Mol. Microbiol. 5:1991;401-407.
38. Strahan K., Chatfield S.N., Tite J., Dougan G., Hormaeche C.E. Impaired resistance to infection does not increase the virulence of Salmonella htrA live vaccines for mice. Microb. Pathogen. 12:1992;311-317.
39. Curtiss R. III, Goldschmidt R.M., Fletchall N.B., Kelly S.M. Avirulent Salmonella typhimurium Δcya Δcrp oral vaccine strains expressing a streptococcal colonization and virulence antigen. Vaccine. 6:1988;155-160.
40. Curtiss R. III, Kelly S.M., Gulig P.A., Nakayama K. Selective delivery of antigens by recombinant bacteria. Curr. Top. Microbiol. Immunol. 146:1989;35-49.
41. Curtiss R. III, Kelly S.M. Salmonella typhimurium deletion mutants lacking adenylate cyclase and cyclic AMP receptor protein are avirulent and immunogenic. Infect. Immun. 55:1987;3035-3043.
42. Galan J.E., Curtiss R. III. Virulence and vaccine potential of phoP mutants of Salmonella typhimurium. Microb. Pathogen. 6:1989;433-443.
43. Miller S.I., Mekalanos J.J., Pulkinnen W.S. Salmonella vaccines with mutations in the phoP virulence regulon. Res. Microbiol. 141:1990;817-821.
44. Hohmann E.L., Oletta C.A., Killeen K.P., Miller S.I. phoP/phoQ-deleted Salmonella typhi (Ty800) is a safe and immunogenic single-dose typhoid fever vaccine in volunteers. J. Infect. Dis. 173:1996;1408-1414.
45. Pasetti M.F., Anderson R.J., Noriega F.R., Levine M.M., Sztein M.B. Attenuated ΔguaBA Salmonella typhi vaccine strain CVD915 as a live vector utilizing prokaryotic or eukaryotic expression systems to deliver foreign antigens and elicit immune responses. Clin. Immunol. 92:1999;76-89.
46. Wang J.Y., Pasetti M.F., Noriega F.R., Anderson R.J., Wasserman S.S., Galen J.E., Sztein M.B., Levine M.M. Construction, genotypic and phenotypic characterization, and immunogenicity of attenuated ΔguaBA Salmonella enterica serovar Typhi strain CVD 915. Infect. Immun. 69:2001;4734-4741.
47. Curtiss R. III, Nakayama K., Kelly S.M. Recombinant avirulent Salmonella vaccine strains with stable maintenance and high level expression of cloned genes in vivo. Immunol. Invest. 18:1989;583-596.
48. Buchmeier N.A., Lipps C.J., So M.Y., Heffron F. Recombination-deficient mutants of Salmonella typhimurium are avirulent and sensitive to the oxidative burst of macrophages. Mol. Microbiol. 7:1993;933-936.
49. Heithoff D.M., Sinsheimer R.L., Low D.A., Mahan M.J. An essential role for DNA adenine methylation in bacterial virulence. Science. 284:1999;967-970.
50. Edwards M.F., Stocker B.A.D. Construction of delta aroA his delta pur strains of Salmonella typhi. J. Bacteriol. 170:1988;3991-3995.
51. Hone D.M., Tacket C.O., Harris A.M., Kay B., Losonsky G., Levine M.M. Evaluation in volunteers of a candidate live oral attenuated Salmonella typhi vector vaccine. J. Clin. Invest. 90:1992;412-420.
52. Tacket C.O., Hone D.M., Losonsky G.A., Guers L., Edelman R., Levine M.M. Clinical acceptability and immunogenicity of CVD 908 Salmonella typhi vaccine strain. Vaccine. 10:1992;443-446.
53. Sztein M.B., Wasserman S.S., Tacket C.O., Edelman R., Hone D., Lindberg A.A., Levine M.M. Cytokine production patterns and lymphoproliferative responses in volunteers orally immunized with attenuated vaccine strains of Salmonella typhi. J. Infect. Dis. 170:1994;1508-1517.
54. Sztein M.B., Tanner M.K., Polotsky Y., Orenstein J.M., Levine M.M. Cytotoxic T lymphocytes after oral immunization with attenuated vaccine strains of Salmonella typhi in humans. J. Immunol. 155:1995;3987-3993.
55. Tacket C.O., Sztein M.B., Wasserman S.S., Losonsky G., Kotloff K.L., Wyant T.L., Nataro J.P., Edelman R., Perry J., Bedford P., Brown D., Chatfield S., Dougan G., Levine M.M. Phase 2 clinical trial of attenuated Salmonella enterica serovar Typhi oral live vector vaccine CVD 908-htrA in U.S. volunteers. Infect. Immun. 68:2000;1196-1201.
