Priming of CD8+ and CD4+ T cells in experimental Leishmaniasis is initiated by different dendritic cell subtypes

Journal of Immunology

Volumn 182, Issue 2, 2009, Pages 774-783

  Brewig, Nancy ^a   Kissenpfennig, Adrien ^b   Malissen, Bernard ^c   Veit, Alexandra ^a   Bickert, Thomas ^a   Fleischer, Bernhard ^a   Mostböck, Sven ^d   Ritter, Uwe ^a,d  

^a BERNHARD NOCHT INSTITUTE FOR TROPICAL MEDICINE   (Germany)

^b QUEEN'S UNIVERSITY BELFAST   (United Kingdom)

^c CNRS   (France)

^d UNIVERSITY OF REGENSBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

DIPHTHERIA TOXIN; LANGERIN; CD207 PROTEIN, MOUSE; LECTIN; MANNOSE BINDING LECTIN; MEMBRANE ANTIGEN;

ADAPTIVE IMMUNITY; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL FUNCTION; CELL PROLIFERATION; CONTROLLED STUDY; DENDRITIC CELL; FEMALE; IMMUNE RESPONSE; LANGERHANS CELL; LEISHMANIA MAJOR; LEISHMANIASIS; LYMPH NODE; MOUSE; NONHUMAN; PRIORITY JOURNAL; SKIN CELL; ANIMAL; C57BL MOUSE; CLASSIFICATION; COMPARATIVE STUDY; EPIDERMIS; GENE TARGETING; GENETICS; IMMUNOLOGY; INNATE IMMUNITY; LYMPHOCYTE ACTIVATION; METABOLISM; METHODOLOGY; PARASITOLOGY; PATHOLOGY; SKIN LEISHMANIASIS; TRANSGENIC MOUSE;

ANIMALS; ANTIGENS, SURFACE; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; DENDRITIC CELLS; EPIDERMIS; FEMALE; GENE KNOCK-IN TECHNIQUES; IMMUNITY, INNATE; LANGERHANS CELLS; LECTINS, C-TYPE; LEISHMANIA MAJOR; LEISHMANIASIS, CUTANEOUS; LYMPH NODES; LYMPHOCYTE ACTIVATION; MANNOSE-BINDING LECTINS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC;

EID: 60549091808     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.182.2.774     Document Type: Article

References (50)

