Langerhans cells are not required for epidermal Vγ3 T cell homeostasis and function

Journal of Leukocyte Biology

Volumn 90, Issue 1, 2011, Pages 61-68

  Taveirne, Sylvie ^a   de Colvenaer, Veerle ^a   van den Broeck, Tina ^a   van Ammel, Els ^a   Bennett, Clare L ^b   Taghon, Tom ^a   Vandekerckhove, Bart ^a   Plum, Jean ^a   Clausen, Björn E ^c   Kaplan, Daniel H ^d   Leclercq, Georges ^a  

^a GHENT UNIVERSITY   (Belgium)

^b University College London Royal Free Campus ^*  (United Kingdom)

^c ERASMUS MEDICAL CENTER   (Netherlands)

^d UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

Author keywords

Langerin DTA mice; Langerin DTR mice; LC deficiency; Skin

Indexed keywords

CD69 ANTIGEN; INTERLEUKIN 2; LYMPHOTACTIN; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN EXPRESSION; ARTICLE; CELL DENSITY; CELL FUNCTION; CELL MATURATION; CYTOKINE PRODUCTION; CYTOTOXICITY; EPIDERMIS; HOMEOSTASIS; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; LANGERHANS CELL; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; SKIN EPITHELIUM; T LYMPHOCYTE;

ANIMALS; CELL DIFFERENTIATION; CELL SEPARATION; EPIDERMIS; FLOW CYTOMETRY; HOMEOSTASIS; IMMUNOHISTOCHEMISTRY; LANGERHANS CELLS; MICE; MICE, TRANSGENIC; RECEPTORS, ANTIGEN, T-CELL, GAMMA-DELTA; SKIN; T-LYMPHOCYTES;

MUS;

EID: 79959832225     PISSN: 07415400     EISSN: None     Source Type: Journal    
DOI: 10.1189/jlb.1010581     Document Type: Article

References (40)

