Advertisement

Immunity to Salmonella Infections

  • Toby K. Eisenstein
  • Duan Huang
  • Martin G. Schwacha
Part of the Infectious Agents and Pathogenesis book series (IAPA)

Abstract

Immunity to typhoid fever has been of interest since the turn of the century, principally because of a desire to develop optimal vaccines for use by military personnel. The British were the first to try vaccination under the direction of Wright and Semple in 1897.(1) The United States Army adopted compulsory vaccination in 1911, using the British method, which involved three injections of heat-killed organisms, spaced 1 week apart.(2) The results were a stunning success, with the number of cases falling from over 350/100,000 to less than 25/100,000 once compulsory vaccination was instituted.(2) At that time the causative organism was designated as Eberthella typhosa, the name being changed later to Salmonella typhosa, and finally to Salmonella typhi. Initially, the major antigens on the organism were determined to be the O (somatic antigens) and the H antigens (flagellar). In 1934 the Vi capsular antigen was discovered by Felix and Pitt(3) and shown to be a major virulence factor of S. typhi. Considerable research was invested in trying to assess the relative contribution of the O and Vi antigens to the protection conferred by vaccination. Since the Vi antigen was preserved better by alcohol than by heat, alcohol-preserved whole-cell vaccines were also tested. In 1953 Landy introduced acetone-killed and dried cells. These various whole killed-cell formulations were compared in extensive double-blind field trials carried out in the late 1950s and 1960s in British Guyana, Yugoslavia, Poland, and Russia under the auspices of the World Health Organization (WHO).(5,6)

Keywords

Cellular Immunity Typhoid Fever Oral Vaccine Protective Capacity Innate Resistance 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Wright, A., and Semple, D., 1897, Remarks on vaccination against typhoid fever, Br. Med. J. 1:256.PubMedCrossRefGoogle Scholar
  2. 2.
    Siler, J. R., et al., 1941, Immunization to Typhoid Fever, Johns Hopkins Press, Baltimore.Google Scholar
  3. 3.
    Felix, A., and Pitt, R. M., 1951, The pathogenic and immunogenic activity of Salmonella typhi in relation to its antigenic constituents, J. Hyg. 49:92–110.PubMedCrossRefGoogle Scholar
  4. 4.
    Robbins, J. D., and Robbins, J. B., 1984, Reexamination of the protective role of the capsular polysaccharide (Vi antigen) of Salmonella typhi [Review], J. Infect. Dis. 150:436–449.PubMedCrossRefGoogle Scholar
  5. 5.
    Joo, I., 1971, Bacterial diseases: The problem, and control by vaccines. Present status and perspectives of vaccination against typhoid fever, in: International Conference on the Application of Vaccines Against Viral, Rickettsial, and Bacterial Diseases of Man, Scientific Publication No. 226, Pan-American World Health Organization, Washington, D.C., pp. 329–341.Google Scholar
  6. 6.
    Eisenstein, T. K., and Sultzer, B. M., 1983, Immunity to Salmonella infection, Adv. Exp. Med. Biol. 162:261–296.PubMedCrossRefGoogle Scholar
  7. 7.
    Ashcroft, M. T., Ritchie, J. M., and Nicholson, C. C., 1964, Controlled field trial in British Guiana school children of heat-killed phenolized and acetone-killed lyophilized typhoid vaccines, Am. J. Hyg. 79:196–206.PubMedGoogle Scholar
  8. 8.
    Spaun, J., and Uemura, K., 1964, International reference preparations of typhoid vaccine. A report on international collaborative laboratory studies, Bull. WHO 31:761–791.PubMedGoogle Scholar
  9. 9.
    Jenkin, C. R., and Rowley, D., 1965, Partial purification of the “protective” antigen of Salmonella typhimurium and its distribution amongst various strains of bacteria, Aust. J. Exp. Biol. Med. Sci. 43:65–78.PubMedCrossRefGoogle Scholar
  10. 10.
    Herzberg, M., Nash, P., and Hino, S., 1972, Degree of immunity induced by killed vaccines to experimental salmonellosis in mice, Infect. Immun. 5:83–90.PubMedGoogle Scholar
  11. 11.
