The Toxoplasma gondii-Shuttling function of dendritic cells is linked to the parasite genotype

Infection and Immunity

Volumn 77, Issue 4, 2009, Pages 1679-1688

  Lambert, Henrik ^a,b   Vutova, Polya P ^a,b   Adams, William C ^a,c   Loré, Karin ^a,c   Barragan, Antonio ^a,b,c  

^a KAROLINSKA INSTITUTE   (Sweden)

^b Department of Parasitology Mycology and Environmental Microbiology ^*  (Sweden)

^c SWEDISH INSTITUTE FOR INFECTIOUS DISEASE CONTROL   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCOPROTEIN P 15095;

ADOPTIVE TRANSFER; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL MIGRATION; CONTROLLED STUDY; DENDRITIC CELL; FEMALE; GENOTYPE; HUMAN; IN VITRO STUDY; IN VIVO CULTURE; LEUKOCYTE; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; TACHYZOITE; TOXOPLASMA GONDII; TOXOPLASMOSIS; ANIMAL; BONE MARROW CELL; CELL CULTURE; CELL MOTION; GENETICS; GROWTH, DEVELOPMENT AND AGING; IMMUNOLOGY; PARASITOLOGY; PATHOGENICITY; PHYSIOLOGY; SPECIES DIFFERENCE; TOXOPLASMA;

ADOPTIVE TRANSFER; ANIMALS; BONE MARROW CELLS; CELL MOVEMENT; CELLS, CULTURED; DENDRITIC CELLS; GENOTYPE; HUMANS; MICE; SPECIES SPECIFICITY; TOXOPLASMA;

EID: 63149149461     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.01289-08     Document Type: Article

References (51)