56. Dilts D.A., Reisenfeld-Orn I., Fulginiti J.P., Ekwall E., Granert C., Nonenmacher J., Brey R.N., Cryz S.J., Karisson K., Bergman K., Thompson T., Hu B., Bruckner A.H., Lindberg A.A. Phase I clinical trials of aroA aroD and aroA aroD htrA attenuated S. typhi vaccines; effect of formulation on safety and immunogenicity. Vaccine. 18:2000;1473-1484.
57. Wang J.-Y., Noriega F.R., Galen J.E., Barry E., Levine M.M. Constitutive expression of the Vi polysaccharide capsular antigen in attenuated Salmonella enterica serovar Typhi oral vaccine strain CVD 909. Infect. Immun. 68:2000;4647-4652.
58. Hohmann E.L., Oletta C.A., Miller S.I. Evaluation of a phoP/phoQ-deleted aroA deleted live oral Salmonella typhi vaccine strain in human volunteers. Vaccine. 14:1995;19-24.
59. Tacket C.O., Kelly S.M., Schödel F., Losonsky G., Nataro J.P., Edelman R., Levine M.M., Curtiss R. III. 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. 65:1997;3381-3385.
60. Frey S.E., Bollen W., Sizemore D., Campbell M., Curtiss R. III. Bacteremia associated with live attenuated chi8110 Salmonella enterica serovar Typhi ISP1820 in healthy adult volunteers. Clin. Immunol. 101:2001;32-37.
61. Cárdenas L., Clements J.D. Oral immunization using live attenuated Salmonella spp. as carriers of foreign antigens. Clin. Microbiol. Rev. 5:1992;328-342.
62. Chatfield, S.N., Dougan, G. and Roberts, M. (1994) Progress in the development of multivalent oral vaccines based on live attenuated Salmonella. In: Modern Vaccinology (Kurstak, E., Ed.), pp. 55-86. Plenum, New York.
63. Hormaeche, C.E., Khan, C.M.A., Mastroeni, P., Villarreal, B., Dougan, G., Roberts, M. and Chatfield, S.N. (1995) Salmonella vaccines: Mechanisms of immunity and their use as carriers of recombinant antigens. In: Molecular and Clinical Aspects of Bacterial Vaccine Development (Ala'Aldeen, D.A.A. and Hormaeche, C.E., Eds.), pp. 119-153. John Wiley and Sons, London.
64. Hone, D.M., Shata, M.T., Pascual, D.W. and Lewis, G.K. (1999) Mucosal vaccination with Salmonella vaccine vectors. In: Intracellular Bacterial Vaccine Vectors: Immunology, Cell Biology and Genetics (Patterson, Y., Ed.), pp. 171-222. John Wiley and Sons, London.
65. Galen J.E., Gomez-Duarte O.G., Losonsky G.A., Halpern J.L., Lauderbaugh C.S., Kaintuck S., Reymann M.K., Levine M.M. A murine model of intranasal immunization to assess the immunogenicity of attenuated Salmonella typhi live vector vaccines in stimulating serum antibody responses to expressed foreign antigens. Vaccine. 15:1997;700-708.
66. Barry E.M., Gomez-Duarte O., Chatfield S.N., Rappuoli R., Pizza M., Losonsky G., Galen J., Levine M.M. Expression and immunogenicity of pertussis toxin S1 subunit-tetanus toxin fragment C fusions in Salmonella typhi vaccine strain CVD 908. Infect. Immun. 64:1996;4172-4181.
67. Gonzalez C.R., Noriega F.R., Huerta S., Santiago A., Vega M., Paniagua J., Ortiz-Navarrete V., Isibasi A., Levine M.M. Immunogenicity of a Salmonella typhi CVD 908 candidate vaccine strain expressing the major surface protein gp63 of Leishmania mexicana mexicana. Vaccine. 16:1998;1043-1052.
68. Pickett Y.E., Pasetti M.F., Galen J.E., Sztein M.B., Levine M.M. In vivo characterization of the murine intranasal model for assessing the immunogenicity of attenuated Salmonella enterica serovar Typhi strains as live mucosal vaccines and as live vectors. Infect. Immun. 68:2000;205-213.
69. Wu S., Beier M., Sztein M.B., Galen J., Pickett T., Holder A.A., Gómez-Duarte O.G., Levine M.M. Construction and immunogenicity in mice of attenuated Salmonella typhi expressing Plasmodium falciparum merozoite surface protein 1 (MSP-1) fused to tetanus toxin fragment C. J. Biotechnol. 83:2000;125-183.
