Langerhans cells promote early germinal center formation in response to Leishmania-derived cutaneous antigens

European Journal of Immunology

Volumn 44, Issue 10, 2014, Pages 2955-2967

  Zimara, Nicole ^a   Florian, Christian ^a   Schmid, Maximilian ^a   Malissen, Bernard ^b   Kissenpfennig, Adrien ^c   Männel, Daniela N ^a   Edinger, Matthias ^d   Hutchinson, James A ^d   Hoffmann, Petra ^d   Ritter, Uwe ^a  

^a UNIVERSITY OF REGENSBURG   (Germany)

^b CENTRE D IMMUNOLOGIE DE MARSEILLE LUMINY   (France)

^c QUEEN'S UNIVERSITY BELFAST   (United Kingdom)

^d UNIVERSITY HOSPITAL REGENSBURG   (Germany)

Author keywords

B cells; Follicular helper; Germinal center reaction; Langerhans cells; Leishmania major; T cells

Indexed keywords

CYTOKINE; LANGERIN; PARASITE ANTIGEN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN SPECIFICITY; ARTICLE; B LYMPHOCYTE; B LYMPHOCYTE DIFFERENTIATION; CD4+ T LYMPHOCYTE; CELL INTERACTION; CONTROLLED STUDY; CYTOKINE PRODUCTION; FEMALE; FOLLICULAR DENDRITIC CELL; FOLLICULAR HELPER T CELL; GENE REARRANGEMENT; GERMINAL CENTER; HELPER CELL; IMMUNE RESPONSE; IN VIVO STUDY; LANGERHANS CELL; LEISHMANIA MAJOR; LYMPHATIC DRAINAGE; MOUSE; NONHUMAN; PRIORITY JOURNAL; SKIN LEISHMANIASIS; SOMATIC HYPERMUTATION; ANIMAL; C57BL MOUSE; CELL DIFFERENTIATION; FLOW CYTOMETRY; IMMUNOHISTOCHEMISTRY; IMMUNOLOGY; LEISHMANIA; LYMPHOCYTE ACTIVATION; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; T LYMPHOCYTE; TRANSGENIC MOUSE;

ANIMALS; ANTIGENS, PROTOZOAN; B-LYMPHOCYTES; CELL DIFFERENTIATION; FEMALE; FLOW CYTOMETRY; GERMINAL CENTER; IMMUNOHISTOCHEMISTRY; LANGERHANS CELLS; LEISHMANIA; LEISHMANIASIS, CUTANEOUS; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; T-LYMPHOCYTES;

EID: 84923673310     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.201344263     Document Type: Article

References (58)