1. Ajzenberg, D., N. Cogne, L. Paris, M. H. Bessieres, P. Thulliez, D. Filisetti, H. Pelloux, P. Marty, and M. L. Darde. 2002. Genotype of 86 Toxoplasma gondii isolates associated with human congenital toxoplasmosis, and correlation with clinical findings. J. Infect. Dis. 186:684-689.
2. Barragan, A., and N. Hitziger. 2008. Transepithelial migration by Toxo- plasma. Subcell. Biochem. 47:198-207.
3. 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.
4. Bierly, A. L., W. J. Shufesky, W. Sukhumavasi, A. E. Morelli, and E. Y. Denkers. 2008. Dendritic cells expressing plasmacytoid marker PDCA-1 are Trojan horses during Toxoplasma gondii infection. J. Immunol. 181:8485-8491.
5. Carme, B., F. Bissuel, D. Ajzenberg, R. Bouyne, C. Aznar, M. Demar, S. Bichat, D. Louvel, A. M. Bourbigot, C. Peneau, P. Neron, and M. L. Darde. 2002. Severe acquired toxoplasmosis in immunocompetent adult patients in French Guiana. J. Clin. Microbiol. 40:4037-4044.
6. Channon, J. Y., R. M. Seguin, and L. H. Kasper. 2000. Differential infectivity and division of Toxoplasma gondii in human peripheral blood leukocytes. Infect. Immun. 68:4822-4826.
7. Courret, N., S. Darche, P. Sonigo, G. Milon, D. Buzoni-Gatel, and I. Tardi-eux. 2006. CD11c- and CD11b-expressing mouse leukocytes transport single Toxoplasma gondii tachyzoites to the brain. Blood 107:309-316.
8. Da Gama, L. M., F. L. Ribeiro-Gomes, U. Guimaraes, Jr., and A. C. Arn- holdt. 2004. Reduction in adhesiveness to extracellular matrix components, modulation of adhesion molecules and in vivo migration of murine macro- phages infected with Toxoplasma gondii. Microbes Infect. 6:1287-1296.
9. Darde, M. L. 2008. Toxoplasma gondii, "new" genotypes and virulence. Parasite (Paris) 15:366-371.
10. Dellacasa-Lindberg, I., N. Hitziger, and A. Barragan. 2007. Localized recrudescence of Toxoplasma infections in the central nervous system of immu-nocompromised mice assessed by in vivo bioluminescence imaging. Microbes Infect. 9:1291-1298.
11. Demar, M., D. Ajzenberg, D. Maubon, F. Djossou, D. Panchoe, W. Punwasi, N. Valery, C. Peneau, J. L. Daigre, C. Aznar, B. Cottrelle, L. Terzan, M. L. Darde, and B. Carme. 2007. Fatal outbreak of human toxoplasmosis along the Maroni River: epidemiological, clinical, and parasitological aspects. Clin. Infect. Dis. 45:e88-e95.
12. Dobrowolski, J. M., and L. D. Sibley. 1996. Toxoplasma invasion of mammalian cells is powered by the actin cytoskeleton of the parasite. Cell 84: 933-939.
13. Dubey, J. P. 1997. Bradyzoite-induced murine toxoplasmosis: stage conversion pathogenesis, and tissue cyst formation in mice fed bradyzoites of different strains of Toxoplasma gondii. J. Eukaryot. Microbiol. 44:592-602.
14. Dubey, J. P., C. A. Speer, S. K. Shen, O. C. H. Kwok, and J. A. Blixt. 1997. Oocyst-induced murine toxoplasmosis: life cycle, pathogenicity, and stage conversion in mice fed Toxoplasma gondii oocysts. J. Parasitol. 83:870-882.
15. Dunay, I. R., R. A. Damatta, B. Fux, R. Presti, S. Greco, M. Colonna, and L. D. Sibley. 2008. Gr1(+) inflammatory monocytes are required for mucosal resistance to the pathogen Toxoplasma gondii. Immunity 29:306-317.
16. Fuentes, I., J. M. Rubio, C. Ramirez, and J. Alvar. 2001. Genotypic characterization of Toxoplasma gondii strains associated with human toxoplasmosis in Spain: direct analysis from clinical samples. J. Clin. Microbiol. 39:1566-1570.
17. Gavrilescu, L. C., and E. Y. Denkers. 2001. IFN-γ overproduction and high level apoptosis are associated with high but not low virulence Toxoplasma gondii infection. J. Immunol. 167:902-909.
18. Geissmann, F., S. Jung, and D. R. Littman. 2003. Blood monocytes consist of two principal subsets with distinct migratory properties. Immunity 19:71-82.
19. Grigg, M. E., J. Ganatra, J. C. Boothroyd, and T. P. Margolis. 2001. Unusual abundance of atypical strains associated with human ocular toxoplasmosis. J. Infect. Dis. 184:633-639.
20. Herrmann, J. L., and P. H. Lagrange. 2005. Dendritic cells and Mycobacterium tuberculosis: which is the Trojan horse? Pathol. Biol. 53:35-40.
21. Hitziger, N., I. Dellacasa, B. Albiger, and A. Barragan. 2005. Dissemination of Toxoplasma gondii to immunoprivileged organs and role of Toll/interleu- kin-1 receptor signaling for host resistance assessed by in vivo biolumines- cence imaging. Cell. Microbiol. 7:837-848.
22. Honore, S., A. Couvelard, Y. J. Garin, C. Bedel, D. Henin, M. L. Darde, and F. Derouin. 2000. Genotyping of Toxoplasma gondii strains from immuno- compromised patients. Pathol. Biol. 48:541-547. (In French.)
23. Howe, D. K., S. Honoré, F. Derouin, and L. D. Sibley. 1997. Determination of genotypes of Toxoplasma gondii strains isolated from patients with toxo-plasmosis. J. Clin. Microbiol. 35:1411-1414.
24. Howe, D. K., and L. D. Sibley. 1995. Toxoplasma gondii comprises three clonal lineages: correlation of parasite genotype with human disease. J. Infect. Dis. 172:1561-1566.
