New technologies in using recombinant attenuated salmonella vaccine vectors

Critical Reviews in Immunology

Volumn 30, Issue 3, 2010, Pages 255-270

  Curtiss III, Roy ^a   Xin, Wei ^a   Li, Yuhua ^a   Kong, Wei ^a   Wanda, Soo Young ^a   Gunn, Bronwyn ^a   Wang, Shifeng ^a  

^a ARIZONA STATE UNIVERSITY   (United States)

Author keywords

Antigen synthesis; Biological containment; Delayed; Delayed attenuation or attenuation; Recombinant vaccines; Salmonella; Vaccine

Indexed keywords

ARABINOSE; BACTERIAL ANTIGEN; BACTERIAL VECTOR; LIPOPOLYSACCHARIDE; O ANTIGEN; PLASMID VECTOR; RECOMBINANT ANTIGEN; RECOMBINANT ATTENUATED SALMONELLOSIS VACCINE; SALMONELLOSIS VACCINE; UNCLASSIFIED DRUG; LIVE VACCINE; RECOMBINANT DNA;

ANTIGEN EXPRESSION; BACTERIAL STRAIN; BACTERIAL VIRULENCE; CHILD CARE; COST MINIMIZATION ANALYSIS; DIARRHEA; DRUG MECHANISM; DRUG SAFETY; DRUG SYNTHESIS; DRUG TOLERABILITY; GASTROINTESTINAL TRACT; GENE MUTATION; GENOTYPE; IMMUNE RESPONSE; IMMUNOGENICITY; LYMPHOID TISSUE; MUCOSAL IMMUNITY; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROMOTER REGION; REGULATORY MECHANISM; REVIEW; STREPTOCOCCUS PNEUMONIAE; VACCINATION; ADVERSE DRUG REACTION; GENE VECTOR; GENETICS; HUMAN; IMMUNOLOGY;

DNA, RECOMBINANT; DRUG-RELATED SIDE EFFECTS AND ADVERSE REACTIONS; GENETIC VECTORS; HUMANS; SALMONELLA VACCINES; STREPTOCOCCUS PNEUMONIAE; VACCINES, ATTENUATED;

EID: 77951004550     PISSN: 10408401     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (97)

