Phagosome acidification has opposite effects on intracellular survival of Bordetella pertussis and B. bronchiseptica

Infection and Immunity

Volumn 68, Issue 12, 2000, Pages 7039-7048

  Schneider, Boris ^a   Gross, Roy ^a   Haas, Albert ^a  

^a UNIVERSITY OF WÜRZBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; AMMONIUM CHLORIDE; BAFILOMYCIN A1; CATHEPSIN D; MEMBRANE PROTEIN; MONENSIN; PROTON PUMP; TRANSFERRIN RECEPTOR;

ACIDIFICATION; ANIMAL CELL; ARTICLE; BACTERIAL GROWTH; BORDETELLA BRONCHISEPTICA; BORDETELLA PERTUSSIS; CELL PH; CELL SURVIVAL; ENDOSOME; LYSOSOME MEMBRANE; MACROPHAGE; NONHUMAN; PHAGOCYTOSIS; PHAGOSOME; PRIORITY JOURNAL;

EID: 0034443266     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.68.12.7039-7048.2000     Document Type: Article

References (64)

1. Authier, F., J. S. Mort, A. W. Bell, B. I. Posner, and J. J. Bergeron. 1995. Proteolysis of glucagon within hepatic endosomes by membrane-associated cathepsins B and D. J. Biol. Chem. 270:15798-15807.
2. Banemann, A., and R. Gross. 1997. Phase variation affects long-term survival of Bordetella bronchiseptica in professional phagocytes. Infect. Immun. 65: 3469-3473.
3. Banemann, A., H. Deppisch, and R. Gross. 1998. The lipopolysaccharide of Bordetella bronchiseptica acts as a protective shield against antimicrobial peptides. Infect. Immun. 66:5507-5612.
4. Barnard, A., B. P. Mahon, J. Watkins, K. Readhead, and K. H. Mills. 1996. 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 87:372-380.
5. Beier, D., B. Schwarz, T. M. Fuchs, and R. Gross. 1995. In vivo characterization of the unorthodox BvgS two-component sensor protein of Bordetella pertussis. J. Mol. Biol. 248:596-610.
6. Bowman, E. J., A. Siebers, and K. Altendorf. 1988. Bafilomycins: a class of inhibitors of membrane ATPases from microorganisms, animal cells, and plant cells. Proc. Natl. Acad. Sci. USA 85:7972-7976.
7. Chen, J. W., T. L. Murphy, M. C. Willingham, I. Pastan, and J. T. August. 1985. Identification of two lysosomal membrane glycoproteins. J. Cell Biol. 101:85-95.
8. Chhatwal, G. S., M. J. Walker, H. Yan, K. N. Timmis, and C. A. Guzman. 1996. Temperature dependent expression of an acid phosphatase by Bordetella bronchiseptica: role in intracellular survival. Microb. Pathog. 22:257-264.
9. Desjardins, M., J. E. Celis, G. van Meer, H. Dieplinger, A. Jahraus, G. Griffiths, and L. A. Huber. 1994. Molecular characterization of phagosomes. J. Biol. Chem. 269:32194-32200.
10. Desjardins, M., L. A. Huber, R. G. Parton, and D. Griffiths. 1994. Biogenesis of phagolysosomes proceeds through a sequential series of interactions with the endocytic apparatus. J. Cell Biol. 124:677-688.
11. Ewanowich, C. A., A. R. Melton, A. A. Weiss, R. K. Sherburne, and M. S. Peppler. 1989. Invasion of HeLa 229 cells by virulent Bordetella pertussis. Infect. Immun. 57:2698-2704.
12. Forde, C. B., R. Parton, and J. G. Coote. 1998. Bioluminescence as a reporter of intracellular survival of Bordetella bronchiseptica in murine phagocytes. Infect. Immun. 66:3198-3207.
