Advances in imaging the innate and adaptive immune response to Toxoplasma gondii

Future Microbiology

Volumn 5, Issue 9, 2010, Pages 1321-1328

  John, Beena ^a   Weninger, Wolfgang ^b   Hunter, Christopher A ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b CENTENARY INSTITUTE   (Australia)

Author keywords

bioluminescence; fuorescent protein; multiphoton microscopy; real time imaging; Toxoplasma gondii

Indexed keywords

GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 2;

ADAPTIVE IMMUNITY; ANTIGEN PRESENTING CELL; BIOLUMINESCENCE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CONFOCAL MICROSCOPY; CYTOKINE PRODUCTION; FLOW CYTOMETRY; HOST PATHOGEN INTERACTION; IMAGING; IMMUNE RESPONSE; IMMUNE SYSTEM; IMMUNOCOMPETENT CELL; IMMUNOCOMPROMISED PATIENT; INNATE IMMUNITY; MULTIPHOTON MICROSCOPY; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; REVIEW; TOXOPLASMA GONDII; TOXOPLASMOSIS;

ADAPTIVE IMMUNITY; ANIMALS; FLUORESCENT DYES; HOST-PATHOGEN INTERACTIONS; HUMANS; IMMUNITY, INNATE; MICE; MICROSCOPY, CONFOCAL; MICROSCOPY, FLUORESCENCE, MULTIPHOTON; TOXOPLASMA; TOXOPLASMOSIS; TOXOPLASMOSIS, ANIMAL;

MUS; PROTOZOA; TOXOPLASMA GONDII;

EID: 77957555106     PISSN: 17460913     EISSN: None     Source Type: Journal    
DOI: 10.2217/fmb.10.97     Document Type: Review

References (64)