    Ornellas, E. P., Roantree, R. J., and Steward, J. P., 1970, The specificity and importance of humoral antibody in the protection of mice against intraperitoneal challenge with complement-sensitive and complement-resistant Salmonella, J. Infect. Dis. 121:113–123.PubMedCrossRefGoogle Scholar
  12. 12.
    Angerman, C. R., and Eisenstein, T. K., 1978, Comparative efficacy and toxicity of a ribosomal vaccine, acetone-killed cells, lipopolysaccharide, and a live cell vaccine prepared from Salmonella typhimurium, Infect. Immun. 19:575–582.PubMedGoogle Scholar
  13. 13.
    Lindberg, A. A., Rosenberg, L. T., Ljunggren, A., Garegg, P. J., Svensson, S., and Wallin, N. H., 1974, Effect of synthetic disaccharide-protein conjugate as an immunogen in Salmonella infection in mice, Infect. Immun. 10:541–545.PubMedGoogle Scholar
  14. 14.
    Svenson, S. B., Nurminen, M., and Lindberg, A. A., 1979, Artificial Salmonella vaccines: O-antigenic oligosaccharide-protein conjugates induce protection against infection with Salmonella typhimurium, Infect. Immun. 25:863–872.PubMedGoogle Scholar
  15. 15.
    Kuusi, N., Nurminen, M., Saxen, H., Valtonen, M., and Makela, P. H., 1979, Immunization with major outer membrane proteins in experimental salmonellosis of mice, Infect. Immun. 25:857–862.PubMedGoogle Scholar
  16. 16.
    Phillips, M., Castagna, R., Sultzer, B. M., and Eisenstein, T. K., 1989, Immunogenic endo-toxin associated protein from a rough strain of Salmonella, FEMS Microbiol. Immunol. 1: 485–490.PubMedCrossRefGoogle Scholar
  17. 17.
    Kuusi, N., Nurminen, M., Saxen, H., and Makela, P. H., 1981, Immunization with major outer membrane protein (porin) preparations in experimental murine salmonellosis: Effect of lipopolysaccharide, Infect. Immun. 34:328–332.PubMedGoogle Scholar
  18. 18.
    Jenkin, C. R., Rowley, D., and Auzins, I., 1965, The basis for immunity to mouse typhoid. I. The carrier state, Aust. J. Exp. Biol. Med. Sci. 42: 215–228.Google Scholar
  19. 19.
    Rowley, D., Auzins, I., and Jenkin, C. R., 1968, Further studies regarding the question of cellular immunity in mouse typhoid, Aust. J. Exp. Biol. Med. Sci. 46:447–463.PubMedCrossRefGoogle Scholar
  20. 20.
    Blanden, R. V., Mackaness, G. B., and Collins, F. M., 1966, Mechanisms of acquired resistance in mouse typhoid, J. Exp. Med. 124:585–600.PubMedCrossRefGoogle Scholar
  21. 21.
    Eisenstein, T. K., Killar, L. M., and Sultzer, B. M., 1984, Immunity to infection with Salmonella typhimurium: Mouse-strain differences in vaccine-and serum-mediated protection, J. Infect. Dis. 150:425–435.PubMedCrossRefGoogle Scholar
  22. 22.
    Hobson, D., 1957, Resistance to reinfection in experimental mouse typhoid, J. Hyg 55:334–343.PubMedCrossRefGoogle Scholar
  23. 23.
    Ushiba, D., Saito, K., Akiyama, T., Nakano, M., Sugiyama, T., and Shirono, S., 1959, Studies on experimental typhoid: Bacterial multiplication and host cell response after infection with Salmonella enteritidis in mice immunized with live and killed vaccines, Jpn. J. Microbiol. 3:231–242.PubMedGoogle Scholar
  24. 24.
    Ushiba, D., 1965, Two types of immunity in experimental typhoid; “Cellular immunity” and “humoral immunity,” Keio J. Med. 14:45–60.PubMedCrossRefGoogle Scholar
  25. 25.
    Collins, F. M., Mackaness, G. B., and Blanden, R. V., 1966, Infection-immunity in experimental salmonellosis, J. Exp. Med. 124:601–619.PubMedCrossRefGoogle Scholar
  26. 26.