70. Gonzalez C., Hone D., Noriega F.R., Tacket C.O., Davis J.R., Losonsky G., Nataro J.P., Hoffman S., Malik A., Nardin E., et al. Salmonella typhi vaccine strain CVD 908 expressing the circumsporozoite protein of Plasmodium falciparum: strain construction and safety and immunogenicity in humans. J. Infect. Dis. 169:1994;927-931.
71. Nardelli-Haefliger D., Kraehenbuhl J.-P., Curtiss R. III, Schödel F., Potts A., Kelly S., De Grandi P. Oral and rectal immunization of adult female volunteers with a recombinant attenuated Salmonella typhi vaccine strain. Infect. Immun. 64:1996;5219-5224.
72. DiPetrillo M.D., Tibbetts T., Kleanthous H., Killeen K.P., Hohmann E.L. Safety and immunogenicity of phoP/phoQ-deleted Salmonella typhi expressing Helicobacter pylori urease in adult volunteers. Vaccine. 18:2000;449-459.
73. Tacket C.O., Galen J.E., Sztein M.B., Losonsky G., Wyant T.L., Nataro J., Wasserman S.S., Edelman R., Chatfield S., Dougan G., Levine M.M. Safety and immune responses to attenuated Salmonella enterica serovar Typhi oral live vector vaccines expressing tetanus toxin fragment C. Clin. Immunol. 97:2000;146-153.
74. Angelakopoulos I., Hohmann E.L. Pilot study of phoP/phoQ-deleted Salmonella enterica serovar Typhimurium expressing Helicobacter pylori urease in adult volunteers. Infect. Immun. 68:2000;2135-2141.
75. Bao J.X., Clements J.D. Prior immunologic experience potentiates the subsequent antibody response when Salmonella strains are used as vaccine carriers. Infect. Immun. 59:1991;3841-3845.
76. Attridge S.R., Davies R., LaBrooy J.T. Oral delivery of foreign antigens by attenuated Salmonella: consequences of prior exposure to the vector strain. Vaccine. 15:1997;155-162.
77. Roberts M., Bacon A., Li J., Chatfield S. Prior immunity to homologous and heterologous Salmonella serotypes suppresses local and systemic anti-fragment C antibody responses and protection from tetanus toxin in mice immunized with Salmonella strains expressing fragment C. Infect. Immun. 67:1999;3810-3815.
78. Kohler J.J., Pathangey L.B., Gillespie S.R., Brown T.A. Effect of preexisting immunity to Salmonella on the immune response to recombinant Salmonella enterica serovar Typhimurium expressing a Porphyromonas gingivalis hemagglutinin. Infect. Immun. 68:2000;3116-3120.
79. Molina N.C., Parker C.D. Murine antibody response to oral infection with live aroA recombinant Salmonella dublin vaccine strains expressing filamentous hemagglutinin antigen from Bordatella pertussis. Infect. Immun. 58:1990;2523-2528.
80. Covone M.G., Brocchi M., Palla M., Dias Da Silveira E., Rappuoli W., Galeotti C.L. Levels of expression and immunogenicity of attenuated Salmonella enterica serovar Typhimurium strains expressing Escherichia coli mutant heat-labile enterotoxin. Infect. Immun. 66:1998;224-231.
81. Fouts T.R., Tuskan R.G., Chada S., Hone D.M., Lewis G.K. Construction and immunogenicity of Salmonella typhimurium vaccine vectors that express HIV-1 gp120. Vaccine. 13:1995;1697-1705.
82. Schodel F., Kelly S.M., Peterson D.L., Milich D.R., Curtiss R. III. Hybrid hepatitis B virus core-pre-S proteins synthesized in avirulent Salmonella typhimurium and Salmonella typhi for oral vaccination. Infect. Immun. 62:1994;1669-1676.
83. Khan C.M., Villarreal-Ramos B., Pierce R.J., Demarco de Hormaeche R., McNeill H., Ali T., Chatfield S., Capron A., Dougan G., Hormaeche C.E. 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. 153:1994;5634-5642.
84. Doggett T.A., Jagusztyn-Krynicka E.K., Curtiss R. III. Immune responses to Streptococcus sobrinus surface protein antigen A expressed by recombinant Salmonella typhimurium. Infect. Immun. 61:1993;1859-1866.
85. Chabalgoity J.A., Khan C.M., Nash A.A., Hormaeche C.E. A Salmonella typhimurium htrA live vaccine expressing multiple copies of a peptide comprising amino acids 8-23 of herpes simplex virus glycoprotein D as a genetic fusion to tetanus toxin fragment C protects mice from herpes simplex virus infection. Mol. Microbiol. 19:1996;791-801.
86. Yan Z.X., Reuss F., Mayer T.F. Construction of an invertible DNA segment for improved antigen expression by a hybrid Salmonella vaccine strain. Res. Microbiol. 141:1990;1003-1004.
