Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Letter
  • Published:

Phagosome acidification blocked by intracellular Toxoplasma gondii

Nature volume 315, pages 416–419 (1985)Cite this article

Abstract

Toxoplasma gondii belongs to a group of highly virulent intracellular parasites that reside in host cell vacuoles which resist typical phagosome–lysosome fusion1. Live Toxoplasma replicate prodigiously within modified phagocytic vacuoles formed during invagination of the host plasma membrane2,3. In contrast, heat-killed Toxoplasma or specific antibody (heat-inactivated)-coated live Toxoplasma-containing vacuoles readily undergo lysosome fusion and digestion in normal macrophages2,4. Of newly recognized significance to Toxoplasma survival is the microbicidal effect of phagosome acidification, which reportedly can occur independently of fusion with other acidic vesicles5–8. We report here that modified live Toxoplasma-containing vacuoles fail to acidify in normal macrophages, as indicated by the sensitive pH probe fluorescein. In contrast, when live Toxoplasma are coated with specific antibody (heat-inactivated), they trigger phagosome acidification when entering normal macrophages. A similar acidification is observed when normal phagocytes ingest dead Toxoplasma. Extracellular Toxoplasma are highly susceptible to acidic pH conditions, indicating that the acidification block in the modified vacuoles may be important for intracellular survival.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Similar content being viewed by others

References

  1. Goren, M. B. A. Rev. Microbiol. 31, 507–533 (1977).

    Article  CAS  Google Scholar 

  2. Jones, T. C., Yeh, S. & Hirsch, G. J. exp. Med. 136, 1157–1172 (1972).

    Article  CAS  Google Scholar 

  3. Aikawa, M., Komata, Y., Asai, T. & Midorikawa, O. Am. J. Path. 87, 285–296 (1977).

    CAS  PubMed  Google Scholar 

  4. Jones, T. C. & Hirsch, J. G. J. exp. Med. 136, 1173–1194 (1972).

    Article  CAS  Google Scholar 

  5. Allen, R. C. in Lysosomes in Biology and Pathology Vol. 6 (eds Dingle, J. T., Jacques, P. J. & Shaw, I. H.) 197–233 (North-Holland, Amsterdam, 1979).

    Google Scholar 

  6. Geisow, M. J., Hart, P. D. & Young, M. R. J. Cell Biol. 89, 645–652 (1981).

    Article  CAS  Google Scholar 

  7. Weidner, E. & Sibley, L. D. J. Protozool. 32, 311–317 (1985).

    Article  CAS  Google Scholar 

  8. Mcneil, P. L., Tanasugarn, L., Meigs, J. B. & Taylor, D. L. J. Cell Biol. 97, 692–702 (1983).

    Article  CAS  Google Scholar 

  9. Galloway, C. J., Dean, G. E., Marsh, M., Rudnick, G. & Mellman, I. Proc. natn. Acad. Sci. U.S.A. 80, 3334–3338 (1983).

    Article  CAS  ADS  Google Scholar 

  10. Forgac, M. & Cantley, L. J. biol. Chem. 259, 8101–8105 (1984).

    CAS  PubMed  Google Scholar 

  11. Xie, X. S., Stone, D. K. & Racker, E. J. biol. Chem. 258, 14834–14838 (1982).

    Google Scholar 

  12. Yamashiro, D. J., Fluss, S. R. & Maxfield, F. R. J. Cell Biol. 97, 929–934 (1983).

    Article  CAS  Google Scholar 

  13. Tycko, B. & Maxfield, F. R. Cell 28, 643–651 (1982).

    Article  CAS  Google Scholar 

  14. Tietze, C., Schlesinger, P. & Stahl, P. J. Cell Biol. 92, 417–424 (1982).

    Article  CAS  Google Scholar 

  15. Yamashiro, D. J., Tycko, B., Fluss, S. R. & Maxfield, F. R. Cell 37, 789–800 (1984).

    Article  CAS  Google Scholar 

  16. Murray, H. W. & Cohn, Z. A. J. exp. Med. 150, 938–949 (1979).

    Article  CAS  Google Scholar 

  17. Nathan, C. F. Trans. R. Soc. trop. Med. Hyg. 77, 620–630 (1983).

    Article  CAS  Google Scholar 

  18. Wilson, C. B., Tsai, V. & Remington, J. S. J. exp. Med. 151, 328–346 (1980).

    Article  CAS  Google Scholar 

  19. Allison, A. C. & Young, M. R. in Lysosomes in Biology and Pathology Vol. 1 (eds Dingle, J. T. & Fell, H. B.) 600–628 (North-Holland, Amsterdam, 1969).

    Google Scholar 

  20. Pfefferkorn, E. R. & Pfefferkorn, L. C. Expl Parasit. 39, 365–376 (1976).

    Article  CAS  Google Scholar 

  21. Ohkuma, S. & Poole, B. Proc. natn. Acad. Sci. U.S.A. 75, 3327–3331 (1978).

    Article  CAS  ADS  Google Scholar 

  22. Heiple, J. M. & Taylor, D. L. J. Cell Biol. 94, 143–149 (1982).

    Article  CAS  Google Scholar 

  23. Allen, R. D. & Fok, A. K. J. Cell Biol. 97, 566–570 (1983).

    Article  CAS  Google Scholar 

  24. Horwitz, M. A. & Maxfield, F. R. J. Cell Biol. 99, 1936–1943 (1984).

    Article  CAS  Google Scholar 

  25. Khavkin, T. N., Freidlin, I. S. & Shustrov, A. K. Acta microbiol. hung. 27, 9–21 (1980).

    CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Zoology and Physiology, Louisiana State University, Baton Rouge, Louisiana, 70803, USA

    L. David Sibley & Earl Weidner

  2. Department of Immunology Research, National Hansen's Disease Center, Carville, Louisiana, 70721, USA

    James L. Krahenbuhl

Authors
  1. L. David Sibley
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Earl Weidner
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. James L. Krahenbuhl
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Sibley, L., Weidner, E. & Krahenbuhl, J. Phagosome acidification blocked by intracellular Toxoplasma gondii. Nature 315, 416–419 (1985). https://doi.org/10.1038/315416a0

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/315416a0

This article is cited by

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing