Pathomechanism of atopic dermatitis in the perspective of T cell subsets and skin barrier functions - "which comes first, the chicken or the egg?"

Dermatologica Sinica

Volumn 30, Issue 4, 2012, Pages 142-146

  Kabashima, Kenji ^a  

^a KYOTO UNIVERSITY   (Japan)

Author keywords

atopic dermatitis; dendritic cell; Langerhans cell; regulatory T cell; skin barrier; T cell

Indexed keywords

CHEMOKINE RECEPTOR CCR4; CHEMOKINE RECEPTOR CCR5; CHEMOKINE RECEPTOR CCR6; CHEMOKINE RECEPTOR CCR7; CYCLOSPORIN; FILAGGRIN; GLUCOCORTICOID; IMMUNOGLOBULIN E; INTERLEUKIN 10; INTERLEUKIN 13; INTERLEUKIN 17; INTERLEUKIN 17F; INTERLEUKIN 1BETA; INTERLEUKIN 22; INTERLEUKIN 23; INTERLEUKIN 26; INTERLEUKIN 4; INTERLEUKIN 6; LANGERIN; MACROPHAGE DERIVED CHEMOKINE; PROFILAGGRIN; RANTES; THYMUS AND ACTIVATION REGULATED CHEMOKINE; TRANSFORMING GROWTH FACTOR BETA;

ALLERGIC RHINITIS; ASTHMA; ATOPIC DERMATITIS; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL DIFFERENTIATION; CELLULAR IMMUNITY; DENDRITIC CELL; EPIDERMIS; FOOD ALLERGY; GROUPS BY AGE; HELPER CELL; HUMAN; IMMUNOPATHOGENESIS; IPEX SYNDROME; KERATINOCYTE; LANGERHANS CELL; LONG TERM EXPOSURE; LOSS OF FUNCTION MUTATION; NONHUMAN; PERMEABILITY BARRIER; PHOTOTHERAPY; PROTEIN LOCALIZATION; REGULATORY T LYMPHOCYTE; REVIEW; SENSITIZATION; SKIN ALLERGY; SKIN FUNCTION; T LYMPHOCYTE SUBPOPULATION; TH1 CELL; TH17 CELL; TH2 CELL; TH22 CELL; ULTRAVIOLET RADIATION;

EID: 84870911874     PISSN: 10278117     EISSN: 2223330X     Source Type: Journal    
DOI: 10.1016/j.dsi.2012.07.003     Document Type: Review

References (71)