    Mackaness, G. B., Blanden, R. V., and Collins, F. M., 1966, Host-parasite relations in mouse typhoid, J. Exp. Med. 124:573–583.PubMedCrossRefGoogle Scholar
  27. 27.
    Mackaness, G. B., 1971, Resistance to intracellular infection, J. Infect. Dis. 123:439–445.PubMedCrossRefGoogle Scholar
  28. 28.
    Collins, F. M., and Mackaness, G. B., 1968, Delayed hypersensitivity and Arthus reactivity in relation to host resistance in Salmonella-infected mice, J. Immunol. 101:830–845.PubMedGoogle Scholar
  29. 29.
    Collins, F. M., 1978, Cellular antimicrobial immunity [Review], Crit. Rev. Microbiol. 7:27–91.CrossRefGoogle Scholar
  30. 30.
    Collins, F. M., 1969, Effect of specific immune mouse serum on the growth of Salmonella enteritidis in mice preimmunized with living or ethyl alcohol-killed vaccines, J. Bacteriol. 97:676–683.PubMedGoogle Scholar
  31. 31.
    Plant, J., and Glynn, A. A., 1974, Natural resistance to Salmonella infection, delayed hypersensitivity and Ir genes in different strains of mice, Science 248:345–347.Google Scholar
  32. 32.
    Plant, J. E., Blackwell, J. M., O’Brien, A. D., Bradley, D.J., and Glynn, A. A., 1982, Are the Lsh and Ity disease resistance genes at one locus on mouse chromosome 1? Nature 297:510–511.PubMedCrossRefGoogle Scholar
  33. 33.
    Vidal, S. M., Malo, D., Vogan, K., Skamene, E., and Gros, P., 1993, Natural resistance to infection with intracellular parasites: Isolation of a candidate for Bcg, Cell 73:469–485.PubMedCrossRefGoogle Scholar
  34. 34.
    Lissner, C. R., Weinstein, D. L., and O’Brien, A. D., 1985, Mouse chromosome 1 Ity locus regulates microbicidal activity of isolated peritoneal macrophages against a diverse group of intracellular and extracellular bacteria, J. Immunol. 135:544–547.PubMedGoogle Scholar
  35. 35.
    Benjamin, W. H., Jr., Hall, P., Roberts, S. J., and Briles, D. E., 1990, The primary effect of the Ity locus is on the rate of growth of Salmonella typhimurium that are relatively protected from killing, J. Immunol. 144:3143–3151.PubMedGoogle Scholar
  36. 36.
    O’Brien, A. D., Scher, I., Campbell, G. H., MacDermott, R. P., and Formal, S. B., 1979, Susceptibility of CBA/N mice to infection with Salmonella typhimurium: Influence of the X-linked gene controlling B lymphocyte function, J. Immunol. 123:720–724.PubMedGoogle Scholar
  37. 37.
    O’Brien, A. D., Rosenstreich, D. L., Scher, I., Campbell, G. H., MacDermott, R. P., and Formal, S. B., 1980, Genetic control of susceptibility to Salmonella typhimurium in mice: Role of the Lps gene, J. Immunol. 124:20–24.PubMedGoogle Scholar
  38. 38.
    Eisenstein, T. K., Deakins, L. W., Killar, L., Saluk, P. H., and Sultzer, B. M., 1982, Dissociation of innate susceptibility to Salmonella infection and endotoxin responsiveness in C3HeB/FeJ mice and other strains in the C3H lineage, Infect. Immun. 36:696–703.PubMedGoogle Scholar
  39. 39.
    O’Brien, A. D., and Rosenstreich, D. L., 1977, Genetic control of the susceptibility of C3HeB/FeJ mice to Salmonella typhimurium is regulated by a locus distinct from known salmonella response genes, J. Immunol. 131:2613–2619.Google Scholar
  40. 40.
    Hormaeche, C. E., 1979, Genetics of natural resistance to salmonellae in mice, J. Immunol. 37:319–327.Google Scholar
  41. 41.
    Benjamin, W. H., Jr., Turnbough, C. L., Jr., Posey, B. S., and Briles, D. E., 1986, Salmonella typhimurium virulence genes necessary to exploit the Ity s/s genotype of the mouse, Infect. Immun. 51:872–878.PubMedGoogle Scholar
  42. 42.
