Cross-presenting dendritic cells are required for control of Leishmania major infection

European Journal of Immunology

Volumn 44, Issue 5, 2014, Pages 1422-1432

  Ashok, Devika ^a   Schuster, Steffen ^a   Ronet, Catherine ^a   Rosa, Muriel ^a   Mack, Vanessa ^a   Lavanchy, Christine ^a   Marraco, Silvia F ^a   Fasel, Nicolas ^a   Murphy, Kenneth M ^b   Tacchini Cottier, Fabienne ^a   Acha Orbea, Hans ^a  

^a UNIVERSITY OF LAUSANNE   (Switzerland)

^b WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Batf 3; Leishmania major

Indexed keywords

CD103 ANTIGEN; CD8 ANTIGEN; GAMMA INTERFERON; IMMUNOGLOBULIN E; IMMUNOGLOBULIN G1; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 13; INTERLEUKIN 17; INTERLEUKIN 4; PROTOZOON ANTIBODY;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELLULAR IMMUNITY; CONTROLLED STUDY; CROSS PRESENTATION; CYTOKINE PRODUCTION; DENDRITIC CELL; EX VIVO STUDY; FEMALE; IMMUNOSTIMULATION; KNOCKOUT MOUSE; LEISHMANIASIS; MALE; MOUSE; NONHUMAN; PARASITE IMMUNITY; PARASITE LOAD; PRIORITY JOURNAL; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; TH17 CELL; TH2 CELL;

BATF-3; CD8Α+ DENDRITIC CELLS; LEISHMANIA MAJOR;

ANIMALS; ANTIBODIES, PROTOZOAN; ANTIGEN PRESENTATION; BASIC-LEUCINE ZIPPER TRANSCRIPTION FACTORS; CD8-POSITIVE T-LYMPHOCYTES; CROSS-PRIMING; DENDRITIC CELLS; IMMUNOGLOBULIN E; INTERFERON-GAMMA; LEISHMANIA MAJOR; LEISHMANIASIS, CUTANEOUS; MICE; MICE, INBRED BALB C; MICE, KNOCKOUT; REPRESSOR PROTEINS; TH2 CELLS;

EID: 84899530490     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.201344242     Document Type: Article

References (50)

