Disruption of the Toxoplasma gondii parasitophorous vacuole by IFNγ-inducible immunity-related GTPases (IRG proteins) triggers necrotic cell death

PLoS Pathogens

Volumn 5, Issue 2, 2009, Pages

  Zhao, Yang O ^a   Khaminets, Aliaksandr ^a   Hunn, Julia P ^a   Howard, Jonathan C ^a  

^a UNIVERSITY OF COLOGNE   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; GUANOSINE TRIPHOSPHATASE; HIGH MOBILITY GROUP B1 PROTEIN; IMMUNITY RELATED GUANOSINE TRIPHOSPHATASE; INTERLEUKIN 1BETA CONVERTING ENZYME; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; AUTOPHAGY; CELL DEATH; CELL VACUOLE; CONTROLLED STUDY; CYTOSOL; FIBROBLAST; MEMBRANE PERMEABILITY; MICROSCOPY; MOUSE; NECROSIS; NONHUMAN; PROTEIN CLEAVAGE; PROTEIN EXPRESSION; PROTEIN SECRETION; TOXOPLASMA GONDII; ANIMAL; FLUORESCENCE MICROSCOPY; GENETICS; IMMUNOLOGY; METABOLISM; PARASITOLOGY; PHASE CONTRAST MICROSCOPY; TOXOPLASMA; TOXOPLASMOSIS;

MAMMALIA; MUS; TOXOPLASMA GONDII;

ANIMALS; AUTOPHAGY; FIBROBLASTS; GTP PHOSPHOHYDROLASES; INTERFERON-GAMMA; MICE; MICROSCOPY, FLUORESCENCE; MICROSCOPY, PHASE-CONTRAST; NECROSIS; TOXOPLASMA; TOXOPLASMOSIS, ANIMAL; VACUOLES;

EID: 61449117883     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1000288     Document Type: Article

References (64)