1. Curtiss R III, Nakayama K, Kelly SM. Recombinant avirulent Salmonella vaccine strains with stable maintenance and high level expression of cloned genes in vivo. Immunol Invest. 1989;18(1-4):583-596
2. Nakayama K, Kelly SM, Curtiss R III. Construction of an Asd+ expression-cloning vector: stable maintenance and high level expression of cloned genes in a Salmonella vaccine strain. Bio/Technology. 1988;6:693-697
3. Curtiss R III, Kelly SM, Gulig PA, Nakayama K. Selective delivery of antigens by recombinant bacteria. Curr Top Microbiol Immunol. 1989;146:35-49.
4. Curtiss R III, Kelly SM, Gulig PA, Nakayama K. Stable recombinant avirulent Salmonella vaccine strains. Adv Exp Med Biol. 1989;251:33-47.
5. Galen JE, Levine MM. Can a 'fawless? live vector vaccine strain be engineered? Trends Microbiol. 2001;9(8):372-376
6. Curtiss R III. Antigen delivery systems: development of live recombinant attenuated bacterial antigen and DNA vaccine delivery vector vaccines. In: Mestecky J, Lamm ME, Strober W, Bienenstock J, McGhee JR, Mayer L, eds. Mucosal immunology. 3rd ed. San Diego: Academic Press, 2005.
7. Kwon YM, Cox MM, Calhoun LN. Salmonella-based vaccines for infectious diseases. Expert Rev Vaccines. 2007;6(2):147-152
8. Galen JE, Pasetti MF, Tennant S, Ruiz-Olvera P, Sztein MB, Levine MM. Salmonella enterica serovar Typhi live vector vaccines fnally come of age. Immunol Cell Biol. 2009 Jul;87(5):400-412
9. Park SM, Ko HJ, Shim DH, Yang JY, Park YH, Curtiss R III, Kweon MN. MyD88 signaling is not essential for induction of antigen-specifc B cell responses but is indispensable for protection against Streptococcus pneumoniae infection following oral vaccination with attenuated Salmonella expressing PspA antigen. J Immunol. 2008;181(9):6447-6455
10. Ko HJ, Yang JY, Shim DH, Yang H, Park SM, Curtiss R III, Kweon MN. Innate immunity mediated by MyD88 signal is not essential for induction of lipopolysaccharide-specifc B cell responses but is indispensable for protection against Salmonella enterica serovar Typhimurium infection. J Immunol. 2009;182(4):2305-2312
11. Foster JW. Te acid tolerance response of Salmonella typhimurium involves transient synthesis of key acid shock proteins. J Bacteriol. 1993;175(7):1981-1987
12. Foster JW. Low pH adaptation and the acid tolerance response of Salmonella typhimurium. Crit Rev Microbiol. 1995;21(4):215-237
13. Gunn JS. Mechanisms of bacterial resistance and response to bile. Microbes Infect. 2000;2(8):907-913
14. Prouty AM, Gunn JS. Salmonella enterica serovar Typhimurium invasion is repressed in the presence of bile. Infect Immun. 2000;68(12):6763-6769
15. Groisman EA, Parra-Lopez C, Salcedo M, Lipps CJ, Hefron F. Resistance to host antimicrobial peptides is necessary for Salmonella virulence. Proc Natl Acad Sci USA. 1992;89(24):11939-11943
16. Curtiss R III, Zhang X, Wanda SY, Kang HY, Konjufca V, Li Y, Gunn B, Wang S, Scarpellini G, Lee IS. Induction of host immune responses using Salmonella-vectored vaccines. In: Brogden KA, Minion FC, Cornick N, Stanton TB, Zhang Q, Nolan LK, Wannemuehler MJ, eds. Virulence mechanisms of bacterial pathogens. 4th ed. Washington DC: ASM Press, 2007.
17. Curtiss R III, Wanda SY, Gunn BM, Zhang X, Tinge SA, Ananthnarayan V, Mo H, Wang S, Kong W. Salmonella enterica serovar Typhimurium strains with regulated delayed attenuation in vivo. Infect Immun. 2009;77(3):1071-1082
18. Chatfeld SN, Strahan K, Pickard D, Charles IG, Hormaeche CE, Dougan G. Evaluation of Salmonella typhimurium strains harbouring defned mutations in htrA and aroA in the murine salmonellosis model. Microb Pathog. 1992;12(2):145-151
19. Curtiss R III. Bacterial infectious disease control by vaccine development. J Clin Invest. 2002;110(8):1061-1066
20. Xin W, Wanda SY, Li Y, Wang S, Mo H, Curtiss R III. Analysis of type II secretion of recombinant pneumo-coccal PspA and PspC in a Salmonella enterica serovar Typhimurium vaccine with regulated delayed antigen synthesis. Infect Immun. 2008;76(7):3241-3254