1. Victora, G. D. and Nussenzweig, M. C., Germinal centers. Annu. Rev. Immunol. 2012. 30: 429-457.
2. MacLennan, I. C., Germinal centers. Annu. Rev. Immunol. 1994. 12: 117-139.
3. Shulman, Z., Gitlin, A. D., Targ, S., Jankovic, M., Pasqual, G., Nussenzweig, M. C. and Victora, G. D., T follicular helper cell dynamics in germinal centers. Science 2013. 341: 673-677.
4. Nurieva, R. I., Chung, Y., Hwang, D., Yang, X. O., Kang, H. S., Ma, L., Wang, Y. H. et al., Generation of T follicular helper cells is mediated by interleukin-21 but independent of T helper 1, 2, or 17 cell lineages. Immunity 2008. 29: 138-149.
5. Hardtke, S., Ohl, L. and Forster, R., Balanced expression of CXCR5 and CCR7 on follicular T helper cells determines their transient positioning to lymph node follicles and is essential for efficient B-cell help. Blood 2005. 106: 1924-1931.
6. Ansel, K. M., McHeyzer-Williams, L. J., Ngo, V. N., McHeyzer-Williams, M. G. and Cyster, J. G., In vivo-activated CD4 T cells upregulate CXC chemokine receptor 5 and reprogram their response to lymphoid chemokines. J. Exp. Med. 1999. 190: 1123-1134.
7. Reinhardt, R. L., Liang, H. E. and Locksley, R. M., Cytokine-secreting follicular T cells shape the antibody repertoire. Nat. Immunol. 2009. 10: 385-393.
8. Vinuesa, C. G., Tangye, S. G., Moser, B. and Mackay, C. R., Follicular B helper T cells in antibody responses and autoimmunity. Nat. Rev. Immunol. 2005. 5: 853-865.
9. Okada, T., Miller, M. J., Parker, I., Krummel, M. F., Neighbors, M., Hartley, S. B., O'Garra, A. et al., Antigen-engaged B cells undergo chemotaxis toward the T zone and form motile conjugates with helper T cells. PLoS Biol. 2005. 3: e150.
10. Basso, K. and Dalla-Favera, R., BCL6: master regulator of the germinal center reaction and key oncogene in B cell lymphomagenesis. Adv. Immunol. 2010. 105: 193-210.
11. Muramatsu, M., Kinoshita, K., Fagarasan, S., Yamada, S., Shinkai, Y. and Honjo, T., Class switch recombination and hypermutation require activation-induced cytidine deaminase (AID), a potential RNA editing enzyme. Cell 2000. 102: 553-563.
12. Malissen, B., Revisiting the follicular helper T cell paradigm. Nat. Immunol. 2009. 10: 371-372.
13. Deenick, E. K., Chan, A., Ma, C. S., Gatto, D., Schwartzberg, P. L., Brink, R. and Tangye, S. G., Follicular helper T cell differentiation requires continuous antigen presentation that is independent of unique B cell signaling. Immunity 2010. 33: 241-253.
14. Moll, H., Epidermal Langerhans cells are critical for immunoregulation of cutaneous leishmaniasis. Immunol. Today 1993. 14: 383-387.
15. Brewig, N., Kissenpfennig, A., Malissen, B., Veit, A., Bickert, T., Fleischer, B., Mostböck, 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.
16. Baumjohann, D., Okada, T. and Ansel, K. M., Cutting edge: distinct waves of BCL6 expression during T follicular helper cell development. J. Immunol. 2011. 187: 2089-2092.
17. Bursch, L. S., Wang, L., Igyarto, B., Kissenpfennig, A., Malissen, B., Kaplan, D. H. and Hogquist, K. A., Identification of a novel population of Langerin + dendritic cells. J. Exp. Med. 2007. 204: 3147-3156.
18. Kissenpfennig, A., Henri, S., Dubois, B., Laplace-Builhe, C., Perrin, P., Romani, N., Tripp, C. H. et al., Dynamics and function of Langerhans cells in vivo: dermal dendritic cells colonize lymph node areas distinct from slower migrating Langerhans cells. Immunity 2005. 22: 643-654.
19. Poulin, L. F., Henri, S., de Bovis, B., Devilard, E., Kissenpfennig, A. and Malissen, B., The dermis contains langerin + dendritic cells that develop and function independently of epidermal Langerhans cells. J. Exp. Med. 2007. 204: 3119-3131.
20. Ginhoux, F., Collin, M. P., Bogunovic, M., Abel, M., Leboeuf, M., Helft, J., Ochando, J. et al., Blood-derived dermal langerin + dendritic cells survey the skin in the steady state. J. Exp. Med. 2007. 204: 3133-3146.
