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. 1997 Aug;65(8):3469–3473. doi: 10.1128/iai.65.8.3469-3473.1997

Phase variation affects long-term survival of Bordetella bronchiseptica in professional phagocytes.

A Banemann 1, R Gross 1
PMCID: PMC175492  PMID: 9234815

Abstract

Several Bordetella bronchiseptica isolates were investigated for intracellular survival in macrophages. A significant number of viable bacteria of all strains could be recovered even after 96 h postinfection. In all cases bvg mutants of the B. bronchiseptica strains showed a significant survival advantage over the respective wild-type strains. The bacteria were already located in phagolysosomes early after uptake. Neither opsonization of the bacteria nor activation of the macrophages with gamma interferon or lipopolysaccharide prior to infection affected uptake and survival of the bacteria.

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Selected References

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  1. Akerley B. J., Monack D. M., Falkow S., Miller J. F. The bvgAS locus negatively controls motility and synthesis of flagella in Bordetella bronchiseptica. J Bacteriol. 1992 Feb;174(3):980–990. doi: 10.1128/jb.174.3.980-990.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Barnard A., Mahon B. P., Watkins J., Redhead K., Mills K. H. Th1/Th2 cell dichotomy in acquired immunity to Bordetella pertussis: variables in the in vivo priming and in vitro cytokine detection techniques affect the classification of T-cell subsets as Th1, Th2 or Th0. Immunology. 1996 Mar;87(3):372–380. doi: 10.1046/j.1365-2567.1996.497560.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Beier D., Schwarz B., Fuchs T. M., Gross R. In vivo characterization of the unorthodox BvgS two-component sensor protein of Bordetella pertussis. J Mol Biol. 1995 May 5;248(3):596–610. doi: 10.1006/jmbi.1995.0245. [DOI] [PubMed] [Google Scholar]
  4. Carbonetti N. H., Khelef N., Guiso N., Gross R. A phase variant of Bordetella pertussis with a mutation in a new locus involved in the regulation of pertussis toxin and adenylate cyclase toxin expression. J Bacteriol. 1993 Oct;175(20):6679–6688. doi: 10.1128/jb.175.20.6679-6688.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Drevets D. A., Canono B. P., Leenen P. J., Campbell P. A. Gentamicin kills intracellular Listeria monocytogenes. Infect Immun. 1994 Jun;62(6):2222–2228. doi: 10.1128/iai.62.6.2222-2228.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Ewanowich C. A., Melton A. R., Weiss A. A., Sherburne R. K., Peppler M. S. Invasion of HeLa 229 cells by virulent Bordetella pertussis. Infect Immun. 1989 Sep;57(9):2698–2704. doi: 10.1128/iai.57.9.2698-2704.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Friedman R. L., Nordensson K., Wilson L., Akporiaye E. T., Yocum D. E. Uptake and intracellular survival of Bordetella pertussis in human macrophages. Infect Immun. 1992 Nov;60(11):4578–4585. doi: 10.1128/iai.60.11.4578-4585.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Graeff-Wohlleben H., Killat S., Banemann A., Guiso N., Gross R. Cloning and characterization of an Mn-containing superoxide dismutase (SodA) of Bordetella pertussis. J Bacteriol. 1997 Apr;179(7):2194–2201. doi: 10.1128/jb.179.7.2194-2201.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Gueirard P., Guiso N. Virulence of Bordetella bronchiseptica: role of adenylate cyclase-hemolysin. Infect Immun. 1993 Oct;61(10):4072–4078. doi: 10.1128/iai.61.10.4072-4078.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Gueirard P., Minoprio P., Guiso N. Intranasal inoculation of Bordetella bronchiseptica in mice induces long-lasting antibody and T-cell mediated immune responses. Scand J Immunol. 1996 Feb;43(2):181–192. doi: 10.1046/j.1365-3083.1996.d01-30.x. [DOI] [PubMed] [Google Scholar]
