Patients with atopic dermatitis have attenuated and distinct contact hypersensitivity responses to common allergens in skin

Journal of Allergy and Clinical Immunology

Volumn 135, Issue 3, 2015, Pages 712-720

  Correa Da Rosa, Joel ^a   Malajian, Dana ^a,b   Shemer, Avner ^c   Rozenblit, Mariya ^a,d   Dhingra, Nikhil ^a,d,e   Czarnowicki, Tali ^a   Khattri, Saakshi ^a   Ungar, Benjamin ^a,d   Finney, Robert ^a,f   Xu, Hui ^a   Zheng, Xiuzhong ^a   Estrada, Yeriel D ^a   Peng, Xiangyu ^a,d   Suárez Fariñas, Mayte ^a   Krueger, James G ^a   Guttman Yassky, Emma ^a,d  

^a ROCKEFELLER UNIVERSITY   (United States)

^b Columbia University College of Physicians and Surg ^*  (United States)

^c Tel Hashomer Hosp   (Israel)

^d MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^e LONG ISLAND JEWISH MEDICAL CENTER   (United States)

^f THOMAS JEFFERSON UNIVERSITY   (United States)

Author keywords

allergic contact dermatitis; Atopic dermatitis; fragrance; human skin; nickel; patch testing; rubber; T cell polarization

Indexed keywords

CALGRANULIN B; CONTACT ALLERGEN; CXCL9 CHEMOKINE; FRAGRANCE; GAMMA INTERFERON INDUCIBLE PROTEIN 10; INTERFERON; INTERLEUKIN 13; INTERLEUKIN 23; INTERLEUKIN 4; INTERLEUKIN 5; INTERSTITIAL COLLAGENASE; MACROPHAGE DERIVED CHEMOKINE; MACROPHAGE ELASTASE; RUBBER; ALLERGEN; COSMETIC; CYTOKINE; LATEX; MMP1 PROTEIN, HUMAN; NICKEL; TRANSCRIPTOME;

ADULT; ARTICLE; CD3+ T LYMPHOCYTE; CELL INFILTRATION; CLINICAL ARTICLE; CONTACT ALLERGY; CONTACT SENSITIZATION; CONTROLLED STUDY; FEMALE; GENE EXPRESSION; HUMAN; IMMUNE RESPONSE; IMMUNOHISTOCHEMISTRY; INNATE IMMUNITY; MALE; PATCH TEST; PHENOTYPE; PREVALENCE; PRIORITY JOURNAL; REGULATOR GENE; SKIN ALLERGY; SKIN BIOPSY; TH17 CELL; UPREGULATION; ATOPIC DERMATITIS; CHEMISTRY; CONTACT DERMATITIS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; MIDDLE AGED; PATHOLOGY; SKIN; TH1 CELL; TH2 CELL;

ADULT; ALLERGENS; CALGRANULIN B; COSMETICS; CYTOKINES; DERMATITIS, ATOPIC; DERMATITIS, CONTACT; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HUMANS; LATEX; MALE; MATRIX METALLOPROTEINASE 1; MATRIX METALLOPROTEINASE 12; MIDDLE AGED; NICKEL; PATCH TESTS; RUBBER; SKIN; TH1 CELLS; TH17 CELLS; TH2 CELLS; TRANSCRIPTOME;

EID: 84924601251     PISSN: 00916749     EISSN: 10976825     Source Type: Journal    
DOI: 10.1016/j.jaci.2014.11.017     Document Type: Article

References (62)

1. E. Guttman-Yassky, K.E. Nograles, and J.G. Krueger Contrasting pathogenesis of atopic dermatitis and psoriasis - part I: clinical and pathologic concepts J Allergy Clin Immunol 127 2011 1110 1118
2. T.E. Shaw, G.P. Currie, C.W. Koudelka, and E.L. Simpson Eczema prevalence in the United States: data from the 2003 National Survey of Children's Health J Invest Dermatol 131 2011 67 73
3. J.P. Thyssen, A. Linneberg, T. Menné, and J.D. Johansen The epidemiology of contact allergy in the general population - prevalence and main findings Contact Dermatitis 57 2007 287 299
4. H17 immune activation compared with extrinsic atopic dermatitis J Allergy Clin Immunol 132 2013 361 370
5. J. Gittler, A. Shemer, M. Suárez-Fariñas, J. Fuentes-Duculan, K.J. Gulewicz, and C.Q.F. Wang Progressive activation of T(H)2/T(H)22 cytokines and selective epidermal proteins characterizes acute and chronic atopic dermatitis J Allergy Clin Immunol 130 2012 1344 1354
6. D. Pennino, K. Eyerich, C. Scarponi, T. Carbone, S. Eyerich, and F. Nasorri IL-17 amplifies human contact hypersensitivity by licensing hapten nonspecific Th1 cells to kill autologous keratinocytes J Immunol 184 2010 4880 4888
7. J.M. Larsen, C.M. Bonefeld, S.S. Poulsen, C. Geisler, and L. Skov IL-23 and T(H)17-mediated inflammation in human allergic contact dermatitis J Allergy Clin Immunol 123 2009 486 492
8. L. Ricciardi, P.L. Minciullo, S. Saitta, D. Trombetta, A. Saija, and S. Gangemi Increased serum levels of IL-22 in patients with nickel contact dermatitis Contact Dermatitis 60 2009 57 58
9. J.K. Gittler, J.G. Krueger, and E. Guttman-Yassky Atopic dermatitis results in intrinsic barrier and immune abnormalities: implications for contact dermatitis J Allergy Clin Immunol 131 2013 300 313
10. H.E. Jones, C.W. Lewis, and S.L. McMarlin Allergic contact sensitivity in atopic dermatitis Arch Dermatol 107 1973 217 222
11. A.C. de Groot The frequency of contact allergy in atopic patients with dermatitis Contact Dermatitis 22 1990 273 277
12. K.K.B. Clemmensen, S.F. Thomsen, G.B.E. Jemec, and T. Agner Pattern of contact sensitization in patients with and without atopic dermatitis in a hospital-based clinical database Contact Dermatitis 71 2014 75 81
13. R. Spiewak Atopy and contact hypersensitivity: a reassessment of the relationship using objective measures Ann Allergy Asthma Immunol 95 2005 61 65
14. L. Landeck, P. Schalock, L. Baden, and E. González Contact sensitization pattern in 172 atopic subjects Int J Dermatol 50 2014 806 810
15. C.N. Shaughnessey, D. Malajian, and D.V. Belsito Cutaneous delayed-type hypersensitivity in patients with atopic dermatitis: reactivity to topical preservatives J Am Dermatol 70 2014 102 107
16. M. Kot, J. Bogaczewicz, B. Krecisz, and A. Wozniacka Contact hypersensitivity to haptens of the European standard series and corticosteroid series in the population of adolescents and adults with atopic dermatitis Dermatitis 25 2014 72 76
17. D. Schena, A. Papagrigoraki, G. Tessari, A. Peroni, C. Sabbadini, and G. Girolomoni Allergic contact dermatitis in children with and without atopic dermatitis Dermatitis 23 2014 275 280
18. E.M. Herro, C. Matiz, K. Sullivan, C. Hamann, and S.E. Jacob Frequency of contact allergens in pediatric patients with atopic dermatitis J Clin Aesthet Dermatol 4 2011 39 41
19. R. Darlenski, J. Kazandjieva, N. Tsankov, and J.W. Fluhr Acute irritant threshold correlates with barrier function, skin hydration and contact hypersensitivity in atopic dermatitis and rosacea Exp Dermatol 22 2013 752 753
20. D. Malajian, and D.V. Belsito Cutaneous delayed-type hypersensitivity in patients with atopic dermatitis J Am Dermatol 69 2013 232 237
21. H. Yamaguchi, R. Kabashima-Kubo, T. Bito, J. Sakabe, T. Shimauchi, and T. Ito High frequencies of positive nickel/cobalt patch tests and high sweat nickel concentration in patients with intrinsic atopic dermatitis J Dermatol Sci 72 2013 240 245
22. M.J. Visser, M.M. Verberk, L.E. Campbell, W.H.I. McLean, F. Calkoen, and J.G. Bakker Filaggrin loss-of-function mutations and atopic dermatitis as risk factors for hand eczema in apprentice nurses: part II of a prospective cohort study Contact Dermatitis 70 2013 139 150
23. J.P. Thyssen, A. Linneberg, K. Ross-Hansen, B.C. Carlsen, M. Meldgaard, and P.B. Szecsi Filaggrin mutations are strongly associated with contact sensitization in individuals with dermatitis Contact Dermatitis 68 2013 273 276
24. L. