Death receptor ligation or exposure to perforin trigger rapid egress of the intracellular parasite Toxoplasma gondii

Journal of Immunology

Volumn 179, Issue 12, 2007, Pages 8357-8365

  Persson, Emma K ^a,b   Agnarson, Abela Mpobela ^a,b   Lambert, Henrik ^a,b   Hitziger, Niclas ^a,b   Yagita, Hideo ^c   Chambers, Benedict J ^a   Barragan, Antonio ^a,b   Grandien, Alf ^a  

^a KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

^b SWEDISH INSTITUTE FOR INFECTIOUS DISEASE CONTROL   (Sweden)

^c JUNTENDO UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; CASPASE; DEATH RECEPTOR; FAS ANTIGEN; PERFORIN;

ANIMAL CELL; ANIMAL CELL CULTURE; ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; C57BL 6 MOUSE; CALCIUM TRANSPORT; CELL DEATH; CELL MEDIATED CYTOTOXICITY; CONTROLLED STUDY; CYTOLYSIS; EFFECTOR CELL; ENZYME ACTIVATION; HOST CELL; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; MOUSE; NONHUMAN; PRIORITY JOURNAL; T LYMPHOCYTE; TOXOPLASMA GONDII; TOXOPLASMOSIS; TRANSGENIC MOUSE; ANIMAL; CELL LINE; CONGENIC STRAIN; CYTOTOXIC T LYMPHOCYTE; CYTOTOXICITY; GENETICS; IMMUNOLOGY; METABOLISM; PARASITOLOGY; TOXOPLASMA;

ANIMALS; ANTIGENS, CD95; APOPTOSIS; CALCIUM; CASPASES; CELL LINE; CYTOTOXICITY, IMMUNOLOGIC; HUMANS; MICE; MICE, CONGENIC; PERFORIN; RECEPTORS, DEATH DOMAIN; T-LYMPHOCYTES, CYTOTOXIC; TOXOPLASMA;

EID: 38849149107     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.179.12.8357     Document Type: Article

References (47)

