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. 1991 Dec;59(12):4391–4397. doi: 10.1128/iai.59.12.4391-4397.1991

Antibody responses in the lungs of mice following oral immunization with Salmonella typhimurium aroA and invasive Escherichia coli strains expressing the filamentous hemagglutinin of Bordetella pertussis.

C A Guzmán 1, R M Brownlie 1, J Kadurugamuwa 1, M J Walker 1, K N Timmis 1
PMCID: PMC259054  PMID: 1937797

Abstract

The filamentous hemagglutinin (FHA) of Bordetella pertussis was expressed in the attenuated aroA mutant of Salmonella typhimurium, SL3261, and in a strain of Escherichia coli harboring Shigella flexneri plasmid pWR110, which encodes bacterial invasiveness for epithelial cells. Expression of FHA in these strains did not interfere with their ability to invade Henle cells. Immunoglobulins A and G specific for FHA were detected in lung washes of mice following oral immunization with the live recombinant organisms; antibody levels were significantly higher than those in mice immunized with killed bacteria administered orally or intraperitoneally. Live oral vaccines carrying protective antigens of B. pertussis may be an important alternative to new-generation component vaccines against whooping cough.

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Selected References

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  1. Bienenstock J., Befus D., McDermott M., Mirski S., Rosenthal K. Regulation of lymphoblast traffic and localization in mucosal tissues, with emphasis on IgA. Fed Proc. 1983 Dec;42(15):3213–3217. [PubMed] [Google Scholar]
  2. Brown A., Hormaeche C. E., Demarco de Hormaeche 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. 1987 Jan;155(1):86–92. doi: 10.1093/infdis/155.1.86. [DOI] [PubMed] [Google Scholar]
  3. Burnette W. N. "Western blotting": electrophoretic transfer of proteins from sodium dodecyl sulfate--polyacrylamide gels to unmodified nitrocellulose and radiographic detection with antibody and radioiodinated protein A. Anal Biochem. 1981 Apr;112(2):195–203. doi: 10.1016/0003-2697(81)90281-5. [DOI] [PubMed] [Google Scholar]
  4. Czerkinsky C., Svennerholm A. M., Quiding M., Jonsson R., Holmgren J. Antibody-producing cells in peripheral blood and salivary glands after oral cholera vaccination of humans. Infect Immun. 1991 Mar;59(3):996–1001. doi: 10.1128/iai.59.3.996-1001.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. De Magistris M. T., Romano M., Nuti S., Rappuoli R., Tagliabue A. Dissecting human T cell responses against Bordetella species. J Exp Med. 1988 Oct 1;168(4):1351–1362. doi: 10.1084/jem.168.4.1351. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Dougan G., Sellwood R., Maskell D., Sweeney K., Liew F. Y., Beesley J., Hormaeche C. In vivo properties of a cloned K88 adherence antigen determinant. Infect Immun. 1986 Apr;52(1):344–347. doi: 10.1128/iai.52.1.344-347.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Fairweather N. F., Chatfield S. N., Makoff A. J., Strugnell R. A., Bester J., Maskell D. J., Dougan G. Oral vaccination of mice against tetanus by use of a live attenuated Salmonella carrier. Infect Immun. 1990 May;58(5):1323–1326. doi: 10.1128/iai.58.5.1323-1326.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Fine P. E., Clarkson J. A. Reflections on the efficacy of pertussis vaccines. Rev Infect Dis. 1987 Sep-Oct;9(5):866–883. doi: 10.1093/clinids/9.5.866. [DOI] [PubMed] [Google Scholar]
  9. Formal S. B., Hale T. L., Kapfer C., Cogan J. P., Snoy P. J., Chung R., Wingfield M. E., Elisberg B. L., Baron L. S. Oral vaccination of monkeys with an invasive Escherichia coli K-12 hybrid expressing Shigella flexneri 2a somatic antigen. Infect Immun. 1984 Nov;46(2):465–469. doi: 10.1128/iai.46.2.465-469.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Frank D. W., Parker C. D. Isolation and characterization of monoclonal antibodies to Bordetella pertussis. J Biol Stand. 1984 Oct;12(4):353–365. doi: 10.1016/s0092-1157(84)80060-8. [DOI] [PubMed] [Google Scholar]