13. Fortier, A. H., D. A. Leiby, R. B. Narayanan, E. Asafoadjei, R. M. Crawford, C. A. Nacy, and M. S. Meltzer. 1995. Growth of Francisella turlarensis LVS in macrophages: the acidic intracellular compartment provides essential iron required for growth. Infect. Immun. 63:1478-1483.
14. Foster, J. W. 1999. When protons attack: microbial strategies of acid adaptation. Curr. Opin. Microbiol. 2:170-174.
15. Fridovich, I. 1978. The biology of oxygen radicals. Science 201:875-880.
16. Friedman, R. L., K. Nordensson, L. Wilson, E. T. Akporiaye, and D. E. Yocum. 1992. Uptake and intracellular survival of Bordetella pertussis in human macrophages. Infect. Immun. 60:4578-4585.
17. Ganz, T., and R. I. Lehrer. 1998. Antimicrobial peptides of vertebrates. Curr. Opin. Immunol. 10:41-44.
18. Goodnow, R. A. 1980. Biology of Bordetella bronchiseptica. Microbiol. Rev. 44:722-738.
19. Graeff-Wohlleben, H., S. Killat, A. Banemann, N. Guiso, and R. Gross. 1997. Cloning and characterization of an Mn-containing superoxide dismutase (SodA) of Bordetella pertussis. J. Bacteriol. 179:2194-2201.
20. Gueirard, P., and N. Guiso. 1993. Virulence of Bordetella bronchiseptica: role of adenylate cyclase-hemolysin. Infect. Immun. 61:4072-4078.
21. Gueirard, P., P. Minoprio, and N. Guiso. 1996. Intranasal inoculation of Bordetella bronchiseptica in mice induces long-lasting antibody and T-cell mediated immune responses. Scand. J. Immunol. 43:181-192.
22. Gueirard, P., C. Weber, A. LeCoustumier, and N. Guiso. 1994. Human Bordetella bronchiseptica infection related to contact with infected animals: persistence of bacteria in the host. J. Clin. Microbiol. 33:2002-2006.
23. Guzman, C. A., M. Rohde, M. Bock, and K. N. Timmis. 1994 Invasion and intracellular survival of Bordetella bronchiseptica in mouse dendritic cells. Infect. Immun. 62:5528-5537.
24. Haas, A. 1998. Reprogramming the phagocytic pathway - intracellular pathogens and their vacuoles. Mol. Membr. Biol. 15:103-121.
25. Haas, A., and W. Goebel. 1992. Microbial strategies to prevent oxygen-dependent killing by phagocytes. Free Radic. Res. Commun. 16:137-157.
26. Hart, P. D., and M. R. Young. 1991. Ammonium chloride, an inhibitor of phagosome-lysosome fusion in macrophages, concurrently induces phagosome-endosome fusion, and opens a novel pathway: studies of a pathogenic Mycobacterium and a nonpathogenic yeast. J. Exp. Med. 174:881-889.
27. Hewlett, E. L. 1995. Bordetella species, p. 2078-2084. In G. L. Mandell, R. G. Douglas, and J. E. Bennett (ed.), Principles and practice of infectious diseases. Churchill Livingstone, New York, N.Y.
28. Horton, M. R., S. Shapiro, C. Bao, C. J. Löwenstein, and P. W. Noble. 1999. Induction and regulation of macrophage metalloelastase by hyaluronan fragments in mouse macrophages. J. Immunol. 162:4171-4176.
29. Imaizumi, A., Y. Suzuki, S. Ono, H. Sato, and Y. Sato. 1983. Effect of heptakis(2,6-O-dimethyl)β-cyclodextrin on the production of pertussis toxin by Bordetella pertussis. Infect. Immun. 41:1138-1143.
30. Jungnitz, H., N. P. West, M. J. Walker, G. S. Chhatwal, and C. A. Guzman. 1998. A second two-component regulatory system of Bordetella bronchiseptica required for bacterial resistance to oxidative stress, production of acid phosphatase, and in vivo persistence. Infect. Immun. 66:4640-4650.