1. Alexander, J., A. R. Satoskar, and D. G. Russell. 1999. Leishmania species: models of intracellular parasitism. J. Cell Sci. 112: 2993-3002.
2. Ritter, U., J. Mattner, J. S. Rocha, C. Bogdan, and H. Körner. 2004. The control of Leishmania (Leishmania) major by TNF in vivo is dependent on the parasite strain. Microbes Infect. 6: 559-565.
3. + regulatory T cells control Leishmania major persistence and immunity. Nature 420: 502-507.
4. Alexander, J., and K. Bryson. 2005. T helper (h)1/Th2 and Leishmania: paradox rather than paradigm. Immunol. Lett. 99: 17-23.
5. + T cells do not mediate a protective immune response. Immunobiology 195: 243-260.
6. von Stebut, E. 2007. Cutaneous Leishmania infection: progress in pathogenesis research and experimental therapy. Exp. Dermatol. 16: 340-346.
7. Stingl, G., and G. Steiner. 1989. Immunological host defense of the skin. Curr. Probl. Dermatol. 18: 22-30.
8. De Creus, A., K. Van Beneden, T. Taghon, F. Stolz, V. Debacker, J. Plum, and G. Leclercq. 2000. Langerhans cells that have matured in vivo in the absence of T cells are fully capable of inducing a helper CD4 as well as a cytotoxic CD8 response. J. Immunol. 165: 645-653.
9. Moll, H. 1993. Epidermal Langerhans cells are critical for immunoregulation of cutaneous leishmaniasis. Immunol. Today 14: 383-387.
10. + T cell polarization in mice is modulated by strain-specific major histocompatibility complex-independent differences within dendritic cells. J. Exp. Med. 198: 201-209.
11. Ritter, U., A. Meissner, C. Scheidig, and H. Körner. 2004. CD8α- and Langerin-negative dendritic cells, but not Langerhans cells, act as principal antigen-presenting cells in leishmaniasis. Eur. J. Immunol. 34: 1542-1550.
12. Carbone, F. R., G. T. Belz, and W. R. Heath. 2004. Transfer of antigen between migrating and lymph node-resident DCs in peripheral T-cell tolerance and immunity. Trends Immunol. 25: 655-658.
13. Valladeau, J., O. Ravel, C. Dezutter-Dambuyant, K. Moore, M. Kleijmeer, Y. Liu, V. Duvert-Frances, C. Vincent, D. Schmitt, J. Davoust, et al. 2000. Langerin, a novel C-type lectin specific to Langerhans cells, is an endocytic receptor that induces the formation of Birbeck granules. Immunity 12: 71-81.
14. Kissenpfennig, A., S. Henri, B. Dubois, C. Laplace-Builhe, P. Perrin, N. Romani, C. H. Tripp, P. Douillard, L. Leserman, D. Kaiserlian, et al. 2005. Dynamics and function of Langerhans cells in vivo: dermal dendritic cells colonize lymph node areas distinct from slower migrating Langerhans cells. Immunity 22: 643-654.
15. + dendritic cells that develop and function independently of epidermal Langerhans cells. J. Exp. Med. 204: 3119-3131.
16. + dendritic cells. J. Exp. Med. 204: 3147-3156.
17. + dendritic cells survey the skin in the steady state. J. Exp. Med. 204: 3133-3146.
18. Stoecklinger, A., I. Grieshuber, S. Scheiblhofer, R. Weiss, U. Ritter, A. Kissenpfennig, B. Malissen, N. Romani, F. Koch, F. Ferreira, J. Thalhamer, and P. Hammerl. 2007. Epidermal Langerhans cells are dispensable for humoral and cell-mediated immunity elicited by gene gun immunization. J. Immunol. 179: 886-893.
19. Solbach, W., K. Forberg, E. Kammerer, C. Bogdan, and M. Röllinghoff. 1986. Suppressive effect of cyclosporin A on the development of Leishmania tropica-induced lesions in genetically susceptible BALB/c mice. J. Immunol. 137: 702-707.
20. Pahl, A., U. Kuhlbrandt, K. Brune, M. Röllinghoff, and A. Gessner. 1999. Quantitative detection of Borrelia burgdorferi by real-time PCR. J. Clin. Microbiol. 37: 1958-1963.
21. Schulz, A., K. Mellenthin, G. Schonian, B. Fleischer, and C. Drosten. 2003. Detection, differentiation, and quantitation of pathogenic Leishmania organisms by a fluorescence resonance energy transfer-based real-time PCR assay. J. Clin. Microbiol. 41: 1529-1535.
22. Weiss, R., S. Scheiblhofer, J. Thalhamer, T. Bickert, U. Richardt, B. Fleischer, and U. Ritter. 2007. Epidermal inoculation of Leishmania-antigen by gold bombardment results in a chronic form of leishmaniasis. Vaccine 25: 25-33.
23. Ritter, U., A. Lechner, K. Scharl, Z. Kiafard, J. Zwirner, and H. Korner. 2007. TNF controls the infiltration of dendritic cells into the site of Leishmania major infection. Med. Microbiol. Immunol. 197: 29-37.
24. Ritter, U., and A. Osterloh. 2007. A new view on cutaneous dendritic cell subsets in experimental leishmaniasis. Med. Microbiol. Immunol. 196: 51-59.
