Skin mast cells control T cell-dependent host defense in Leishmania major infections

FASEB Journal

Volumn 20, Issue 14, 2006, Pages 2460-2467

  Maurer, Marcus ^a,b   Lopez Kostka, Susanna ^a   Siebenhaar, Frank ^a,b   Moelle, Katharina ^a   Metz, Martin ^a   Knop, Jürgen ^a   Von Stebut, Esther ^a,c  

^a UNIVERSITY MEDICAL CENTER MAINZ   (Germany)

^b CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^c JOHANNES GUTENBERG UNIVERSITY   (Germany)

Author keywords

Cytokine release; Dendritic cell; Leishmaniasis; Th1 Th2

Indexed keywords

CYTOKINE; INTERLEUKIN 12;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL FUNCTION; CONTROLLED STUDY; DENDRITIC CELL; HOST RESISTANCE; INFLAMMATION; LEISHMANIA MAJOR; LEISHMANIASIS; MACROPHAGE; MAST CELL; MOUSE; NEUTROPHIL; NONHUMAN; PARASITE IMMUNITY; PRIORITY JOURNAL; SKIN; T LYMPHOCYTE; TH1 CELL; TH2 CELL;

ANIMALS; GENE DELETION; LEISHMANIA MAJOR; LEISHMANIASIS, CUTANEOUS; MAST CELLS; MICE; MICE, INBRED C57BL; SKIN; T-LYMPHOCYTES; TIME FACTORS;

LEISHMANIA MAJOR;

EID: 33845673298     PISSN: 08926638     EISSN: None     Source Type: Journal    
DOI: 10.1096/fj.06-5860com     Document Type: Article

References (37)

