Tolerance induction by hair-specific keratins in murine alopecia areata

Journal of Leukocyte Biology

Volumn 94, Issue 4, 2013, Pages 845-857

  Erb, Ulrike ^a   Freyschmidt Paul, Pia ^b   Zöller, Margot ^a,c  

^a UNIVERSITY HOSPITAL HEIDELBERG   (Germany)

^b UNIVERSITY HOSPITAL MARBURG   (Germany)

^c GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

Author keywords

Autoantigen; Mouse; Therapy; Vaccination

Indexed keywords

GAMMA INTERFERON; KERATIN; KERATIN 31; KERATIN 71; UNCLASSIFIED DRUG;

ALOPECIA AREATA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL PROLIFERATION; CLONAL ANERGY; CONTROLLED STUDY; FULL THICKNESS SKIN GRAFT; HAIR; HAIR FOLLICLE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SKIN TRANSPLANTATION; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; VACCINATION;

AUTOANTIGEN; MOUSE; THERAPY; VACCINATION;

ALOPECIA AREATA; ANIMALS; AUTOANTIGENS; CELL PROLIFERATION; DISEASE MODELS, ANIMAL; IMMUNE TOLERANCE; KERATINS, HAIR-SPECIFIC; LYMPHOCYTE ACTIVATION; MICE; PEPTIDES; SKIN TRANSPLANTATION; SOLUBILITY; T-LYMPHOCYTES; VACCINATION;

EID: 84884891905     PISSN: 07415400     EISSN: 19383673     Source Type: Journal    
DOI: 10.1189/jlb.0413196     Document Type: Article

References (65)

