Entry of Borrelia burgdorferi into macrophages is end-on and leads to degradation in lysosomes

Infection and Immunity

Volumn 64, Issue 7, 1996, Pages 2867-2872

  Montgomery, Ruth R ^a   Malawista, Stephen E ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BACTERIAL COLONIZATION; BACTERIUM ADHERENCE; BORRELIA BURGDORFERI; ENDOSOME; IMMUNOPATHOGENESIS; LYME DISEASE; LYSOSOME; MACROPHAGE FUNCTION; MICROSCOPY; MOUSE; NONHUMAN; PRIORITY JOURNAL;

EID: 0029920187     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/iai.64.7.2867-2872.1996     Document Type: Article

References (37)

1. Barral-Netto, M., A. Barrai, C. E. Brownell, Y. A. W. Skeiky, L. R. Ellingsworth, D. R. Twardzik, and S. R. Reed. 1992. Transforming growth factor-β in leishmanial infection: a parasite escape mechanism. Science 257: 545-548.
2. Benach, J. L., H. B. Fleit, G. S. Habicht, J. L. Coleman, E. M. Bosler, and B. P. Lane. 1984. Interactions of phagocytes with the Lyme disease spirochete: role of the Fc receptor. J. Infect. Dis. 150:497-507.
3. Bockenstedt, L. K., and S. E. Malawista. 1995. Lyme disease, p. 1234-1249. In R. R. Rich (ed.), Clinical immunology. Mosby-Year Book, St. Louis.
4. Borst, P., and D. R. Greaves. 1987. Programmed gene rearrangements altering gene expression. Science 235:658-667.
5. Brause, B. D., and R. B. Roberts. 1978. Attachment of virulent Treponema pallidum to human mononuclear phagocytes. Br. J. Vener. Dis. 54:218-224.
6. Charon, N. W., C. W. Lawrence, and S. O'Brien. 1981. Movement of antibody-coated latex beads attached to the spirochete Leptospira interrogans. Proc. Natl. Acad. Sci. USA 78:7166-7170.
7. IIbβ, on human platelets. Infect. Immun. 62:5559-5567.
8. Cohn, Z. A. 1982. The macrophage - versatile element of inflammation. Harvey Lect. 77:63-80.
9. Coleman, J. L., T. J. Sellati, J. E. Testa, R. R. Kew, M. B. Furie, and J. L. Benach. 1995. Borrelia burgdorferi binds plasminogen, resulting in enhanced penetration of endothelial monolayers. Infect. Immun. 63:2478-2484.
10. Dawson, J. R., and R. P. Ellen. 1994. Clustering of fibronectin adhesins toward Treponema denticola tips upon contact with immobilized fibronectin. Infect. Immun. 62:2214-2221.
11. Fields, P. I, E. A. Groisman, and F. Heffron. 1989. A Salmonella locus that controls resistance to microbicidal proteins from phagocytic cells. Science 243:1059-1062.
12. Fikrig, E., S. W. Barthold, F. S. Kantor, and R. A. Flavell. 1990. Protection of mice against the Lyme disease agent by immunizing with recombinant OspA. Science 250:553-556.
13. Fischetti, V. A. 1989. Streptococcal M protein: molecular design and biological behavior. Clin. Microbiol. Rev. 2:285-314.
14. Hall, B. F., and K. A. Joiner. 1991. Strategies of obligate intracellular parasites for evading host defences. Immunol. Today 12:A22-A27.
15. Horwitz, M. A. 1984. Phagocytosis of the Legionnaire's disease bacterium (Legionella pneumophila) occurs by a novel mechanism: engulfment with a pseudopod coil. Cell 36:27-33.
16. Howe, C. L., B. L. Granger, M. Hull, S. A. Green, C. A. Gabel, A. Helenius, and I. Mellman. 1988. Derived protein sequence, oligosaccharides, and membrane insertion of the 120-kDa lysosomal membrane glycoprotein (Igp): identification of a highly conserved family of lysosomal membrane glycoproteins. Proc. Natl. Acad. Sci. USA 85:7577-7581.
17. Hulinska, D., P. Bartak, J. Hercogova, J. Hancil, J. Basta, and J. Schramlova. 1994. Electron microscopy of Langerhans cells and Borrelia burgdorferi in Lyme disease patients. Int. J. Med. Microbiol. Virol. Parasitol. Infect. Dis. 280:348-359.
18. Joiner, K. A., S. A. Fuhrman, H. M. Miettinen, L. H. Kasper, and I. Mellman. 1990. Toxoplasma gondii: fusion competence of parasitophorous vacuoles in Fc receptor-transfected fibroblasts. Science 249:641-646.
