Induction of dendritic cell migration upon Toxoplasma gondii infection potentiates parasite dissemination

Cellular Microbiology

Volumn 8, Issue 10, 2006, Pages 1611-1623

  Lambert, Henrik ^a,b   Hitziger, Niclas ^a,b   Dellacasa, Isabel ^b,c   Svensson, Mattias ^a   Barragan, Antonio ^a,b  

^a KAROLINSKA INSTITUTE   (Sweden)

^b SWEDISH INSTITUTE FOR INFECTIOUS DISEASE CONTROL   (Sweden)

^c KAROLINSKA INSTITUTE   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

CD11 ANTIGEN; CD18 ANTIGEN; CELL ADHESION MOLECULE; CHEMOKINE RECEPTOR CCR5; CHEMOKINE RECEPTOR CCR7; INHIBITORY GUANINE NUCLEOTIDE BINDING PROTEIN; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 1 RECEPTOR; LIPOPOLYSACCHARIDE; PERTUSSIS TOXIN; TOLL LIKE RECEPTOR; UNCOUPLING PROTEIN;

ANIMAL CELL; ARTICLE; CELL INVASION; CELL MATURATION; CELL MIGRATION; CELL MOTILITY; CHEMOTAXIS; CONTROLLED STUDY; DENDRITIC CELL; DISEASE EXACERBATION; ENDOTHELIUM CELL; HOST CELL; HUMAN; HUMAN CELL; IN VITRO STUDY; INOCULATION; MESENTERY LYMPH NODE; MOUSE; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SPLEEN; TOXOPLASMA GONDII; TOXOPLASMOSIS; UPREGULATION;

ADOPTIVE TRANSFER; ANIMALS; BONE MARROW CELLS; CELL MOVEMENT; CELLS, CULTURED; DENDRITIC CELLS; GREEN FLUORESCENT PROTEINS; GTP-BINDING PROTEIN ALPHA SUBUNITS, GI-GO; HUMANS; INTERLEUKIN-1; LYMPH NODES; MICE; MICE, INBRED C57BL; RECEPTORS, CCR5; RECEPTORS, CCR7; RECEPTORS, CHEMOKINE; SIGNAL TRANSDUCTION; SPLEEN; TOXOPLASMA; TOXOPLASMOSIS;

MURINAE; TOXOPLASMA; TOXOPLASMA GONDII;

EID: 33748469339     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/j.1462-5822.2006.00735.x     Document Type: Article

References (56)