25. Anderson, C. F., M. Oukka, V. J. Kuchroo, and D. Sacks. 2007. CD4(+) CD25(-)Foxp3(-) Th1 cells are the source of IL-10-mediated immune suppression in chronic cutaneous leishmaniasis. J. Exp. Med. 204: 285-297.
26. Gallatin, W. M., I. L. Weissman, and E. C. Butcher. 1983. A cell-surface molecule involved in organ-specific homing of lymphocytes. Nature 304: 30-34.
27. Oehen, S., and K. Brduscha-Riem. 1998. Differentiation of naive CTL to effector and memory CTL: correlation of effector function with phenotype and cell division. J. Immunol. 161: 5338-5346.
28. Bogdan, C., A. Gessner, W. Solbach, and M. Röllinghoff. 1996. Invasion, control and persistence of Leishmania parasites. Curr. Opin. Immunol. 8: 517-525.
29. Belkaid, Y., S. Mendez, R. Lira, N. Kadambi, G. Milon, and D. Sacks. 2000. A natural model of Leishmania major infection reveals a prolonged "silent" phase of parasite amplification in the skin before the onset of lesion formation and immunity. J. Immunol. 165: 969-977.
30. Moll, H., H. Fuchs, C. Blank, and M. Röllinghoff. 1993. Langerhans cells transport Leishmania major from the infected skin to the draining lymph node for presentation to antigen-specific T cells. Eur. J. Immunol. 23: 1595-1601.
31. Moll, H., U. Ritter, S. Flohe, K. Erb, C. Bauer, and C. Blank. 1996. Cutaneous leishmaniasis: a model for analysis of the immunoregulation by accessory cells. Med. Microbiol. Immunol. 184: 163-168.
32. Titus, R. G., M. Marchand, T. Boon, and J. A. Louis. 1985. A limiting dilution assay for quantifying Leishmania major in tissues of infected mice. Parasite Immunol. 7: 545-555.
33. van der Kwast, T. H., J. G. Olthof, H. de Ruiter, and R. Benner. 1979. Secondary delayed type hypersensitivity to sheep red blood cells in mice: dependence on long-lived memory cells. Cell. Immunol. 43: 94-102.
34. Wilhelm, P., U. Ritter, S. Labbow, N. Donhauser, M. Röllinghoff, C. Bogdan, and H. Körner. 2001. Rapidly fatal leishmaniasis in resistant C57BL/6 mice lacking TNF. J. Immunol. 166: 4012-4019.
35. Villadangos, J. A., and P. Schnorrer. 2007. Intrinsic and cooperative antigen-presenting functions of dendritic-cell subsets in vivo. Nat. Rev. 7: 543-555.
36. Bennett, C. L., E. van Rijn, S. Jung, K. Inaba, R. M. Steinman, M. L. Kapsenberg, and B. E. Clausen. 2005. Inducible ablation of mouse Langerhans cells diminishes but fails to abrogate contact hypersensitivity. J. Cell Biol. 169: 569-576.
37. Kaplan, D. H., M. C. Jenison, S. Saeland, W. D. Shlomchik, and M. J. Shlomchik. 2005. Epidermal Langerhans cell-deficient mice develop enhanced contact hypersensitivity. Immunity 23: 611-620.
38. Fukunaga, A., N. M. Khaskhely, C. S. Sreevidya, S. N. Byrne, and S. E. Ullrich. 2008. Dermal dendritic cells, and not Langerhans cells, play an essential role in inducing an immune response. J. Immunol. 180: 3057-3064.
39. Germain, R. N., F. Castellino, M. Chieppa, J. G. Egen, A. Y. Huang, L. Y. Koo, and H. Qi. 2005. An extended vision for dynamic high-resolution intravital immune imaging. Semin. Immunol. 17: 431-441.
40. Katakai, T., T. Hara, J. H. Lee, H. Gonda, M. Sugai, and A. Shimizu. 2004. A novel reticular stromal structure in lymph node cortex: an immuno-platform for interactions among dendritic cells, T cells and B cells. Int. Immunol. 16: 1133-1142.
41. + T cytotoxic 1 cells inducing keratinocyte apoptosis. J. Immunol. 168: 3079-3087.
42. + T cells by a transporter associated with antigen processing-independent pathway in vitro and in vivo. J. Immunol. 177: 3525-3533.
43. Lin, M. L., Y. Zhan, J. A. Villadangos, and A. M. Lew. 2008. The cell biology of cross-presentation and the role of dendritic cell subsets. Immunol. Cell Biol. 86: 353-362.
44. + T cells. J. Immunol. 178: 6861-6866.
45. - but not plasmacytoid dendritic cells. J. Exp. Med. 205: 1621-1634.
46. Muller, I. 1992. Role of T cell subsets during the recall of immunologic memory to Leishmania major. Eur. J. Immunol. 22: 3063-3069.
47. + T cells are required for primary immunity in C57BL/6 mice following low-dose, intradermal challenge with Leishmania major. J. Immunol. 168: 3992-4000.
48. Moreno, J. 2007. Changing views on Langerhans cell functions in leishmaniasis. Trends Parasitol. 23: 86-88.
49. - Th1 cells are the major source of host-protective regulatory IL-10 during intracellular protozoan infection. J. Exp. Med. 204: 273-283.
50. Scott, P. 2005. Immunologic memory in cutaneous leishmaniasis. Cell. Microbiol. 7: 1707-1713.