Langerhans cells maintain local tissue tolerance in a model of systemic autoimmune disease

Journal of Immunology

Volumn 195, Issue 2, 2015, Pages 464-476

  King, Jennifer K ^a   Philips, Rachael L ^a   Eriksson, Anna U ^a   Kim, Peter J ^a   Halder, Ramesh C ^a   Lee, Delphine J ^b   Singh, Ram Raj ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b SAINT JOHN'S HEALTH CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AUTOANTIBODY; AUTOANTIGEN; DESMOGLEIN 3; DOUBLE STRANDED DNA ANTIBODY; INTERLEUKIN 10; DSG3 PROTEIN, MOUSE; IL10 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY DETECTION; ARTICLE; AUTOIMMUNE DISEASE; AUTOIMMUNITY; CD4+ T LYMPHOCYTE; CELL INFILTRATION; CELL ISOLATION; CONTROLLED STUDY; DERMATITIS; DERMIS; EPIDERMIS; FLOW CYTOMETRY; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; IMMUNOLOGICAL TOLERANCE; IMMUNOREGULATION; KIDNEY; LANGERHANS CELL; LIVER; LUNG; LUPUS DERMATITIS; LYMPH NODE; LYMPHOCYTE; MACROPHAGE; MOUSE; NONHUMAN; PRIORITY JOURNAL; SYSTEMIC LUPUS ERYTHEMATOSUS; ANIMAL; BIOSYNTHESIS; C57BL MOUSE; CELL MOTION; DISEASE MODEL; DRUG EFFECTS; FEMALE; GENE EXPRESSION; GENETICS; IMMUNOLOGY; LUPUS ERYTHEMATOSUS, CUTANEOUS; MURPHY ROTHS LARGE LYMPHOPROLIFERATIVE MOUSE; PATHOLOGY; SKIN;

ANIMALS; AUTOANTIBODIES; AUTOANTIGENS; AUTOIMMUNITY; CD4-POSITIVE T-LYMPHOCYTES; CELL MOVEMENT; DESMOGLEIN 3; DISEASE MODELS, ANIMAL; FEMALE; GENE EXPRESSION; IMMUNE TOLERANCE; INTERLEUKIN-10; LANGERHANS CELLS; LUPUS ERYTHEMATOSUS, CUTANEOUS; LYMPH NODES; MACROPHAGES; MICE; MICE, INBRED C57BL; MICE, INBRED MRL LPR; SKIN;

EID: 84936792302     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1402735     Document Type: Article

References (58)