1. Adachi, O., Kawai, T., Takeda, K., Matsumoto, M., Tsutsui, H., Sakagami, M., et al. (1998) Targeted disruption of the MyD88 gene results in loss of IL-1- and IL-18-mediated function. Immunity 9: 143-150.
2. Aliberti, J., Valenzuela, J.G., Carruthers, V.B., Hieny, S., Andersen, J., Charest, H., et al. (2003) Molecular mimicry of a CCR5 binding-domain in the microbial activation of dendritic cells. Nat Immunol 4: 485-490.
3. Ammon, C., Meyer, S.P., Schwarzfischer, L., Krause, S.W., Andreesen, R., and Kreutz, M. (2000) Comparative analysis of integrin expression on monocyte-derived macrophages and monocyte-derived dendritic cells. Immunology 100: 364-369.
4. Banchereau, J., and Steinman, R.M. (1998) Dendritic cells and the control of immunity. Nature 392: 245-252.
5. Barragan, A., and Sibley, L.D. (2002) Transepithelial migration of Toxoplasma gondii is linked to parasite motility and virulence. J Exp Med 195: 1625-1633.
6. Barragan, A., and Sibley, L.D. (2003) Migration of Toxoplasma gondii across biological barriers. Trends Microbiol 11: 426-430.
7. Barragan, A., Brossier, F., and Sibley, L.D. (2005) 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.
8. Brand, U., Bellinghausen, I., Enk, A.H., Jonuleit, H., Becker, D., Knop, J., and Saloga, J. (1998) Influence of extracellular matrix proteins on the development of cultured human dendritic cells. Eur J Immunol 28: 1673-1680.
9. Burns, S., Hardy, S.J., Buddle, J., Yong, K.L., Jones, G.E., and Thrasher, A.J. (2004) Maturation of DC is associated with changes in motile characteristics and adherence. Cell Motil Cytoskeleton 57: 118-132.
10. Carruthers, V.B., and Sibley, L.D. (1999) Mobilization of intracellular calcium stimulates microneme discharge in Toxoplasma gondii. Mol Microbiol 31: 421-428.
11. Caux, C., Ait-Yahia, S., Chemin, K., de Bouteiller, O., Dieu-Nosjean, M.C., Homey, B., et al. (2000) Dendritic cell biology and regulation of dendritic cell trafficking by chemokines. Springer Semin Immunopathol 22: 345-369.
12. Channon, J.Y., Seguin, R.M., and Kasper, L.H. (2000) Differential infectivity and division of Toxoplasma gondii in human peripheral blood leukocytes. Infect Immun 68: 4822-4826.
13. Chen, T., Guo, J., Yang, M., Han, C., Zhang, M., Chen, W., et al. (2004) Cyclosporin A impairs dendritic cell migration by regulating chemokine receptor expression and inhibiting cyclooxygenase-2 expression. Blood 103: 413-421.
14. Courret, N., Darche, S., Sonigo, P., Milon, G., Buzoni-Gatel, D., and Tardieux, I. (2006) CD11c and CD11b expressing mouse leukocytes transport single Toxoplasma gondii tachyzoites to the brain. Blood 107: 309-316.
15. Da Gama, L.M., Ribeiro-Gomes, F.L., Guimaraes, U., Jr, and Arnholdt, A.C. (2004) Reduction in adhesiveness to extracellular matrix components, modulation of adhesion molecules and in vivo migration of murine macrophages infected with Toxoplasma gondii. Microbes Infect 6: 1287-1296.
16. Desmonts, G., and Couvreur, J. (1974) Congenital toxoplasmosis: A prospective study of 378 pregnancies. N Engl J Med 290: 1110-1116.
17. Dobrowolski, J.M., and Sibley, L.D. (1996) Toxoplasma invasion of mammalian cells is powered by the actin cytoskeleton of the parasite. Cell 84: 933-939.
18. Donald, R.G.K., and Roos, D.S. (1993) Stable molecular transformation of Toxoplasma gondii: A selectable dihydrofolate reductase-thymidylate synthase marker based on drug resistance mutations in malaria. Proc Natl Acad Sci USA 90: 11703-11707.
19. Drevets, D.A., Dillon, M.J., Schawang, J.S., Van Rooijen, N., Ehrchen, J., Sunderkotter, C., and Leenen, P.J. (2004) The Ly-6Chigh monocyte subpopulation transports Listeria monocytogenes into the brain during systemic infection of mice. J Immunol 172: 4418-4424.
20. 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.
21. Dubey, J.P., and Beattie, C.P. (1988) Toxoplasmosis of Animals and Man. Boca Raton: CRC Press.
22. Entschladen, F., Bastian, P., Niggemann, B., Zaenker, K.S., and Lang, K. (2004) Inhibition of cell migration via G protein-coupled receptors to opioid peptides and angiotensin. Ann N Y Acad Sci 1028: 320-328.
23. Fischer, H.G., Bonifas, U., and Reichmann, G. (2000) Phenotype and functions of brain dendritic cells emerging during chronic infection of mice with Toxoplasma gondii. J Immunol 164: 4826-4834.
24. Gualde, N., and Harizi, H. (2004) Prostanoids and their receptors that modulate dendritic cell-mediated immunity. Immunol Cell Biol 82: 353-360.
25. Gubbels, M.J., Striepen, B., Shastri, N., Turkoz, M., and Robey, E.A. (2005) Class I major histocompatibility complex presentation of antigens that escape from the parasitophorous vacuole of Toxoplasma gondii. Infect Immun 73: 703-711.
26. Hitziger, N., Dellacasa, I., Albiger, B., and Barragan, A. (2005) Dissemination of Toxoplasma gondii to immunoprivileged organs and role of Toll/interleukin-1 receptor signaling for host resistance assessed by in vivo bioluminescence imaging. Cell Microbiol 7: 837-848.
27. Joiner, K.A., and Dubremetz, J.F. (1993) Toxoplasma gondii: A protozoan for the nineties. Infect Immun 61: 1169-1172.
28. Kasper, L., Courret, N., Darche, S., Luangsay, S., Mennechet, F., Minns, L., et al. (2004) Toxoplasma gondii and mucosal immunity. Int J Parasitol 34: 401-409.