21. Li Y, Wang S, Scarpellini G, Gunn B, Xin W, Wanda SY, Roland KL, Curtiss R III. Evaluation of new generation Salmonella enterica serovar Typhimurium vaccines with regulated delayed attenuation to induce immune responses against PspA. Proc Natl Acad Sci USA. 2009;106(2):593-598
22. Greenwood B. Te epidemiology of pneumococcal infection in children in the developing world. Philos Trans R Soc Lond B Biol Sci. 1999;354(1384):777-785
23. Nnalue NA, Lindberg AA. Salmonella choleraesuis strains defcient in O antigen remain fully virulent for mice by parenteral inoculation but are avirulent by oral administration. Infect Immun. 1990;58(8):2493-2501
24. Roantree RJ. Te relationship of lipopolysaccharide structure to bacterial virulence. In: Weinbaum G, Kadis S, Ajl S, eds. Microbial toxins. Vol 5. New York: Academic Press, 1971.
25. Finlay BB, Starnbach MN, Francis CL, Stocker BA, Chatfeld S, Dougan G, Falkow S. Identifcation and characterization of TnphoA mutants of Salmonella that are unable to pass through a polarized MDCK epithelial cell monolayer. Mol Microbiol. 1988;2(6): 757-766
26. Stone BJ, Garcia CM, Badger JL, Hassett T, Smith RI, Miller VL. Identifcation of novel loci afecting entry of Salmonella enteritidis into eukaryotic cells. J Bacteriol. 1992;174(12):3945-3952
27. Fields PI, Swanson RV, Haidaris CG, Hefron F. Mutants of Salmonella typhimurium that cannot survive within the macrophage are avirulent. Proc Natl Acad Sci USA. 1986;83(14):5189-5193
28. Finlay BB, Brumell JH. Salmonella interactions with host cells: in vitro to in vivo. Philos Trans R Soc Lond B Biol Sci. 2000;355(1397):623-631
29. Reeves P. Role of O-antigen variation in the immune response. Trends Microbiol. 1995;3(10):381-386
30. Rowley D. Sensitivity of rough gram-negative bacteria to the bactericidal action of serum. J Bacteriol. 1968;95(5):1647-1650
31. Hensel M, Shea JE, Gleeson C, Jones MD, Dalton E, Holden DW. Simultaneous identifcation of bacterial virulence genes by negative selection. Science. 1995;269(5222):400-403
32. Mahan MJ, Heithof DM, Sinsheimer RL, Low DA. Assessment of bacterial pathogenesis by analysis of gene expression in the host. Annu Rev Genet. 2000;34:139-164
33. Muotiala A, Hovi M, Makela PH. Protective immunity in mouse salmonellosis: comparison of smooth and rough live and killed vaccines. Microb Pathog. 1989;6(1):51-60.
34. Smith HW. Te use of live vaccines in experimental Salmonella gallinarum infections in chickens with observations on their interference efect. J Hygiene. 1956;54(3):419-432
35. Lin ECC. Dissimilatory pathways for sugars, polyols, and carbohydrates. In: Neidhardt FC, Curtiss R III, Ingraham JL, Lin ECC, Low KB, Magasanik B, Reznikof WS, Riley M, Schaechter M, Umbarger HE, eds. Escherichia coli and Salmonella: cellular and molecular biology. 2nd ed. Washington, DC: ASM Press, 1996.
36. Raetz CRH. Bacterial lipopolysaccharides: a remakable family of bioactive macroamphiphiles. In: Neidhardt FC, Curtiss R III, Ingraham JL, Lin ECC, Low KB, Magasanik B, Reznikof WS, Riley M, Schaechter M, Umbarger HE, eds. Escherichia coli and Salmonella: cellular and molecular biology. 2nd ed. Washington, DC: ASM Press, 1996.
37. Germanier R, Furer E. Immunity in experimental salmonellosis. II. Basis for the avirulence and protective capacity of galE mutants of Salmonella typhimurium. Infect Immun. 1971;4(6):663-673
38. Fukasawa T, Nikaido H. Galactose sensitive mutants of Salmonella. Nature. 1959;184:1168-1169
39. Fukasawa T, Nikaido H. Galactose sensitive mutants of Salmonella II. Bacteriolysis induced by galactose. Biochim Biophys Acta. 1961;48:470-483
40. Clarke RC, Gyles CL. Galactose epimeraseless mutants of Salmonella typhimurium as live vaccines for calves. Can J Vet Res. 1986;50(2):165-173
41. Nnalue NA, Stocker BA. Test of the virulence and live-vaccine efcacy of auxotrophic and galE derivatives of Salmonella choleraesuis. Infect Immun. 1987;55(4):955-962
42. Markovitz A, Sydiskis RJ, Lieberman MM. Genetic and biochemical studies on mannose-negative mutants that are defcient in phosphomannose isomerase in Escherichia coli K-12. J Bacteriol. 1967;94(5):1492-1496