1. Gilhar, A., Etzioni, A., Paus, R. (2012) Alopecia areata. N. Engl. J. Med. 366, 1515-1525.
2. McElwee, K. J., Freyschmidt-Paul, P., Zöller, M., Hoffmann, R. (2003) Alopecia areata susceptibility in rodent models. J. Investig. Dermatol. Symp. Proc. 8, 182-187.
3. Meyer, K. C., Klatte, J. E., Dinh, H. V., Harries, M. J., Reithmayer, K., Meyer, W., Sinclair, R., Paus, R. (2008) Evidence that the bulge region is a site of relative immune privilege in human hair follicles. Br. J. Dermatol. 159, 1077-1085.
4. Höglund, P., Brodin, P. (2010) Current perspectives of natural killer cell education by MHC class I molecules. Nat. Rev. Immunol. 10, 724-734.
5. Ito, T., Ito, N., Saatoff, M., Hashizume, H., Fukamizu, H., Nickoloff, B. J., Takigawa, M., Paus, R. (2008) Maintenance of hair follicle immune privilege is linked to prevention of NK cell attack. J. Invest. Dermatol. 128, 1196-1206.
6. Gilhar, A., Landau, M., Assy, B., Ullmann, Y., Shalaginov, R., Serafimovich, S., Kalish, R. S. (2003) Transfer of alopecia areata in the human scalp graft/Prkdc(scid) (SCID) mouse system is characterized by a TH1 response. Clin. Immunol. 106, 181-187.
7. McElwee, K. J., Freyschmidt-Paul, P., Hoffmann, R., Kissling, S., Hummel, S., Vitacolonna, M., Zöller, M. (2005) Transfer of CD8+ cells induces localized hair loss while CD4+CD25+ cells promote systemic alopecia areata and CD4+/CD25+ cells blockade disease onset in the C3H/HeJ mouse model. J. Invest. Dermatol. 124, 947-957.
8. Sanli, H., Kusak, F., Arat, M., Ekmekci, P., Ilhan, O. (2004) Simultaneous onset of chronic graft versus host disease and alopecia areata following allogeneic haematopoietic cell transplantation. Acta Derm. Venereol. 84, 86-87.
9. McElwee, K. J., Hoffmann, R., Freyschmidt-Paul, P., Wenzel, E., Kissling, S., Sundberg, J. P., Zöller, M. (2002) Resistance to alopecia areata in C3H/HeJ mice is associated with increased expression of regulatory cytokines and a failure to recruit CD4+ and CD8+ cells. J. Invest. Dermatol. 119, 1426-1433.
10. Skurkovich, B., Skurkovich, S. (2007) Autoimmune diseases are connected with disturbances in cytokine synthesis, and therapy with IFN-γ blockers is their main pathogenetic treatment. Ann. N. Y. Acad. Sci. 1109, 167-177.
11. Shimizu, T., Hizawa, N., Honda, A., Zhao, Y., Abe, R., Watanabe, H., Nishihira, J. Nishimura M., Shimizu, H. (2005) Promoter region polymorphism of macrophage migration inhibitory factor is strong risk factor for young onset of extensive alopecia areata. Genes Immun. 6, 285-289.
12. Freyschmidt-Paul, P., Hoffmann, R., McElwee, K. J., Sundberg, J. P., Kissling, S., Wenzel, E., Sundberg, J. P., Zöller, M., Hoffmann, R. (2005) Reduced expression of interleukin-2 decreases the frequency of alopecia areata onset in C3H/HeJ mice. J. Invest. Dermatol. 125, 945-951.
13. Freyschmidt-Paul, P., McElwee, K. J., Happle, R., Kissling, S., Wenzel, E., Sundberg, J. P., Zöller, M., Hoffmann, R. (2002) Interleukin-10-deficient mice are less susceptible to the induction of alopecia areata. J. Invest. Dermatol. 119, 980-982.
14. Marhaba, R., Vitacolonna, M., Hildebrand, D., Baniyash, M., Freyschmidt-Paul, P., Zöller, M. (2007) The importance of myeloid-derived suppressor cells in the regulation of autoimmune effector cells by a chronic contact eczema. J. Immunol. 179, 5071-5081.
15. Mills, K. H. (2011) TLR-dependent T cell activation in autoimmunity. Nat. Rev. Immunol. 11, 807-822.
16. Freyschmidt-Paul, P., McElwee, K. J., Botchkarev, V., Kissling, S., Wenzel, E., Sundberg, J. P., Happle, R., Hoffmann, R. (2003) Fas-deficient C3. MRL-Tnfrsf6lpr mice and FasL-deficient C3H/HeJ-Tnfsf6gld are relatively resistant to the induction of alopecia areata by grafting of alopecia areata-affected skin from C3H/HeJ mice. J. Invest. Dermatol. Symp. Proc. 8, 104-108.
17. Singh, V., Mueller, U., Freyschmidt-Paul, P., Zöller, M. (2011) Delayed type hypersensitivity-induced myeloid-derived suppressor cells regulate autoreactive T cells. Eur. J. Immunol. 41, 2871-2882.
18. Freyschmidt-Paul, P., McElwee, K. J., Hoffmann, R. (2003) Alopecia areata: treatment of today and tomorrow. J. Invest. Dermatol. 8, 12-17.
