Toxoplasma co-opts host cells it does not invade

PLoS Pathogens

Volumn 8, Issue 7, 2012, Pages 18-

  Koshy, Anita A ^a   Dietrich, Hans K ^a   Christian, David A ^b   Melehani, Jason H ^a,c   Shastri, Anjali J ^a   Hunter, Christopher A ^b   Boothroyd, John C ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HYBRID PROTEIN; PROTEIN TYROSINE KINASE; PROTOZOAL PROTEIN; ROP16 PROTEIN, TOXOPLASMA GONDII; STAT6 PROTEIN;

ANIMAL EXPERIMENT; ARTICLE; BRAIN; BRAIN NERVE CELL; CELL CULTURE; CELL INVASION; CELL MANIPULATION; HOST CELL; HOST PARASITE INTERACTION; IMMUNOCOMPETENT CELL; IN VITRO STUDY; MOUSE; NONHUMAN; TOXOPLASMA; TOXOPLASMA GONDII; TOXOPLASMOSIS; ANIMAL; C57BL MOUSE; CELL LINE; FIBROBLAST; HUMAN; METABOLISM; PARASITOLOGY; PATHOGENICITY;

MUS; PROTOZOA; TOXOPLASMA; TOXOPLASMA GONDII;

ANIMALS; CELL LINE; FIBROBLASTS; HOST-PARASITE INTERACTIONS; HUMANS; MICE; MICE, INBRED C57BL; PROTEIN-TYROSINE KINASES; PROTOZOAN PROTEINS; STAT6 TRANSCRIPTION FACTOR; TOXOPLASMA;

EID: 84864585429     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1002825     Document Type: Article

References (41)