43. Rosen SM, Zeleznick LD, Fraenkel D, Wiener IM, Osborn MJ, Horecker BL. Characterization of the cell wall lipopolysaccharide of a mutant of Salmonella typhimurium lacking phosphomannose isomerase. Biochem Z. 1965;342(4):375-386
44. Collins LV, Attridge S, Hackett J. Mutations at rfc or pmi attenuate Salmonella typhimurium virulence for mice. Infect Immun. 1991;59(3):1079-1085
45. Kuehn MJ, Kesty NC. Bacterial outer membrane vesicles and the host-pathogen interaction. Genes Dev. 2005;19(22):2645-2655
46. Alaniz RC, Deatherage BL, Lara JC, Cookson BT. Membrane vesicles are immunogenic facsimiles of Salmonella typhimurium that potently activate dendritic cells, prime B and T cell responses, and stimulate protective immunity in vivo. J Immunol. 2007;179(11):7692-7701
47. Nnalue NA. All accessible epitopes in the Salmonella lipopolysaccharide core are associated with branch residues. Infect Immun. 1999;67(2):998-1003.
48. Stanislavsky ES, Makarenko TA, Kholodkova EV, Lugowski C. R-form lipopolysaccharides (LPS) of Gram-negative bacteria as possible vaccine antigens. FEMS Immunol Med Microbiol. 1997;18(3): 139-145
49. Jansson PE, Lindberg AA, Lindberg B, Wollin R. Structural studies on the hexose region of the core in lipopolysaccharides from Enterobacteriaceae. Eur J Biochem. 1981;115(3):571-577
50. Lüderitz O, Westphal O, Staub AM, Nikaido H. Isolation and chemical and immunological characterization of bacterial lipopolysaccharides. In: Weinbaum G, Kadis S, Ajl S, eds. Microbial toxins. Vol 4. New York: Academic Press, 1971.
51. Olsthoorn MM, Petersen BO, Schlecht S, Haverkamp J, Bock K, Tomas-Oates JE, Holst O. Identifcation of a novel core type in Salmonella lipopolysaccharide. Complete structural analysis of the core region of the lipopolysaccharide from Salmonella enterica sv. Arizonae O62. J Biol Chem. 1998;273(7):3817-3829
52. Kong W, Wanda SY, Zhang X, Bollen W, Tinge SA, Roland KL, Curtiss R III. Regulated programmed lysis of recombinant Salmonella in host tissues to release protective antigens and confer biological containment. Proc Natl Acad Sci USA. 2008;105(27):9361-9366
53. Guzman LM, Belin D, Carson MJ, Beckwith J. Tight regulation, modulation, and high-level expression by vectors containing the arabinose PBAD promoter. J Bacteriol. 1995;177(14):4121-4130
54. Menon KP, Lee NL. Activation of ara operons by a truncated AraC protein does not require inducer. Proc Natl Acad Sci USA. 1990;87(10):3708-3712
55. Miller SI, Kukral AM, Mekalanos JJ. A two-component regulatory system (phoP phoQ) controls Salmonella typhimurium virulence. Proc Natl Acad Sci USA. 1989;86(13):5054-5058
56. Curtiss R III, Kelly SM. Salmonella typhimurium deletion mutants lacking adenylate cyclase and cyclic AMP receptor protein are avirulent and immunogenic. Infect Immun. 1987;55(12):3035-3043
57. Dunn TM, Schleif R. Deletion analysis of the Escherichia coli ara PC and PBAD promoters. J Mol Biol. 1984;180(1):201-204
58. Zambrano MM, Siegele DA, Almiron M, Tormo A, Kolter R. Microbial competition: Escherichia coli mutants that take over stationary phase cultures. Science. 1993;259(5102):1757-1760
59. Fang FC, Libby SJ, Buchmeier NA, Loewen PC, Switala J, Harwood J, Guiney DG. Te alternative sigma factor katF (rpoS) regulates Salmonella virulence. Proc Natl Acad Sci USA. 1992;89(24):11978-11982
60. Takayanagi Y, Tanaka K, Takahashi H. Structure of the 5? upstream region and the regulation of the rpoS gene of Escherichia coli. Mol Gen Genet. 1994;243(5):525-531
61. Galán JE, Nakayama K, Curtiss R III. Cloning and characterization of the asd gene of Salmonella typhimurium: use in stable maintenance of recom-binant plasmids in Salmonella vaccine strains. Gene. 1990;94(1):29-35.
62. Galen JE, Nair J, Wang JY, Wasserman SS, Tanner MK, Sztein MB, Levine MM. Optimization of plas-mid maintenance in the attenuated live vector vaccine strain Salmonella typhi CVD 908-htrA. Infect Immun. 1999;67(12):6424-6433
63. Gerdes K. Te parB (hok/sok) locus of plasmid R1: a general purpose plasmid stabilization system. Bio/Technology. 1988;6:1402-1405
