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. 1992 Oct;60(10):4205–4212. doi: 10.1128/iai.60.10.4205-4212.1992

Coiling phagocytosis is the preferential phagocytic mechanism for Borrelia burgdorferi.

M G Rittig 1, A Krause 1, T Häupl 1, U E Schaible 1, M Modolell 1, M D Kramer 1, E Lütjen-Drecoll 1, M M Simon 1, G R Burmester 1
PMCID: PMC257454  PMID: 1398932

Abstract

The uptake mechanism for the spirochete Borrelia burgdorferi, the causative agent of Lyme disease, was investigated by electron microscopy for human and murine phagocytes. Spirochetes of both a low- and a high-passage strain were preferentially internalized by coiling rather than by conventional phagocytosis. The spirochetes engulfed by coiling phagocytosis were found to disintegrate in an organelle exclusion zone without evident participation of lysosomes. Preincubation of B. burgdorferi with monoclonal antibody to the spirochetal OspA enhanced phagocytosis in general but did not consistently influence the uptake mechanism. Quantitative and kinetic differences concerning the phagocytic rate and mechanism were evident between cells from different lineages, different human individuals, and mice and humans. In general, when few phagocytes participated in spirochete uptake, the active cells displayed a high ratio of coiling versus conventional phagocytosis. These results suggest that coiling phagocytosis of B. burgdorferi plays a critical role in the control of spirochetal infection. More detailed studies on the molecular basis of this phagocytic mechanism may lead to new insights into the pathogenesis of Lyme borreliosis, a disease which is frequently characterized by the host's inability to eliminate the pathogenic spirochete.