  11. Gueirard P., Weber C., Le Coustumier A., Guiso N. Human Bordetella bronchiseptica infection related to contact with infected animals: persistence of bacteria in host. J Clin Microbiol. 1995 Aug;33(8):2002–2006. doi: 10.1128/jcm.33.8.2002-2006.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Guzman C. A., Rohde M., Timmis K. N. Mechanisms involved in uptake of Bordetella bronchiseptica by mouse dendritic cells. Infect Immun. 1994 Dec;62(12):5538–5544. doi: 10.1128/iai.62.12.5538-5544.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Khelef N., Zychlinsky A., Guiso N. Bordetella pertussis induces apoptosis in macrophages: role of adenylate cyclase-hemolysin. Infect Immun. 1993 Oct;61(10):4064–4071. doi: 10.1128/iai.61.10.4064-4071.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Kuhn M., Goebel W. Induction of cytokines in phagocytic mammalian cells infected with virulent and avirulent Listeria strains. Infect Immun. 1994 Feb;62(2):348–356. doi: 10.1128/iai.62.2.348-356.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Langermans J. A., Van der Hulst M. E., Nibbering P. H., Hiemstra P. S., Fransen L., Van Furth R. IFN-gamma-induced L-arginine-dependent toxoplasmastatic activity in murine peritoneal macrophages is mediated by endogenous tumor necrosis factor-alpha. J Immunol. 1992 Jan 15;148(2):568–574. [PubMed] [Google Scholar]
  16. Lee C. K., Roberts A. L., Finn T. M., Knapp S., Mekalanos J. J. A new assay for invasion of HeLa 229 cells by Bordetella pertussis: effects of inhibitors, phenotypic modulation, and genetic alterations. Infect Immun. 1990 Aug;58(8):2516–2522. doi: 10.1128/iai.58.8.2516-2522.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Mahon B. P., Ryan M. S., Griffin F., Mills K. H. Interleukin-12 is produced by macrophages in response to live or killed Bordetella pertussis and enhances the efficacy of an acellular pertussis vaccine by promoting induction of Th1 cells. Infect Immun. 1996 Dec;64(12):5295–5301. doi: 10.1128/iai.64.12.5295-5301.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Mills K. H., Barnard A., Watkins J., Redhead K. Cell-mediated immunity to Bordetella pertussis: role of Th1 cells in bacterial clearance in a murine respiratory infection model. Infect Immun. 1993 Feb;61(2):399–410. doi: 10.1128/iai.61.2.399-410.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Redhead K., Watkins J., Barnard A., Mills K. H. Effective immunization against Bordetella pertussis respiratory infection in mice is dependent on induction of cell-mediated immunity. Infect Immun. 1993 Aug;61(8):3190–3198. doi: 10.1128/iai.61.8.3190-3198.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Saukkonen K., Cabellos C., Burroughs M., Prasad S., Tuomanen E. Integrin-mediated localization of Bordetella pertussis within macrophages: role in pulmonary colonization. J Exp Med. 1991 May 1;173(5):1143–1149. doi: 10.1084/jem.173.5.1143. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Savelkoul P. H., Kremer B., Kusters J. G., van der Zeijst B. A., Gaastra W. Invasion of HeLa cells by Bordetella bronchiseptica. Microb Pathog. 1993 Feb;14(2):161–168. doi: 10.1006/mpat.1993.1016. [DOI] [PubMed] [Google Scholar]
  22. Schipper H., Krohne G. F., Gross R. Epithelial cell invasion and survival of Bordetella bronchiseptica. Infect Immun. 1994 Jul;62(7):3008–3011. doi: 10.1128/iai.62.7.3008-3011.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Schwan W. R., Demuth A., Kuhn M., Goebel W. Phosphatidylinositol-specific phospholipase C from Listeria monocytogenes contributes to intracellular survival and growth of Listeria innocua. Infect Immun. 1994 Nov;62(11):4795–4803. doi: 10.1128/iai.62.11.4795-4803.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Steed L. L., Akporiaye E. T., Friedman R. L. Bordetella pertussis induces respiratory burst activity in human polymorphonuclear leukocytes. Infect Immun. 1992 May;60(5):2101–2105. doi: 10.1128/iai.60.5.2101-2105.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Steed L. L., Setareh M., Friedman R. L. Intracellular survival of virulent Bordetella pertussis in human polymorphonuclear leukocytes. J Leukoc Biol. 1991 Oct;50(4):321–330. doi: 10.1002/jlb.50.4.321. [DOI] [PubMed] [Google Scholar]
  26. Weiss A. A., Hewlett E. L. Virulence factors of Bordetella pertussis. Annu Rev Microbiol. 1986;40:661–686. doi: 10.1146/annurev.mi.40.100186.003305. [DOI] [PubMed] [Google Scholar]
  27. Wels W., Baldrich M., Chakraborty T., Gross R., Goebel W. Expression of bacterial cytotoxin genes in mammalian target cells. Mol Microbiol. 1992 Sep;6(18):2651–2659. doi: 10.1111/j.1365-2958.1992.tb01442.x. [DOI] [PubMed] [Google Scholar]
  28. Woolfrey B. F., Moody J. A. Human infections associated with Bordetella bronchiseptica. Clin Microbiol Rev. 1991 Jul;4(3):243–255. doi: 10.1128/cmr.4.3.243. [DOI] [PMC free article] [PubMed] [Google Scholar]

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