1. Singh, R. R., S. Dubey, and J. Pinkhasov. 2013. Immune tolerance defects in lupus. In Dubois' Lupus Erythematosus and Related Syndromes, 8th Ed. D. J. Wallace, and B. H. Hahn, eds. Elsevier Saunders, Philadelphia, p. 256-272.
2. Teichmann, L. L., M. L. Ols, M. Kashgarian, B. Reizis, D. H. Kaplan, and M. J. Shlomchik. 2010. Dendritic cells in lupus are not required for activation of T and B cells but promote their expansion, resulting in tissue damage. Immunity 33: 967-978.
3. Ganguly, D., S. Haak, V. Sisirak, and B. Reizis. 2013. The role of dendritic cells in autoimmunity. Nat. Rev. Immunol. 13: 566-577.
4. Steinman, R. M., and M. C. Nussenzweig. 2002. Avoiding horror autotoxicus: the importance of dendritic cells in peripheral T cell tolerance. Proc. Natl. Acad. Sci. USA 99: 351-358.
5. Clausen, B. E., and J. M. Kel. 2010. Langerhans cells: critical regulators of skin immunity? Immunol. Cell Biol. 88: 351-360.
6. Azukizawa, H., H. Kosaka, S. Sano, W. R. Heath, I. Takahashi, X. H. Gao, Y. Sumikawa, M. Okabe, K. Yoshikawa, and S. Itami. 2003. Induction of T-cell-mediated skin disease specific for antigen transgenically expressed in keratino-cytes. Eur. J. Immunol. 33: 1879-1888.
7. Mayerova, D., E. A. Parke, L. S. Bursch, O. A. Odumade, and K. A. Hogquist. 2004. Langerhans cells activate naive self-antigen-specific CD8 T cells in the steady state. Immunity 21: 391-400.
8. Kanauchi, H., F. Furukawa, and S. Imamura. 1989. Evaluation of ATPase-positive Langerhans' cells in skin lesions of lupus erythematosus and experimentally induced inflammations. Arch. Dermatol. Res. 281: 327-332.
9. Sontheimer, R. D., and P. R. Bergstresser. 1982. Epidermal Langerhans cell involvement in cutaneous lupus erythematosus. J. Invest. Dermatol. 79: 237-243.
10. Andrews, B. S., A. Schenk, R. Barr, G. Friou, G. Mirick, and P. Ross. 1986. Immunopathology of cutaneous human lupus erythematosus defined by murine monoclonal antibodies. J. Am. Acad. Dermatol. 15: 474-481.
11. Bergroth, V., Y. T. Konttinen, and E. Johansson. 1985. Langerhans cells in SLE skin. A role in lymphocyte migration and activation in situ. Scand. J. Rheumatol. 14: 411-416.
12. Hahn, B. H., and R. R. Singh. 2007. Animal models of systemic lupus eryth-ematosus. In Dubois' Lupus Erythematosus, 7th Ed. D. J. Wallace and B. H. Hahn, eds. Lippincott Williams & Wilkins, Philadelphia, p. 299-355.
13. Amagai, M., V. Klaus-Kovtun, and J. R. Stanley. 1991. Autoantibodies against a novel epithelial cadherin in pemphigus vulgaris, a disease of cell adhesion. Cell 67: 869-877.
14. Nishimura, H., and J. L. Strominger. 2006. Involvement of a tissue-specific autoantibody in skin disorders of murine systemic lupus erythematosus and autoinflammatory diseases. Proc. Natl. Acad. Sci. USA 103: 3292-3297.
15. Takahashi, H., M. Kouno, K. Nagao, N. Wada, T. Hata, S. Nishimoto, Y. Iwakura, A. Yoshimura, T. Yamada, M. Kuwana, et al. 2011. Desmoglein 3-specific CD4+ T cells induce pemphigus vulgaris and interface dermatitis in mice. J. Clin. Invest. 121: 3677-3688.
16. Eriksson, A. U., and R. R. Singh. 2008. Cutting edge: migration of langerhans dendritic cells is impaired in autoimmune dermatitis. J. Immunol. 181: 7468-7472.
17. 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.
18. Igyártó, B. Z., and D. H. Kaplan. 2013. Antigen presentation by Langerhans cells. Curr. Opin. Immunol. 25: 115-119.
19. 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.
20. Kissenpfennig, A., S. Henri, B. Dubois, C. Laplace-Builhé, 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.
21. Singh, R. R., F. M. Ebling, E. E. Sercarz, and B. H. Hahn. 1995. Immune tolerance to autoantibody-derived peptides delays development of autoimmunity in murine lupus. J. Clin. Invest. 96: 2990-2996.
22. Yang, J. Q., A. K. Singh, M. T. Wilson, M. Satoh, A. K. Stanic, J. J. Park, S. Hong, S. D. Gadola, A. Mizutani, S. R. Kakumanu, et al. 2003. Immuno-regulatory role of CD1d in the hydrocarbon oil-induced model of lupus nephritis. J. Immunol. 171: 2142-2153.
23. Yang, J. Q., T. Chun, H. Liu, S. Hong, H. Bui, L. Van Kaer, C. R. Wang, and R. R. Singh. 2004. CD1d deficiency exacerbates inflammatory dermatitis in MRL-lpr/lpr mice. Eur. J. Immunol. 34: 1723-1732.