87. Tijhaar E.J., Zheng-Xin Y., Karlas J.A., Meyer T.F., Stukart M.J., Osterhaus A.D., Mooi F.R. Construction and evaluation of an expression vector allowing the stable expression of foreign antigens in a Salmonella typhimurium vaccine strain. Vaccine. 12:1994;1004-1011.
88. Yan Z.X., Meyer T.F. Mixed population approach for vaccination with live recombinant Salmonella strains. J. Biotechnol. 44:1996;197-201.
89. Oxer M.D., Bently C.M., Doyle J.G., Peakman T.C., Charles I.G., Makoff A.J. High level heterologous expression in E. coli using the anaerobically-activated nirB promoter. Nucleic Acids Res. 19:1991;1889-1892.
90. Everest P., Frankel G., Li J., Lund P., Chatfield S., Dougan G. Expression of LacZ from the htrA, nirB and groE promoters in a Salmonella vaccine strain: influence of growth in mammalian cells. FEMS Microbiol. Lett. 126:1995;97-102.
91. Chatfield S.N., Charles I.G., Makoff A.J., Oxer M.D., Dougan G., Pickard D., Slater D., Fairweather N. 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. 10:1992;888-892.
92. McSorely S.J., Xu D., Liew F.Y. Vaccine efficacy of Salmonella strains expressing glycoprotein 63 with different promoters. Infect. Immun. 65:1997;171-178.
93. Dunstan S.J., Simmons C.P., Strugnell R.A. Use of in vivo-regulated promoters to deliver antigens from attenuated Salmonella enterica var. Typhimurium. Infect. Immun. 67:1999;5133-5141.
94. Khan C.M., Villarreal-Ramos B., Pierce R.J., Riveau G., Demarco de Hormaeche R., McNeill H., Ali T., Fairweather N., Chatfield S., Capron A., Dougan G., Hormaeche C.E. Construction, expression, and immunogenicity of the Schistosoma mansoni P28 glutathione S-transferase expressed as a genetic fusion to tetanus toxin fragment C in a live Aro attenuated vaccine strain of Salmonella. Proc. Natl. Acad. Sci. USA. 91:1994;11261-11265.
95. Chabalgoity J.A., Harrison J.A., Esteves A., Demarco de Hormaeche R., Ehrich R., Khan C.M., Hormaeche C.E. Expression and immunogenicity of an Echinococcus granulosus fatty acid-binding protein in live attenuated Salmonella vaccine strains. Infect. Immun. 65:1997;2402-2412.
96. Londono L.P., Chatfield S., Tindle R.W., Herd K., Gao X.M., Frazer I., Dougan G. Immunisation of mice using Salmonella typhimurium expressing human papillomavirus type 16 E7 epitopes inserted into hepatitis B virus core antigen. Vaccine. 14:1996;545-552.
97. Huang Y., Hajishengallis G., Michalek S.M. Construction and characterization of a Salmonella enterica serovar Typhimurium clone expressing a salivary adhesin of Streptococcus mutans under the control of the anaerobically inducible nirB promoter. Infect. Immun. 68:2000;1549-1556.
98. Chen H., Schifferli D.M. Enhanced immune responses to viral epitopes by combining macrophage-inducible expression with multimeric display on a Salmonella vector. Vaccine. 19:2001;3009-3018.
99. Roberts M., Li J., Bacon A., Chatfield S.N. Oral vaccination against tetanus: comparison of the immunogenicities of Salmonella strains expressing fragment C from the nirB and htrA promoters. Infect. Immun. 66:1998;3080-3087.
100. Orr N., Galen J.E., Levine M.M. Novel use of anaerobically induced promoter, dmsA, for controlled expression of fragment C of tetanus toxin in live attenuated Salmonella enterica serovar Typhi strain CVD 908-htrA. Vaccine. 19:2001;1697-1700.
101. Hohmann E.L., Oletta C.A., Loomis W.P., Miller S.I. Macrophage-inducible expression of a model antigen in Salmonella typhimurium enhances immunogenicity. Proc. Natl. Acad. Sci. USA. 92:1995;2904-2908.
102. Bullifent H.L., Griffin K.F., Jones S.M., Yates A., Harrington L., Titball R.W. Antibody responses to Yersinia pestis F1-antigen expressed in Salmonella typhimurium aroA from in vivo-inducible promoters. Vaccine. 18:2000;2668-2676.
103. Marshall D.G., Haque A., Fowler R., Del Guidice G., Dorman C.J., Dougan G., Bowe F. Use of the stationary phase inducible promoters, spv and dps, to drive heterologous antigen expression in Salmonella vaccine strains. Vaccine. 18:2000;1298-1306.