1. Sacks, D. and Noben-Trauth, N., The immunology of susceptibility and resistance to Leishmania major in mice. Nat. Rev. Immunol. 2002. 2: 845-858.
2. Reiner, S. L. and Locksley, R. M., The regulation of immunity to Leishmania major. Annu. Rev. Immunol. 1995. 13: 151-177.
3. Muller, I., Pedrazzini, T., Farrell, J. P. and Louis, J., T-cell responses and immunity to experimental infection with Leishmania major. Annu. Rev. Immunol. 1989. 7: 561-578.
4. Tacchini-Cottier, F., Weinkopff, T. and Launois, P., Does T helper differentiation correlate with resistance or susceptibility to infection with L. major? Some insights from the murine model. Front Immunol. 2012. 3: 32.
5. Mattner, F., Di Padova, K. and Alber, G., Interleukin-12 is indispensable for protective immunity against Leishmania major. Infect Immun. 1997. 65: 4378-4383.
6. Lopez Kostka, S., Dinges, S., Griewank, K., Iwakura, Y., Udey, M. C. and von Stebut, E., IL-17 promotes progression of cutaneous leishmaniasis in susceptible mice. J. Immunol. 2009. 182: 3039-3046.
7. Brandonisio, O., Spinelli, R. and Pepe, M., Dendritic cells in Leishmania infection. Microb. Infect 2004. 6: 1402-1409.
8. Liu, Y. J., Dendritic cell subsets and lineages, and their functions in innate and adaptive immunity. Cell 2001. 106: 259-262.
9. Charmoy, M., Brunner-Agten, S., Aebischer, D., Auderset, F., Launois, P., Milon, G., Proudfoot, A. E. et al., Neutrophil-derived CCL3 is essential for the rapid recruitment of dendritic cells to the site of Leishmania major inoculation in resistant mice. PLoS Pathog. 2010. 6: e1000755.
10. Ribeiro-Gomes, F. L., Peters, N. C., Debrabant, A. and Sacks, D. L., Efficient capture of infected neutrophils by dendritic cells in the skin inhibits the early anti-Leishmania response. PLoS Pathog. 2012. 8: e1002536.
11. Leon, B., Lopez-Bravo, M. and Ardavin, C., Monocyte-derived dendritic cells formed at the infection site control the induction of protective T helper 1 responses against Leishmania. Immunity 2007. 26: 519-531.
12. Ginhoux, F., Liu, K., Helft, J., Bogunovic, M., Greter, M., Hashimoto, D., Price, J. et al., The origin and development of nonlymphoid tissue CD103 +DCs. J. Exp. Med. 2009. 206: 3115-3130.
13. Misslitz, A. C., Bonhagen, K., Harbecke, D., Lippuner, C., Kamradt, T. and Aebischer, T., Two waves of antigen-containing dendritic cells in vivo in experimental Leishmania major infection. Eur. J. Immunol. 2004. 34: 715-725.
14. Ng, L. G., Hsu, A., Mandell, M. A., Roediger, B., Hoeller, C., Mrass, P., Iparraguirre, A. et al., Migratory dermal dendritic cells act as rapid sensors of protozoan parasites. PLoS Pathog. 2008. 4: e1000222.
15. Ritter, U., Meissner, A., Scheidig, C. and Korner, H., CD8 alpha- and Langerin-negative dendritic cells, but not Langerhans cells, act as principal antigen-presenting cells in leishmaniasis. Eur. J. Immunol. 2004. 34: 1542-1550.
16. Moll, H., Fuchs, H., Blank, C. and Rollinghoff, M., Langerhans cells transport Leishmania major from the infected skin to the draining lymph node for presentation to antigen-specific T cells. Eur. J. Immunol. 1993. 23: 1595-1601.
17. Kautz-Neu, K., Noordegraaf, M., Dinges, S., Bennett, C. L., John, D., Clausen, B. E. and von Stebut, E., Langerhans cells are negative regulators of the anti-Leishmania response. J. Exp. Med. 2011. 208: 885-891.
18. Iezzi, G., Frohlich, A., Ernst, B., Ampenberger, F., Saeland, S., Glaichenhaus, N. and Kopf, M., Lymph node resident rather than skin-derived dendritic cells initiate specific T cell responses after Leishmania major infection. J. Immunol. 2006. 177: 1250-1256.