25. Jang, M. H., N. Sougawa, T. Tanaka, T. Hirata, T. Hiroi, K. Tohya, Z. Guo, E. Umemoto, Y. Ebisuno, B. G. Yang, J. Y. Seoh, M. Lipp, H. Kiyono, and M. Miyasaka. 2006. CCR7 is critically important for migration of dendritic cells in intestinal lamina propria to mesenteric lymph nodes. J. Immunol. 176:803-810.
26. Johansson-Lindbom, B., M. Svensson, O. Pabst, C. Palmqvist, G. Marquez, R. Forster, and W. W. Agace. 2005. Functional specialization of gut CD103 + dendritic cells in the regulation of tissue-selective T cell homing. J. Exp. Med. 202:1063-1073.
27. Joynson, D. H. M., and T. G. Wreghitt (ed.). 2001. Toxoplasmosis: a comprehensive clinical guide. Cambridge University Press, Cambridge, United Kingdom.
28. 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.
29. Kim, L., B. A. Butcher, C. W. Lee, S. Uematsu, S. Akira, and E. Y. Denkers. 2006. Toxoplasma gondii genotype determines MyD88-dependent signaling in infected macrophages. J. Immunol. 177:2584-2591.
30. 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.
31. Lehmann, T., P. L. Marcet, D. H. Graham, E. R. Dahl, and J. P. Dubey. 2006. Globalization and the population structure of Toxoplasma gondii. Proc. Natl. Acad. Sci. USA 103:11423-11428.
32. Liu, C. H., Y. T. Fan, A. Dias, L. Esper, R. A. Corn, A. Bafica, F. S. Machado, and J. Aliberti. 2006. 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.
33. Lore, K., W. C. Adams, M. J. Havenga, M. L. Precopio, L. Holterman, J. Goudsmit, and R. A. Koup. 2007. Myeloid and plasmacytoid dendritic cells are susceptible to recombinant adenovirus vectors and stimulate polyfunc- tional memory T cell responses. J. Immunol. 179:1721-1729.
34. Masso, M. 2003. DC-SIGN points the way to a novel mechanism for HIV-1 transmission. MedGenMed 5:2.
35. McKee, A. S., F. Dzierszinski, M. Boes, D. S. Roos, and E. J. Pearce. 2004. Functional inactivation of immature dendritic cells by the intracellular parasite Toxoplasma gondii. J. Immunol. 173:2632-2640.
36. 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.
37. Pepper, M., F. Dzierszinski, E. Wilson, E. Tait, Q. Fang, F. Yarovinsky, T. M. Laufer, D. Roos, and C. A. Hunter. 2008. Plasmacytoid dendritic cells are activated by Toxoplasma gondii to present antigen and produce cytokines. J. Immunol. 180:6229-6236.
38. Persson, C. M., H. Lambert, P. P. Vutova, I. Dellacasa-Lindberg, J. Nederby, H. Yagita, H.-G. Ljunggren, A. Grandien, A. Barragan, and B. J. Chambers. 2009. Transmission of Toxoplasma gondii from infected dendritic cells to natural killer cells. Infect. Immun. 77:970-976.
39. Persson, E. K., A. M. Agnarson, H. Lambert, N. Hitziger, H. Yagita, B. J. Chambers, A. Barragan, and A. Grandien. 2007. Death receptor ligation or exposure to perforin trigger rapid egress of the intracellular parasite Toxo- plasma gondii. J. Immunol. 179:8357-8365.
40. Randolph, G. J., J. Ochando, and S. Partida-Sanchez. 2008. Migration of dendritic cell subsets and their precursors. Annu. Rev. Immunol. 26:293-316.
41. Reis e Sousa, C., S. Hieny, T. Scharton-Kersten, D. Jankovic, H. Charest, R. N. Germain, and A. Sher. 1997. In vivo microbial stimulation induces rapid CD40 ligand-independent production of interleukin 12 by dendritic cells and their redistribution to T cell areas. J. Exp. Med. 186:1819-1829.
42. Robben, P. M., D. G. Mordue, S. M. Truscott, K. Takeda, S. Akira, and L. D. Sibley. 2004. Production of IL-12 by macrophages infected with Toxoplasma gondii depends on the parasite genotype. J. Immunol. 172:3686-3694.
43. Sacks, D., and A. Sher. 2002. Evasion of innate immunity by parasitic protozoa. Nat. Immunol. 3:1041-1047.
44. Saeij, J. P., S. Coller, J. P. Boyle, M. E. Jerome, M. W. White, and J. C. Boothroyd. 2007. Toxoplasma co-opts host gene expression by injection of a polymorphic kinase homologue. Nature 445:324-327.
45. Sibley, L. D. 2004. Intracellular parasite invasion strategies. Science 304:248-253.
46. Sibley, L. D., and J. C. Boothroyd. 1992. Virulent strains of Toxoplasma gondii comprise a single clonal lineage. Nature (London) 359:82-85.
47. Su, C., D. Evans, R. H. Cole, J. C. Kissinger, J. W. Ajioka, and L. D. Sibley. 2003. Recent expansion of Toxoplasma through enhanced oral transmission. Science 299:414-416.
48. Sumyuen, M. H., Y. J. F. Garin, and F. Derouin. 1995. Early kinetics of Toxoplasma gondii infection in mice orally infected with cysts of an avirulent strain. J. Parasitol. 81:327-329.
49. Taylor, S., A. Barragan, C. Su, B. Fux, S. J. Fentress, K. Tang, W. L. Beatty, H. E. Hajj, M. Jerome, M. S. Behnke, M. White, J. C. Wootton, and L. D. Sibley. 2006. A secreted serine-threonine kinase determines virulence in the eukaryotic pathogen Toxoplasma gondii. Science 314:1776-1780.
50. Velmurugan, G. V., J. P. Dubey, and C. Su. 2008. Genotyping studies of Toxoplasma gondii isolates from Africa revealed that the archetypal clonal lineages predominate as in North America and Europe. Vet. Parasitol. 155:314-318.
51. Zenner, L., F. Darcy, A. Capron, and M. F. Cesbron-Delauw. 1998. Toxo- plasma gondii: kinetics of the dissemination in the host tissues during the acute phase of infection in rats and mice. Exp. Parasitol. 90:86-94.