104. Valentine P.J., Meyer K., Rivera M.M., Lipps C., Pauza D., Maziarz R.T., So M., Heffron F. Induction of SIV capsid-specific CTL and mucosal sIgA in mice immunized with a recombinant S. typhimurium aroA mutant. Vaccine. 14:1996;138-146.
105. Maskell D.J., Sweeney K.J., O'Callaghan D., Hormaeche C.E., Liew F.Y., Dougan G. Salmonella typhimurium aroA mutants as carriers of the Escherichia coli heat-labile enterotoxin B subunit to the murine secretory and systemic immune systems. Microb. Pathogen. 2:1987;211-221.
106. Hone D., Attridge S., Van den Bosche L., Hackett J. A chromosomal integration system for stabilization of heterologous genes in Salmonella based vaccine strains. Microb. Pathogen. 5:1988;407-418.
107. Strugnell R.A., Maskell D., Fairweather N., Pickard D., Cockayne A., Penn C., Dougan G. Stable expression of foreign antigens from the chromosome of Salmonella typhimurium vaccine strains. Gene. 88:1990;57-63.
108. Strugnell R., Dougan G., Chatfield S., Charles I., Fairweather N., Tite J., Li J.L., Beesley J., Roberts M. Characterization of a Salmonella typhimurium aro vaccine strain expressing the P.69 antigen of Bordatella pertussis. Infect. Immun. 60:1992;3994-4002.
109. Lee E., Platt R., Kang S., Roth J.A., Phillips G.J. Chromosomal integration and expression of the Escherichia coli K88 gene cluster in Salmonella enterica ser. Choleraesuis strain 54 (SC54). Vet. Microbiol. 83:2001;177-183.
110. + expression cloning vector: stable maintenance and high level expression of cloned genes in a Salmonella vaccine strain. BioTechnology. 6:1988;693-697.
111. Galan J.E., Nakayama K., Curtiss R.D. Cloning and characterization of the asd gene of Salmonella typhimurium: use in stable maintenance of recombinant plasmids in Salmonella vaccine strains. Gene. 94:1990;29-35.
112. Zhang T., Stanley S.L. Jr. Expression of the serine rich Entamoeba histolytica protein (SREHP) in the avirulent vaccine strain Salmonella typhi TY2 χ4297 (Δcya Δcrp Δasd): safety and immunogenicity in mice. Vaccine. 15:1997;1319-1322.
113. McNeill H.V., Sinha K.A., Hormaeche C.E., Lee J.J., Khan C.M.A. Development of a nonantibiotic dominant marker for positively selecting expression plasmids in multivalent Salmonella vaccines. Appl. Environ. Microbiol. 66:2000;1216-1219.
114. Galen J.E., Nair J., Wang J.Y., Wasserman S.S., Tanner M.K., Sztein M.B., Levine M.M. Optimization of plasmid maintenance in the attenuated live vaccine vector strain Salmonella typhi CVD 908-htrA. Infect. Immun. 67:1999;6424-6433.
115. Forrest B.D., LaBrooy J.T., Attridge S.R., Boehm G., Beyer L., Morona R., Shearmen D.J., Rowley D. Immunogenicity of a candidate live oral typhoid/cholera hybrid vaccine in humans. J. Infect. Dis. 159:1989;145-146.
116. Tacket C.O., Forrest B., Morona R., Attridge S.R., LaBrooy J., Tall B.D., Reymann M., Rowley D., Levine M.M. Safety, immunogenicity, and efficacy against cholera challenge in humans of a typhoid-cholera hybrid vaccine derived from Salmonella typhi Ty21a. Infect. Immun. 58:1990;1620-1627.
117. Gomez-Duarte O.G., Galen J., Chatfield S.N., Rappuoli R., Eidels L., Levine M.M. Expression of fragment C of tetanus toxin fused to a carboxyl-terminal fragment of diptheria toxin in Salmonella typhi CVD 908 vaccine strain. Vaccine. 13:1995;1596.
118. Barry E.M., Gomez-Duarte O., Chatfield S., Rappuoli R., Pizza M., Losonsky G., Galen J., Levine M.M. Expression and immunogenicity of pertussis toxin S1 subunit-tetanus toxin fragment C fusions in Salmonella typhi vaccine strain CVD 908. Infect. Immun. 64:1996;4172.
119. Fouts T.R., Lewis G.K., Hone D.M. Construction and characterization of a Salmonella typhi-based human immunodeficiency virus type 1 vector vaccine. Vaccine. 13:1995;561.
120. O'Callaghan D., Charbit A., Martineau P., Leclerc C., Van der Werf S., Nauciel C., Hofnung M. Immunogenicity of foreign peptides expressed in bacterial envelope proteins. Res. Microbiol. 141:1990;963-969.