1. Galli, S. J., Maurer, M., and Lantz, C. S. (1999) Mast cells as sentinels of innate immunity. Curr. Opin. Immunol. 11, 53-59
2. Henz, B. M., Maurer, M., Lippert, U., Worm, M., and Babina, M. (2001) Mast cells as initiators of immunity and host defense. Exp. Dermatol. 10, 1-10
3. Echtenacher, B., Mannel, D. N., and Hultner, L. (1996) Critical protective role of mast cells in a model of acute septic peritonitis. Nature 381, 75-77
4. Maurer, M., Echtenacher, B., Hultner, L., Kollias, G., Mannel, D. N., Langley, K. E., and Galli, S. J. (1998) The c-kit ligand, stem cell factor, can enhance innate immunity through effects on mast cells. J. Exp. Med. 188, 2343-2348
5. Li, E., Zhou, P., Petrin, Z., and Singer, S. M. (2004) Mast cell-dependent control of Giardia lamblia infections in mice. Infect. Immun. 72, 6642-6649
6. Artis, D., Villarino, A., Silverman, M., He, W., Thornton, E. M., Mu, S., Summer, S., Covey, T. M., Huang, E., Yoshida, H., et al. (2004) The IL-27 receptor (WSX-1) is an inhibitor of innate and adaptive elements of type 2 immunity. J. Immunol. 173, 5626-5634
7. Knight, P. A., Pemberton, A. D., Robertson, K. A., Roy, D. J., Wright, S. H., and Miller, H. R. (2004) Expression profiling reveals novel innate and inflammatory responses in the jejunal epithelial compartment during infection with Trichinella spiralis. Infect. Immun. 72, 6076-6086
8. Onah, D. N., and Nawa, Y. (2004) Mucosal mast cell-derived chondroitin sulphate levels in and worm expulsion from FcR-gamma-knockout mice following oral challenge with Strongyloides venezuelensis. J. Vet. Sci. 5, 221-226
9. Finkelman, F. D., Shea-Donohue, T., Morris, S. C., Gildea, L., Strait, R., Madden, K. B., Schopf, L., and Urban J. F., Jr. (2004) Interleukin-4- and interleukin-13-mediated host protection against intestinal nematode parasites. Immunol. Rev. 201, 139-155
10. Wershil, B. K., Theodos, C. M., Galli, S. J., and Titus, R. G. (1994) Mast cells augment lesion size and persistence during experimental Leishmania major infection in the mouse. J. Immunol. 152, 4563-4571
11. Katakura, K., Saito, S., Hamada, A., Matsuda, H., and Watanabe, N. (1993) Cutaneous leishmaniasis in mast cell-deficient W/Wv mice. Infect. Immun. 61, 2242-2244
12. Saha, B., Tonkal, A. M., Croft, S., and Roy, S. (2004) Mast cells at the host-pathogen interface: host-protection versus immune evasion in leishmaniasis. Clin. Exp. Immunol. 137, 19-23
13. Reiner, S. L., and Locksley, R. M. (1995) The regulation of immunity to Leishmania major. Annu. Rev. Immunol. 13, 151-177
14. Weber, A., Knop, J., and Maurer, M. (2003) Pattern analysis of human cutaneous mast cell populations by total body surface mapping. Br. J. Dermatol. 148, 224-228
15. Bidri, M., Vouldoukis, I., Mossalayi, M. D., Debre, P., Guillosson, J. J., Mazier, D., and Arock, M. (1997) Evidence for direct interaction between mast cells and Leishmania parasites. Parasite Immunol. 19, 475-483
16. Von Stebut, E., Metz, M., Milon, G., Knop, J., and Maurer, M. (2003) Early macrophage influx to sites of cutaneous granuloma formation is dependent on MIP-1alpha/beta released from neutrophils recruited by mast cell-derived TNFalpha. Blood 101, 210-215
17. Sacks, D., and Noben-Trauth, N. (2002) The immunology of susceptibility and resistance to Leishmania major in mice. Nat. Rev. Immunol. 2, 845-858
18. Von Stebut, E., Belkaid, Y., Jakob, T., Sacks, D. L., and Udey, M. C. (1998) Uptake of Leishmania major amastigotes results in activation and interleukin 12 release from murine skin-derived dendritic cells: implications for the initiation of anti-Leishmania immunity. J. Exp. Med. 188, 1547-1552
19. Von Stebut, E., Ehrchen, J. M., Belkaid, Y., Lopez Kostka, S., Molle, K., Knop, J., Sunderkotter, C., and Udey, M. C. (2003) Interleukin 1alpha promotes Th1 differentiation and inhibits disease progression in Leishmania major-susceptible BALB/c mice. J. Exp. Med. 198, 191-199
20. Wershil, B. K., Murakami, T., and Galli, S. J. (1988) Mast cell-dependent amplification of an immunologically nonspecific inflammatory response. Mast cells are required for the full expression of cutaneous acute inflammation induced by phorbol 12-myristate 13-acetate. J. Immunol. 140, 2356-2360
21. Galli, S. J., and Kitamura, Y. (1987) Animal model of human disease. Genetically mast cell-deficient W/Wv and Sl/Sld mice: their value for the analysis of the roles of mast cells in biological responses in vivo. Am. J. Pathol. 127, 191-198
22. Belkaid, Y., Mendez, S., Lira, R., Kadambi, N., Milon, G., and Sacks, D. L. (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
23. Chen, J. C., Chang, M. L., and Muench, M. O. (2003) A kinetic study of the murine mixed lymphocyte reaction by 5,6-carboxy-fluorescein diacetate succinimidyl ester labeling. J. Immunol. Methods. 279, 123-133
24. Adkins, B., Williamson, T., Guevara, P., and Bu, Y. (2003) Murine neonatal lymphocytes show rapid early cell cycle entry and cell division. J. Immunol. 170, 4548-4556
25. Ritter, U., Meissner, A., Scheidig, C., and Korner, H. (2004) CD8 alpha- and Langerin-negative dendritic cells, but not Langerhans cells, act as principal antigen-presenting cells in leishmaniasis. Eur. J. Immunol. 34, 1542-1550
26. Grimaldi, G., Jr., Soares, M. J., and Moriearty, P. L. (1984) Tissue eosinophilia and Leishmania mexicana mexicana eosinophil interactions in murine cutaneous leishmaniasis. Parasite Immunol. 6, 397-408
27. De Oliveira, M. P., Lima, M. C., Calheiros, A. S., Martins, M. A., Antas, P. R., De Luca, P. M., and Pirmez, C. (2005) Leishmania (Viannia) braziliensis: human mast cell line activation induced by logarithmic and stationary promastigote derived-lysates. Exp. Parasitol. 109, 72-79
28. Wershil, B. K., Mekori, Y. A., Murakami, T., and Galli, S. J. (1987) 125I-fibrin deposition in IgE-dependent immediate hypersensitivity reactions in mouse skin. Demonstration of the role of mast cells using genetically mast cell-deficient mice locally reconstituted with cultured mast cells. J. Immunol. 139, 2605-2614
29. Flohe, S. B., Bauer, C., Flohe, S., and Moll, H. (1998) Antigen-pulsed epidermal Langerhans cells protect susceptible mice from infection with the intracellular parasite Leishmania major. Eur. J. Immunol. 28, 3800-3811
30. Ahuja, S. S., Reddick, R. L., Sato, N., Montalbo, E., Kostecki, V., Zhao, W., Dolan, M. J., Melby, P. C., and Ahuja, S. K. (1999) Dendritic cell (DC)-based anti-infective strategies: DCs engineered to secrete IL-12 are a potent vaccine in a murine model of an intracellular infection. J. Immunol. 163, 3890-3897
31. Nakae, S., Suto, H., Kakurai, M., Sedgwick, J. D., Tsai, M., and Galli, S. J. (2005) Mast cells enhance T cell activation: importance of mast cell-derived TNF. Proc. Natl. Acad. Sci. U. S. A. 102, 6467-6472
32. Tacchini-Cottier, F., Zweifel, C., Belkaid, Y., Mukankundiye, C., Vasei, M., Launois, P., Milon, G., and Louis, J. A. (2000) An immunomodulatory function for neutrophils during the induction of a CD4+ Th2 response in BALB/c mice infected with Leishmania major. J. Immunol. 165, 2628-2636
33. + T cells are required for primary immunity in C57BL/6 mice following low-dose, intradermal challenge with Leishmania major. J. Immunol. 168, 3992-4000
34. Carrera, L., Gazzinelli, R. T., Badolato, R., Hieny, S., Muller, W., Kuhn, R., and Sacks, D. L. (1996) Leishmania promastigotes selectively inhibit interleukin 12 induction in bone marrow-derived macrophages from susceptible and resistant mice. J. Exp. Med. 183, 515-526
35. Belkaid, Y., Butcher, B., and Sacks, D. L. (1998) Analysis of cytokine production by inflammatory mouse macrophages at the single-cell level: selective impairment of IL-12 induction in Leishmania-infected cells. Eur. J. Immunol. 28, 1389-1400
36. Von Stebut, E., Belkaid, Y., Nguyen, B. V., Cushing, M., Sacks, D. L., and Udey, M. C. (2000) Leishmania major-infected murine Langerhans cell-like dendritic cells from susceptible mice release IL-12 after infection and vaccinate against experimental cutaneous leishmaniasis. Eur. J. Immunol. 30, 3498-3506
37. Galli, S. J., Nakae, S., and Tsai, M. (2005) Mast cells in the development of adaptive immune responses. Nat. Immunol. 6, 135-142