31. Khelef, N., A. Zychlinsky, and N. Guiso. 1993. Bordetella pertussis induces apoptosis in macrophages: role of adenylate cyclase-hemolysin. Infect. Immun. 61:4064-4071.
32. Lee, C. K., A. L. Roberts, T. M. Finn, S. Knapp, and J. J. Mekalanos. 1990. A new assay for invasion of HeLa229 cells by Bordetella pertussis: effect of inhibitors, phenotypic modulation, and genetic alterations. Infect. Immun. 58:2516-2522.
33. Leininger, E., M. Roberts, M. G. Kenimer, I. G. Charles, N. Fairweather, P. Novotny, and M. J. Brennan. 1991. Pertactin, an Arg-Gly-Asp-containing Bordetella pertussis surface protein that promotes adherence of mammalian cells. Proc. Natl. Acad. Sci. USA 88:345-349.
34. Lin, J., I. S. Lee, J. Frey, J. L. Slonczewski, and J. W. Foster. 1995. Comparative analysis of extreme acid survival in Salmonella typhimurium, Shigella flexneri, and Escherichia coli. J. Bacteriol. 177:4097-4104.
35. Mahon, B. P., M. S. Ryan, F. Griffin, and K. H. Mills. 1996. 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. 64:5295-5301.
36. Mbawuike, I. N., and H. B. Hercowitz. 1989. MH-S, a murine alveolar macrophage cell line: morphological, cytochemical, and functional characteristics. J. Leukoc. Biol. 46:119-127.
37. McMillan, D. J., M. Shojaei, G. S. Chhatwal, C. A. Guzman, and M. J. Walker. 1996. Molecular analysis of the bvg-repressed urease of Bordetella bronchiseptica. Microb. Pathog. 21:379-394.
38. Middendorf, B., and R. Gross. 1999. Representational difference analysis identifies a strain-specific LPS biosynthesis locus in Bordetella spp. Mol. Gen. Genet. 262:189-198.
39. Mills, I. G., A. T. Johnes, and M. J. Clague. 1998. Involvement of the endosomal autoantigen EEA1 in homotypic fusion of early endosomes. Curr. Biol. 8:881-884.
40. Mills, K. H., A. Barnard, J. Watkins, and K. Redhead. 1993. Cell-mediated immunity to Bordetella pertussis: role of Th1 cells in bacterial clearance in a murine respiratory infection model. Infect. Immun. 61:399-410.
41. Nolta, V. K., H. Padh, and T. L. Steck. 1993. An immunocytochemical analysis of the vacuolar pump in Dictyostelium discoideum. J. Cell Sci. 105: 849-859.
42. Oh, Y. K., C. Alpuche-Aranda, E. Berthiaume, T. Jinks, S. I. Miller, and J. A. Swanson. 1996. Rapid and complete fusion of macrophage lysosomes with phagosomes containing Salmonella typhimurium. Infect. Immun. 64:3877-3883.
43. Ohkuma, S., and B. Poole. 1978. Fluorescence probe measurement of the intralysosomal pH in living cells and the perturbation of pH by various agents. Proc. Natl. Acad. Sci. USA 75:3327-3331.
44. Ojcius, D. M., F. Niedergang, A. Subtil, R. Hellio, and A. Dautry-Varsat. 1996. Immunology and the confocal microscope. Res. Immunol. 147:175-188.
45. Pearson, R. D., P. Symes, M. Conboy, A. A. Weiss, and E. L. Hewlett. 1987. Inhibition of monocyte oxidative responses by Bordetella pertussis adenylate cyclase toxin. J. Immunol. 139:2749-2754.
46. Pitt, A., L. S. Mayorga, P. D. Stahl, and A. L. Schwartz. 1992. Alterations in the protein composition of maturing phagosomes. J. Clin. Investig. 90:1978-1983.