1. O'Brien, V. 1998. Viruses and apoptosis. J. Gen. Virol. 79: 1833-1845.
2. Byrne, G. I., and D. M. Ojcius. 2004. Chlamydia and apoptosis: life and death decisions of an intracellular pathogen. Nat. Rev. Microbiol. 2: 802-808.
3. James, E. R., and D. R. Green. 2004. Manipulation of apoptosis in the host-parasite interaction. Trends Parasitol. 20: 280-287.
4. Hengartner, M. O. 2000. The biochemistry of apoptosis. Nature 407: 770-776.
5. Voskoboinik, I., M. J. Smyth, and J. A. Trapani. 2006. Perforin-mediated target-cell death and immune homeostasis. Nat. Rev. Immunol. 6: 940-952.
6. Kavurma, M. M., and L. M. Khachigian. 2003. Signaling and transcriptional control of Fas ligand gene expression. Cell Death Differ. 10: 36-44.
7. Joynson, D. H., and T. J. Wreghitt. 2001. Toxoplasmosis: A Comprehensive Clinical Guide. Cambridge University Press, Cambridge.
8. Sibley, L. D. 2004. Intracellular parasite invasion strategies. Science 304: 248-253.
9. Denkers, E. Y. 1999. T lymphocyte-dependent effector mechanisms of immunity to Toxoplasma gondii. Microbes Infect. 1: 699-708.
10. Denkers, E. Y., G. Yap, T. Scharton-Kersten, H. Charest, B. A. Butcher, P. Caspar, S. Heiny, and A. Sher. 1997. Perforin-mediated cytolysis plays a limited role in host resistance to Toxoplasma gondii. J. Immunol. 159: 1903-1908.
11. Mordue, D. G., F. Monroy, M. La Regina, C. A. Dinarello, and L. D. Sibley. 2001. Acute toxoplasmosis leads to lethal overproduction of Th1 cytokines. J. Immunol. 167: 4574-4584.
12. Shen, D. F., D. M. Matteson, N. Tuaillon, B. K. Suedekum, R. R. Buggage, and C. C. Chan. 2001. Involvement of apoptosis and interferon-γ in murine toxoplasmosis. Invest. Ophthalmol. Visual Sci. 42: 2031-2036.
13. Wang, X., H. Kang, T. Kikuchi, and Y. Suzuki. 2004. Gamma interferon production, but not perforin-mediated cytolytic activity, of T cells is required for prevention of toxoplasmic encephalitis in BALB/c mice genetically resistant to the disease. Infect. Immun. 72: 4432-4438.
14. Carmen, J. C., L. Hardi, and A. P. Sinai. 2006. Toxoplasma gondii inhibits ultraviolet light-induced apoptosis through multiple interactions with the mitochondrion-dependent programmed cell death pathway. Cell. Microbiol. 8: 301-315.
15. Goebel, S., U. Gross, and C. G. Luder. 2001. Inhibition of host cell apoptosis by Toxoplasma gondii is accompanied by reduced activation of the caspase cascade and alterations of poly(ADP-ribose) polymerase expression. J. Cell Sci. 114: 3495-3505.
16. Keller, P., F. Schaumburg, S. F. Fischer, G. Hacker, U. Gross, and C. G. Luder. 2006. Direct inhibition of cytochrome c-induced caspase activation in vitro by Toxoplasma gondii reveals novel mechanisms of interference with host cell apoptosis. FEMS Microbiol. Lett. 258: 312-319.
17. Kim, J. Y., M. H. Ahn, H. S. Jun, J. W. Jung, J. S. Ryu, and D. Y. Min. 2006. Toxoplasma gondii inhibits apoptosis in infected cells by caspase inactivation and NF-κB activation. Yonsei Med. J. 47: 862-869.
18. Kim, L., and E. Y. Denkers. 2006. Toxoplasma gondii triggers Gi-dependent PI 3-kinase signaling required for inhibition of host cell apoptosis. J. Cell Sci. 119: 2119-2126.
19. Molestina, R. E., T. M. Payne, I. Coppens, and A. P. Sinai. 2003. Activation of NF-κB by Toxoplasma gondii correlates with increased expression of antiapoptotic genes and localization of phosphorylated IκB to the parasitophorous vacuole membrane. J. Cell Sci. 116: 4359-4371.
20. Nash, P. B., M. B. Purner, R. P. Leon, P. Clarke, R. C. Duke, and T. J. Curiel. 1998. Toxoplasma gondii-infected cells are resistant to multiple inducers of apoptosis. J. Immunol. 160: 1824-1830.
21. Payne, T. M., R. E. Molestina, and A. P. Sinai. 2003. Inhibition of caspase activation and a requirement for NF-κB function in the Toxoplasma gondii-mediated blockade of host apoptosis. J. Cell Sci. 116: 4345-4358.
22. Vutova, P., M. Wirth, D. Hippe, U. Gross, K. Schulze-Osthoff, I. Schmitz, and C. G. Luder. 2007. Toxoplasma gondii inhibits Fas/CD95-triggered cell death by inducing aberrant processing and degradation of caspase 8. Cell Microbiol. 9: 1556-1570.
23. Luder, C. G., and U. Gross. 2005. Apoptosis and its modulation during infection with Toxoplasma gondii: molecular mechanisms and role in pathogenesis. Curr. Top. Microbiol. Immunol. 289: 219-237.
24. Sinai, A. P., T. M. Payne, J. C. Carmen, L. Hardi, S. J. Watson, and R. E. Molestina. 2004. Mechanisms underlying the manipulation of host apoptotic pathways by Toxoplasma gondii. Int. J. Parasitol. 34: 381-391.
