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

Journal of Investigative Dermatology

Volumn 119, Issue 6, 2002, Pages 1426-1433

  McElwee, Kevin J ^a   Hoffmann, Rolf ^a   Freyschmidt Paul, Pia ^a   Wenzel, Elke ^a   Kissling, Sabina ^a   Sundberg, John P ^b   Zöller, Margot ^c  

^a PHILIPPS UNIVERSITY MARBURG   (Germany)

^b JACKSON LABORATORY   (United States)

^c GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

Author keywords

Autoimmune diseases; Disease models; Immune tolerance; Inflammation

Indexed keywords

B7 ANTIGEN; CD28 ANTIGEN; CD4 ANTIGEN; CD40 ANTIGEN; CD40 LIGAND; CD44V ANTIGEN; CD8 ANTIGEN; CD86 ANTIGEN; CYTOKINE; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4; INTERLEUKIN 10; INTERLEUKIN 4; SOYBEAN OIL;

ALOPECIA AREATA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN PRESENTING CELL; ARTICLE; AUTOIMMUNE DISEASE; CONTROLLED STUDY; CROSS LINKING; DIET; DISEASE PREDISPOSITION; DOWN REGULATION; HELPER CELL; IMMUNE RESPONSE; INFLAMMATION; LYMPH NODE; LYMPH NODE CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SKIN GRAFT; SPLEEN; TH1 CELL; TH2 CELL;

EID: 0036911686     PISSN: 0022202X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1523-1747.2002.19620.x     Document Type: Article

References (55)