1. T. Bieber Atopic dermatitis N Engl J Med 358 2008 1483 1494
2. C.A. Akdis, M. Akdis, and T. Bieber Diagnosis and treatment of atopic dermatitis in children and adults: European Academy of Allergology and Clinical Immunology/American Academy of Allergy, Asthma and Immunology/PRACTALL Consensus Report J Allergy Clin Immunol 118 2006 152 169 (Pubitemid 43946480)
3. G. Egawa, and K. Kabashima Skin as a peripheral lymphoid organ: revisiting the concept of skin-associated lymphoid tissues J Invest Dermatol 131 2011 2178 2185
4. J. Heimall, and J.M. Spergel Filaggrin mutations and atopy: consequences for future therapeutics Expert Rev Clin Immunol 8 2012 189 197
5. O. Johansson, Y. Liang, J.D. Heilborn, and J.A. Marcusson Langerhans cells in prurigo nodularis investigated by HLA-DR and S-100 immunofluorescence double staining J Dermatol Sci 17 1998 24 32 (Pubitemid 28253043)
6. D.H. Kaplan, B.Z. Igyarto, and A.A. Gaspari Early immune events in the induction of allergic contact dermatitis Nat Rev Immunol 12 2012 114 124
7. F. Rippke, V. Schreiner, T. Doering, and H.I. Maibach Stratum corneum pH in atopic dermatitis: impact on skin barrier function and colonization with Staphylococcus Aureus Am J Clin Dermatol 5 2004 217 223 (Pubitemid 39127965)
8. T. Ouchi, A. Kubo, and M. Yokouchi Langerhans cell antigen capture through tight junctions confers preemptive immunity in experimental staphylococcal scalded skin syndrome J Exp Med 208 2011 2607 2613
9. C.N. Palmer, A.D. Irvine, and A. Terron-Kwiatkowski Common loss-of-function variants of the epidermal barrier protein filaggrin are a major predisposing factor for atopic dermatitis Nat Genet 38 2006 441 446
10. A. Briot, C. Deraison, and M. Lacroix Kallikrein 5 induces atopic dermatitis-like lesions through PAR2-mediated thymic stromal lymphopoietin expression in Netherton syndrome J Exp Med 206 2009 1135 1147
11. M. Furuse, M. Hata, and K. Furuse Claudin-based tight junctions are crucial for the mammalian epidermal barrier: a lesson from claudin-1-deficient mice J Cell Biol 156 2002 1099 1111 (Pubitemid 34839858)
12. S. Hadj-Rabia, L. Baala, and P. Vabres Claudin-1 gene mutations in neonatal sclerosing cholangitis associated with ichthyosis: a tight junction disease Gastroenterology 127 2004 1386 1390 (Pubitemid 39457765)
13. P. Vijayanand, G. Seumois, and L.J. Simpson Interleukin-4 production by follicular helper T cells requires the conserved Il4 enhancer hypersensitivity site V Immunity 36 2012 175 187
14. E. Proksch, R. Folster-Holst, and J.M. Jensen Skin barrier function, epidermal proliferation and differentiation in eczema J Dermatol Sci 43 2006 159 169 (Pubitemid 44189201)
15. E. Candi, R. Schmidt, and G. Melino The cornified envelope: a model of cell death in the skin Nat Rev Mol Cell Biol 6 2005 328 340 (Pubitemid 40516899)
16. P. Listwan, and J.A. Rothnagel Keratin bundling proteins Methods Cell Biol 78 2004 817 827
17. S.J. Brown, K. Kroboth, and A. Sandilands Intragenic copy number variation within filaggrin contributes to the risk of atopic dermatitis with a dose-dependent effect J Invest Dermatol 132 2012 98 104
18. C.S. Moniaga, and K. Kabashima Filaggrin in atopic dermatitis: flaky tail mice as a novel model for developing drug targets in atopic dermatitis Inflamm Allergy Drug Targets 10 2011 477 485
19. P.G. Fallon, T. Sasaki, and A. Sandilands A homozygous frameshift mutation in the mouse Flg gene facilitates enhanced percutaneous allergen priming Nat Genet 41 2009 602 608
20. M.K. Oyoshi, G.F. Murphy, and R.S. Geha Filaggrin-deficient mice exhibit TH17-dominated skin inflammation and permissiveness to epicutaneous sensitization with protein antigen J Allergy Clin Immunol 124 2009 485 493 493 e1
21. S.J. Brown, Y. Asai, and H.J. Cordell Loss-of-function variants in the filaggrin gene are a significant risk factor for peanut allergy J Allergy Clin Immunol 127 2011 661 667
22. C.S. Moniaga, G. Egawa, and H. Kawasaki Flaky tail mouse denotes human atopic dermatitis in the steady state and by topical application with dermatophagoides pteronyssinus extract Am J Pathol 176 2010 2385 2393
23. Y. Tokura Extrinsic and intrinsic types of atopic dermatitis J Dermatol Sci 58 2010 1 7
24. R. Kabashima-Kubo, M. Nakamura, and J. Sakabe A group of atopic dermatitis without IgE elevation or barrier impairment shows a high Th1 frequency: possible immunological state of the intrinsic type J Dermatol Sci 67 2012 37 43
25. F. Ginhoux, M.P. Collin, and M. Bogunovic Blood-derived dermal langerin+ dendritic cells survey the skin in the steady state J Exp Med 204 2007 3133 3146