47. Pittman, M. 1984. Genus Bordetella, p. 388-393. In N. R. Krieg and J. G. Holt (ed.), Bergey's manual of systematic bacteriology, vol. 1. The Williams & Wilkins Co., Baltimore, Md.
48. Pizza, M., A. Bartoloni, A. Prugnola, S. Silvestri, and Rappuoli. 1988. Subunit S1 of pertussis toxin: mapping of the regions essential for ADP-ribosyltransferase activity. Proc. Natl. Acad. Sci. USA 85:7521-7525.
49. Porte, F., J. P. Liautard, and S. Köhler. 1999. Early acidification of phagosomes containing Brucella suis is essential for intracellular survival in murine macrophages. Infect. Immun. 67:4041-4047.
50. Prabhananda, B. S., and M. H. Kombrail. 1992. Monensin-mediated transports of H+, Na+, K+ and Li+ ions across vesicular membranes: T-jump studies. Biochim. Biophys. Acta 1106:171-177.
51. Racoosin, E. L., and J. A. Swanson. 1994. Labeling of endocytic vesicles using fluorescent probes for fluid-phase endocytosis. In J. E. Celis (ed.), Cell biology: a laboratory handbook. Academic Press, New York, N.Y.
52. Rathman, M., M. D. Sjaastad, and S. Falkow. 1996. Acidification of phagosomes containing Salmonella typhimurium in murine macrophages. Infect. Immun. 64:2765-2773.
53. Redhead, K., J. Watkins, A. Barnard, and K. H. Mills. 1993. Effective immunization against Bordetella pertussis respiratory infection in mice is dependent on induction of cell-mediated immunity. Infect. Immun. 61:3190-3198.
54. Savelkoul, P. H. M., B. Kremer, J. G. Kusters, B. A. M. van der Zeijst, and W. Gaastra. 1993. Invasion of HeLa cells by Bordetella bronchiseptica. Microb. Pathog. 14:161-168.
55. Schipper, H., G. Krohne, and R. Gross. 1994. Epithelial cell invasion and survival of Bordetella bronchiseptica. Infect. Immun. 62:3008-3011.
56. Stainer, D. W., and M. J. Scholte. 1970. A simple chemically defined medium for production of phase I Bordetella pertussis. J. Gen. Microbiol. 63:211-220.
57. Steed, L. L., E. T. Akporiaye, and R. L. Friedman. 1992. Bordetella pertussis induces respiratory burst activity in human polymorphonuclear leukocytes. Infect. Immun. 60:2101-2105.
58. Steed, L. L., M. Setareh, and R. L. Friedman. 1991. Host-parasite interactions between Bordetella pertussis and human polymorphonuclear leukocytes. J. Leukoc. Biol. 50:321-330.
59. Vergne, I., P. Constant, and G. Laneelle. 1998. Phagosomal pH determination by dual fluorescence flow cytometry. Anal. Biochem. 255:127-132.
60. Weingart, C. L., G. Broitman-Maduro, G. Dean, S. Newman, M. Peppler, and A. A. Weiss. 1999. Fluorescent labels influence phagocytosis of Bordetella pertussis by human neutrophils. Infect. Immun. 67:4264-4267.
61. Weiss, A. A., and S. Falkow. 1984. Genetic analysis of phase change in Bordetella pertussis. Infect. Immun. 43:263-269.
62. Weiss, A. A., and E. L. Hewlett. 1986. Virulence factors of Bordetella pertussis. Annu. Rev. Microbiol. 40:661-686.
63. Woolfrey, F. B., and J. A. Moody. 1991. Human infections associated with Bordetella bronchiseptica. Clin. Microbiol. Rev. 4:234-255.
64. Zinder, N. D., and J. Lederberg. 1952. Genetic exchange in Salmonella. J. Bacteriol. 64:679-699.