21. Bollig, N., Brustle, A., Kellner, K., Ackermann, W., Abass, E., Raifer, H., Camara, B. et al., Transcription factor IRF4 determines germinal center formation through follicular T-helper cell differentiation. Proc. Natl. Acad. Sci. USA 2012. 109: 8664-8669.
22. Fooksman, D. R., Schwickert, T. A., Victora, G. D., Dustin, M. L., Nussenzweig, M. C. and Skokos, D., Development and migration of plasma cells in the mouse lymph node. Immunity 2010. 33: 118-127.
23. Kelsoe, G., The germinal center: a crucible for lymphocyte selection. Semin. Immunol. 1996. 8: 179-184.
24. Hsu, S. M. and Jaffe, E. S., Phenotypic expression of B-lymphocytes. 1. Identification with monoclonal antibodies in normal lymphoid tissues. Am. J. Pathol. 1984. 114: 387-395.
25. Klein, U. and Dalla-Favera, R., Germinal centres: role in B-cell physiology and malignancy. Nat. Rev. Immunol. 2008. 8: 22-33.
26. Cattoretti, G., Chang, C. C., Cechova, K., Zhang, J., Ye, B. H., Falini, B., Louie, D. C. et al., BCL-6 protein is expressed in germinal-center B cells. Blood 1995. 86: 45-53.
27. Allman, D., Jain, A., Dent, A., Maile, R. R., Selvaggi, T., Kehry, M. R. and Staudt, L. M., BCL-6 expression during B-cell activation. Blood 1996. 87: 5257-5268.
28. Ranuncolo, S. M., Polo, J. M., Dierov, J., Singer, M., Kuo, T., Greally, J., Green, R. et al., Bcl-6 mediates the germinal center B cell phenotype and lymphomagenesis through transcriptional repression of the DNA-damage sensor ATR. Nat. Immunol. 2007. 8: 705-714.
29. Ye, B. H., Cattoretti, G., Shen, Q., Zhang, J., Hawe, N., de Waard, R., Leung, C. et al., The BCL-6 proto-oncogene controls germinal-centre formation and Th2-type inflammation. Nat. Genet. 1997. 16: 161-170.
30. Coico, R. F., Bhogal, B. S. and Thorbecke, G. J., Relationship of germinal centers in lymphoid tissue to immunologic memory. VI. Transfer of B cell memory with lymph node cells fractionated according to their receptors for peanut agglutinin. J. Immunol. 1983. 131: 2254-2257.
31. Phan, T. G., Green, J. A., Gray, E. E., Xu, Y. and Cyster, J. G., Immune complex relay by subcapsular sinus macrophages and noncognate B cells drives antibody affinity maturation. Nat. Immunol. 2009. 10: 786-793.
32. Palm, N. W. and Medzhitov, R., Immunostimulatory activity of haptenated proteins. Proc. Natl. Acad. Sci. USA 2009. 106: 4782-4787.
33. Presicce, P., Taddeo, A., Conti, A., Villa, M. L. and Della Bella, S., Keyhole limpet hemocyanin induces the activation and maturation of human dendritic cells through the involvement of mannose receptor. Mol. Immunol. 2008. 45: 1136-1145.
34. Teitz-Tennenbaum, S., Li, Q., Davis, M. A. and Chang, A. E., Dendritic cells pulsed with keyhole limpet hemocyanin and cryopreserved maintain anti-tumor activity in a murine melanoma model. Clin. Immunol. 2008. 129: 482-491.
35. Noelle, R. J., Snow, E. C., Uhr, J. W. and Vitetta, E. S., Activation of antigen-specific B cells: role of T cells, cytokines, and antigen in induction of growth and differentiation. Proc. Natl. Acad. Sci. USA 1983. 80: 6628-6631.
36. Crotty, S., Follicular helper CD4 T Cells (T(FH)). Annu. Rev. Immunol. 2011. 29: 621-663.
37. Crotty, S., Johnston, R. J. and Schoenberger, S. P., Effectors and memories: Bcl-6 and Blimp-1 in T and B lymphocyte differentiation. Nat. Immunol. 2010. 11: 114-120.
38. Goenka, R., Barnett, L. G., Silver, J. S., O'Neill, P. J., Hunter, C. A., Cancro, M. P. and Laufer, T. M., Cutting edge: dendritic cell-restricted antigen presentation initiates the follicular helper T cell program but cannot complete ultimate effector differentiation. J. Immunol. 2011. 187: 1091-1095.
39. Merad, M., Ginhoux, F. and Collin, M., Origin, homeostasis and function of Langerhans cells and other langerin-expressing dendritic cells. Nat. Rev. Immunol. 2008. 8: 935-947.
40. 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.