    Benbernou, N., and Nauciel, C., 1994, Influence of mouse genotype and bacterial virulence in the generation of interferon-gamma-producing cells during the early phase of Salmonella typhimurium infection, Immunology 83:245–249.PubMedGoogle Scholar
  43. 43.
    Gowen, J. W., and Stadler, J., 1967, Genetic characteristics influencing vaccine-conferred immunity, J. Infect. Dis. 117:129–150.PubMedCrossRefGoogle Scholar
  44. 44.
    Robson, H. G., and Vas, S. I., 1972, Resistance of inbred mice to Salmonella typhimurium, J. Infect. Dis. 126:378–386.PubMedCrossRefGoogle Scholar
  45. 45.
    Hormaeche, C. E., 1979, Natural resistance to Salmonella typhimurium in different inbred mouse strains, Immunology 37:311–318.PubMedGoogle Scholar
  46. 46.
    Nauciel, C., Vilde, F., and Ronco, E., 1985, Host response to infection with a temperature-sensitive mutant of Salmonella typhimurium in a susceptible and a resistant strain of mice, Infect. Immun. 49:523–527.PubMedGoogle Scholar
  47. 47.
    Killar, L. M., and Eisenstein, T. K., 1984, Differences in delayed-type hypersensitivity responses in various mouse strains in the C3H lineage infected with Salmonella typhimurium, strain SL3235, J. Immunol. 133:1190–1196.PubMedGoogle Scholar
  48. 48.
    Eisenstein, T. K., and Angerman, C. R., 1978, Immunity to experimental Salmonella infection: Studies on the protective capacity and immunogenicity of lipopolysaccharide, acetone-killed cells, and ribosome-rich extracts of Salmonella typhimurium in C3H/HeJ and CD-1 mice, J. Immunol. 121:1010–1014.PubMedGoogle Scholar
  49. 49.
    Acharya, I. L., Lowe, C. U., Thapa, R., Gurubacharya, V. L., Shrestha, M. B., Bact, D., Cadoz, M., Schultz, D., Armand, J., Bryla, D. A., Trollfors, B., Cramton, T., Schneerson, R., and Robbins, J. B., 1987, Prevention of typhoid fever in Nepal with the Vi capsular polysac-charide of Salmonella typhi in mice, N. Engl. J. Med. 317:1101–1104.PubMedCrossRefGoogle Scholar
  50. 50.
    Klugman, K., Gilberson, I. T., Koornhof, H. J., Robbins, J. B., Schneerson, R., Schulz, D., Cadoz, M., and Armand, J., 1987, Vaccination advisory committee: Protective activity of Vi capsular polysaccharide vaccine against typhoid fever, Lancet 2:1165–1169.PubMedCrossRefGoogle Scholar
  51. 51.
    Ivanoff, B., Levine, M. M., and Lambert, P. H., 1994, Vaccination against typhoid fever: Present status [Review], Bull. WHO 72:957–971.PubMedGoogle Scholar
  52. 52.
    Marmion, D. E., Naylor, G. R. E., and Stewart, I. P., 1953, Second attacks of typhoid fever, J. Hyg. 51:260.PubMedCrossRefGoogle Scholar
  53. 53.
    Islam, A., Butler, T., and Ward, L. R., 1987, Reinfection with a different Vi-phage type of Salmonella typhi in an endemic area, J. Infect. Dis. 155:155–156.PubMedCrossRefGoogle Scholar
  54. 54.
    Hochadel, J. F., and Keller, K. E., 1977, Protective effects of passively transferred immune T-or B-lymphocytes in mice infected with Salmonella typhimurium, J. Infect. Dis. 135:813–823.PubMedCrossRefGoogle Scholar
  55. 55.
    Morris, J. A., Wray, C., and Sojka, W. J., 1976, The effect of T and B lymphocyte depletion on the protection of mice vaccinated with a Gal E mutant of Salmonella typhimurium, Br. J. Exp. Pathol. 57:354–360.PubMedGoogle Scholar
  56. 56.
    Davies, R., and Kotlarski, I., 1976, The role of thymus-derived cells in immunity to Salmonella infection, Aust. J. Exp. Biol. Med. Sci. 54:221–236.PubMedCrossRefGoogle Scholar
  57. 57.