1. Havran, W. L., Grell, S., Duwe, G., Kimura, J., Wilson, A., Kruisbeek, A. M., O'Brien, R. L., Born, W., Tigelaar, R. E., Allison, J. P. (1989) Limited diversity of T-cell receptor γ-chain expression of murine Thy-1+ dendritic epidermal cells revealed by V γ 3-specific monoclonal antibody. Proc. Natl. Acad. Sci. USA 86, 4185-4189.
2. Doisne, J. M., Becourt, C., Amniai, L., Duarte, N., Le Luduec, J. B., Eberl, G., Benlagha, K. (2009) Skin and peripheral lymph node invariant NKT cells are mainly retinoic acid receptor-related orphan receptor (γ)t+ and respond preferentially under inflammatory conditions. J. Immunol. 183, 2142-2149.
3. Garman, R. D., Doherty, P. J., Raulet, D. H. (1986) Diversity, rearrangement, and expression of murine T cell γ genes. Cell 45, 733-742.
4. Havran, W. L., Allison, J. P. (1990) Origin of Thy-1+ dendritic epidermal cells of adult mice from fetal thymic precursors. Nature 344, 68-70.
5. Xiong, N., Zhang, L., Kang, C., Raulet, D. H. (2008) Gene placement and competition control T cell receptor γ variable region gene rearrangement. J. Exp. Med. 205, 929-938.
6. Boyden, L. M., Lewis, J. M., Barbee, S. D., Bas, A., Girardi, M., Hayday, A. C., Tigelaar, R. E., Lifton, R. P. (2008) Skint1, the prototype of a newly identified immunoglobulin superfamily gene cluster, positively selects epidermal γδ T cells. Nat. Genet. 40, 656-662.
7. Zhang, Y., Cado, D., Asarnow, D. M., Komori, T., Alt, F. W., Raulet, D. H., Allison, J. P. (1995) The role of short homology repeats and TdT in generation of the invariant γδ antigen receptor repertoire in the fetal thymus. Immunity 3, 439-447.
8. Kang, J., Coles, M., Raulet, D. H. (1999) Defective development of γδ T cells in interleukin 7 receptor-deficient mice is due to impaired expression of T cell receptor γ genes. J. Exp. Med. 190, 973-982.
9. De Creus, A., Van Beneden, K., Stevenaert, F., Debacker, V., Plum, J., Leclercq, G. (2002) Developmental and functional defects of thymic and epidermal Vγ3 cells in IL-15-deficient and IFN regulatory factor-1-deficient mice. J. Immunol. 168, 6486-6493.
10. Girardi, M., Oppenheim, D. E., Steele, C. R., Lewis, J. M., Glusac, E., Filler, R., Hobby, P., Sutton, B., Tigelaar, R. E., Hayday, A. C. (2001) Regulation of cutaneous malignancy by γδ T cells. Science 294, 605-609.
11. Van Beneden, K., De Creus, A., Stevenaert, F., Debacker, V., Plum, J., Leclercq, G. (2002) Expression of inhibitory receptors Ly49E and CD94/ NKG2 on fetal thymic and adult epidermal TCR Vγ3 lymphocytes. J. Immunol. 168, 3295-3302.
12. Jameson, J., Ugarte, K., Chen, N., Yachi, P., Fuchs, E., Boismenu, R., Havran, W. L. (2002) A role for skin Vγ3 T cells in wound repair. Science 296, 747-749.
13. Girardi, M., Lewis, J., Glusac, E., Filler, R. B., Geng, L., Hayday, A. C., Tigelaar, R. E. (2002) Resident skin-specific γδ T cells provide local, nonredundant regulation of cutaneous inflammation. J. Exp. Med. 195, 855-867.
14. Havran, W. L., Chien, Y. H., Allison, J. P. (1991) Recognition of self antigens by skin-derived T cells with invariant γδ antigen receptors. Science 252, 1430-1432.
15. Katz, S. I., Tamaki, K., Sachs, D. H. (1979) Epidermal Langerhans cells are derived from cells originating in bone marrow. Nature 282, 324-326.
16. Frelinger, J. G., Hood, L., Hill, S., Frelinger, J. A. (1979) Mouse epidermal Ia molecules have a bone marrow origin. Nature 282, 321-323.
17. Chorro, L., Sarde, A., Li, M., Woollard, K. J., Chambon, P., Malissen, B., Kissenpfennig, A., Barbaroux, J. B., Groves, R., Geissmann, F. (2009) Langerhans cell (LC) proliferation mediates neonatal development, homeostasis, and inflammation-associated expansion of the epidermal LC network. J. Exp. Med. 206, 3089-3100.
18. Merad, M., Manz, M. G., Karsunky, H., Wagers, A., Peters, W., Charo, I., Weissman, I. L., Cyster, J. G., Engleman, E. G. (2002) Langerhans cells renew in the skin throughout life under steady-state conditions. Nat. Immunol. 3, 1135-1141.
19. Birbeck, M. S., Breathnach, A. S., Everall, J. D. (1961) An electron microscope study of basal melanocytes and high-level clear cells (Langerhans cells) in vitiligo1. J. Invest. Dermatol. 37, 51-64.