41. Weiss, R., Scheiblhofer, S., Thalhamer, J., Bickert, T., Richardt, U., Fleischer, B. and Ritter, U., Epidermal inoculation of Leishmania-antigen by gold bombardment results in a chronic form of leishmaniasis. Vaccine 2007. 25: 25-33.
42. Brown, D. R. and Reiner, S. L., Polarized helper-T-cell responses against Leishmania major in the absence of B cells. Infect. Immun. 1999. 67: 266-270.
43. Itano, A. A. and Jenkins, M. K., Antigen presentation to naive CD4 T cells in the lymph node. Nat. Immunol. 2003. 4: 733-739.
44. Itano, A. A., McSorley, S. J., Reinhardt, R. L., Ehst, B. D., Ingulli, E., Rudensky, A. Y. and Jenkins, M. K., Distinct dendritic cell populations sequentially present antigen to CD4 T cells and stimulate different aspects of cell-mediated immunity. Immunity 2003. 19: 47-57.
45. Bennett, C. L., Noordegraaf, M., Martina, C. A. and Clausen, B. E., Langerhans cells are required for efficient presentation of topically applied hapten to T cells. J. Immunol. 2007. 179: 6830-6835.
46. Johnston, R. J., Poholek, A. C., DiToro, D., Yusuf, I., Eto, D., Barnett, B., Dent, A. L. et al., Bcl6 and Blimp-1 are reciprocal and antagonistic regulators of T follicular helper cell differentiation. Science 2009. 325: 1006-1010.
47. Nurieva, R. I., Chung, Y., Martinez, G. J., Yang, X. O., Tanaka, S., Matskevitch, T. D., Wang, Y. H. et al., Bcl6 mediates the development of T follicular helper cells. Science 2009. 325: 1001-1005.
48. King, C., Tangye, S. G. and Mackay, C. R., T follicular helper (TFH) cells in normal and dysregulated immune responses. Annu. Rev. Immunol. 2008. 26: 741-766.
49. Kageyama, R., Cannons, J. L., Zhao, F., Yusuf, I., Lao, C., Locci, M., Schwartzberg, P. L. et al., The receptor Ly108 functions as a SAP adaptor-dependent on-off switch for T cell help to B cells and NKT cell development. Immunity 2012. 36: 986-1002.
50. Qi, H., Cannons, J. L., Klauschen, F., Schwartzberg, P. L. and Germain, R. N., SAP-controlled T-B cell interactions underlie germinal centre formation. Nature 2008. 455: 764-769.
51. Cannons, J. L., Qi, H., Lu, K. T., Dutta, M., Gomez-Rodriguez, J., Cheng, J., Wakeland, E. K. et al., Optimal germinal center responses require a multistage T cell:B cell adhesion process involving integrins, SLAM-associated protein, and CD84. Immunity 2008. 32: 253-265.
52. Ritter, U., Mattner, J., Rocha, J. S., Bogdan, C. and Korner, H., The control of Leishmania (Leishmania) major by TNF in vivo is dependent on the parasite strain. Microbes Infect. 2004. 6: 559-565.
53. Aebischer, T., Moody, S. F. and Handman, E., Persistence of virulent Leishmania major in murine cutaneous leishmaniasis: a possible hazard for the host. Infect. Immun. 1993. 61: 220-226.
54. Ritter, U., Frischknecht, F. and van Zandbergen, G., Are neutrophils important host cells for Leishmania parasites? Trends Parasitol. 2009. 25: 505-510.
55. Wiethe, C., Debus, A., Mohrs, M., Steinkasserer, A., Lutz, M. and Gessner, A., Dendritic cell differentiation state and their interaction with NKT cells determine Th1/Th2 differentiation in the murine model of Leishmania major infection. J. Immunol. 2008. 180: 4371-4381.
56. Solbach, W., Forberg, K., Kammerer, E., Bogdan, C. and Rollinghoff, M., Suppressive effect of cyclosporin A on the development of Leishmania tropica-induced lesions in genetically susceptible BALB/c mice. J. Immunol. 1986. 137: 702-707.
57. Florian, C., Barth, T., Wege, A. K., Mannel, D. N. and Ritter, U., An advanced approach for the characterization of dendritic cell-induced T cell proliferation in situ. Immunobiology 2010. 215: 855-862.
58. Steiner, G. E., Ecker, R. C., Kramer, G., Stockenhuber, F. and Marberger, M. J., Automated data acquisition by confocal laser scanning microscopy and image analysis of triple stained immunofluorescent leukocytes in tissue. J. Immunol. Methods 2000. 237: 39-50.