26. L.S. Bursch, L. Wang, and B. Igyarto Identification of a novel population of Langerin+ dendritic cells J Exp Med 204 2007 3147 3156
27. L.F. Poulin, S. Henri, B. de Bovis, E. Devilard, A. Kissenpfennig, and B. Malissen The dermis contains langerin+ dendritic cells that develop and function independently of epidermal Langerhans cells J Exp Med 204 2007 3119 3131
28. A. Kissenpfennig, S. Henri, and B. Dubois Dynamics and function of Langerhans cells in vivo: dermal dendritic cells colonize lymph node areas distinct from slower migrating Langerhans cells Immunity 22 2005 643 654 (Pubitemid 40719199)
29. T. Honda, S. Nakajima, and G. Egawa Compensatory role of Langerhans cells and langerin-positive dermal dendritic cells in the sensitization phase of murine contact hypersensitivity J Allergy Clin Immunol 125 2010 1154-1156 e2
30. A. Kubo, K. Nagao, M. Yokouchi, H. Sasaki, and M. Amagai External antigen uptake by Langerhans cells with reorganization of epidermal tight junction barriers J Exp Med 206 2009 2937 2946
31. A. Elentner, D. Finke, and M. Schmuth Langerhans cells are critical in the development of atopic dermatitis-like inflammation and symptoms in mice J Cell Mol Med 13 2009 2658 2672
32. J. Yoo, M. Omori, and D. Gyarmati Spontaneous atopic dermatitis in mice expressing an inducible thymic stromal lymphopoietin transgene specifically in the skin J Exp Med 202 2005 541 549 (Pubitemid 41186952)
33. V. Soumelis, P.A. Reche, and H. Kanzler Human epithelial cells trigger dendritic cell mediated allergic inflammation by producing TSLP Nat Immunol 3 2002 673 680 (Pubitemid 34752477)
34. S. Nakajima, B.Z. Igyarto, and T. Honda Langerhans cells are critical in epicutaneous sensitization with protein antigen via thymic stromal lymphopoietin receptor signaling J Allergy Clin Immunol 129 2012 1048-1055 e6
35. H. Kitagaki, S. Fujisawa, K. Watanabe, K. Hayakawa, and T. Shiohara Immediate-type hypersensitivity response followed by a late reaction is induced by repeated epicutaneous application of contact sensitizing agents in mice J Invest Dermatol 105 1995 749 755 (Pubitemid 26006351)
36. K. Hattori, M. Nishikawa, and K. Watcharanurak Sustained exogenous expression of therapeutic levels of IFN-gamma ameliorates atopic dermatitis in NC/Nga mice via Th1 polarization J Immunol 184 2010 2729 2735
37. J.M. Spergel, E. Mizoguchi, J.P. Brewer, T.R. Martin, A.K. Bhan, and R.S. Geha Epicutaneous sensitization with protein antigen induces localized allergic dermatitis and hyperresponsiveness to methacholine after single exposure to aerosolized antigen in mice J Clin Invest 101 1998 1614 1622 (Pubitemid 28198490)
38. M. Grewe, S. Walther, K. Gyufko, W. Czech, E. Schopf, and J. Krutmann Analysis of the cytokine pattern expressed in situ in inhalant allergen patch test reactions of atopic dermatitis patients J Invest Dermatol 105 1995 407 410
39. I. Nomura, E. Goleva, and M.D. Howell Cytokine milieu of atopic dermatitis, as compared to psoriasis, skin prevents induction of innate immune response genes J Immunol 171 2003 3262 3269 (Pubitemid 37093553)
40. A. Di Cesare, P. Di Meglio, and F.O. Nestle A role for Th17 cells in the immunopathogenesis of atopic dermatitis? J Invest Dermatol 128 2008 2569 2571
41. T. Honda, Y. Miyachi, and K. Kabashima The role of regulatory T cells in contact hypersensitivity Recent Pat Inflamm Allergy Drug Discov 4 2010 85 89
42. T. Honda, Y. Miyachi, and K. Kabashima Regulatory T cells in cutaneous immune responses J Dermatol Sci 63 2011 75 82
43. M. Tomura, T. Honda, and H. Tanizaki Activated regulatory T cells are the major T cell type emigrating from the skin during a cutaneous immune response in mice J Clin Invest 120 2010 883 893
44. L.A. Tesmer, S.K. Lundy, S. Sarkar, and D.A. Fox Th17 cells in human disease Immunol Rev 223 2008 87 113 (Pubitemid 351986173)
45. R. He, M.K. Oyoshi, H. Jin, and R.S. Geha Epicutaneous antigen exposure induces a Th17 response that drives airway inflammation after inhalation challenge Proc Natl Acad Sci U S A 104 2007 15817 15822 (Pubitemid 350035382)
46. M. Toda, D.Y. Leung, and S. Molet Polarized in vivo expression of IL-11 and IL-17 between acute and chronic skin lesions J Allergy Clin Immunol 111 2003 875 881 (Pubitemid 36470263)
47. C. Koga, K. Kabashima, N. Shiraishi, M. Kobayashi, and Y. Tokura Possible pathogenic role of Th17 cells for atopic dermatitis J Invest Dermatol 128 2008 2625 2630
48. P.F. Cheung, C.K. Wong, and C.W. Lam Molecular mechanisms of cytokine and chemokine release from eosinophils activated by IL-17A, IL-17F, and IL-23: implication for Th17 lymphocytes-mediated allergic inflammation J Immunol 180 2008 5625 5635