19. Jones, T. C., S. Yeh, and J. G. Hirsch. 1972. The interaction between Toxoplasma gondii and mammalian cells. I. Mechanism of entry and intracellular fate of the parasite. J. Exp. Med. 136:1157-1172.
20. Klempner, M. S., R. Noring, M. P. Epstein, B. McCloud, R. Hu, S. A. Limentani, and R. A. Rogers. 1995. Binding of human plasminogen and urokinase-type plasminogen activator to the Lyme disease spirochete, Borrelia burgdorferi. J. Infect. Dis. 171:1258-1265.
21. Klempner, M. S., R. Noring, and R. A. Rogers. 1993. Invasion of human skin fibroblasts by the Lyme disease spirochete, Borrelia burgdorferi. J. Infect. Dis. 167:1074-1081.
22. Kopp, P. A., M. Schmitt, H.-J. Wellensiek, and H. Blobel. 1995. Isolation and characterization of fibronectin-binding sites of Borrelia garinii N34. Infect. Immun. 63:3804-3808.
23. Lang, T., M.-T. Tassin, and A. Ryter. 1988. Bacterial antigen immunolabeling in macrophages after phagocytosis and degradation of Bacillus subtilis. Infect. Immun. 56:468-478.
24. Lukehart, S. A., and J. N. Miller. 1978. Demonstration of the in vitro phagocytosis of Treponema pallidum by rabbit peritoneal macrophages. J. Immunol. 121:2014-2023.
25. Montgomery, R. R., and S. E. Malawista. 1994. Borrelia burgdorferi and the macrophage: routine annihilation but occasional haven? Parasitol. Today 10:154-157.
26. Montgomery, R. R., S. E. Malawista, K. J. M. Feen, and L. K. Bockenstedt. 1996. Direct demonstration of antigenic substitution of Borrelia burgdorferi ex vivo: exploration of the paradox of the early immune response to outer surface proteins A and C in Lyme disease. J. Exp. Med. 183:261-270.
27. Montgomery, R. R., M. H. Nathanson, and S. E. Malawista. 1993. The fate of Borrelia burgdorferi, the agent for Lyme disease, in mouse macrophages: destruction, survival, recovery. J. Immunol. 150:909-915.
28. Montgomery, R. R., M. H. Nathanson, and S. E. Malawista. 1994. Fc and non Fc-mediated phagocytosis of Borrelia burgdorferi by macrophages. J. Infect. Dis. 170:890-893.
29. Montgomery, R. R., P. Webster, and I. Mellman. 1991. Accumulation of indigestible substances reduces fusion competence of macrophage lysosomes. J. Immunol. 147:3087-3095.
30. Peterson. P. K., C. C. Clawson, D. A. Lee, D. J. Garlich, P. G. Quie, and R. C. Johnson. 1984. Human phagocyte interactions with the Lyme disease spirochete. Infect. Immun. 46:608-611.
31. Rittig, M. G., T. Haupl, A. Krause, M. Kressel, P. Groscurth, and G. R. Burmester. 1994. Borrelia burgdorferi-induced ultrastructural alterations in human phagocytes: a clue to pathogenicity? J. Pathol. 173:269-282.
32. Rittig, M. G., A. Krause, T. Häupl, U. E. Schaible, M. Modolell, M. D. Kramer, E. Lütjen-Drecoll, M. M. Simon, and G. R. Burmester. 1992. Coiling phagocytosis is the preferential phagocytic mechanism for Borrelia burgdorferi. Infect. Immun. 60:4205-4212.
33. Sadziene, A., D. D. Thomas, and A. G. Barbour. 1995. Borrelia burgdorferi mutant lacking Osp: biological and immunological characterization. Infect. Immun. 63:1573-1580.
34. Sell, S., S. Baker-Zander, and H. C. Powell. 1982. Experimental syphilitic orchitis in rabbits: ultrastructural appearance of Treponema pallidum during phagocytosis and dissolution by macrophages in vivo. Lab. Invest. 46:355-364.
35. Szczepanski, A., and H. B. Fielt. 1988. Interaction between Borrelia burgdorferi and polymorphonuclear leukocytes: phagocytosis and the induction of the respiratory burst. Ann. N. Y. Acad. Sci. 539:425-428.
36. Thomas, D. D., J. B. Baseman, and J. F. Alderete. 1985. Fibronectin tetrapeptide is target for syphilis spirochete cytadherence. J. Exp. Med. 162:1715-1719.
37. Thomas, D. D., and L. E. Comstock. 1989. Interaction of Lyme disease spirochetes with cultured eucaryotic cells. Infect. Immun. 57:1324-1326.