1. Saeij JP, Boyle JP, Boothroyd JC (2005) Differences among the three major strains of Toxoplasma gondii and their specific interactions with the infected host. Trends Parasitol 21: 476-481.
2. Sibley LD, Boothroyd JC (1992) Virulent strains of Toxoplasma gondii comprise a single clonal lineage. Nature 359: 82-85.
3. Frenkel JK (1988) Pathophysiology of toxoplasmosis. Parasitol Today 4: 273-278.
4. Hunter CA, Remington JS (1994) Immunopathogenesis of toxoplasmic encephalitis. J Infect Dis 170: 1057-1067.
5. Yap GS, Sher A (1999) Cell-mediated immunity to Toxoplasma gondii: initiation, regulation and effector function. Immunobiology 201: 240-247.
6. Scharton-Kersten TM, Wynn TA, Denkers EY, Bala S, Grunvald E, et al. (1996) In the absence of endogenous IFN-gamma, mice develop unimpaired IL-12 responses to Toxoplasma gondii while failing to control acute infection. J Immunol 157: 4045-4054.
7. Scharton-Kersten TM, Yap G, Magram J, Sher A (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.
8. Yap GS, Ortmann R, Shevach E, Sher A (2001) A heritable defect in IL-12 signaling in B10.Q/J mice. II. Effect on acute resistance to Toxoplasma gondii and rescue by IL-18 treatment. J Immunol 166: 5720-5725.
9. Boehm U, Guethlein L, Klamp T, Ozbek K, Schaub A, et al. (1998) Two families of GTPases dominate the complex cellular response to interferon-g. J Immunol 161: 6715-6723.
10. Halonen SK, Taylor GA, Weiss LM (2001) Gamma Interferon-Induced Inhibition of Toxoplasma gondii in Astrocytes Is Mediated by IGTP. Infection and Immunity 69: 5573-5576.
11. Taylor GA, Collazo CM, Yap GS, Nguyen K, Gregorio TA, et al. (2000) Pathogen-specific loss of host resistance in mice lacking the IFN-gamma-inducible gene IGTP. Proc Natl Acad Sci U S A 97: 751-755.
12. Collazo CM, Yap GS, Sempowski GD, Lusby KC, Tessarollo L, et al. (2001) Inactivation of LRG-47 and IRG-47 Reveals a Family of Interferon {gamma}-inducible Genes with Essential, Pathogen-specific Roles in Resistance to Infection. J Exp Med 194: 181-188.
13. Könen-Waisman S, Howard JC (2007) Cell-autonomous immunity to Toxoplasma gondii in mouse and man. Microbes Infect 9: 1652-1661.
14. Pfefferkorn ER, Guyre PM (1984) Inhibition of growth of Toxoplasma gondii in cultured fibroblasts by human recombinant gamma interferon. Infect Immun 44: 211-216.
15. Pfefferkorn ER (1984) Interferon gamma blocks the growth of Toxoplasma gondii in human fibroblasts by inducing the host cells to degrade tryptophan. Proc Natl Acad Sci U S A 81: 908-912.
16. Melzer T, Duffy A, Weiss LM, Halonen SK (2008) IGTP is necessary for Toxoplasma Vacuolar Disruption and Induces Parasite Egression in IFN {gamma} Stimulated Astrocytes. Infect Immun 76: 4883-4894.
17. Martens S, Parvanova I, Zerrahn J, Griffiths G, Schell G, et al. (2005) Disruption of Toxoplasma gondii parasitophorous vacuoles by the mouse p47 resistance GTPases. PLoS Pathog 1: e24. doi:10.1371/journal.ppat.0010024.
18. Butcher BA, Greene RI, Henry SC, Annecharico KL, Weinberg JB, et al. (2005) p47 GTPases Regulate Toxoplasma gondii Survival in Activated Macrophages. Infect Immun 73: 3278-3286.
19. Ling YM, Shaw MH, Ayala C, Coppens I, Taylor GA, et al. (2006) Vacuolar and plasma membrane stripping and autophagic elimination of Toxoplasma gondii in primed effector macrophages. J Exp Med 203: 2063-2071.
20. Hunn JP, Koenen-Waisman S, Papic N, Schroeder N, Pawlowski N, et al. (2008) Regulatory interactions between IRG resistance GTPases in the cellular response to Toxoplasma gondii. Embo J 27: 2495-2509.
21. Zhao ZJ, Fux B, Goodwin M, DUnay IR, Strong D, et al. (2008) ATG5 is essential for cellular immunity in vivo and recruitment of a p47 GTPase to the Toxoplasma gondii parasitophorous vacuole in activated macrophages. Cell Host Microbe 4: 458-469.
22. Scaffidi P, Misteli T, Bianchi ME (2002) Release of chromatin protein HMGB1 by necrotic cells triggers inflammation. Nature 418: 191-195.