1. Vázquez-Boland JA, Kuhn M, Berche P, Chakraborty T, Domínguez-Bernal G, et al. (2001) Listeria pathogenesis and molecular virulence determinants. Clin Microbiol Rev 14: 584-640.
2. Ibarra JA, Steele-Mortimer O, (2009) Salmonella-the ultimate insider. Salmonella virulence factors that modulate intracellular survival. Cell Microbiol 11: 1579-1586.
3. Saeij JPJ, 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.
4. Kulp A, Kuehn MJ, (2010) Biological functions and biogenesis of secreted bacterial outer membrane vesicles. Annu Rev Microbiol 64: 163-184.
5. Geddes K, Cruz F, Heffron F, (2007) Analysis of cells targeted by Salmonella type III secretion in vivo. PLoS Pathog 3: e196.
6. Koshy AA, Fouts AE, Lodoen MB, Alkan O, Blau HM, et al. (2010) Toxoplasma secreting Cre recombinase for analysis of host-parasite interactions. Nat Methods 7: 307-309.
7. Whitmarsh RJ, Gray CM, Gregg B, Christian DA, May MJ, et al. (2011) A critical role for SOCS3 in innate resistance to Toxoplasma gondii. Cell Host Microbe 10: 224-236.
8. Dubey JP, (2008) The history of Toxoplasma gondii-the first 100 years. J Eukaryot Microbiol 55: 467-475.
9. Coppens I, Dunn JD, Romano JD, Pypaert M, Zhang H, et al. (2006) Toxoplasma gondii sequesters lysosomes from mammalian hosts in the vacuolar space. Cell 125: 261-274.
10. Laliberté J, Carruthers VB, (2008) Host cell manipulation by the human pathogen Toxoplasma gondii. Cell Mol Life Sci 65: 1900-1915.
11. Ong Y-C, Reese ML, Boothroyd JC, (2010) Toxoplasma rhoptry protein 16 (ROP16) subverts host function by direct tyrosine phosphorylation of STAT6. J Biol Chem 285: 28731-28740.
12. Bradley PJ, Sibley LD, (2007) Rhoptries: an arsenal of secreted virulence factors. Curr Opin Microbiol 10: 582-587.
13. Steinfeldt T, Könen-Waisman S, Tong L, Pawlowski N, Lamkemeyer T, et al. (2010) Phosphorylation of mouse immunity-related GTPase (IRG) resistance proteins is an evasion strategy for virulent Toxoplasma gondii. PLoS Biol 8: e1000576.
14. Dubremetz JF, (2007) Rhoptries are major players in Toxoplasma gondii invasion and host cell interaction. Cell Microbiol 9: 841-848.
15. Kafsack BFC, Carruthers VB, Pineda FJ, (2007) Kinetic modeling of Toxoplasma gondii invasion. J Theor Biol 249: 817-825.
16. Tyler JS, Boothroyd JC, (2011) The C-terminus of Toxoplasma RON2 provides the crucial link between AMA1 and the host-associated invasion complex. PLoS Pathog 7: e1001282.
17. Kasper CA, Sorg I, Schmutz C, Tschon T, Wischnewski H, et al. (2010) Cell-cell propagation of NF-κB transcription factor and MAP kinase activation amplifies innate immunity against bacterial infection. Immunity 33: 804-816.
18. 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.
19. Yap GS, Sher A, (1999) Effector cells of both nonhemopoietic and hemopoietic origin are required for interferon (IFN)-gamma- and tumor necrosis factor (TNF)-alpha-dependent host resistance to the intracellular pathogen, Toxoplasma gondii. J Exp Med 189: 1083-1092.
20. Lodoen MB, Gerke C, Boothroyd JC, (2010) A highly sensitive FRET-based approach reveals secretion of the actin-binding protein toxofilin during Toxoplasma gondii infection. Cell Microbiol 12: 55-66.
21. Marketon MM, DePaolo RW, DeBord KL, Jabri B, Schneewind O, (2005) Plague bacteria target immune cells during infection. Science 309: 1739-1741.
22. Madisen L, Zwingman TA, Sunkin SM, Oh SW, Zariwala HA, et al. (2010) A robust and high-throughput Cre reporting and characterization system for the whole mouse brain. Nat Neurosci 13: 133-140.
23. Howard JC, Hunn JP, Steinfeldt T, (2011) The IRG protein-based resistance mechanism in mice and its relation to virulence in Toxoplasma gondii. Curr Opin Microbiol 14: 414-421.
24. Ferguson DJ, Hutchison WM, (1987) The host-parasite relationship of Toxoplasma gondii in the brains of chronically infected mice. Virchows Arch A Pathol Anat Histopathol 411: 39-43.
25. Ming G-L, Song H, (2011) Adult neurogenesis in the mammalian brain: significant answers and significant questions. Neuron 70: 687-702.
26. Brown JP, Couillard-Després S, Cooper-Kuhn CM, Winkler J, Aigner L, et al. (2003) Transient expression of doublecortin during adult neurogenesis. J Comp Neurol 467: 1-10.
27. Kim S-K, Karasov A, Boothroyd JC, (2007) Bradyzoite-specific surface antigen SRS9 plays a role in maintaining Toxoplasma gondii persistence in the brain and in host control of parasite replication in the intestine. Infect Immun 75: 1626-1634.
28. Dellacasa-Lindberg I, Hitziger N, Barragan A, (2007) Localized recrudescence of Toxoplasma infections in the central nervous system of immunocompromised mice assessed by in vivo bioluminescence imaging. Microbes Infect 9: 1291-1298.
29. Ferguson DJ, Hutchison WM, (1987) An ultrastructural study of the early development and tissue cyst formation of Toxoplasma gondii in the brains of mice. Parasitol Res 73: 483-491.
30. Feng G, Mellor RH, Bernstein M, Keller-Peck C, Nguyen QT, et al. (2000) Imaging neuronal subsets in transgenic mice expressing multiple spectral variants of GFP. Neuron 28: 41-51.
31. Livet J, Weissman TA, Kang H, Draft RW, Lu J, et al. (2007) Transgenic strategies for combinatorial expression of fluorescent proteins in the nervous system. Nature 450: 56-62.
32. Zhao Z, Fux B, Goodwin M, Dunay IR, Strong D, et al. (2008) Autophagosome-independent essential function for the autophagy protein Atg5 in cellular immunity to intracellular pathogens. Cell Host Microbe 4: 458-469.
33. Subauste CS, (2009) Autophagy in immunity against Toxoplasma gondii. Curr Top Microbiol Immunol 335: 251-265.
34. Jackson WT, Giddings TH Jr, Taylor MP, Mulinyawe S, Rabinovitch M, et al. (2005) Subversion of cellular autophagosomal machinery by RNA viruses. PLoS Biol 3: e156.
35. Orvedahl A, MacPherson S, Sumpter R Jr, Tallóczy Z, Zou Z, et al. (2010) Autophagy protects against Sindbis virus infection of the central nervous system. Cell Host Microbe 7: 115-127.
36. Frickel E-M, Sahoo N, Hopp J, Gubbels M-J, Craver MPJ, et al. (2008) Parasite stage-specific recognition of endogenous Toxoplasma gondii-derived CD8+ T cell epitopes. J Infect Dis 198: 1625-1633.
37. Berdoy M, Webster JP, Macdonald DW, (2000) Fatal attraction in rats infected with Toxoplasma gondii. Proc Biol Sci 267: 1591-1594.
38. Vyas A, Kim S-K, Giacomini N, Boothroyd JC, Sapolsky RM, (2007) Behavioral changes induced by Toxoplasma infection of rodents are highly specific to aversion of cat odors. Proc Natl Acad Sci USA 104: 6442-6447.
39. Donald RG, Roos DS, (1998) Gene knock-outs and allelic replacements in Toxoplasma gondii: HXGPRT as a selectable marker for hit-and-run mutagenesis. Mol Biochem Parasitol 91: 295-305.
40. Donald RG, Carter D, Ullman B, Roos DS, (1996) Insertional tagging, cloning, and expression of the Toxoplasma gondii hypoxanthine-xanthine-guanine phosphoribosyltransferase gene. Use as a selectable marker for stable transformation. J Biol Chem 271: 14010-14019.
41. Burg JL, Perelman D, Kasper LH, Ware PL, Boothroyd JC, (1988) Molecular analysis of the gene encoding the major surface antigen of Toxoplasma gondii. J Immunol 141: 3584-3591.