24. Yang, J. Q., V. Saxena, H. Xu, L. Van Kaer, C. R. Wang, and R. R. Singh. 2003. Repeated alpha-galactosylceramide administration results in expansion of NK T cells and alleviates inflammatory dermatitis in MRL-lpr/lpr mice. J. Immunol. 171: 4439-4446.
25. Bursch, L. S., L. Wang, B. Igyarto, A. Kissenpfennig, B. Malissen, D. H. Kaplan, and K. A. Hogquist. 2007. Identification of a novel population of Langerin+ dendritic cells. J. Exp. Med. 204: 3147-3156.
26. Ginhoux, F., M. P. Collin, M. Bogunovic, M. Abel, M. Leboeuf, J. Helft, J. Ochando, A. Kissenpfennig, B. Malissen, M. Grisotto, et al. 2007. Blood-derived dermal langerin+ dendritic cells survey the skin in the steady state. J. Exp. Med. 204: 3133-3146.
27. Poulin, L. F., S. Henri, B. de Bovis, E. Devilard, A. Kissenpfennig, and B. Malissen. 2007. The dermis contains langerin+ dendritic cells that develop and function independently of epidermal Langerhans cells. J. Exp. Med. 204: 3119-3131.
28. Lutz, M. B., A. Döhler, and H. Azukizawa. 2010. Revisiting the tolerogenicity of epidermal Langerhans cells. Immunol. Cell Biol. 88: 381-386.
29. Noordegraaf, M., V. Flacher, P. Stoitzner, and B. E. Clausen. 2010. Functional redundancy of Langerhans cells and Langerin+ dermal dendritic cells in contact hypersensitivity. J. Invest. Dermatol. 130: 2752-2759.
30. Huber, S., N. Gagliani, E. Esplugues, W. O'Connor, Jr., F. J. Huber, A. Chaudhry, M. Kamanaka, Y. Kobayashi, C. J. Booth, A. Y. Rudensky, et al. 2011. Th17 cells express interleukin-10 receptor and are controlled by Foxp3? and Foxp3+ regulatory CD4+ T cells in an interleukin-10-dependent manner. Immunity 34: 554-565.
31. Waithman, J., R. S. Allan, H. Kosaka, H. Azukizawa, K. Shortman, M. B. Lutz, W. R. Heath, F. R. Carbone, and G. T. Belz. 2007. Skin-derived dendritic cells can mediate deletional tolerance of class I-restricted self-reactive T cells. J. Immunol. 179: 4535-4541.
32. Groth, S., K. Vafia, A. Recke, C. Dähnrich, D. Zillikens, W. Stöcker, A. Kuhn, and E. Schmidt. 2012. Antibodies to the C-terminus of laminin g1 are present in a distinct subgroup of patients with systemic and cutaneous lupus erythematosus. Lupus 21: 1482-1483.
33. Hanrotel-Saliou, C., I. Segalen, Y. Le Meur, P. Youinou, and Y. Renaudineau. 2011. Glomerular antibodies in lupus nephritis. Clin. Rev. Allergy Immunol. 40: 151-158.
34. Renaudineau, Y., B. Deocharan, S. Jousse, E. Renaudineau, C. Putterman, and P. Youinou. 2007. Anti-alpha-actinin antibodies: A new marker of lupus nephritis. Autoimmun. Rev. 6: 464-468.
35. Ben-Yehuda, A., L. Rasooly, R. Bar-Tana, G. Breuer, B. Tadmor, R. Ulmansky, and Y. Naparstek. 1995. The urine of SLE patients contains antibodies that bind to the laminin component of the extracellular matrix. J. Autoimmun. 8: 279-291.
36. Florea, F., C. Bernards, M. Caproni, J. Kleindienst, T. Hashimoto, M. Koch, and C. Sitaru. 2014. Ex vivo pathogenicity of anti-laminin g1 autoantibodies. Am. J. Pathol. 184: 494-506.
37. Lee, Y. F., C. C. Cheng, J. L. Lan, T. Y. Hsieh, N. N. Lin, H. Y. Lin, and Y. T. Chiu. 2013. Effects of mycophenolate mofetil on cutaneous lupus eryth-ematosus in (NZB 3 NZW) F1 mice. J. Chin. Med. Assoc. 76: 615-623.
38. Shklovskaya, E., B. J. O'Sullivan, L. G. Ng, B. Roediger, R. Thomas, W. Weninger, and B. Fazekas de St Groth. 2011. Langerhans cells are pre-committed to immune tolerance induction. Proc. Natl. Acad. Sci. USA 108: 18049-18054.
39. Schwarz, A., M. Noordegraaf, A. Maeda, K. Torii, B. E. Clausen, and T. Schwarz. 2010. Langerhans cells are required for UVR-induced immuno-suppression. J. Invest. Dermatol. 130: 1419-1427.
40. O'Garra, A., P. L. Vieira, P. Vieira, and A. E. Goldfeld. 2004. IL-10-producing and naturally occurring CD4+ Tregs: limiting collateral damage. J. Clin. Invest. 114: 1372-1378.
41. Singh, R. R., B. H. Hahn, and E. E. Sercarz. 1996. Neonatal peptide exposure can prime T cells and, upon subsequent immunization, induce their immune deviation: implications for antibody vs. T cell-mediated autoimmunity. J. Exp. Med. 183: 1613-1621.
42. Clausen, B. E., and M. J. Girard-Madoux. 2013. IL-10 control of dendritic cells in the skin. OncoImmunology 2: e23186.