121. Pistor S., Hobom G. OmpA haemagglutinin fusion protein for oral immunization with live attenuated Salmonella. Res. Microbiol. 141:1990;879-881.
122. Wu S., Pascual D.W., Lewis G.K., Hone D.M. Induction of mucosal and systemic responses against human immunodeficiency virus type 1 glycoprotein 120 in mice after oral immunization with a single dose of a Salmonella-HIV vector. AIDS Res. Hum. Retroviruses. 13:1997;1187-1194.
123. Charbit A., Martineau P., Ronco J., Leclerc R., Lo-Man V., Michel O.C.D., Hofnung M. 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 to two Escherichia coli carrier proteins. Vaccine. 11:1993;1221-1228.
124. Hess J., Gentschev I., Miko D., Welzel M., Ladel C., Goebel W., Kaufmann S.H.E. Superior efficacy of secreted over somatic antigen display in recombinant Salmonella vaccine induced protection against listeriosis. Proc. Natl. Acad. Sci. USA. 93:1996;1458-1463.
125. Hess J., Dietrich G., Gentschev I., Miko D., Goebel W., Kaufmann S.H.E. Protection against murine listeriosis by an attenuated recombinant Salmonella typhimurium vaccine strain that secretes the naturally somatic antigen superoxide dismutase. Infect. Immun. 65:1997;1286-1292.
126. Russmann H., Shams H., Poblete F., Fu Y., Galan J.E., Donis R.O. Delivery of epitopes by the Salmonella type III secretion system for vaccine development. Science. 281:1998;565-568.
127. Gentschev I., Sokolovic Z., Kohler S., Krohne G.F., Hof H., Wagner J., Goebel W. Identification of p60 antibodies in human sera and presentation of this listerial antigen on the surface of attenuated Salmonellae by the HlyB-HlyD secretion system. Infect. Immun. 60:1992;5091-5098.
128. Tzschaschel B.D., Guzman C.A., Timmis K.N., De Lorenzo V. An Escherichia coli hemolysin transport system-based vector for the export of polypeptides: export of Shiga-like toxin IIeB subunit by Salmonella typhimurium aroA. Nature Biotechnol. 14:1996;765-769.
129. Brown A., Hormaeche C.E., Demarco de Hormaech R., Winther M., Dougan G., Maskell D.J., Stocker B.A. An attenuated aroA Salmonella typhimurium vaccine elicits humoral and cellular immunity to cloned beta-galactosidase in mice. J. Infect. Dis. 155:1987;86-92.
130. Lee J.J., Sinha K.A., Harrison J.A., Demarco de Hormaeche R., Riveau G., Pierce R.J., Capron A., Wilson R.A., Khan C.M.A. Tetanus toxin fragment C expressed in live Salmonella vaccines enhances antibody responses to its fusion partner Schistosoma haematobium glutathione S-transferase. Infect. Immun. 68:2000;2503-2512.
131. Francis M.J., Hastings G.Z., Syred A.D., McGinn B., Brown F., Rowlands D.J. Nonresponsiveness to a foot-and-mouth disease virus peptide overcome by addition of foreign helper T cell determinants. Nature. 330:1987;168-170.
132. Jagusztyn-Krynicka E.K., Clark-Curtiss J.E., Curtiss R. III. Escherichia coli heat-labile toxin subunit B fusions with Streptococcus sobrinus antigens expressed by Salmonella typhimurium oral vaccine strains: importance of the linker for antigenicity and biological properties of the hybrid proteins. Infect. Immun. 61:1993;1004-1015.
133. Cárdenas L., Clements J.D. Development of mucosal protection against the heat-stable enterotoxin (ST) of Escherichia coli by oral immunization with a genetic fusion delivered by a bacterial vector. Infect. Immun. 61:1993;4629-4636.
134. Foss D.L., Murtaugh M.P. Mechanisms of vaccine adjuvanticity at mucosal surfaces. Animal Health Res. Rev. 1:2000;3-24.
135. Carrier M.J., Chatfield S.N., Dougan G., Nowicka U.T., O'Callaghan D., Beesley J.E., Milano S., Cillari E., Liew F.Y. Expression of human Il-1 beta in Salmonella typhimurium. A model system for the delivery of recombinant therapeutic proteins in vivo. J. Immunol. 148:1992;1176-1181.
136. Denich K., Borlin P., O'Hanley P.D., Howard M., Heath A.W. Expression of the murine interleukin-4 gene in an attenuated aroA strain of Salmonella typhimurium: persistence and immune response in BALB/c mice and susceptibility to macrophage killing. Infect. Immun. 61:1993;4818-4827.