25. Barragan, A., and L. D. Sibley. 2002. Transepithelial migration of Toxoplasma gondii is linked to parasite motility and virulence. J. Exp. Med. 195: 1625-1633.
26. 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.
27. Norbury, C. C., B. J. Chambers, A. R. Prescott, H. G. Ljunggren, and C. Watts. 1997. Constitutive macropinocytosis allows TAP-dependent major histocompatibility complex class I presentation of exogenous soluble antigen by bone marrow-derived dendritic cells. Eur. J. Immunol. 27: 280-288.
28. Kim, K. J., C. Kanellopoulos-Langevin, R. M. Merwin, D. H. Sachs, and R. Asofsky. 1979. Establishment and characterization of BALB/c lymphoma lines with B cell properties. J. Immunol. 122: 549-554.
29. Djerbi, M., T. Darreh-Shori, B. Zhivotovsky, and A. Grandien. 2001. Characterization of the human FLICE-inhibitory protein locus and comparison of the antiapoptotic activity of four different flip isoforms. Scand. J. Immunol. 54: 180-189.
30. Kayagaki, N., N. Yamaguchi, F. Nagao, S. Matsuo, H. Maeda, K. Okumura, and H. Yagita. 1997. Polymorphism of murine Fas ligand that affects the biological activity. Proc. Natl. Acad. Sci. USA 94: 3914-3919.
31. + T cell-mediated cytotoxicity. J. Immunol. 162: 2639-2647.
32. Takeda, K., Y. Hayakawa, M. J. Smyth, N. Kayagaki, N. Yamaguchi, S. Kakuta, Y. Iwakura, H. Yagita, and K. Okumura. 2001. Involvement of tumor necrosis factor-related apoptosis-inducing ligand in surveillance of tumor metastasis by liver natural killer cells. Nat. Med. 7: 94-100.
33. Endo, T., K. K. Sethi, and G. Piekarski. 1982. Toxoplasma gondii: calcium ionophore A23187-mediated exit of trophozoites from infected murine macrophages. Exp. Parasitol. 53: 179-188.
34. Black, M. W., G. Arrizabalaga, and J. C. Boothroyd. 2000. Ionophore-resistant mutants of Toxoplasma gondii reveal host cell permeabilization as an early event in egress. Mol. Cell. Biol. 20: 9399-9408.
35. Scoltock, A. B., C. D. Bortner, G. St. J. Bird, J. W. Putney, Jr., and J. A. Cidlowski. 2000. A selective requirement for elevated calcium in DNA degradation, but not early events in anti-Fas-induced apoptosis. J. Biol. Chem. 275: 30586-30596.
36. Franksson, L., M. Petersson, R. Kiessling, and K. Karre. 1993. Immunization against tumor and minor histocompatibility antigens by eluted cellular peptides loaded on antigen processing defective cells. Eur. J. Immunol. 23: 2606-2613.
37. Moss, J. E., A. O. Aliprantis, and A. Zychlinsky. 1999. The regulation of apoptosis by microbial pathogens. Int. Rev. Cytol. 187: 203-259.
38. Fruth, I. A., and G. Arrizabalaga. 2007. Toxoplasma gondii: Induction of egress by the potassium ionophore nigericin. Int. J. Parasitol. 37: 1559-1567.
39. Lambert, H., N. Hitziger, I. Dellacasa, M. Svensson, and A. Barragan. 2006. Induction of dendritic cell migration upon Toxoplasma gondii infection potentiates parasite dissemination. Cell. Microbiol. 8: 1611-1623.
40. Luangsay, S., L. H. Kasper, N. Rachinel, L. A. Minns, F. J. Mennechet, A. Vandewalle, and D. Buzoni-Gatel. 2003. CCR5 mediates specific migration of Toxoplasma gondii-primed CD8 lymphocytes to inflammatory intestinal epithelial cells. Gastroenterology 125: 491-500.
41. Bliss, S. K., L. C. Gavrilescu, A. Alcaraz, and E. Y. Denkers. 2001. Neutrophil depletion during Toxoplasma gondii infection leads to impaired immunity and lethal systemic pathology. Infect. Immun. 69: 4898-4905.
42. Suzuki, Y., M. A. Orellana, R. D. Schreiber, and J. S. Remington. 1988. Interferon-γ: the major mediator of resistance against Toxoplasma gondii. Science 240: 516-518.
43. Kang, H., J. S. Remington, and Y. Suzuki. 2000. Decreased resistance of B cell-deficient mice to infection with Toxoplasma gondii despite unimpaired expression of IFN-γ, TNF-α, and inducible nitric oxide synthase. J. Immunol. 164: 2629-2634.
44. Ehrlich, S., C. Infante-Duarte, B. Seeger, and F. Zipp. 2003. Regulation of soluble and surface-bound TRAIL in human T cells, B cells, and monocytes. Cytokine 24: 244-253.
45. Hickey, W. F. 2001. Basic principles of immunological surveillance of the normal central nervous system. Glia 36: 118-124.
46. Subauste, C. S., and J. S. Remington. 1993. Immunity to Toxoplasma gondii. Curr. Opin. Immunol. 5: 532-537.
47. Herbeuval, J. P., J. Nilsson, A. Boasso, A. W. Hardy, M. J. Kruhlak, S. A. Anderson, M. J. Dolan, M. Dy, J. Andersson, and G. M. Shearer. 2006. Differential expression of IFN-α and TRAIL/DR5 in lymphoid tissue of progressor versus nonprogressor HIV-1-infected patients. Proc. Natl. Acad. Sci. USA 103: 7000-7005.