Vacuolar and plasma membrane stripping and autophagic elimination of Toxoplasma gondii in primed effector macrophages

Journal of Experimental Medicine

Volumn 203, Issue 9, 2006, Pages 2063-2071

  Ling, Yun M ^a   Shaw, Michael H ^a   Ayala, Carol ^b   Coppens, Isabelle ^c   Taylor, Gregory A ^d   Ferguson, David J P ^e   Yap, George S ^a  

^a BROWN UNIVERSITY   (United States)

^b RHODE ISLAND HOSPITAL   (United States)

^c JOHNS HOPKINS UNIVERSITY   (United States)

^d DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CD11B ANTIGEN; GAMMA INTERFERON; GUANOSINE TRIPHOSPHATASE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN P47; BAFILOMYCIN A1;

ANIMAL CELL; APICOPLAST; ARTICLE; AUTOPHAGY; CELL DISRUPTION; CELL MEMBRANE; EFFECTOR CELL; ENZYME ACTIVITY; IMMUNITY; LYSOSOME; MACROPHAGE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; TONOPLAST; TOXOPLASMA GONDII; ANIMAL EXPERIMENT; CONTROLLED STUDY; HOST CELL; PARASITE; PARASITOSIS; PATHOGENESIS;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ANIMALS; AUTOPHAGY; CELL MEMBRANE; GTP PHOSPHOHYDROLASES; HUMANS; IMMUNOHISTOCHEMISTRY; INTERFERON TYPE II; LYSOSOMES; MACROPHAGES; MEMBRANE FUSION; MICE; MICE, INBRED STRAINS; MICE, KNOCKOUT; TOXOPLASMA; VACUOLES;

PROTOZOA; TOXOPLASMA GONDII;

EID: 33748444233     PISSN: 00221007     EISSN: 00221007     Source Type: Journal    
DOI: 10.1084/jem.20061318     Document Type: Article

References (30)