64. Kang HY, Srinivasan J, Curtiss R III. Immune responses to recombinant pneumococcal PspA antigen delivered by live attenuated Salmonella enterica serovar Typhimurium vaccine. Infect Immun. 2002;70(4):1739-1749
65. Rüssmann H, Shams H, Poblete F, Fu Y, Galán JE, Donis RQ. Delivery of epitopes by the Salmonella type III secretion system for vaccine development. Science. 1998;281:565-568
66. Konjufca V, Jenkins M, Wang S, Juarez-Rodriguez MD, Curtiss R III. Immunogenicity of recombinant attenuated Salmonella enterica serovar Typhimurium vaccine strains carrying a gene that encodes Eimeria tenella antigen SO7. Infect Immun. 2008;76(12):5745-5753
67. Husseiny MI, Hensel M. Evaluation of Salmonella live vaccines with chromosomal expression cassettes for translocated fusion proteins. Vaccine. 2009;27(28):3780-3787
68. Chatfeld SN, Charles IG, Makof AJ, Oxer MD, Dougan G, Pickard D, Slater D, Fairweather NF. 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. Bio/Technology. 1992;10:888-892
69. Schödel F, Kelly SM, Peterson D, Milich D, Hughes J, Tinge S, Wirtz R, Curtiss R III. Development of recombinant Salmonellae expressing hybrid hepatitis B virus core particles as candidate oral vaccines. Dev Biol Stand. 1994;82:151-158
70. Hohmann EL, Oletta CA, Loomis WP, Miller SI. Macrophage-inducible expression of a model antigen in Salmonella typhimurium enhances immunogenicity. Proc Natl Acad Sci USA. 1995;92(7):2904-2908
71. Bumann D. Regulated antigen expression in live recombinant Salmonella enterica serovar Typhimurium strongly afects colonization capabilities and specific CD4(+)-T-cell responses. Infect Immun. 2001;69(12):7493-7500
72. Orr N, Galen JE, Levine MM. Novel use of anaerobi-cally induced promoter, dmsA, for controlled expression of fragment C of tetanus toxin in live attenuated Salmonella enterica serovar Typhi strain CVD 908-htrA. Vaccine. 2001;19(13-14):1694-1700
73. Stratford R, McKelvie ND, Hughes NJ, Aldred E, Wiseman C, Curtis J, Bellaby T, Bentley M, Hindle Z, Brennan FR, Chatfeld SN, Dougan G, Khan SA. Optimization of Salmonella enterica serovar typhi DeltaaroC DeltassaV derivatives as vehicles for delivering heterologous antigens by chromosomal integration and in vivo inducible promoters. Infect Immun. 2005;73(1):362-368
74. Terry TD, Downes JE, Dowideit SJ, Mabbett AN, Jennings MP. Investigation of ansB and sspA derived promoters for multi-and single-copy antigen expression in attenuated Salmonella enterica var. typhimurium. Vaccine. 2005;23(36):4521-4531
75. Kang HY, Curtiss R III. Immune responses dependent on antigen location in recombinant attenuated Salmonella typhimurium vaccines following oral immunization. FEMS Immunol Med Microbiol. 2003;37(2-3):99-104.
76. Zekarias B, Mo H, Curtiss R III. Recombinant attenuated Salmonella enterica serovar typhimurium expressing the carboxy-terminal domain of alpha toxin from Clostridium perfringens induces protective responses against necrotic enteritis in chickens. Clin Vaccine Immunol. 2008;15(5):805-816
77. Osorio M, Wu Y, Singh S, Merkel TJ, Bhattacharyya S, Blake MS, Kopecko DJ. Anthrax protective antigen delivered by Salmonella enterica serovar Typhi Ty21a protects mice from a lethal anthrax spore challenge. Infect Immun. 2009;77(4):1475-1482
78. Hotz C, Fensterle J, Goebel W, Meyer SR, Kirchgraber G, Heisig M, Furer A, Dietrich G, Rapp UR, Gentschev I. Improvement of the live vaccine strain Salmonella enterica serovar Typhi Ty21a for antigen delivery via the hemolysin secretion system of Escherichia coli. Int J Med Microbiol. 2009;299(2):109-119
79. Galen JE, Zhao L, Chinchilla M, Wang JY, Pasetti MF, Green J, Levine MM. Adaptation of the endogenous Salmonella enterica serovar Typhi clyA-encoded hemo-lysin for antigen export enhances the immunogenicity of anthrax protective antigen domain 4 expressed by the attenuated live-vector vaccine strain CVD 908-htrA. Infect Immun. 2004;72(12):7096-7106
80. Rüssmann H, Igwe EI, Sauer J, Hardt WD, Bubert A, Geginat G. Protection against murine listeriosis by oral vaccination with recombinant Salmonella expressing hybrid Yersinia type III proteins. J Immunol. 2001;167(1):357-365