19. Ito, T. (2012) Advances in the management of alopecia areata. J. Dermatol. 39, 11-17.
20. Gardner, S., Freyschmidt-Paul, P., Hoffmann, R., Sundberg, J. P., Happle, R., Lindsey, N. J., Tobin, D. J. (2000) Normalisation of hair follicle morphology in C3H/HeJ alopecia areata mice after treatment with squaric acid dibutylester. Eur. J. Dermatol. 10, 443-450.
21. Alkhalifah, A., Alsantali, A., Wang, E., McElwee, K. J., Shapiro, J. (2010) Alopecia areata update: part II. Treatment. J. Am. Acad. Dermatol. 62, 191-202.
22. Paus, R., Slominski, A., Czarnetzki, B. M. (1993) Is alopecia areata an autoimmune-response against melanogenesis-related proteins, exposed by abnormal MHC class I expression in the anagen hair bulb? Yale J. Biol. Med. 66, 541-554.
23. Gilhar, A., Landau, M., Assy, B., Shalaginov, R., Serafimovich, S., Kalish, R. S. (2001) Melanocyte-associated T cell epitopes can function as autoantigens for transfer of alopecia areata to human scalp explants on Prkdc(scid) mice. J. Invest. Dermatol. 117, 1357-1362.
24. Kitahara, T., Ogawa, H. (1993) Coexpression of keratins characteristic of skin and hair differentiation in nail cells. J. Invest. Dermatol. 100, 171-175.
25. Tobin, D. J., Sundberg, J. P., King L. E., Jr., Boggess, D., Bystryn, J. C. (1997) Autoantibodies to hair follicles in C3H/HeJ mice with alopecia areata-like hair loss. J. Invest. Dermatol. 109, 329-333.
26. Leung, M. C., Sutton, C. W., Fenton, D. A., Tobin, D. J. (2010) Trichohyalin is a potential major autoantigen in human alopecia areata. J. Proteome Res. 9, 5153-5163.
27. Gilhar, A., Ullmann, Y., Berkutzki, T., Assy, B., Kalish, R. S. (1998) Autoimmune hair loss (alopecia areata) transferred by T lymphocytes to human scalp explants on SCID mice. J. Clin. Invest. 101, 62-67.
28. Tobin, D. J., Fenton, D. A., Kendall, M. D. (1991) Cell degeneration in alopecia areata. An ultrastructural study. Am. J. Dermatopathol. 13, 248-256.
29. Tobin, D. J. (2011) The cell biology of human hair follicle pigmentation. Pigment Cell Melanoma Res. 24, 75-88.
30. Tobin, D. J., Bystryn, J. C. (1996) Different populations of melanocytes are present in hair follicles and epidermis. Pigment Cell Res. 9, 304-310.
31. Kemp, E. H., Sandhu, H. K., Weetman, A. P., McDonagh, A. J. (2011) Demonstration of autoantibodies against tyrosine hydroxylase in patients with alopecia areata. Br. J. Dermatol. 165, 1236-1243.
32. Bertolini, M., Gilhar, A., Paus, R. (2012) Alopecia areata as a model for T cell-dependent autoimmune diseases. Exp. Dermatol. 21, 477-479.
33. Schweizer, J., Langbein, L., Rogers, M. A., Winter, H. (2007) Hair follicle-specific keratins and their diseases. Exp. Cell Res. 313, 2010-2020.
34. Tobin, D. J. (2003) Characterization of hair follicle antigens targeted by the anti-hair follicle immune response. J. Investig. Dermatol. Symp. Proc. 8, 176-181.
35. Tobin, D. J., Alhaidari, Z., Olivry, T. (1998) Equine alopecia areata autoantibodies target multiple hair follicle antigens and may alter hair growth. A preliminary study. Exp. Dermatol. 7, 289-297.
36. Tobin, D. J., Gardner, S. H., Lindsey, N. J., Hoffmann, R., Happle, R., Freyschmidt-Paul, P. (2002) Diphencyprone immunotherapy alters antihair follicle antibody status in patients with alopecia areata. Eur. J. Dermatol. 12, 327-334.
37. Alli, R., Nguyen, P., Boyd, K., Sundberg, J. P., Geiger, T. L. (2012) A mouse model of clonal CD8+ T lymphocyte-mediated alopecia areata progressing to alopecia universalis. J. Immunol. 188, 477-486.
38. McMichael, A. J., Pearce, D. J., Wasserman, D., Camacho, F. T., Fleischer A. B., Jr., Feldman, S. R., Balkrishnan, R. (2007) Alopecia in the United States: outpatient utilization and common prescribing patterns. J. Am. Acad. Dermatol. 57 (Suppl. 2), S49-S51.
39. Chu, S. Y., Chen, Y. J., Tseng, W. C., Lin, M. W., Chen, T. J., Hwang, C. Y., Chen, C. C., Lee, D. D., Chang, Y. T., Wang, W. J., Liu, H. N. (2011) Comorbidity profiles among patients with alopecia areata: the importance of onset age, a nationwide population-based study. J. Am. Acad. Dermatol. 65, 949-956.
40. Delamere, F. M., Sladden, M. M., Dobbins, H. M., Leonardi-Bee, J. (2008) Interventions for alopecia areata. Cochrane Database Syst. Rev. 2, CD004413.