  11. Gearing A. J., Bird C. R., Redhead K., Thomas M. Human cellular immune responses to Bordetella pertussis infection. FEMS Microbiol Immunol. 1989 Mar;1(4):205–211. doi: 10.1111/j.1574-6968.1989.tb02384.x. [DOI] [PubMed] [Google Scholar]
  12. Guzmán C. A., Walker M. J., Rohde M., Timmis K. N. Direct expression of Bordetella pertussis filamentous hemagglutinin in Escherichia coli and Salmonella typhimurium aroA. Infect Immun. 1991 Oct;59(10):3787–3795. doi: 10.1128/iai.59.10.3787-3795.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Hale T. L. Hybrid vaccines using Escherichia coli as an antigen carrier. Res Microbiol. 1990 Sep-Oct;141(7-8):913–919. doi: 10.1016/0923-2508(90)90130-i. [DOI] [PubMed] [Google Scholar]
  14. Hale T. L., Sansonetti P. J., Schad P. A., Austin S., Formal S. B. Characterization of virulence plasmids and plasmid-associated outer membrane proteins in Shigella flexneri, Shigella sonnei, and Escherichia coli. Infect Immun. 1983 Apr;40(1):340–350. doi: 10.1128/iai.40.1.340-350.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Herrero M., de Lorenzo V., Timmis K. N. Transposon vectors containing non-antibiotic resistance selection markers for cloning and stable chromosomal insertion of foreign genes in gram-negative bacteria. J Bacteriol. 1990 Nov;172(11):6557–6567. doi: 10.1128/jb.172.11.6557-6567.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Hoiseth S. K., Stocker B. A. Aromatic-dependent Salmonella typhimurium are non-virulent and effective as live vaccines. Nature. 1981 May 21;291(5812):238–239. doi: 10.1038/291238a0. [DOI] [PubMed] [Google Scholar]
  17. Kimura A., Mountzouros K. T., Relman D. A., Falkow S., Cowell J. L. Bordetella pertussis filamentous hemagglutinin: evaluation as a protective antigen and colonization factor in a mouse respiratory infection model. Infect Immun. 1990 Jan;58(1):7–16. doi: 10.1128/iai.58.1.7-16.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
  19. 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. 1987 May 9;1(8541):1049–1052. doi: 10.1016/s0140-6736(87)90480-6. [DOI] [PubMed] [Google Scholar]
  20. Maurelli A. T., Baudry B., d'Hauteville H., Hale T. L., Sansonetti P. J. Cloning of plasmid DNA sequences involved in invasion of HeLa cells by Shigella flexneri. Infect Immun. 1985 Jul;49(1):164–171. doi: 10.1128/iai.49.1.164-171.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. McDermott M. R., Bienenstock J. Evidence for a common mucosal immunologic system. I. Migration of B immunoblasts into intestinal, respiratory, and genital tissues. J Immunol. 1979 May;122(5):1892–1898. [PubMed] [Google Scholar]
  22. Miller D. L., Alderslade R., Ross E. M. Whooping cough and whooping cough vaccine: the risks and benefits debate. Epidemiol Rev. 1982;4:1–24. doi: 10.1093/oxfordjournals.epirev.a036242. [DOI] [PubMed] [Google Scholar]
  23. Miller E., Ashworth L. A., Robinson A., Waight P. A., Irons L. I. Phase II trial of whole-cell pertussis vaccine vs an acellular vaccine containing agglutinogens. Lancet. 1991 Jan 12;337(8733):70–73. doi: 10.1016/0140-6736(91)90735-8. [DOI] [PubMed] [Google Scholar]
  24. 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 Bordetella pertussis. Infect Immun. 1990 Aug;58(8):2523–2528. doi: 10.1128/iai.58.8.2523-2528.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Neutra M. R., Phillips T. L., Mayer E. L., Fishkind D. J. Transport of membrane-bound macromolecules by M cells in follicle-associated epithelium of rabbit Peyer's patch. Cell Tissue Res. 1987 Mar;247(3):537–546. doi: 10.1007/BF00215747. [DOI] [PubMed] [Google Scholar]
  26. Newton S. M., Jacob C. O., Stocker B. A. Immune response to cholera toxin epitope inserted in Salmonella flagellin. Science. 1989 Apr 7;244(4900):70–72. doi: 10.1126/science.2468182. [DOI] [PubMed] [Google Scholar]