    Nauciel, C., 1990, Role of CD4+ T cells and T-independent mechanisms in acquired resistance to Salmonella typhimurium infection, J. Immunol. 145:1265–1269.PubMedGoogle Scholar
  58. 58.
    Mixter, P. R., Camerini, V., Stone, B. J., Miller, V. L., and Kronenberg, M., 1994, Mouse T lymphocytes that express a gamma delta T-cell antigen receptor contribute to resistance to Salmonella infection in vivo, Infect. Immun. 62:4618–4621.PubMedGoogle Scholar
  59. 59.
    Chander, R., Sainis, K. B., and Lewis, N. F., 1995, Role of thymus-derived lymphocytes in acquired immunity to salmonellosis in mice, Microbiol. Immunol. 30:1299–1306.Google Scholar
  60. 60.
    Guilloteau, L., Buzoni-Gatel, D., Bernard, F., Lantier, I., and Lantier, F., 1993, Salmonella abortusovis infection in susceptible BALB/cby mice: Importance of Lyt-2+ and L3T4+ T cells in acquired immunity and granuloma formation, Microb. Pathog. 14:45–55.PubMedCrossRefGoogle Scholar
  61. 61.
    Hougen, H. P., and Jensen, E. T., 1990, Experimental Salmonella typhimurium infections in rats. III. Transfer of immunity with primed lymphocyte subpopulations, Acta Pathol. Microbiol. Immunol. Scand. 98:1015–1021.Google Scholar
  62. 62.
    Mastroeni, P., Villarreal-Ramos, B., and Hormaeche, C. E., 1993, Adoptive transfer of immunity to oral challenge with virulent salmonellae in innately susceptible BALB/c mice requires both immune serum and T cells, Infect. Immun. 61:3981–3984.PubMedGoogle Scholar
  63. 63.
    Paul, C., Shalala, K., Warren, R., and Smith, R., 1985, Adoptive transfer of murine host protection to salmonellosis with T-cell growth factor-dependent, Salmonella-specific T-cell lines, Infect. Immun. 48:40–43.PubMedGoogle Scholar
  64. 64.
    Paul, C. C., and Smith, R. A., 1988, Transfer of murine host protection by using interleukin-2-dependent T-lymphocyte lines, Infect. Immun. 56:2189–2192.PubMedGoogle Scholar
  65. 65.
    Killar, L. M., and Eisenstein, T. K., 1985, Immunity to Salmonella typhimurium infection in C3H/HeJ and C3H/HeNCrlBR mice: Studies with an aromatic-dependent live S. typhimurium strain as a vaccine, Infect. Immun. 47:605–612.PubMedGoogle Scholar
  66. 66.
    Maskell, D.J., Hormaeche, C. E., Harrington, K. A., Joysey, H. S., and Liew, F. Y., 1987, The initial suppression of bacterial growth in a salmonella infection is mediated by a localized rather than a systemic response, Microb. Pathog. 2:295–305.PubMedCrossRefGoogle Scholar
  67. 67.
    Hof, H., Emmerling, P., Hacker, J., and Hughes, C., 1982, The role of macrophages in primary and secondary infection of mice with Salmonella typhimurium, Ann. Immunol. (Inst. Pasteur) 133:21–32.CrossRefGoogle Scholar
  68. 68.
    O’Brien, A. D., Scher, I., and Formal, S. B., 1979, Effect of silica on the innate resistance of inbred mice to Salmonella typhimurium infection, Infect. Immun. 25:513–520.PubMedGoogle Scholar
  69. 69.
    Killar, L. M., and Eisenstein, T. K., 1986, Delayed-type hypersensitivity and immunity to Salmonella typhimurium, Infect. Immun. 52:504–508.PubMedGoogle Scholar
  70. 70.
    O’Brien, A. D., and Metcalf, E. S., 1982, Control of early Salmonella typhimurium growth in innately Salmonella-resistant mice does not require functional T lymphocytes, J. Immunol. 129:1349–1351.PubMedGoogle Scholar
  71. 71.
    Hormaeche, C. E., Mastroeni, P., Arena, A., Uddin, J., and Joysey, H. S., 1990, T cells do not mediate the initial suppression of a Salmonella infection in the RES, Immunology 70:247–250.PubMedGoogle Scholar
  72. 72.