23. Edinger AL, Thompson CB (2004) Death by design: apoptosis, necrosis and autophagy. Curr Opin Cell Biol 16: 663-669.
24. Vermes I, Haanen C, Steffens-Nakken H, Reutelingsperger C (1995) A novel assay for apoptosis. Flow cytometric detection of phosphatidylserine expression on early apoptotic cells using fluorescein labelled Annexin V. J Immunol Methods 184: 39-51.
25. Goldstein JC, Waterhouse NJ, Juin P, Evan GI, Green DR (2000) The coordinate release of cytochrome c during apoptosis is rapid, complete and kinetically invariant. Nat Cell Biol 2: 156-162.
26. Tewari M, Quan LT, O'Rourke K, Desnoyers S, Zeng Z, et al. (1995) Yama/CPP32 beta, a mammalian homolog of CED-3, is a CrmA-inhibitable protease that cleaves the death substrate poly(ADP-ribose) polymerase. Cell 81: 801-809.
27. Brennan MA, Cookson BT (2000) Salmonella induces macrophage death by caspase-1-dependent necrosis. Mol Microbiol 38: 31-40.
28. Cervantes J, Nagata T, Uchijima M, Shibata K, Koide Y (2008) Intracytosolic Listeria monocytogenes induces cell death through caspase-1 activation in murine macrophages. Cell Microbiol 10: 41-52.
29. Schroeder GN, Jann NJ, Hilbi H (2007) Intracellular type III secretion by cytoplasmic Shigella flexneri promotes caspase-1-dependent macrophage cell death. Microbiology 153: 2862-2876.
30. Yu HB, Finlay BB (2008) The caspase-1 inflammasome: a pilot of innate immune responses. Cell Host Microbe 4: 198-208.
31. Hentze H, Lin XY, Choi MS, Porter AG (2003) Critical role for cathepsin B in mediating caspase-1-dependent interleukin-18 maturation and caspase-1-independent necrosis triggered by the microbial toxin nigericin. Cell Death Differ 10: 956-968.
32. Cheneval D, Ramage P, Kastelic T, Szelestenyi T, Niggli H, et al. (1998) Increased mature interleukin-1beta (IL-1beta) secretion from THP-1 cells induced by nigericin is a result of activation of p45 IL-1beta-converting enzyme processing. J Biol Chem 273: 17846-17851.
33. Willingham SB, Bergstralh DT, O'Connor W, Morrison AC, Taxman DJ, et al. (2007) Microbial pathogen-induced necrotic cell death mediated by the inflammasome components CIAS1/cryopyrin/NLRP3 and ASC. Cell Host Microbe 2: 147-159.
34. Levine B (2005) Eating oneself and uninvited guests; autophagy-related pathways in cellular defense. Cell 120: 159-162.
35. Levine B, Deretic V (2007) Unveiling the roles of autophagy in innate and adaptive immunity. Nat Rev Immunol 7: 767-777.
36. Schmid D, Munz C (2007) Innate and adaptive immunity through autophagy. Immunity 27: 11-21.
37. Zhao YO, Rohde C, Lilue JT, Könen-Waisman S, Khaminets A, et al. (2009) Toxoplasma gondii and the IRG resistance system in mice. Mem Inst Oswaldo Cruz;In press.
38. Singh SB, Davis AS, Taylor GA, Deretic V (2006) Human IRGM Induces Autophagy to Eliminate Intracellular Mycobacteria. Science 313: 1438-1441.
39. Gutierrez MG, Master SS, Singh SB, Taylor GA, Colombo MI, et al. (2004) Autophagy is a defense mechanism inhibiting BCG and Mycobacterium tuberculosis survival in infected macrophages. Cell 119: 753-766.
40. Papic N, Hunn JP, Pawlowski N, Zerrahn J, Howard JC (2008) Inactive and active states of the interferon-inducible resistance GTPase, Irga6, In Vivo. J Biol Chem 283: 32143-32151.
41. Saeij JP, Boyle JP, Coller S, Taylor S, Sibley LD, et al. (2006) Polymorphic secreted kinases are key virulence factors in toxoplasmosis. Science 314: 1780-1783.
42. Saeij JP, Coller S, Boyle JP, Jerome ME, White MW, et al. (2007) Toxoplasma co-opts host gene expression by injection of a polymorphic kinase homologue. Nature 445: 324-327.
43. Taylor S, Barragan A, Su C, Fux B, Fentress SJ, et al. (2006) A secreted serine-threonine kinase determines virulence in the eukaryotic pathogen Toxoplasma gondii. Science 314: 1776-1780.
44. Praefcke GJK, McMahon HT (2004) The dynamin superfamily: universal membrane tubulation and fission molecules? Nature Reviews Molecular Cell Biology 5: 133-147.