137. Ianaro A., Xu D., O'Donnell C.A., Di Rosa M., Liew F.Y. Expression of TGF-beta in attenuated Salmonella typhimurium: oral administration leads to the reduction of inflammation, IL-2 and IFN-gamma, but enhancement of IL-10, in carrageenin-induced oedema in mice. Immunology. 84:1995;8-15.
138. Dunstan S.J., Ramsay A.J., Strugnell R.A. Studies of immunity and bacterial invasiveness in mice given a recombinant Salmonella vector encoding murine interleukin-6. Infect. Immun. 64:1996;2730-2736.
139. Saltzman D.A., Heise C.P., Hasz D.E., Zebede M., Kelly S.M., Curtiss R. III, Leonard A.S., Anderson P.M. Attenuated Salmonella typhimurium containing interleukin-2 decreases MC-38 hepatic metastases: a novel anti-tumor agent. Cancer Biother. Radiopharm. 11:1996;145-153.
140. Whittle B.L., Lee E., Wier R.C., Verma N.K. Enhancement of the
141. Hahn H.P., Hess C., Gabelsberger J., Domdey H., Von Specht B.U. A Salmonella typhimurium strain genetically engineered to secrete effectively a bioactive human interleukin (hIL)-6 via the Escherichia coli hemolysin secretion apparatus. FEMS Immunol. Med. Microbiol. 20:1998;111-119.
142. Xu D., McSorely S.J., Tetley L., Chatfield S., Dougan G., Chan W.L., Satoskar A., David J.R., Liew F.Y. Protective effect on Lieshmania major infection of migration inhibitory factor, TNF-α, and IFN-γ administered orally via attenuated Salmonella typhimurium. J. Immunol. 160:1998;1285-1289.
143. + gene: application to cholera vaccine development. Gene. 107:1991;139-144.
144. Tuteja R. DNA vaccines: a ray of hope. Crit. Rev. Biochem. Mol. Biol. 34:1999;1-24.
145. Corr M., Tighe H. Plasmid DNA vaccination: mechanism of antigen presentation. Springer Semin. Immunopathol. 19:1997;139-145.
146. Sizemore D.R., Branstrom A.A., Sadoff J.C. Attenuated bacteria as an oral DNA delivery vehicle for DNA-mediated immunization. Science. 270:1995;299-302.
147. Darji A., Guzmán C.A., Gerstel B., Wachholz P., Timmis K.N., Wehland J., Chakraborty T., Weiss S. Oral somatic transgene vaccination using attenuated S. typhimurium. Cell. 91:1997;765-775.
148. Paglia P., Medina E., Arioli I., Guzman C.A., Colombo M.P. Gene transfer in dendritic cells, induced by oral DNA vaccination with Salmonella typhimurium, results in protective immunity against a murine fibrosarcoma. Blood. 92:1998;3172-3176.
149. Paglia P., Terrazzini N., Schulze K., Guzmán C.A., Colombo M.P. In vivo correction of genetic defects of monocyte/macrophages using attenuated Salmonella as oral vectors for targeted gene delivery. Gene Ther. 7:2000;1725-1730.
150. Zöller M., Christ O. Prophylactic tumor vaccination: comparison of effector mechanisms initiated by protein versus DNA vaccination. J. Immunol. 166:2001;3440-3450.
151. Gentschev I., Dietrich G., Spreng S., Kolb-Mäurer A., Brinkmann V., Grode L., Hess J., Kaufmann S.H.E., Goebel W. Recombinant attenuated bacteria for the delivery of subunit vaccines. Vaccine. 19:2001;2621-2628.
152. Darji A., zur Lage S., Garbe A.I., Chakraborty T., Weiss S. Oral delivery of DNA vaccines using attenuated Salmonella typhimurium as carrier. FEMS Immunol. Med. Microbiol. 27:2000;341-349.
153. Catic A., Dietrich G., Gentschev I., Goebel W., Kaufmann S.H.E., Hess J. Introduction of protein or DNA delivered via recombinant Salmonella typhimurium into the major histocompatibility complex class I presentation pathway of macrophages. Microbes Infect. 2:1998;112-121.
154. Brunham R.C., Zhang D.-J. Transgene as vaccine for chlamydia. Am. Heart J. 138:1999;S519-S522.
155. Urashima M., Suzuki H., Yuza Y., Akiyama M., Ohno N., Eto Y. An oral CD40 ligand gene therapy against lymphoma using attenuated Salmonella typhimurium. Blood. 95:2000;1258-1263.
156. Montosi G., Paglia P., Garuti C., Guzman C.A., Bastin J.M., Colombo M.P., Pietrangelo A. Wild-type HFE protein normalizes transferring iron accumulation in macrophages from subjects with hereditary hemochromatosis. Blood. 96:2000;1125-1129.