29. Kim, K., Eaton, M.S., Schubert, W., Wu, S., and Tang, J. (2001) Optimized expression of green flourescent protein in Toxoplasma gondii using thermostable green flourescent protein mutants. Mol Biochem Parasitol 113: 309-313.
30. Kuida, K., Lippke, J.A., Ku, G., Harding, M.W., Livingston, D.J., Su, M.S., and Flavell, R.A. (1995) Altered cytokine export and apoptosis in mice deficient in interleukin-1 beta converting enzyme. Science 267: 2000-2003.
31. Lebedeva, T., Dustin, M.L., and Sykulev, Y. (2005) ICAM-1 co-stimulates target cells to facilitate antigen presentation. Curr Opin Immunol 17: 251-258.
32. Lingelbach, K., and Joiner, K.A. (1998) The parasitophorous vacuole membrane surrounding Plasmodium and Toxoplasma: An unusual compartment in infected cells. J Cell Sci 111 (Part 11): 1467-1475.
33. Lipscomb, M.F., and Masten, B.J. (2002) Dendritic cells: Immune regulators in health and disease. Physiol Rev 82: 97-130.
34. Luft, B.J., Hafner, R., Korzun, A.H., Leport, C., Antoniskis, D., Bosler, E.M., et al. (1993) Toxoplasmic encephalitis in patients with the acquired immunodeficiency syndrome. N Engl J Med 329: 995-1000.
35. McKee, A.S., Dzierszinski, F., Boes, M., Roos, D.S., and Pearce, E.J. (2004) Functional inactivation of immature dendritic cells by the intracellular parasite Toxoplasma gondii. J Immunol 173: 2632-2640.
36. Matrajt, M., Platt, C.D., Sagar, A.D., Lindsay, A., Moulton, C., and Roos, D.S. (2004) Transcript initiation, polyadenylation, and functional promoter mapping for the dihydrofolate reductase-thymidylate synthase gene of Toxoplasma gondii. Mol Biochem Parasitol 137: 229-238.
37. Mempel, T.R., Henrickson, S.E., and Von Andrian, U.H. (2004) T-cell priming by dendritic cells in lymph nodes occurs in three distinct phases. Nature 427: 154-159.
38. Mordue, D.G., Desai, N., Dustin, M., and Sibley, L.D. (1999) Invasion by Toxoplasma gondii establishes a moving junction that selectively excludes host cell plasma membrane proteins on the basis of their membrane anchoring. J Exp Med 190: 1783-1792.
39. Mordue, D.G., Monroy, F., La Regina, M., Dinarello, C.A., and Sibley, L.D. (2001) Acute toxoplasmosis leads to lethal overproduction of Th1 cytokines. J Immunol 167: 4574-4584.
40. Morisaki, J.H., Heuser, J.E., and Sibley, L.D. (1995) Invasion of Toxoplasma gondii occurs by active penetration of the host cell. J Cell Sci 108: 2457-2464.
41. Norbury, C.C., Chambers, B.J., Prescott, A.R., Ljunggren, H.G., and Watts, C. (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.
42. Reis e Sousa, C., Hieny, S., Scharton-Kersten, T., Jankovic, D., Charest, H., Germain, R.N., and Sher, A. (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.
43. Riol-Blanco, L., Sanchez-Sanchez, N., Torres, A., Tejedor, A., Narumiya, S., Corbi, A.L., et al. (2005) The chemokine receptor CCR7 activates in dendritic cells two signaling modules that independently regulate chemotaxis and migratory speed. J Immunol 174: 4070-4080.
44. Roberts, F., and McLeod, R. (1999) Pathogenesis of toxoplasmic retinochoroiditis. Parasitol Today 15: 51-57.
45. Sacks, D., and Sher, A. (2002) Evasion of innate immunity by parasitic protozoa. Nat Immunol 3: 1041-1047.
46. Sallusto, F., and Lanzavecchia, A. (1994) Efficient presentation of soluble antigen by cultured human dendritic cells is maintained by granulocyte/macrophage colony-stimulating factor plus interleukin 4 and downregulated by tumor necrosis factor alpha. J Exp Med 179: 1109-1118.
47. Sallusto, F., Lenig, D., Forster, R., Lipp, M., and Lanzavecchia, A. (1999) Two subsets of memory T lymphocytes with distinct homing potentials and effector functions. Nature 401: 708-712.
48. Scanga, C.A., Aliberti, J., Jankovic, D., Tilloy, F., Bennouna, S., Denkers, E.Y., et al. (2002) Cutting edge: MyD88 is required for resistance to Toxoplasma gondii infection and regulates parasite-induced IL-12 production by dendritic cells. J Immunol 168: 5997-6001.
49. Scott, P., and Hunter, C.A. (2002) Dendritic cells and immunity to leishmaniasis and toxoplasmosis. Curr Opin Immunol 14: 466-470.
50. Sousa, C.R., Hieny, S., Scharton-Kersten, T., Jankovic, D., Charest, H., Germain, R.N., and Sher, A. (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.
51. Steinman, R.M. (2003) Some interfaces of dendritic cell biology. APMIS 111: 675-697.
52. Steinman, R.M., Granelli-Piperno, A., Pope, M., Trumpfheller, C., Ignatius, R., Arrode, G., et al. (2003) The interaction of immunodeficiency viruses with dendritic cells. Curr Top Microbiol Immunol 276: 1-30.
53. Suzuki, Y., Claflin, J., Wang, X., Lengi, A., and Kikuchi, T. (2005) Microglia and macrophages as innate producers of interferon-gamma in the brain following infection with Toxoplasma gondii. Int J Parasitol 35: 83-90.
54. Urban, B.C., Ferguson, D.J., Pain, A., Willcox, N., Plebanski, M., Austyn, J.M., and Roberts, D.J. (1999) Plasmodium falciparum - infected erythrocytes modulate the maturation of dendritic cells. Nature 400: 73-77.
55. Wei, S., Marches, F., Borvak, J., Zou, W., Channon, J., White, M., et al. (2002) Toxoplasma gondii -infected human myeloid dendritic cells induce T-lymphocyte dysfunction and contact-dependent apoptosis. Infect Immun 70: 1750-1760.
56. Yarovinsky, F., Zhang, D., Andersen, J.F., Bannenberg, G.L., Serhan, C.N., Hayden, M.S., et al. (2005) TLR11 activation of dendritic cells by a protozoan profilin-like protein. Science 308: 1626-1629.