1. Schlundt J, Toyofuku H, Jansen J, Herbst SA: Emerging food-borne zoonoses. Rev. Sci. Tech. 23, 513-533 (2004).
2. Barragan A, Hitziger N: Transepithelial migration by Toxoplasma. Subcell. Biochem. 47, 198-207 (2008).
3. Montoya JG, Liesenfeld O: Toxoplasmosis. Lancet 363, 1965-1976 (2004).
4. Denkers EY, Gazzinelli RT: Regulation and function of T-cell-mediated immunity during Toxoplasma gondii infection. Clin. Microbiol. Rev. 11, 569-588 (1998).
5. Gazzinelli RT, Hayashi S, Wysocka M et al.: Role of IL-12 in the initiation of cell mediated immunity by Toxoplasma gondii and its regulation by IL-10 and nitric oxide. J. Eukaryot. Microbiol. 41, 9S (1994).
6. Gazzinelli RT, Wysocka M, Hayashi S et al.: Parasite-induced IL-12 stimulates early IFN-g synthesis and resistance during acute infection with Toxoplasma gondii. J. Immunol. 153, 2533-2543 (1994).
7. Denkers EY, Butcher BA, Del Rio L, Bennouna S: Neutrophils, dendritic cells and Toxoplasma. Int. J. Parasitol. 34, 411-421 (2004).
8. Hunter CA, Remington JS: Immunopathogenesis of toxoplasmic encephalitis. J. Infect. Dis. 170, 1057-1067 (1994).
9. Suzuki Y: Host resistance in the brain against Toxoplasma gondii. J. Infect. Dis. 185(Suppl. 1), S58-S65 (2002).
10. Bousso P, Robey E: Dynamics of CD8+ T cell priming by dendritic cells in intact lymph nodes. Nat. Immunol. 4, 579-585 (2003).
11. Chtanova T, Schaeffer M, Han SJ et al.: Dynamics of neutrophil migration in lymph nodes during infection. Immunity 29(3), 487-496 (2008).
12. Dzierszinski F, Pepper M, Stumhofer JS et al.: Presentation of Toxoplasma gondii antigens via the endogenous major histocompatibility complex class I pathway in nonprofessional and professional antigen-presenting cells. Infect. Immun. 75, 5200-5209 (2007).
13. John B, Harris TH, Tait ED et al.: Dynamic Imaging of CD8+ T cells and dendritic cells during infection with Toxoplasma gondii. PLoS Pathog. 5, e1000505 (2009).
14. Wilson EH Harris HT, Mrass P, John B et al.: Behavior of parasite-specific effector CD8+ T cells in the brain and visualization of a kinesis-associated system of reticular fibers. Immunity 30, 300-311 (2009).
15. Hitziger N, Dellacasa I, Albiger B, Barragan A: 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 (2005).
16. Coombes JL, Robey EA: Dynamic imaging of host-pathogen interactions in vivo. Nat. Rev. Immunol. 10, 353-364 (2010).
17. Barragan A, Brossier F, Sibley LD: Transepithelial migration of Toxoplasma gondii involves an interaction of intercellular adhesion molecule 1 (ICAM-1) with the parasite adhesin MIC2. Cell Microbiol. 7, 561-568 (2005).
18. Chtanova T, Han SJ, Schaeffer M et al.: Dynamics of T cell, antigen-presenting cell, and pathogen interactions during recall responses in the lymph node. Immunity 31, 342-355 (2009).
19. Dellacasa-Lindberg I, Hitziger N, Barragan A: Localized recrudescence of Toxoplasma infections in the central nervous system of immunocompromised mice assessed by in vivo bioluminescence imaging. Microbes Infect. 9, 1291-1298 (2007).
20. Goldszmid RS, Coppens I, Lev A et al.: Host ER-parasitophorous vacuole interaction provides a route of entry for antigen cross-presentation in Toxoplasma gondii-infected dendritic cells. J. Exp. Med. 206(2), 399-410 (2009).
21. Pepper M, Dzierszinski F, Crawford A, Hunter CA, Roos D: Development of a system to study CD4+-T-cell responses to transgenic ovalbumin-expressing Toxoplasma gondii during toxoplasmosis. Infect. Immun. 72, 7240-7246 (2007).
22. Schaeffer M, Han SJ, Chtanova T et al.: Dynamic imaging of T cell-parasite interactions in the brains of mice chronically infected with Toxoplasma gondii. J. Immunol. 182, 6379-6393 (2009).
23. Boothroyd JC: Toxoplasma gondii: 25 years and 25 major advances for the field. Int. J. Parasitol. 39, 935-946 (2009).
24. Tait ED, Hunter CA: Advances in understanding immunity to Toxoplasma gondii. Mem. Inst. Oswaldo Cruz. 104, 201-210 (2009).
25. Dubremetz JF, Ferguson DJ: The role played by electron microscopy in advancing our understanding of Toxoplasma gondii and other apicomplexans. Int. J. Parasitol. 39, 883-893 (2009).
26. Dzierszinski FS, Hunter CA: Advances in the use of genetically engineered parasites to study immunity to Toxoplasma gondii. Parasite Immunol. 30, 235-244 (2008).
27. Gubbels MJ, Striepen B: Studying the cell biology of apicomplexan parasites using fluorescent proteins. Microsc. Microanal. 10, 568-579 (2004).
28. Striepen B, He CY, Matrajt M, Soldati D, Roos DS: Expression, selection, and organellar targeting of the green fluorescent protein in Toxoplasma gondii. Mol. Biochem. Parasitol. 92, 325-338 (1998).
29. Gubbels MJ, Li C, Striepen B: High-throughput growth assay for Toxoplasma gondii using yellow fluorescent protein. Antimicrob. Agents Chemother. 47, 309-316 (2003).
30. Gubbels MJ, Wieffer M, Striepen B: Fluorescent protein tagging in Toxoplasma gondii: identification of a novel inner membrane complex component conserved among Apicomplexa. Mol. Biochem. Parasitol. 137, 99-110 (2004).
31. Wille U, Villegas EN, Striepen B, Roos DS, Hunter CA: Interleukin-10 does not contribute to the pathogenesis of a virulent strain of Toxoplasma gondii. Parasite Immunol. 23, 291-296 (2001).
32. Courret N, Darche S, Sonigo P et al.: CD11c-and CD11b-expressing mouse leukocytes transport single Toxoplasma gondii tachyzoites to the brain. Blood 107, 309-316 (2006).
33. Lambert H, Hitziger N, Dellacasa I, Svensson M, Barragan A: Induction of dendritic cell migration upon Toxoplasma gondii infection potentiates parasite dissemination. Cell Microbiol. 8, 1611-1623 (2006).