157. Lode N.H., Pertl U., Xiang R., Gaedicke G., Riesfeld R.A. Tyrosine hydroxylase-based DNA-vaccination is effective against murine neuroblastoma. Med. Pediatr. Oncol. 35:2000;641-646.
158. Xiang R., Lode H.N., Chao T.-H., Ruehmann J.M., Dolman C.S., Rodriguez F., Whitton J.L., Overwijk W.W., Restifo N.P., Reisfeld R.A. An autologous oral DNA vaccine protects against murine melanoma. Proc. Natl. Acad. Sci. USA. 97:2000;5492-5497.
159. Niethammer A.G., Xiang R., Ruehlmann J.M., Lode H.N., Dolman C.S., Gillies S.D., Riesfeld R.A. Targeted interleukin 2 therapy enhances protective immunity induced by an autologous oral DNA vaccine against murine melanoma. Cancer Res. 61:2001;6178-6184.
160. Weth R., Christ O., Stevanovic S., Zöller M. Gene delivery by attenuated Salmonella typhimurium: comparing the efficacy of helper versus cytotoxic T cell priming in tumor vaccination. Cancer Gene Ther. 8:2001;599-611.
161. Woo P.C., Tsoi H.W., Leung H.C., Wong L.P., Wong S.S., Chan E., Yuen K.Y. Enhancement by ampicillin of antibody responses induced by a protein antigen and a DNA vaccine carried by live-attenuated Salmonella enterica serovar Typhi. Clin. Diagn. Lab. Immunol. 7:2000;596-599.
162. Woo P.C., Wong L.-P., Zheng B.-J., Yuen K.-Y. Unique immunogenicity of hepatitis B virus DNA vaccine presented by live-attenuated Salmonella typhimurium. Vaccine. 19:2001;2945-2954.
163. Zheng B., Woo P.C., Ng M., Wong L., Yuen K. A crucial role of macrophages in the immune responses to oral DNA vaccination against hepatitis B virus in a murine model. Vaccine. 20:2001;140-147.
164. Shiau A.-L., Chen Y.-L., Liao C.-Y., Huang Y.-S., Wu C.-L. Prothymosin α enhances protective immune responses induced by oral vaccination against pseudorabies delivered by Salmonella choleraesuis. Vaccine. 19:2001;1947-1956.
165. Fló J., Tisminetzky S., Baralle F. Oral transgene vaccination mediated by attenuated Salmonellae is an effective method to prevent Herpes simplex virus-2 induced disease in mice. Vaccine. 19:2001;1772-1782.
166. Mollenkopf H.J., Groine-Triebkorn D., Andersen P., Hess J., Kaufmann S.H. Protective efficacy against tuberculosis of ESAT-6 secreted by a live Salmonella typhimurium vaccine carrier strain and expressed by naked DNA. Vaccine. 19:2001;4028-4035.
167. Niethammer A.G., Primus F.J., Xiang R., Dolman C.S., Ruehlmann J.M., Ba Y., Gillies S.D., Riesfeld R.A. An oral DNA vaccine against human carcinoembryonic antigen (CEA) prevents grwoth and dissemination of Lewis lung carcinoma in CEA transgenic mice. Vaccine. 20:2001;421-429.
168. Wedemeyer H., Gagneten S., Davis A., Bartenschlager R., Feinstone S., Rehermann B. Oral immunization with HCV-NS3-transformed Salmonella: induction of HCV-specific CTL in a transgenic mouse model. Gastroenterology. 121:2001;1158-1166.
169. Shata M.T., Reitz M.S. Jr., DeVico A.L., Lewis G.K., Hone D.M. Mucosal and systemic HIV-1 Env-specific CD8(+) T-cells develop after intragastric vaccination with a Salmonella Env DNA vaccine vector. Vaccine. 20:2001;623-629.
170. Jain V., Mekalanos J.J. Use of lambda phage S and R gene products in an inducible lysis system for Vibrio cholerae and Salmonella enterica serovar Typhimurium-based DNA vaccine delivery systems. Infect. Immun. 68:2000;986-989.
171. Dietrich G., Bubert A., Gentschev I., Sokolovic Z., Simm A., Catic A., Kaufmann S.H.E., Hess J., Szalay A.A., Goebel W. Delivery of antigen-encoding plasmid DNA into the cytosol of macrophages by attenuated suicide Listeria monocytogenes. Nature Biotechnol. 16:1998;181-185.
172. Pawelek J.M., Low K.B., Bermudes D. Tumor-targeted Salmonella as a novel anticancer vector. Cancer Res. 57:1997;4537-4544.
173. Medina E., Guzmán C.A., Staendner L.H., Colombo M.P., Paglia P. Salmonella vaccine carrier strains: effective delivery system to trigger anti-tumor immunity by oral route. Eur. J. Immunol. 29:1999;693-699.