20. Valladeau, J., Ravel, O., Dezutter-Dambuyant, C., Moore, K., Kleijmeer, M., Liu, Y., Duvert-Frances, V., Vincent, C., Schmitt, D., Davoust, J., Caux, C., Lebecque, S., Saeland, S. (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.
21. Wilson, N. S., Villadangos, J. A. (2004) Lymphoid organ dendritic cells: beyond the Langerhans cells paradigm. Immunol. Cell Biol. 82, 91-98.
22. Schuler, G., Steinman, R. M. (1985) Murine epidermal Langerhans cells mature into potent immunostimulatory dendritic cells in vitro. J. Exp. Med. 161, 526-546.
23. Steinman, R. M., Nussenzweig, M. C. (2002) Avoiding horror autotoxicus: the importance of dendritic cells in peripheral T cell tolerance. Proc. Natl. Acad. Sci. USA 99, 351-358.
24. Allan, R. S., Smith, C. M., Belz, G. T., van Lint, A. L., Wakim, L. M., Heath, W. R., Carbone, F. R. (2003) Epidermal viral immunity induced by CD8α+ dendritic cells but not by Langerhans cells. Science 301, 1925-1928.
25. Bursch, L. S., Wang, L., Igyarto, B., Kissenpfennig, A., Malissen, B., Kaplan, D. H., Hogquist, K. A. (2007) Identification of a novel population of Langerin+ dendritic cells. J. Exp. Med. 204, 3147-3156.
26. Münz, C., Dao, T., Ferlazzo, G., de Cos, M. A., Goodman, K., Young, J. W. (2005) Mature myeloid dendritic cell subsets have distinct roles for activation and viability of circulating human natural killer cells. Blood 105, 266-273.
27. Hochweller, K., Striegler, J., Hammerling, G. J., Garbi, N. (2008) A novel CD11c.DTR transgenic mouse for depletion of dendritic cells reveals their requirement for homeostatic proliferation of natural killer cells. Eur. J. Immunol. 38, 2776-2783.
28. Do, J. S., Min, B. (2009) IL-15 produced and trans-presented by DCs underlies homeostatic competition between CD8 and γδ T cells in vivo. Blood 113, 6361-6371.
29. Yokota, K., Ariizumi, K., Kitajima, T., Bergstresser, P. R., Street, N. E., Takashima, A. (1996) Cytokine-mediated communication between dendritic epidermal T cells and Langerhans cells. In vitro studies using cell lines. J. Immunol. 157, 1529-1537.
30. Takashima, A., Bergstresser, P. R. (1996) Cytokine-mediated communication by keratinocytes and Langerhans cells with dendritic epidermal T cells. Semin. Immunol. 8, 333-339.
31. Schreiber, S., Kilgus, O., Payer, E., Kutil, R., Elbe, A., Mueller, C., Stingl, G. (1992) Cytokine pattern of Langerhans cells isolated from murine epidermal cell cultures. J. Immunol. 149, 3524-3534.
32. De Creus, A., Van Beneden, K., Taghon, T., Stolz, F., Debacker, V., Plum, J., Leclercq, G. (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.
33. Asli, B., Lantz, O., DiSanto, J. P., Saeland, S., Geissmann, F. (2004) Roles of lymphoid cells in the differentiation of Langerhans dendritic cells in mice. Immunobiology 209, 209-221.
34. Bennett, C. L., van Rijn, E., Jung, S., Inaba, K., Steinman, R. M., Kapsenberg, M. L., Clausen, B. E. (2005) Inducible ablation of mouse Langerhans cells diminishes but fails to abrogate contact hypersensitivity. J. Cell Biol. 169, 569-576.
35. Kaplan, D. H., Jenison, M. C., Saeland, S., Shlomchik, W. D., Shlomchik, M. J. (2005) Epidermal Langerhans cell-deficient mice develop enhanced contact hypersensitivity. Immunity 23, 611-620.
36. Gallatin, W. M., Weissman, I. L., Butcher, E. C. (2006) A cell-surface molecule involved in organ-specific homing of lymphocytes. J. Immunol. 177, 5-9.
37. Fraser, K. P., Gays, F., Robinson, J. H., van Beneden, K., Leclercq, G., Vance, R. E., Raulet, D. H., Brooks, C. G. (2002) NK cells developing in vitro from fetal mouse progenitors express at least one member of the Ly49 family that is acquired in a time-dependent and stochastic manner independently of CD94 and NKG2. Eur. J. Immunol. 32, 868-878.
38. Leclercq, G., Plum, J., Nandi, D., De Smedt, M., Allison, J. P. (1993) Intrathymic differentiation of V γ 3 T cells. J. Exp. Med. 178, 309-315.
39. Strid, J., Roberts, S. J., Filler, R. B., Lewis, J. M., Kwong, B. Y., Schpero, W., Kaplan, D. H., Hayday, A. C., Girardi, M. (2008) Acute upregulation of an NKG2D ligand promotes rapid reorganization of a local immune compartment with pleiotropic effects on carcinogenesis. Nat. Immunol. 9, 146-154.
40. Jameson, J. M., Sharp, L. L., Witherden, D. A., Havran, W. L. (2004) Regulation of skin cell homeostasis by γδ T cells. Front. Biosci. 9, 2640-2651.