  27. Olander R. M., Muotiala A., Karvonen M., Kuronen T., Runeberg-Nyman K. Serum antibody response to B. pertussis Tn5 mutants, purified PT and FHA in two different mouse strains and passive protection in the murine intranasal infection model. Microb Pathog. 1990 Jan;8(1):37–45. doi: 10.1016/0882-4010(90)90006-c. [DOI] [PubMed] [Google Scholar]
  28. Pruzanski W., Saito S., Nitzan D. W. The influence of lysostaphin on phagocytosis, intracellular bactericidal activity, and chemotaxis of human polymorphonuclear cells. J Lab Clin Med. 1983 Aug;102(2):298–305. [PubMed] [Google Scholar]
  29. Romanus V., Jonsell R., Bergquist S. O. Pertussis in Sweden after the cessation of general immunization in 1979. Pediatr Infect Dis J. 1987 Apr;6(4):364–371. doi: 10.1097/00006454-198704000-00005. [DOI] [PubMed] [Google Scholar]
  30. Rudzik R., Clancy R. L., Perey D. Y., Day R. P., Bienenstock J. Repopulation with IgA-containing cells of bronchial and intestinal lamina propria after transfer of homologous Peyer's patch and bronchial lymphocytes. J Immunol. 1975 May;114(5):1599–1604. [PubMed] [Google Scholar]
  31. Sadoff J. C., Ballou W. R., Baron L. S., Majarian W. R., Brey R. N., Hockmeyer W. T., Young J. F., Cryz S. J., Ou J., Lowell G. H. Oral Salmonella typhimurium vaccine expressing circumsporozoite protein protects against malaria. Science. 1988 Apr 15;240(4850):336–338. doi: 10.1126/science.3281260. [DOI] [PubMed] [Google Scholar]
  32. Sandermann H., Jr, Strominger J. L. Purification and properties of C 55 -isoprenoid alcohol phosphokinase from Staphylococcus aureus. J Biol Chem. 1972 Aug 25;247(16):5123–5131. [PubMed] [Google Scholar]
  33. Sansonetti P. J., Hale T. L., Dammin G. J., Kapfer C., Collins H. H., Jr, Formal S. B. Alterations in the pathogenicity of Escherichia coli K-12 after transfer of plasmid and chromosomal genes from Shigella flexneri. Infect Immun. 1983 Mar;39(3):1392–1402. doi: 10.1128/iai.39.3.1392-1402.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Sansonetti P. J., Kopecko D. J., Formal S. B. Involvement of a plasmid in the invasive ability of Shigella flexneri. Infect Immun. 1982 Mar;35(3):852–860. doi: 10.1128/iai.35.3.852-860.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Sansonetti P. J., Ryter A., Clerc P., Maurelli A. T., Mounier J. Multiplication of Shigella flexneri within HeLa cells: lysis of the phagocytic vacuole and plasmid-mediated contact hemolysis. Infect Immun. 1986 Feb;51(2):461–469. doi: 10.1128/iai.51.2.461-469.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Sato Y., Cowell J. L., Sato H., Burstyn D. G., Manclark C. R. Separation and purification of the hemagglutinins from Bordetella pertussis. Infect Immun. 1983 Jul;41(1):313–320. doi: 10.1128/iai.41.1.313-320.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Stainer D. W., Scholte M. J. A simple chemically defined medium for the production of phase I Bordetella pertussis. J Gen Microbiol. 1970 Oct;63(2):211–220. doi: 10.1099/00221287-63-2-211. [DOI] [PubMed] [Google Scholar]
  38. Storsaeter J., Hallander H., Farrington C. P., Olin P., Möllby R., Miller E. Secondary analyses of the efficacy of two acellular pertussis vaccines evaluated in a Swedish phase III trial. Vaccine. 1990 Oct;8(5):457–461. doi: 10.1016/0264-410x(90)90246-i. [DOI] [PubMed] [Google Scholar]
  39. Thomas M. G., Ashworth L. A., Miller E., Lambert H. P. Serum IgG, IgA, and IgM responses to pertussis toxin, filamentous hemagglutinin, and agglutinogens 2 and 3 after infection with Bordetella pertussis and immunization with whole-cell pertussis vaccine. J Infect Dis. 1989 Nov;160(5):838–845. doi: 10.1093/infdis/160.5.838. [DOI] [PubMed] [Google Scholar]
  40. Walker M. J., Rohde M., Wehland J., Timmis K. N. Construction of minitransposons for constitutive and inducible expression of pertussis toxin in bvg-negative Bordetella bronchiseptica. Infect Immun. 1991 Nov;59(11):4238–4248. doi: 10.1128/iai.59.11.4238-4248.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]

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