1. Dubey, J.P., and C.P. Beattie. 1988. Toxoplasmosis of Animals and Man. CRC Press, Boca Raton. 220 pp.
2. Miller, L.H., D.I. Baruch, K. Marsh, and O.K. Doumbo. 2002. The pathogenic basis of malaria. Nature. 415:673-679.
3. Sinai, A.P., and K.A. Joiner. 1997. Safe haven: the cell biology of nonfusogenic pathogen vacuoles. Annu. Rev. Microbiol. 51:415-462.
4. Jones, T.C., and J.G. Hirsch. 1972. The interaction between Toxoplasma gondii and mammalian cells. II. The absence of lysosomal fusion with phagocytic vacuoles containing living parasites. J. Exp. Med. 136:1173-1194.
5. Schwab, J.C., C.J. Beckers, and K.A. Joiner. 1994. The parasitophorous vacuole membrane surrounding intracellular Toxoplasma gondii functions as a molecular sieve. Proc. Natl. Acad. Sci. USA. 91:509-513.
6. Sinai, A.P., P. Webster, and K.A. Joiner. 1997. Association of host cell endoplasmic reticulum and mitochondria with the Toxoplasma gondii parasitophorous vacuole membrane: a high affinity interaction. J. Cell Sci. 110:2117-2128.
7. Yap, G.S., and A. Sher. 1999. Effector cells of both nonhemopoietic and hemopoietic origin are required for interferon (IFN)-γ- and tumor necrosis factor (TNF)-α-dependent host resistance to the intracellular pathogen, Toxoplasma gondii. J. Exp. Med. 189:1083-1092.
8. Adams, L.B., J.B. Hibbs Jr., R.R. Taintor, and J.L. Krahenbuhl. 1990. Microbiostatic effect of murine-activated macrophages for Toxoplasma gondii. Role for synthesis of inorganic nitrogen oxides from L-arginine. J. Immunol. 144:2725-2729.
9. Pfefferkorn, E.R. 1984. Interferon gamma blocks the growth of Toxoplasma gondii in human fibroblasts by inducing the host cells to degrade tryptophan. Proc. Natl. Acad. Sci. USA. 81:908-912.
10. Fox, B.A., and D.J. Bzik. 2002. De novo pyrimidine biosynthesis is required for virulence of Toxoplasma gondii. Nature. 415:926-929.
11. Remington, J.S., J.L. Krahenbuhl, and J.W. Mendenhall. 1972. A role for activated macrophages in resistance to infection with Toxoplasma. Infect. Immun. 6:829-834.
12. Taylor, G.A., C.M. Collazo, G.S. Yap, K. Nguyen, T.A. Gregorio, L.S. Taylor, B. Eagleson, L. Secrest, E.A. Southon, S.W. Reid, et al. 2000. Pathogen-specific loss of host resistance in mice lacking the IFN-gamma-inducible gene IGTP. Proc. Natl. Acad. Sci. USA. 97:751-755.
13. Scharton-Kersten, T.M., G. Yap, J. Magram, and A. Sher. 1997. Inducible nitric oxide is essential for host control of persistent but not acute infection with the intracellular pathogen Toxoplasma gondii. J. Exp. Med. 185:1261-1273.
14. Mordue, D.G., S. Hakansson, I. Niesman, and L.D. Sibley. 1999. Toxoplasma gondii resides in a vacuole that avoids fusion with host cell endocytic and exocytic vesicular trafficking pathways. Exp. Parasitol. 92:87-99.
15. Haupts, U., S. Maiti, P. Schwille, and W.W. Webb. 1998. Dynamics of fluorescence fluctuations in green fluorescent protein observed by fluorescence correlation spectroscopy. Proc. Natl. Acad. Sci. USA. 95:13573-13578.
16. Martens, S., I. Parvanova, J. Zerrahn, G. Griffiths, G. Schell, G. Reichmann, and J.C. Howard. 2005. Disruption of Toxoplasma gondii parasitophorous vacuoles by the mouse p47-resistance GTPases. PLoS Pathog. 1:e24.
17. Shintani, T., and D.J. Klionsky. 2004. Autophagy in health and disease: a double-edged sword. Science. 306:990-995.
18. Nakagawa, I., A. Amano, N. Mizushima, A. Yamamoto, H. Yamaguchi, T. Kamimoto, A. Nara, J. Funao, M. Nakata, K. Tsuda, et al. 2004. Autophagy defends cells against invading group A Streptococcus. Science. 306:1037-1040.
19. Ogawa, M., T. Yoshimori, T. Suzuki, H. Sagara, N. Mizushima, and C. Sasakawa. 2005. Escape of intracellular Shigella from autophagy. Science. 307:727-731.
20. Kirkegaard, K., M.P. Taylor, and W.T. Jackson. 2004. Cellular autophagy: surrender, avoidance and subversion by microorganisms. Nat. Rev. Microbiol. 2:301-314.
21. Petiot, A., E. Ogier-Denis, E.F. Blommaart, A.J. Meijer, and P. Codogno. 2000. Distinct classes of phosphatidylinositol 3′-kinases are involved in signaling pathways that control macroautophagy in HT-29 cells. J. Biol. Chem. 275:992-998.
22. Munafo, D.B., and M.I. Colombo. 2001. A novel assay to study autophagy: regulation of autophagosome vacuole size by amino acid deprivation. J. Cell Sci. 114:3619-3629.
23. Dunn, W.A., Jr. 1990. Studies on the mechanisms of autophagy: formation of the autophagic vacuole. J. Cell Biol. 110:1923-1933.
24. Butcher, B.A., R.I. Greene, S.C. Henry, K.L. Annecharico, J.B. Weinberg, E.Y. Denkers, A. Sher, and G.A. Taylor. 2005. p47 GTPases regulate Toxoplasma gondii survival in activated macrophages. Infect. Immun. 73:3278-3286.
25. Gutierrez, M.G., S.S. Master, S.B. Singh, G.A. Taylor, M.I. Colombo, and V. Deretic. 2004. Autophagy is a defense mechanism inhibiting BCG and Mycobacterium tuberculosis survival in infected macrophages. Cell. 119:753-766.
26. Bekpen, C., J.P. Hunn, C. Rohde, I. Parvanova, L. Guethlein, D.M. Dunn, E. Glowalla, M. Leptin, and J.C. Howard. 2005. The interferon-inducible p47 (IRG) GTPases in vertebrates: loss of the cell autonomous resistance mechanism in the human lineage. Genome Biol. 6:R92.
27. Kim, K., M.S. Eaton, W. Schubert, S. Wu, and J. Tang. 2001. Optimized expression of green fluorescent protein in Toxoplasma gondii using thermostable green fluorescent protein mutants. Mol. Biochem. Parasitol. 113:309-313.
28. Roy, D., D.R. Liston, V.J. Idone, A. Di, D.J. Nelson, C. Pujol, J.B. Bliska, S. Chakrabarti, and N.W. Andrews. 2004. A process for controlling intracellular bacterial infections induced by membrane injury. Science. 304:1515-1518.
29. Ferguson, D.J., F.L. Henriquez, M.J. Kirisits, S.P. Muench, S.T. Prigge, D.W. Rice, C.W. Roberts, and R.L. McLeod. 2005. Maternal inheritance and stage-specific variation of the apicoplast in Toxoplasma gondii during development in the intermediate and definitive host. Eukaryot. Cell. 4:814-826.
30. Folsch, H., M. Pypaert, P. Schu, and I. Mellman. 2001. Distribution and function of AP-1 clathrin adaptor complexes in polarized epithelial cells. J. Cell Biol. 152:595-606.