    Schafer, R., and Eisenstein, T. K., 1992, Natural killer cells mediate protection induced by a Salmonella aroA mutant, Infect. Immun. 60:791–797.PubMedGoogle Scholar
  73. 73.
    Nakoneczna, I., and Hsu, H. S., 1980, The comparative histopathology of primary and secondary lesions in murine salmonellosis, Br. J. Exp. Pathol. 61:76–84.PubMedGoogle Scholar
  74. 74.
    Dunlap, N. E., Benjamin, W. H., Berry, K. A., Eldridge, J. H., and Briles, D. E., 1992, A “safe site” for Salmonella typhimurium is within the splenic polymorphonuclear cells, Microb. Pathog. 13:181–190.PubMedCrossRefGoogle Scholar
  75. 75.
    Matsumura, H., Onozuka, K., Terada, Y., Nakano, Y and Nakano, M., 1990, Effect of murine recombinant interferon-7 in the protection of mice against Salmonella, Int.J. Immunophar-macol. 12:49–56.CrossRefGoogle Scholar
  76. 76.
    Nakano, Y., Onozuka, K., Terada, Y., Shinomiya, H., and Nakano, M., 1990, Protective effect of recombinant tumor necrosis factor-α in murine salmonellosis, J. Immunol. 144:1935–1941.PubMedGoogle Scholar
  77. 77.
    Muotiala, A., and Makela, P. H., 1990, The role of IFN-7 in murine Salmonella typhimurium infection, Microb. Pathog. 8:135–141.PubMedCrossRefGoogle Scholar
  78. 78.
    Nauciel, C., and Espinasse-Maes, F., 1992, Role of gamma interferon and tumor necrosis factor alpha in resistance to Salmonella typhimurium infection, Infect. Immun. 60:450–454.PubMedGoogle Scholar
  79. 79.
    Muotiala, A., and Makela, P. H., 1993, Role of gamma interferon in late stages of murine salmonellosis, Infect. Immun. 61:4248–4253.PubMedGoogle Scholar
  80. 80.
    Mastroeni, P., Villarreal-Ramos, B., and Hormaeche, C. E., 1993, Effect of late administration of anti-TNF alpha antibodies on a Salmonella infection in the mouse model, Microb. Pathog. 14:473–480.PubMedCrossRefGoogle Scholar
  81. 81.
    Mastroeni, P., Villarreal-Ramos, B., and Hormaeche, C. E., 1992, Role of T cells, TNF alpha and IFN gamma in recall of immunity to oral challenge with virulent salmonellae in mice vaccinated with live attenuated aro-Salmonella vaccines, Microb. Pathog. 13:477–491.PubMedCrossRefGoogle Scholar
  82. 82.
    Ramarathinam, L., Niesel, D. W., and Kumpel, G. R., 1993, Ity influences the production of IFN-7 by murine splenocytes stimulated in vitro with Salmonella typhimurium, J. Immunol. 150: 3965–3972.PubMedGoogle Scholar
  83. 83.
    Morrissey, P. J., and Charrier, K., 1994, Treatment of mice with IL-1 before infection increases resistance to a lethal challenge with Salmonella typhimurium. The effect correlates with the resistance allele at the Ity locus, J. Immunol. 153:212–219.PubMedGoogle Scholar
  84. 84.
    Nakano, Y., Kasahara, T., Mukaida, N., Ko, Y. C., Nakano, M., and Matsushima, K., 1994, Protection against lethal bacterial infection in mice by monocyte-chemotactic and-activating factor, Infect. Immun. 62:377–383.PubMedGoogle Scholar
  85. 85.
    Carter, P. B., and Collins, F. M., 1974, The route of enteric infection in normal mice, J. Exp. Med. 139:1189–1203.PubMedCrossRefGoogle Scholar
  86. 86.
    Wahdan, M. H., Serie, C., Cerisier, Y., Sallam, S., and Germanier, R., 1982, A controlled field trial of live Salmonella typhi strain Ty21a oral vaccine against typhoid: Three-year results, J. Infect. Dis. 145:292–295.PubMedCrossRefGoogle Scholar
  87. 87.
    Levine, M. M., and Hone, D. M., 1991, Typhoid fever, in: Vaccines and Immunotherapy (S. J. J. Cryz, ed.), Pergamon Press, New York, pp. 59–72.Google Scholar
  88. 88.
    Gilman, R. H., Hornick, R. B., Woodward, W. E., DuPont, H. L., Snyder, M.J., Levine, M. M., and Libonati, J. P., 1977, Evaluation of a UDP-glucose-4-epimeraseless mutant of Salmonella typhi as a live oral vaccine, J. Infect. Dis. 136:717–723.PubMedCrossRefGoogle Scholar
  89. 89.
    D’Amelio, R., Tagliabue, A., Nencioni, L., Di Addario, A., Villa, L., Manganaro, M., Boraschi, D., Le Moli, S., Nisini, R., and Matricardi, P. M., 1988, Comparative analysis of immunological responses to oral (Ty21a) and parenteral (TAB) typhoid vaccines, Infect. Immun. 56:2731–2735.PubMedGoogle Scholar
  90. 90.
    Hoiseth, S. K., and Stocker, B. A. D., 1981, Aromatic-dependent Salmonella typhimurium are non-virulent and effective as live vaccines, Nature 291:238–239.PubMedCrossRefGoogle Scholar
  91. 91.
    Cardenas, L., and Clements, J. D., 1992, Oral immunization using live attenuated Salmonella spp. as carriers of foreign antigens [Review], Clin. Microbiol. Rev. 5:328–342.PubMedGoogle Scholar
  92. 92.
    Flynn, J. L., Weiss, W. R., Norris, K. A., Seifert, H. S., Kumar, S., and So, M., 1990, Generation of a cytotoxic T-lymphocyte response using a Salmonella antigen delivery system, Mol. Microbiol. 4:2111–2118.PubMedCrossRefGoogle Scholar
  93. 93.
    Brown, A., Hormaeche, C. E., Demarco de Hormaeche, R., Winther, M., Dougan, G., and Stocker, B. A., 1987, An attenuated aroA Salmonella typhimurium vaccine elicits humoral and cellular immunity to cloned beta-galactosidase in mice, J. Infect. Dis. 155:86–92.PubMedCrossRefGoogle Scholar
  94. 94.
    Michetti, P., Mahan, M. J., Slauch, J. M., Mekalanos, J. J., and Neutra, M. R., 1992, Monoclonal secretory immunoglobulin A protects mice against oral challenge with the invasive pathogen Salmonella typhimurium, Infect. Immun. 60:1786–1792.PubMedGoogle Scholar
  95. 95.
    Bao, J. X., and Clements, J. D., 1991, Prior immunologic experience potentiates the subsequent antibody response when Salmonella strains are used as vaccine carriers, Infect. Immun. 59:3841–3845.PubMedGoogle Scholar
  96. 96.
    Lee, J. C., Gibson, C. W., and Eisenstein, T. K., 1985, Macrophage-mediated mitogenic suppression induced in mice of the C3H lineage by a vaccine strain of Salmonella typhi-murium, Cell. Immunol. 91:75–91.PubMedCrossRefGoogle Scholar
  97. 97.
    Al-Ramadi, B. K., Meissler, J.J., Jr., Huang, D., and Eisenstein, T. K., 1992, Immunosuppres-sion induced by nitric oxide and its inhibition by interleukin-4, Eur. J. Immunol. 22:2249–2254.PubMedCrossRefGoogle Scholar
  98. 98.
    Al-Ramadi, B. K., Greene, J. M., Meissler, J. J., Jr., and Eisenstein, T. K., 1992, Immunosup-pression induced by attenuated Salmonella: Effect of LPS responsiveness on development of suppression, Microb. Pathog. 12:267–278.PubMedCrossRefGoogle Scholar
  99. 99.
    Eisenstein, T. K., Killar, L. M., Stocker, B. A., and Sultzer, B. M., 1984, Cellular immunity induced by avirulent Salmonella in LPS-defective C3H/HeJ mice, J. Immunol. 133:958–961.PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 1996

Authors and Affiliations

  • Toby K. Eisenstein
    • 1
  • Duan Huang
    • 1
  • Martin G. Schwacha
    • 1
  1. 1.Department of Microbiology and Immunology, School of MedicineTemple UniversityPhiladelphiaUSA

Personalised recommendations