49. K.E. Nograles, L.C. Zaba, and A. Shemer IL-22-producing "T22" T cells account for upregulated IL-22 in atopic dermatitis despite reduced IL-17-producing TH17 T cells J Allergy Clin Immunol 123 2009 1244-52 e2
50. B. Homey, H. Alenius, and A. Muller CCL27-CCR10 interactions regulate T cell-mediated skin inflammation Nat Med 8 2002 157 165 (Pubitemid 34155127)
51. K. Boniface, F.X. Bernard, M. Garcia, A.L. Gurney, J.C. Lecron, and F. Morel IL-22 inhibits epidermal differentiation and induces proinflammatory gene expression and migration of human keratinocytes J Immunol 174 2005 3695 3702 (Pubitemid 40354080)
52. B.D. Sather, P. Treuting, and N. Perdue Altering the distribution of Foxp3(+) regulatory T cells results in tissue-specific inflammatory disease J Exp Med 204 2007 1335 1347 (Pubitemid 46919872)
53. J.C. Dudda, N. Perdue, E. Bachtanian, and D.J. Campbell Foxp3+ regulatory T cells maintain immune homeostasis in the skin J Exp Med 205 2008 1559 1565
54. E. Yurchenko, M. Tritt, V. Hay, E.M. Shevach, Y. Belkaid, and C.A. Piccirillo CCR5-dependent homing of naturally occurring CD4+ regulatory T cells to sites of Leishmania major infection favors pathogen persistence J Exp Med 203 2006 2451 2460 (Pubitemid 44664615)
55. H. Kitagaki, N. Ono, K. Hayakawa, T. Kitazawa, K. Watanabe, and T. Shiohara Repeated elicitation of contact hypersensitivity induces a shift in cutaneous cytokine milieu from a T helper cell type 1 to a T helper cell type 2 profile J Immunol 159 1997 2484 2491 (Pubitemid 127681044)
56. H.D. Ochs, S.F. Ziegler, and T.R. Torgerson FOXP3 acts as a rheostat of the immune response Immunol Rev 203 2005 156 164 (Pubitemid 40179700)
57. L.S. Ou, E. Goleva, C. Hall, and D.Y. Leung T regulatory cells in atopic dermatitis and subversion of their activity by superantigens J Allergy Clin Immunol 113 2004 756 763 (Pubitemid 38530433)
58. D. Hijnen, I. Haeck, and A.A. van Kraats Cyclosporin A reduces CD4(+)CD25(+) regulatory T-cell numbers in patients with atopic dermatitis J Allergy Clin Immunol 124 2009 856 858
59. Y. Ito, Y. Adachi, and T. Makino Expansion of FOXP3-positive CD4+CD25 + T cells associated with disease activity in atopic dermatitis Ann Allergy Asthma Immunol 103 2009 160 165
60. C. Brandt, V. Pavlovic, A. Radbruch, M. Worm, and R. Baumgrass Low-dose cyclosporine A therapy increases the regulatory T cell population in patients with atopic dermatitis Allergy 64 2009 1588 1596
61. J. Verhagen, M. Akdis, and C. Traidl-Hoffmann Absence of T-regulatory cell expression and function in atopic dermatitis skin J Allergy Clin Immunol 117 2006 176 183 (Pubitemid 43017157)
62. C. Schnopp, R. Rad, and A. Weidinger Fox-P3-positive regulatory T cells are present in the skin of generalized atopic eczema patients and are not particularly affected by medium-dose UVA1 therapy Photodermatol Photoimmunol Photomed 23 2007 81 85 (Pubitemid 46844989)
63. M. Caproni, D. Torchia, E. Antiga, W. Volpi, E. del Bianco, and P. Fabbri The effects of tacrolimus ointment on regulatory T lymphocytes in atopic dermatitis J Clin Immunol 26 2006 370 375 (Pubitemid 44051384)
64. A.J. Reefer, S.M. Satinover, and M.D. Solga Analysis of CD25hiCD4+ "regulatory" T-cell subtypes in atopic dermatitis reveals a novel T(H)2-like population J Allergy Clin Immunol 121 2008 415 422 e3
65. R. Baumgrass, C. Brandt, F. Wegner, M. Abdollahnia, and M. Worm Low-dose, but not high-dose, cyclosporin A promotes regulatory T-cell induction, expansion, or both J Allergy Clin Immunol 126 2010 183 184 author reply 4
66. G. Stary, I. Klein, and W. Bauer Glucocorticosteroids modify Langerhans cells to produce TGF-beta and expand regulatory T cells J Immunol 186 2011 103 112
67. K. Loser, and S. Beissert Regulation of cutaneous immunity by the environment: an important role for UV irradiation and vitamin D Int Immunopharmacol 9 2009 587 589
68. M.K. Oyoshi, R.P. Larson, S.F. Ziegler, and R.S. Geha Mechanical injury polarizes skin dendritic cells to elicit a T(H)2 response by inducing cutaneous thymic stromal lymphopoietin expression J Allergy Clin Immunol 126 2010 976 984 84 e1-5
69. A. Onoue, K. Kabashima, M. Kobayashi, T. Mori, and Y. Tokura Induction of eosinophil- and Th2-attracting epidermal chemokines and cutaneous late-phase reaction in tape-stripped skin Exp Dermatol 18 2009 1036 1043
70. M.D. Howell, B.E. Kim, and P. Gao Cytokine modulation of atopic dermatitis filaggrin skin expression J Allergy Clin Immunol 120 2007 150 155 (Pubitemid 46990506)
71. D. Gutowska-Owsiak, A.L. Schaupp, and M. Salimi IL-17 downregulates filaggrin and affects keratinocyte expression of genes associated with cellular adhesion Exp Dermatol 21 2012 104 110