45. Martens S, Howard J (2006) The Interferon-Inducible GTPases. Annu Rev Cell Dev Biol 22: 559-589.
46. Degrandi D, Konermann C, Beuter-Gunia C, Kresse A, Wurthner J, et al. (2007) Extensive characterization of IFN-induced GTPases mGBP1 to mGBP10 involved in host defense. J Immunol 179: 7729-7740.
47. Halonen SK, Weiss LM (2000) Investigation into the mechanism of gamma interferon-mediated inhibition of Toxoplasma gondii in murine astrocytes. Infect Immun 68: 3426-3430.
48. Hitziger N, Dellacasa I, Albiger B, Barragan A (2005) Dissemination of Toxoplasma gondii to immunoprivileged organs and role of Toll/interleukin-1 receptor signalling for host resistance assessed by in vivo bioluminescence imaging. Cell Microbiol 7: 837-848.
49. Carmen JC, Sinai AP (2007) Suicide prevention: disruption of apoptotic pathways by protozoan parasites. Mol Microbiol 64: 904-916.
50. Bekpen C, Hunn JP, Rohde C, Parvanova I, Guethlein L, et al. (2005) The interferon-inducible p47 (IRG) GTPases in vertebrates: loss of the cell autonomous resistance mechanism in the human lineage. Genome Biol 6: R92.
51. Butcher BA, Kim L, Johnson PF, Denkers EY (2001) Toxoplasma gondii tachyzoites inhibit proinflammatory cytokine induction in infected macrophages by preventing nuclear translocation of the transcription factor NF-kappa B. J Immunol 167: 2193-2201.
52. Nash PB, Purner MB, Leon RP, Clarke P, Duke RC, et al. (1998) Toxoplasma gondii-infected cells are resistant to multiple inducers of apoptosis. J Immunol 160: 1824-1830.
53. Payne TM, Molestina RE, Sinai AP (2003) Inhibition of caspase activation and a requirement for NF-kappaB function in the Toxoplasma gondii-mediated blockade of host apoptosis. J Cell Sci 116: 4345-4358.
54. Molestina RE, Payne TM, Coppens I, Sinai AP (2003) Activation of NF-kappaB by Toxoplasma gondii correlates with increased expression of antiapoptotic genes and localization of phosphorylated IkappaB to the parasitophorous vacuole membrane. J Cell Sci 116: 4359-4371.
55. Carmen JC, Hardi L, Sinai AP (2006) Toxoplasma gondii inhibits ultraviolet light-induced apoptosis through multiple interactions with the mitochondrion-dependent programmed cell death pathway. Cell Microbiol 8: 301-315.
56. Nishikawa Y, Makala L, Otsuka H, Mikami T, Nagasawa H (2002) Mechanisms of apoptosis in murine fibroblasts by two intracellular protozoan parasites, Toxoplasma gondii and Neospora caninum. Parasite Immunol 24: 347-354.
57. Caldas LA, de Souza W, Attias M (2007) Calcium ionophore-induced egress of Toxoplasma gondii shortly after host cell invasion. Vet Parasitol 147: 210-220.
58. Persson EK, Agnarson AM, Lambert H, Hitziger N, Yagita H, et al. (2007) Death receptor ligation or exposure to perforin trigger rapid egress of the intracellular parasite Toxoplasma gondii. J Immunol 179: 8357-8365.
59. Moudy R, Manning TJ, Beckers CJ (2001) The loss of cytoplasmic potassium upon host cell breakdown triggers egress of Toxoplasma gondii. J Biol Chem 276: 41492-41501.
60. Coers J, Bernstein-Hanley I, Grotsky D, Parvanova I, Howard JC, et al. (2008) Chlamydia muridarum evades growth restriction by the IFN-gamma-inducible host resistance factor Irgb10. J Immunol 180: 6237-6245.
61. Dubey JP, Shen SK, Kwok OC, Frenkel JK (1999) Infection and immunity with the RH strain of Toxoplasma gondii in rats and mice. J Parasitol 85: 657-662.
62. Coers J, Starnbach MN, Howard JC (2009) Modeling infectious disease in mice: co-adaptation and the role of host-specific IFNγ responses. PLoS Pathog; In press.
63. MacKenzie CR, Heseler K, Muller A, Daubener W (2007) Role of indoleamine 2,3-dioxygenase in antimicrobial defence and immuno-regulation: tryptophan depletion versus production of toxic kynurenines. Curr Drug Metab 8: 237-244.
64. Gubbels MJ, Li C, Striepen B (2003) High-throughput growth assay for Toxoplasma gondii using yellow fluorescent protein. Antimicrob Agents Chemother 47: 309-316.