19. Lemos, M. P., Esquivel, F., Scott, P. and Laufer, T. M., MHC class II expression restricted to CD8alpha+ and CD11b +dendritic cells is sufficient for control of Leishmania major. J. Exp. Med. 2004. 199: 725-730.
20. Henri, S., Curtis, J., Hochrein, H., Vremec, D., Shortman, K. and Handman, E., Hierarchy of susceptibility of dendritic cell subsets to infection by Leishmania major: inverse relationship to interleukin-12 production. Infect Immun. 2002. 70: 3874-3880.
21. Park, A. Y., Hondowicz, B., Kopf, M. and Scott, P., The role of IL-12 in maintaining resistance to Leishmania major. J. Immunol. 2002. 168: 5771-5777.
22. Scott, P., Hondowicz, B., Eaton, A. and Scharton-Kersten, T., The role of IL-12 in regulation of T helper cell subsets in vivo. Lessons from experimental cutaneous leishmaniasis. Ann. N Y Acad. Sci. 1996. 795: 250-256.
23. Shrimpton, R. E., Butler, M., Morel, A. S., Eren, E., Hue, S. S. and Ritter, M. A., CD205 (DEC-205): a recognition receptor for apoptotic and necrotic self. Mol. Immunol. 2009. 46: 1229-1239.
24. Poulin, L. F., Reyal, Y., Uronen-Hansson, H., Schraml, B. U., Sancho, D., Murphy, K. M., Hakansson, U. K. et al., DNGR-1 is a specific and universal marker of mouse and human Batf3-dependent dendritic cells in lymphoid and nonlymphoid tissues. Blood 2012. 119: 6052-6062.
25. Belz, G. T., Behrens, G. M., Smith, C. M., Miller, J. F., Jones, C., Lejon, K., Fathman, C. G. et al., The CD8alpha(+) dendritic cell is responsible for inducing peripheral self-tolerance to tissue-associated antigens. J. Exp. Med. 2002. 196: 1099-1104.
26. Bedoui, S., Whitney, P. G., Waithman, J., Eidsmo, L., Wakim, L., Caminschi, I., Allan, R. S. et al., Cross-presentation of viral and self antigens by skin-derived CD103+ dendritic cells. Nat. Immunol. 2009. 10: 488-495.
27. Hildner, K., Edelson, B. T., Purtha, W. E., Diamond, M., Matsushita, H., Kohyama, M., Calderon, B. et al., Batf3 deficiency reveals a critical role for CD8alpha +dendritic cells in cytotoxic T cell immunity. Science 2008. 322: 1097-1100.
28. Shortman, K. and Heath, W. R., The CD8+ dendritic cell subset. Immunol. Rev. 2010. 234: 18-31.
29. Mashayekhi, M., Sandau, M. M., Dunay, I. R., Frickel, E. M., Khan, A., Goldszmid, R. S., Sher, A. et al., CD8alpha(+) dendritic cells are the critical source of interleukin-12 that controls acute infection by Toxoplasma gondii tachyzoites. Immunity 2011. 35: 249-259.
30. Edelson, B. T., Bradstreet, T. R., Hildner, K., Carrero, J. A., Frederick, K. E., Kc, W., Belizaire, R. et al., CD8alpha(+) dendritic cells are an obligate cellular entry point for productive infection by Listeria monocytogenes. Immunity 2011. 35: 236-248.
31. Lin, M. L., Zhan, Y., Proietto, A. I., Prato, S., Wu, L., Heath, W. R., Villadangos, J. A. et al., Selective suicide of cross-presenting CD8+ dendritic cells by cytochrome c injection shows functional heterogeneity within this subset. Proc. Natl. Acad. Sci. USA 2008. 105: 3029-3034.
32. Matthews, D. J., Emson, C. L., McKenzie, G. J., Jolin, H. E., Blackwell, J. M. and McKenzie, A. N., IL-13 is a susceptibility factor for Leishmania major infection. J. Immunol. 2000. 164: 1458-1462.
33. Gonzalez-Lombana, C., Gimblet, C., Bacellar, O., Oliveira, W. W., Passos, S., Carvalho, L. P., Goldschmidt, M. et al., IL-17 mediates immunopathology in the absence of IL-10 following Leishmania major infection. PLoS Pathog. 2013. 9: e1003243.
34. Belkaid, Y., Hoffmann, K. F., Mendez, S., Kamhawi, S., Udey, M. C., Wynn, T. A. and Sacks, D. L., The role of interleukin (IL)-10 in the persistence of Leishmania major in the skin after healing and the therapeutic potential of anti-IL-10 receptor antibody for sterile cure. J. Exp. Med. 2001. 194: 1497-1506.