34. Unno A, Suzuki K, Batanova T et al.: Visualization of Toxoplasma gondii stage conversion by expression of stage-specific dual fluorescent proteins. Parasitology 136, 579-588 (2009).
35. Saeij JP, Boyle JP, Grigg ME, Arrizabalaga G, Boothroyd JC: Bioluminescence imaging of Toxoplasma gondii infection in living mice reveals dramatic differences between strains. Infect. Immun. 73, 695-702 (2005).
36. Hutchens M, Luker GD: Applications of bioluminescence imaging to the study of infectious diseases. Cell Microbiol. 9, 2315-2322 (2007).
37. Lambert H, Vutova PP, Adams WC, Lore K, Barragan A: The Toxoplasma gondii-shuttling function of dendritic cells is linked to the parasite genotype. Infect. Immun. 77, 1679-1688 (2009).
38. Koshy AA, Fouts AE, Lodoen MB et al.: Toxoplasma secreting Cre recombinase for analysis of host-parasite interactions. Nat. Methods 7(4), 307-309 (2010).
39. Boothroyd JC, Dubremetz JF: Kiss and spit: the dual roles of Toxoplasma rhoptries. Nat. Rev. Microbiol. 6, 79-88 (2008).
40. Sauer B: Inducible gene targeting in mice using the Cre/lox system. Methods 14, 381-392 (1998).
41. Gubbels MJ, Striepen B, Shastri N, Turkoz M, Robey EA: Class I major histocompatibility complex presentation of antigens that escape from the parasitophorous vacuole of Toxoplasma gondii. Infect. Immun. 73, 703-711 (2005).
42. McSorley SJ, Asch S, Costalonga M, Reinhardt RL, Jenkins MK: Tracking salmonella-specific CD4 T cells in vivo reveals a local mucosal response to a disseminated infection. Immunity 16, 365-377 (2002).
43. Pope CS, Kim K, Marzo A et al.: Organ-specific regulation of the CD8 T cell response to Listeria monocytogenes infection. J. Immunol. 166, 3402-3409 (2001).
44. Kumar S, Tarleton RL: Antigen-specific Th1 but not Th2 cells provide protection from lethal Trypanosoma cruzi infection in mice. J. Immunol. 166, 4596-4603 (2001).
45. Pepper M, Dzierszinski F, Wilson E et al.: Plasmacytoid dendritic cells are activated by Toxoplasma gondii to present antigen and produce cytokines. J. Immunol. 180, 6229-6236 (2008).
46. Blanchard N, Gonzalez F, Schaeffer M et al.: Immunodominant, protective response to the parasite Toxoplasma gondii requires antigen processing in the endoplasmic reticulum. Nat. Immunol. 9, 937-944 (2008).
47. Frickel EM, Sahoo N, Hopp J et al.: Parasite stage-specific recognition of endogenous Toxoplasma gondii-derived CD8+ T cell epitopes. J. Infect. Dis. 198, 1625-1633 (2008).
48. Wilson DC, Grotenbreg GM, Liu K et al.: Differential regulation of effector-and central-memory responses to Toxoplasma gondii infection by IL-12 revealed by tracking of Tgd057-specific CD8+ T cells. PLoS Pathog. 6, e1000815 (2010).
49. Kirak O, Frickel EM, Grotenbreg GM et al.: Transnuclear mice with predefined T cell receptor specificities against Toxoplasma gondii obtained via SCNT. Science 328, 243-248 (2010).
50. Mempel TR, Henrickson SE, Von Andrian UH: T-cell priming by dendritic cells in lymph nodes occurs in three distinct phases. Nature 427, 154-159 (2004).
51. Miller MJ, Safrina O, Parker I, Cahalan MD: Imaging the single cell dynamics of CD4+ T cell activation by dendritic cells in lymph nodes. J. Exp. Med. 200, 847-856 (2004).
52. Miller MJ, Wei SH, Cahalan MD, Parker I: Autonomous T cell trafficking examined in vivo with intravital two-photon microscopy. Proc. Natl Acad. Sci. USA 100, 2604-9260 (2003).
53. Hickman HD, Takeda K, Skon CN et al.: Direct priming of antiviral CD8+ T cells in the peripheral interfollicular region of lymph nodes. Nat. Immunol. 9, 155-165 (2008).
54. Junt T, Moseman EA, Iannacone M et al.: Subcapsular sinus macrophages in lymph nodes clear lymph-borne viruses and present them to antiviral B cells. Nature 450, 110-114 (2007).
55. Ng LG, Hsu A, Mandell MA et al.: Migratory dermal dendritic cells act as rapid sensors of protozoan parasites. PLoS Pathog. 4, e1000222 (2008).
56. Peters NC, Egen JG, Secundino N et al.: In vivo imaging reveals an essential role for neutrophils in leishmaniasis transmitted by sand flies. Science 321, 970-974 (2008).
57. Liu CH, Fan YT, Dias A et al.: Cutting edge: dendritic cells are essential for in vivo IL-12 production and development of resistance against Toxoplasma gondii infection in mice. J. Immunol. 177, 31-35 (2006).
58. Persson CM, Lambert H, Vutova PP et al.: Transmission of Toxoplasma gondii from infected dendritic cells to natural killer cells. Infect. Immun. 77, 970-976 (2009).
59. Tait ED, Jordan KA, Dupont CD et al.: Virulence of Toxoplasma gondii is associated with distinct dendritic cell responses and reduced numbers of activated CD8+ T cells. J. Immunol. 185(3), 1502-1512 (2010).
60. Reinhardt RL, Hong S, Kang SJ, Wang ZE, Locksley RM: Visualization of IL-12/23p40 in vivo reveals immunostimulatory dendritic cell migrants that promote Th1 differentiation. J. Immunol. 177, 1618-1627 (2006).
61. Suzuki Y: Immunopathogenesis of cerebral toxoplasmosis. J. Infect. Dis. 186(Suppl. 2), S234-S240 (2002).
62. Chieppa M, Rescigno M, Huang AY, Germain RN: Dynamic imaging of dendritic cell extension into the small bowel lumen in response to epithelial cell TLR engagement. J. Exp. Med. 203, 2841-2852 (2006).
63. Kim JV, Kang SS, Dustin ML, McGavern DB: Myelomonocytic cell recruitment causes fatal CNS vascular injury during acute viral meningitis. Nature 457, 191-195 (2009).
64. Beattie L, Peltan A, Maroof A et al.: Dynamic imaging of experimental Leishmania donovani-induced hepatic granulomas detects Kupffer cell-restricted antigen presentation to antigen-specific CD8 T cells. PLoS Pathog. 6, e1000805 (2010).