41. McElwee, K. J., Boggess, D., King L. E., Jr., Sundberg, J. P. (1998) Experimental induction of alopecia areata-like hair loss in C3H/HeJ mice using full-thickness skin grafts. J. Invest. Dermatol. 111, 797-803.
42. Daubeuf, S., Bordier, C., Hudrisier, D., Joly, E. (2009) Suitability of various membrane lipophilic probes for the detection of trogocytosis by flow cytometry. Cytometry A 75, 380-389.
43. Shapiro, J. (2011) Dermatologic therapy: alopecia areata update. Dermatol. Ther. 24, 301.
44. Miteva, M., Tosti, A. (2012) Treatment options for alopecia: an update, looking to the future. Expert Opin. Pharmacother. 13, 1271-1281.
45. Schneider, M. R., Schmidt-Ullrich, R., Paus, R. (2009) The hair follicle as a dynamic miniorgan. Curr. Biol. 19, R132-R142.
46. Cotsarelis, G. (2006) Epithelial stem cells: a folliculocentric view. J. Invest. Dermatol. 126, 1459-1468.
47. Aoki, N., Sawada, S., Rogers, M. A., Schweizer, J., Shimomura, Y., Tsujimoto, T., Ito, K., Ito, M. (2001) A novel type II cytokeratin, mK6irs, is expressed in the Huxley and Henle layers of the mouse inner root sheath. J. Invest. Dermatol. 116, 359-365.
48. Ozcan, D., Cevlik Aydoǧan, F. (2012) Concurrence of alopecia areata and vitiligo at the same anatomical site. Australas J. Dermatol. 53, e61-e63.
49. Moll, R., Divo, M., Langbein, L. (2008) The human keratins: biology and pathology. Histochem. Cell Biol. 129, 705-733.
50. Niederkorn, J. Y. (2006) See no evil, hear no evil, do no evil: the lessons of immune privilege. Nat. Immunol. 7, 354-359.
51. Petukhova, L., Cabral, R. M., Mackay-Wiggan, J., Clynes, R., Christiano, A. M. (2011) The genetics of alopecia areata: what's new and how will it help our patients? Dermatol. Ther. 24, 326-336.
52. Tosti, A., Duque-Estrada, B. (2009) Treatment strategies for alopecia. Expert. Opin. Pharmacother. 10, 1017-1026.
53. Yano, K., Brown, L. F., Detmar, M. (2001) Control of hair growth and follicle size by VEGF-mediated angiogenesis. J. Clin. Invest. 107, 409-417.
54. Zhou, N., Fan, W., Li, M. (2009) Angiogenin is expressed in human dermal papilla cells and stimulates hair growth. Arch. Dermatol. Res. 301, 139-149.
55. Moldaver, D., Larché, M. (2011) Immunotherapy with peptides. Allergy 66, 784-791.
56. Lutz, M. B., Kurts, C. (2009) Induction of peripheral CD4+ T-cell tolerance and CD8+ T-cell cross-tolerance by dendritic cells. Eur. J. Immunol. 39, 2325-2330.
57. 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.
58. Bedoui, S., Whitney, P. G., Waithman, J., Eidsmo, L., Wakim, L., Caminschi, I., Allan, R. S. Wojtasiak, M., Shortman, K., Carbone, F. R., Brooks, A. G., Heath, W. R. (2009) Cross-presentation of viral and self antigens by skin-derived CD103+ dendritic cells. Nat. Immunol. 10, 488-495.
59. Greenwald, R. J., Freeman, G. J., Sharpe, A. H. (2005) The B7 family revisited. Annu. Rev. Immunol. 23, 515-548.
60. Arens, R. (2012) Rational design of vaccines: learning from immune evasion mechanisms of persistent viruses and tumors. Adv. Immunol. 114, 217-243.
61. Wilke, C. M., Wei, S., Wang, L., Kryczek, I., Kao, J., Zou, W. (2011) Dual biological effects of the cytokines interleukin-10 and interferon-γ. Cancer Immunol. Immunother. 60, 1529-1541.
62. Zhou, X., Kong, N., Zou, H., Brand, D., Li, X., Liu, Z., Zheng, S. G. (2011) Therapeutic potential of TGF-β-induced CD4(+) Foxp3(+) regulatory T cells in autoimmune diseases. Autoimmunity 44, 43-50.
63. Mantel, P. Y., Schmidt-Weber, C. B. (2011) Transforming growth factor-β: recent advances on its role in immune tolerance. Methods Mol. Biol. 677, 303-338.
64. Petukhova, L., Duvic, M., Hordinsky, M., Norris, D., Price, V., Shimomura, Y., Kim, H., Singh, P., Lee, A., Chen, W. V., Meyer, K. C., Paus, R., Jahoda, C. A., Amos, C. I., Gregersen, P. K., Christiano, A. M. (2010) Genome-wide association study in alopecia areata implicates both innate and adaptive immunity. Nature 466, 113-117.
65. Jabbari, A., Petukhova, L., Cabral, R. M., Clynes, R., Christiano, A. M. (2013) Genetic basis of alopecia areata: a roadmap for translational research. Dermatol. Clin. 31, 109-117.