1. Anderton S, Burkhart C, Metzler B,Wraith D: Mechanisms of central and peripheral T-cell tolerance: Lessons from experimental models of multiple sclerosis. Immunol Rev 169:123-137, 1999
2. Bernard CC: Suppressor T cells prevent experimental autoimmune encephalomyelitis in mice. Clin Exp Immunol 29:100-109, 1977
3. Bernard CC, Leydon J, Mackay IR: T cell necessity in the pathogenesis of experimental autoimmune encephalomyelitis in mice. Eur J Immunol 6:655-660, 1976
4. Braley-Mullen H, Johnson M, Sharp GC, Kyriakos M: Induction of experimental autoimmune thyroiditis in mice with in vitro activated splenic T cells. Cell Immunol 93:132-143, 1985
5. Bröcker EB, Echternacht-Happle K, Hamm H, Happle R: Abnormal expression of class I and class II major histocompatibility antigens in alopecia areata: Modulation by topical immunotherapy. J Invest Dermatol 88:564-568, 1987
6. Carroll JM, McElwee KJ, King LE Jr, Byrne M, Sundberg JP: Gene array profiling and immunomodulation studies define a cell mediated immune response underlying the pathogenesis of alopecia areata in a mouse model and humans. J Invest Dermatol 119:392-402, 2002
7. DeGrendele HC, Estess P, Siegelman MH: Requirement for CD44 in activated T cell extravasation into an inflammatory site. Science 278:672-675, 1997
8. Feili-Hariri M, Dong X, Alber SM, Watkins SC, Salter RD, Morel PA: Immunotherapy of NOD mice with bone marrow-derived dendritic cells. Diabetes 48:2300-2308, 1999
9. Freeman GJ, Borriello F, Hodes RJ, et al: Murine B1-2, an alternative CTLA4 counter-receptor that costimulates T cell proliferation and interleukin 2 production. J Exp Med 178:2185-2192, 1993
10. Freyschmidt-Paul P, Sundberg JP, Happle R, McElwee KJ, Metz S, Boggess D, Hoffmann R: Successful treatment of alopecia areata-like hair loss with the contact sensitizer squaric acid dibutylester (SADBE) in C3H/HeJ mice. J Invest Dermatol 113:61-68, 1999
11. Freyschmidt-Paul P, Seiter S, Zöller M, et al: Treatment with an anti-CD44v10-specific antibody inhibits the onset of alopecia areata in C3H/HeJ mice. J Invest Dermatol 115:653-657, 2000
12. lpr mice are not susceptible to alopecia areata after grafting of alopecia areata-affected skin from C3H/HeJ mice. J Invest Dermatol Symp Proc, in press
13. Galvin F, Freeman GJ, Razi-Wolf Z, Hall W Jr, Benacerraf B, Nadler L, Reiser H: Murine B7 antigen provides a sufficient costimulatory signal for antigen-specific and MHC-restricted T cell activation. J Immunol 149:3802-3808, 1992
14. Gilhar A, Ullmann Y, Berkutzki T, Assy B, Kalish RS: Autoimmune hair loss (alopecia areata) transferred by T lymphocytes to human scalp explants on SCID mice. J Clin Invest 101:62-67, 1998
15. Gilhar A, Landau M, Assy B, Shalaginov R, Serafimovich S, Kalish RS: 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, 2001
16. Gross JA, Callas E, Allison JP: Identification and distribution of the costimulatory receptor CD28 in the mouse. J Immunol 149:380-388, 1992
17. Halliday GM, Muller HK: Induction of tolerance via skin depleted of Langerhans cells by a chemical carcinogen. Cell Immunol 99:220-227, 1986
18. Harding FA, McArthur JG, Gross JA, Raulet DH, Allison JP: CD28-mediated signalling co-stimulates murine T-cells and prevents induction of energy in T-cell clones. Nature 356:607-609, 1992
19. Hathcock KS, Laszlo G, Pucillo C, Linsley P, Hodes RJ: Comparative analysis of B7-1 and B7-2 costimulatory ligands: expression and function. J Exp Med 180:631-640, 1994
20. Hession C, Moy P, Tizard R, et al: Cloning of murine and rat vascular cell adhesion molecule-1. Biochem Biophys Res Commun 183:163-169, 1992
21. Hoffmann R, Wenzel E, Huth A, van der Steen P, Schaufele M, Henninger HP, Happle R: Cytokine mRNA levels in alopecia areata before and after treatment with the contact allergen diphenylcyclopropenone. J Invest Dermatol 103:530-533, 1994
22. Hutchings PR, Cooke A, Dawe K, Waldmann H, Roitt IM: Active suppression induced by anti-CD4. Eur J Immunol 23:965-968, 1993
23. Itoh M, Mukasa A, Tokunaga Y, Hiramine C, Hojo K: New experimental model for adoptive transfer of murine autoimmune orchitis. Andrologia 23:415-420, 1991
24. Jemison LM, Williams SK, Lublin FD, Knobler RL, Korngold R: Interferon-gamma-inducible endothelial cell class II major histocompatibility complex expression correlates with strain- and site-specific susceptibility to experimental allergic encephalomyelitis. J Neuroimmunol 47:15-22, 1993
25. June CH, Bluestone JA, Nadler LM, Thompson CB: The B7 and CD28 receptor families. Immunol Today 15:321-331, 1994
26. Karussis D, Vourka-Karussis U, Mizrachi-Koll R, Abramsky O: Acute/relapsing experimental autoimmune encephalomyelitis. induction of long lasting, antigen-specific tolerance by syngeneic bone marrow transplantation. Mult Scler 5:17-21, 1999