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Selected References

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  1. Banfi E., Cinco M., Perticarari S., Presani G. Rapid flow cytometric studies of Borrelia burgdorferi phagocytosis by human polymorphonuclear leukocytes. J Appl Bacteriol. 1989 Jul;67(1):37–45. doi: 10.1111/j.1365-2672.1989.tb04952.x. [DOI] [PubMed] [Google Scholar]
  2. Barbour A. G. Isolation and cultivation of Lyme disease spirochetes. Yale J Biol Med. 1984 Jul-Aug;57(4):521–525. [PMC free article] [PubMed] [Google Scholar]
  3. Barbour A. G. Laboratory aspects of Lyme borreliosis. Clin Microbiol Rev. 1988 Oct;1(4):399–414. doi: 10.1128/cmr.1.4.399. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Benach J. L., Fleit H. B., Habicht G. S., Coleman J. L., Bosler E. M., Lane B. P. Interactions of phagocytes with the Lyme disease spirochete: role of the Fc receptor. J Infect Dis. 1984 Oct;150(4):497–507. doi: 10.1093/infdis/150.4.497. [DOI] [PubMed] [Google Scholar]
  5. Chang K. P. Leishmania donovani: promastigote--macrophage surface interactions in vitro. Exp Parasitol. 1979 Oct;48(2):175–189. doi: 10.1016/0014-4894(79)90097-3. [DOI] [PubMed] [Google Scholar]
  6. Dooley D. C., Simpson J. F., Meryman H. T. Isolation of large numbers of fully viable human neutrophils: a preparative technique using percoll density gradient centrifugation. Exp Hematol. 1982 Aug;10(7):591–599. [PubMed] [Google Scholar]
  7. Georgilis K., Steere A. C., Klempner M. S. Infectivity of Borrelia burgdorferi correlates with resistance to elimination by phagocytic cells. J Infect Dis. 1991 Jan;163(1):150–155. doi: 10.1093/infdis/163.1.150. [DOI] [PubMed] [Google Scholar]
  8. Grellner W., Erbguth F., Brade V. Serodiagnostik bei Lyme-Borreliose: Antikörpertiter und -spezifität im IFT und Western-Blot. Immun Infekt. 1989 Dec;17(6):189–194. [PubMed] [Google Scholar]
  9. Horisberger M. Colloidal gold : a cytochemical marker for light and fluorescent microscopy and for transmission and scanning electron microscopy. Scan Electron Microsc. 1981;(Pt 2):9–31. [PubMed] [Google Scholar]
  10. Horwitz M. A. Formation of a novel phagosome by the Legionnaires' disease bacterium (Legionella pneumophila) in human monocytes. J Exp Med. 1983 Oct 1;158(4):1319–1331. doi: 10.1084/jem.158.4.1319. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Horwitz M. A. Phagocytosis of the Legionnaires' disease bacterium (Legionella pneumophila) occurs by a novel mechanism: engulfment within a pseudopod coil. Cell. 1984 Jan;36(1):27–33. doi: 10.1016/0092-8674(84)90070-9. [DOI] [PubMed] [Google Scholar]
  12. Kramer M. D., Schaible U. E., Wallich R., Moter S. E., Petzoldt D., Simon M. M. Characterization of Borrelia burgdorferi associated antigens by monoclonal antibodies. Immunobiology. 1990 Nov;181(4-5):357–366. doi: 10.1016/S0171-2985(11)80504-8. [DOI] [PubMed] [Google Scholar]
  13. Krause A., Brade V., Schoerner C., Solbach W., Kalden J. R., Burmester G. R. T cell proliferation induced by Borrelia burgdorferi in patients with Lyme borreliosis. Autologous serum required for optimum stimulation. Arthritis Rheum. 1991 Apr;34(4):393–402. doi: 10.1002/art.1780340404. [DOI] [PubMed] [Google Scholar]
  14. McKenney E. C., Smith S. B., Haines H. G., Sigel M. M. Phagocytosis by fish cells. J Reticuloendothel Soc. 1977 Feb;21(2):89–95. [PubMed] [Google Scholar]
  15. Munder P. G., Modolell M., Hoelzl Wallach D. F. Cell propagation on films of polymeric fluorocarbon as a means to regulate pericellular pH and pO(2) in cultured monolayers. FEBS Lett. 1971 Jun 24;15(3):191–196. doi: 10.1016/0014-5793(71)80309-5. [DOI] [PubMed] [Google Scholar]
  16. Payne N. R., Horwitz M. A. Phagocytosis of Legionella pneumophila is mediated by human monocyte complement receptors. J Exp Med. 1987 Nov 1;166(5):1377–1389. doi: 10.1084/jem.166.5.1377. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Peterson P. K., Clawson C. C., Lee D. A., Garlich D. J., Quie P. G., Johnson R. C. Human phagocyte interactions with the Lyme disease spirochete. Infect Immun. 1984 Nov;46(2):608–611. doi: 10.1128/iai.46.2.608-611.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Schaible U. E., Kramer M. D., Eichmann K., Modolell M., Museteanu C., Simon M. M. Monoclonal antibodies specific for the outer surface protein A (OspA) of Borrelia burgdorferi prevent Lyme borreliosis in severe combined immunodeficiency (scid) mice. Proc Natl Acad Sci U S A. 1990 May;87(10):3768–3772. doi: 10.1073/pnas.87.10.3768. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Schaible U. E., Kramer M. D., Justus C. W., Museteanu C., Simon M. M. Demonstration of antigen-specific T cells and histopathological alterations in mice experimentally inoculated with Borrelia burgdorferi. Infect Immun. 1989 Jan;57(1):41–47. doi: 10.1128/iai.57.1.41-47.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Schaible U. E., Kramer M. D., Wallich R., Tran T., Simon M. M. Experimental Borrelia burgdorferi infection in inbred mouse strains: antibody response and association of H-2 genes with resistance and susceptibility to development of arthritis. Eur J Immunol. 1991 Oct;21(10):2397–2405. doi: 10.1002/eji.1830211016. [DOI] [PubMed] [Google Scholar]
  21. Southwick F. S., Stossel T. P. Contractile proteins in leukocyte function. Semin Hematol. 1983 Oct;20(4):305–321. [PubMed] [Google Scholar]
  22. Steere A. C. Lyme disease. N Engl J Med. 1989 Aug 31;321(9):586–596. doi: 10.1056/NEJM198908313210906. [DOI] [PubMed] [Google Scholar]
  23. Stevens D. R., Moulton J. E. Ultrastructural and immunological aspects of the phagocytosis of Trypanosoma brucei by mouse peritoneal macrophages. Infect Immun. 1978 Mar;19(3):972–982. doi: 10.1128/iai.19.3.972-982.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Szczepanski A., Benach J. L. Lyme borreliosis: host responses to Borrelia burgdorferi. Microbiol Rev. 1991 Mar;55(1):21–34. doi: 10.1128/mr.55.1.21-34.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]

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