81. Shams H, F. Poblete, H. Russmann, J. E. Galán, and R. Q. Donis. Induction of specifc CD8+ memory T cells and long lasting protection following immunization with Salmonella typhimurium expressing a lymphocytic choriomeningitis MHC class I-restricted epitope. Vaccine. 2001;20(3-4):577-585
82. Provence DL, Curtiss R III. Isolation and characterization of a gene involved in hemagglutination by an avian pathogenic Escherichia coli strain. Infect Immun. 1994;62(4):1369-1380
83. Buddenborg C, Daudel D, Liebrecht S, Greune L, Humberg V, Schmidt MA. Development of a tripartite vector system for live oral immunization using a gram-negative probiotic carrier. Int J Med Microbiol. 2008;298(1-2):105-114
84. Srinivasan J, Tinge S, Wright R, Herr JC, Curtiss R III. Oral immunization with attenuated Salmonella expressing human sperm antigen induces antibodies in serum and the reproductive tract. Biol Reprod. 1995;53(2):462-471
85. Kane JF. Efects of rare codon clusters on high-level expression of heterologous proteins in Escherichia coli. Curr Opin Biotechnol. 1995;6(5):494-500.
86. Gustafsson C, Govindarajan S, Minshull J. Codon bias and heterologous protein expression. Trends in biotechnology. 2004;22(7):346-353
87. Burgess-Brown NA, Sharma S, Sobott F, Loenarz C, Oppermann U, Gileadi O. Codon optimization can improve expression of human genes in Escherichia coli: A multi-gene study. Protein expression and purifcation. 2008;59(1):94-102.
88. Stenström CM, Jin H, Major LL, Tate WP, Isaksson LA. Codon bias at the 3?-side of the initiation codon is correlated with translation initiation efciency in Escherichia coli. Gene. 2001;263(1-2):273-284
89. Witholt B, Boekhout M, Brock M, Kingma J, Heerikhuizen HV, Leij LD. An efcient and reproducible procedure for the formation of spheroplasts from variously grown Escherichia coli. Anal Biochem. 1976;74(1):160-170
90. Curtiss R III, Pereira DA, Hsu JC, Hull SC, Clark JE, Maturin LJ Sr, Goldschmidt R, Moody R, Inoue M, Alexander L. Biological containment: Te subordination of Escherichia coil K-12. In: Beers RF, Jr, Bassett EG, eds. Recombinant molecules: impact on science and society. New York: Raven Press, 1976.
91. Link C, Ebensen T, Standner L, Dejosez M, Reinhard E, Rharbaoui F, Guzman CA. An SopB-mediated immune escape mechanism of Salmonella enterica can be subverted to optimize the performance of live attenuated vaccine carrier strains. Microbes Infect. 2006;8(8):2262-2269
92. Li Y, Wang S, Xin W, Scarpellini G, Shi Z, Gunn B, Roland KL, Curtiss R III. A sopB deletion mutation enhances the immunogenicity and protective efcacy of a heterologous antigen delivered by live attenuated Salmonella enterica vaccines. Infect Immun. 2008;76(11):5238-5246
93. Dilts DA, Riesenfeld-Orn I, Fulginiti J P, Ekwall E, Granert C, Nonenmacher J, Brey RN, Cryz SJ, Karlsson K, Bergman K, Tompson T, Hu B, Bruckner AH, Lindberg AA. Phase I clinical trials of aroA aroD and aroA aroD htrA attenuated S. typhi vaccines; efect of formulation on safety and immunogenicity. Vaccine. 2000;18(15):1473-1784
94. Levine MM, Galen J, Tacket CO, Barry EM, Pasetti F, Sztein MB. Attenuated strains of Salmonella enterica serovar Typhi as live oral vaccines against typhoid fever. In: Levine MM, Kaper JB, Rappuoli R, Liu MA, Good MF, eds. New generation vaccines. New York: Marcel Dekker, 2004.
95. Hone DM, Attridge SR, Forrest B, Morona R, Daniels D, LaBrooy JT, Bartholomeusz RC, Shearman DJ, Hackett J. A galE via (Vi antigen-negative) mutant of Salmonella typhi Ty2 retains virulence in humans. Infect Immun. 1988;56(5):1326-1333
96. Tacket CO, Hone DM, Curtiss R III, Kelly SM, Losonsky G, Guers L, Harris AM, Edelman R, Levine MM. Comparison of the safety and immunogenic-ity of?aroC?aroD and?cya?crp Salmonella typhi strains in adult volunteers. Infect Immun. 1992;60(2): 536-541
97. Gahan ME, Webster DE, Wijburg OL, Wesselingh SL, Strugnell RA. Impact of prior immunological exposure on vaccine delivery by Salmonella enter-ica serovar Typhimurium. Vaccine. 2008;26(49): 6212-6220