27. Kuhr T, Hala K, Dietrich H, Herold M,Wick G: Genetically determined target organ susceptibility in the pathogenesis of spontaneous autoimmune thyroiditis: Aberrant expression of MHC-class II antigens and the possible role of virus. J Autoimmun 7:13-25, 1994
28. Lane P: Regulation of T and B cell responses by modulating interactions between CD28/CTLA4 and their ligands, CD80 and CD86. Ann N Y Acad Sci 815:392-400, 1997
29. Ludewig B, Odermatt B, Ochsenbein AF, Zinkernagel RM, Hengartner H: Role of dendritic cells in the induction and maintenance of autoimmune diseases. Immunol Rev 169:45-54, 1999
30. McElwee KJ, Boggess D, Olivry T, et al: Comparison of alopecia areata in human and nonhuman mammalian species. Pathobiology 66:90-107, 1998a
31. McElwee KJ, Boggess D, King LE Jr, Sundberg JP: Experimental induction of alopecia areata-like hair loss in C3H/HeJ mice using full-thickness skin grafts. J Invest Dermatol 111:797-803, 1998b
32. McElwee KJ, Boggess D, Miller J, King LE Jr, Sundberg JP: Spontaneous alopecia areata-like hair loss in one congenic and seven inbred laboratory mouse strains. J Invest Dermatol Symp Proc 4:202-206, 1999a
33. McElwee KJ, Tobin DJ, Bystryn JC, King LE Jr, Sundberg JP: Alopecia areata: An autoimmune disease? Exp Dermatol 8:371-379, 1999b
34. McElwee KJ, Freyschmidt-Paul P, Ziegler A, Happle R, Hoffmann R: Genetic susceptibility and severity of alopecia areata in human and animal models. Eur J Dermatol 11:11-16, 2001
35. McElwee KJ, Nijyama S, Freyschmidt-Paul P, Wenzel E, Kissling S, Sundberg JP, Hoffmann R: Dietary soy oil content and soy derived phytoestrogen genistein increase resistance to alopecia areata onset in C3H/HeJ mice. Exp Dermatol, in press
36. Messenger AG, Bleehen SS: Expression of HLA-DR by anagen hair follicles in alopecia areata. J Invest Dermatol 85:569-572, 1985
37. van Parijs L, Abbas AK: Role of Fas-mediated cell death in the regulation of immune responses. Curr Opin Immunol 8:355-361, 1996
38. Paus R, Slominski A, Czarnetzki BM: 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, 1993
39. Paus R, Christoph T, Müller-Röver S: Immunology of the hair follicle: A short journey into terra incognita. J Invest Dermatol Symp Proc 4:226-234, 1999
40. Razi-Wolf Z, Freeman GJ, Galvin F, Benacerraf B, Nadler L, Reiser H: Expression and function of the murine B7 antigen, the major costimulatory molecule expressed by peritoneal exudate cells. Proc Natl Acad Sci USA 89:4210-4214, 1992
41. Reich EP, Scaringe D,Yagi J, Sherwin RS, Janeway CA Jr: Prevention of diabetes in NOD mice by injection of autoreactive T-lymphocytes. Diabetes 38:1647-1651, 1989
42. Relyea MJ, Miller J, Boggess D, Sundberg JP: Necropsy methods for laboratory mice. biological characterization of a new mutation. In: Sundberg JP, Boggess D (eds). Systematic Approach to Evaluation of Mouse Mutations. Boca Raton: CRC Press, 1999; pp 57-90
43. Rösel M, Seiter S, Zöller M: CD44v10 expression in the mouse and functional activity in delayed type hypersensitivity. J Cell Physiol 171:305-317, 1997
44. Sabelko-Downes KA, Russell JH: The role of Fas ligand in vivo as a cause and regulator of pathogenesis. Curr Opin Immunol 12:330-335, 2000
45. Seiter S, Engel P, Föhr N, Zöller M: Mitigation of delayed-type hypersensitivity reactions by a CD44 variant isoform v3-specific antibody: Blockade of leukocyte egress. J Invest Dermatol 113:11-21, 1999
46. Seiter S, Schmidt DS, Zöller M: The CD44 variant isoforms CD44v6 and CD44v7 are expressed by distinct leukocyte subpopulations and exert non-overlapping functional activities. Int Immunol 12:37-49, 2000
47. Smith SC, Allen PM: Expression of myosin-class II major histocompatibility complexes in the normal myocardium occurs before induction of autoimmune myocarditis. Proc Natl Acad Sci USA 89:9131-9135, 1992
48. Strobel S, Mowat AM: Immune responses to dietary antigens: oral tolerance. Immunol Today 19:173-181, 1998
49. Sundberg JP, Cordy WR, King LE Jr: Alopecia areata in aging C3H/HeJ mice. J Invest Dermatol 102:847-856, 1994
50. Wicker LS, Miller BJ, Mullen Y:Transfer of autoimmune diabetes mellitus with splenocytes from nonobese diabetic (NOD) mice. Diabetes 35:855-860, 1986
51. Wittig B, Schwärzler C, Föhr N, Günthert U, Zöller M: Curative treatment of an experimentally induced colitis by a CD44 variant V7-specific antibody. J Immunol 161:1069-1073, 1998
52. Woods GM, Doherty KV, Malley RC, Rist MJ, Muller HK: Carcinogen-modified dendritic cells induce immunosuppression by incomplete T-cell activation resulting from impaired antigen uptake and reduced CD86 expression. Immunology 99:16-22, 2000
53. Zhang JZ, Davidson L, Eisenbarth G, Weiner HL: Suppression of diabetes in NOD mice by oral administration of porcine insulin. Proc Natl Acad Sci USA 88:10252-10256, 1991
54. Zöller M: Costimulatory molecules and their ligands as therapeutic targets in autoimmune disease. Eur J Dermatol 11:335-342, 2001
55. + regulatory T cells in C3H/HeJ mice with alopecia areata. J Invest Dermatol 118:983-992, 2002