35. Noben-Trauth, N., Lira, R., Nagase, H., Paul, W. E. and Sacks, D. L., The relative contribution of IL-4 receptor signaling and IL-10 to susceptibility to Leishmania major. J. Immunol. 2003. 170: 5152-5158.
36. Schwarz, T., Remer, K. A., Nahrendorf, W., Masic, A., Siewe, L., Muller, W., Roers, A. et al., T cell-derived IL-10 determines leishmaniasis disease outcome and is suppressed by a dendritic cell based vaccine. PLoS Pathog. 2013. 9: e1003476.
37. Belkaid, Y., Piccirillo, C. A., Mendez, S., Shevach, E. M. and Sacks, D. L., CD4+CD25 + regulatory T cells control Leishmania major persistence and immunity. Nature 2002. 420: 502-507.
38. Suffia, I., Reckling, S. K., Salay, G. and Belkaid, Y., A role for CD103 in the retention of CD4+CD25+ Treg and control of Leishmania major infection. J. Immunol. 2005. 174: 5444-5455.
39. Tussiwand, R., Lee, W. L., Murphy, T. L., Mashayekhi, M., Wumesh, K. C., Albring, J. C., Satpathy, A. T. et al., Compensatory dendritic cell development mediated by BATF-IRF interactions. Nature 2012. 490: 502-507.
40. Seillet, C., Jackson, J. T., Markey, K. A., Brady, H. J., Hill, G. R., Macdonald, K. P., Nutt, S. L. et al., CD8alpha+ DCs can be induced in the absence of transcription factors Id2, Nfil3, and Batf3. Blood 2013. 121: 1574-1583.
41. Murphy, T. L., Tussiwand, R. and Murphy, K. M., Specificity through cooperation: BATF-IRF interactions control immune-regulatory networks. Nat. Rev. Immunol. 2013. 13: 499-509.
42. Brewig, N., Kissenpfennig, A., Malissen, B., Veit, A., Bickert, T., Fleischer, B., Mostbock, S. et al., Priming of CD8+ and CD4+ T cells in experimental leishmaniasis is initiated by different dendritic cell subtypes. J. Immunol. 2009. 182: 774-783.
43. von Stebut, E. and Udey, M. C., Requirements for Th1-dependent immunity against infection with Leishmania major. Microb. Infect 2004. 6: 1102-1109.
44. Park, A. Y., Hondowicz, B. D. and Scott, P., IL-12 is required to maintain a Th1 response during Leishmania major infection. J. Immunol. 2000. 165: 896-902.
45. Sypek, J. P., Chung, C. L., Mayor, S. E., Subramanyam, J. M., Goldman, S. J., Sieburth, D. S., Wolf, S. F. et al., Resolution of cutaneous leishmaniasis: interleukin 12 initiates a protective T helper type 1 immune response. J. Exp. Med. 1993. 177: 1797-1802.
46. Stobie, L., Gurunathan, S., Prussin, C., Sacks, D. L., Glaichenhaus, N., Wu, C. Y. and Seder, R. A., The role of antigen and IL-12 in sustaining Th1 memory cells in vivo: IL-12 is required to maintain memory/effector Th1 cells sufficient to mediate protection to an infectious parasite challenge. Proc. Natl. Acad. Sci. USA 2000. 97: 8427-8432.
47. Matheoud, D., Moradin, N., Bellemare-Pelletier, A., Shio, M. T., Hong, W. J., Olivier, M., Gagnon, E. et al., Leishmania evades host immunity by inhibiting antigen cross-presentation through direct cleavage of the SNARE VAMP8. Cell Host Microbe 2013. 14: 15-25.
48. Bertholet, S., Goldszmid, R., Morrot, A., Debrabant, A., Afrin, F., Collazo-Custodio, C., Houde, M. et al., Leishmania antigens are presented to CD8+ T cells by a transporter associated with antigen processing-independent pathway in vitro and in vivo. J. Immunol. 2006. 177: 3525-3533.
49. Titus, R. G., Marchand, M., Boon, T. and Louis, J. A., A limiting dilution assay for quantifying Leishmania major in tissues of infected mice. Parasite Immunol. 1985. 7: 545-555.
50. Da Silva, R. P., Hall, B. F., Joiner, K. A. and Sacks, D. L., CR1, the C3b receptor, mediates binding of infective Leishmania major metacyclic promastigotes to human macrophages. J. Immunol. 1989. 143: 617-622.