43. Ouchi, T., A. Kubo, M. Yokouchi, T. Adachi, T. Kobayashi, D. Y. Kitashima, H. Fujii, B. E. Clausen, S. Koyasu, M. Amagai, and K. Nagao. 2011. Langerhans cell antigen capture through tight junctions confers preemptive immunity in experimental staphylococcal scalded skin syndrome. J. Exp. Med. 208: 2607-2613.
44. Kautz-Neu, K., M. Noordegraaf, S. Dinges, C. L. Bennett, D. John, B. E. Clausen, and E. von Stebut. 2011. Langerhans cells are negative regulators of the anti-Leishmania response. J. Exp. Med. 208: 885-891.
45. Bos, J. D., I. D. van Garderen, S. R. Krieg, and L. W. Poulter. 1986. Different in situ distribution patterns of dendritic cells having Langerhans (T6+) and inter-digitating (RFD1+) cell immunophenotype in psoriasis, atopic dermatitis, and other inflammatory dermatoses. J. Invest. Dermatol. 87: 358-361.
46. Yin, Z., G. Bahtiyar, N. Zhang, L. Liu, P. Zhu, M. E. Robert, J. McNiff, M. P. Madaio, and J. Craft. 2002. IL-10 regulates murine lupus. J. Immunol. 169: 2148-2155.
47. Roers, A., L. Siewe, E. Strittmatter, M. Deckert, D. Schlüter, W. Stenzel, A. D. Gruber, T. Krieg, K. Rajewsky, and W. Müller. 2004. T cell-specific in-activation of the interleukin 10 gene in mice results in enhanced T cell responses but normal innate responses to lipopolysaccharide or skin irritation. J. Exp. Med. 200: 1289-1297.
48. Rubtsov, Y. P., J. P. Rasmussen, E. Y. Chi, J. Fontenot, L. Castelli, X. Ye, P. Treuting, L. Siewe, A. Roers, W. R. Henderson, Jr., et al. 2008. Regulatory T cell-derived interleukin-10 limits inflammation at environmental interfaces. Immunity 28: 546-558.
49. Duramad, O., K. L. Fearon, J. H. Chan, H. Kanzler, J. D. Marshall, R. L. Coffman, and F. J. Barrat. 2003. IL-10 regulates plasmacytoid dendritic cell response to CpG-containing immunostimulatory sequences. Blood 102: 4487-4492.
50. Vermi, W., S. Lonardi, M. Morassi, C. Rossini, R. Tardanico, M. Venturini, R. Sala, A. Tincani, P. L. Poliani, P. G. Calzavara-Pinton, et al. 2009. Cutaneous distribution of plasmacytoid dendritic cells in lupus erythematosus. Selective tropism at the site of epithelial apoptotic damage. Immunobiology 214: 877-886.
51. Bogdan, C., Y. Vodovotz, and C. Nathan. 1991. Macrophage deactivation by interleukin 10. J. Exp. Med. 174: 1549-1555.
52. Bobr, A., I. Olvera-Gomez, B. Z. Igyarto, K. M. Haley, K. A. Hogquist, and D. H. Kaplan. 2010. Acute ablation of Langerhans cells enhances skin immune responses. J. Immunol. 185: 4724-4728.
53. Igyarto, B. Z., M. C. Jenison, J. C. Dudda, A. Roers, W. Müller, P. A. Koni, D. J. Campbell, M. J. Shlomchik, and D. H. Kaplan. 2009. Langerhans cells suppress contact hypersensitivity responses via cognate CD4 interaction and langerhans cell-derived IL-10. J. Immunol. 183: 5085-5093.
54. Honda, T., S. Nakajima, G. Egawa, K. Ogasawara, B. Malissen, Y. Miyachi, and K. Kabashima. 2010. Compensatory role of Langerhans cells and langerin-positive dermal dendritic cells in the sensitization phase of murine contact hy-persensitivity. J. Allergy Clin. Immunol. 125: 1154-1156.e1152.
55. Divekar, A. A., S. Dubey, P. R. Gangalum, and R. R. Singh. 2011. Dicer insufficiency and microRNA-155 overexpression in lupus regulatory T cells: an apparent paradox in the setting of an inflammatory milieu. J. Immunol. 186: 924-930.
56. Chan, O. T., V. Paliwal, J. M. McNiff, S. H. Park, A. Bendelac, and M. J. Shlomchik. 2001. Deficiency in beta(2)-microglobulin, but not CD1, accelerates spontaneous lupus skin disease while inhibiting nephritis in MRL-Fas(lpr) nice: an example of disease regulation at the organ level. J. Immunol. 167: 2985-2990.
57. Peng, S. L., J. M. McNiff, M. P. Madaio, J. Ma, M. J. Owen, R. A. Flavell, A. C. Hayday, and J. Craft. 1997. alpha beta T cell regulation and CD40 ligand dependence in murine systemic autoimmunity. J. Immunol. 158: 2464-2470.
58. Kökény, G., M. Godó, E. Nagy, M. Kardos, K. Kotsch, P. Casalis, C. Bodor, L. Rosivall, H. D. Volk, A. C. Zenclussen, and P. Hamar. 2007. Skin disease is prevented but nephritis is accelerated by multiple pregnancies in autoimmune MRL/LPR mice. Lupus 16: 465-477.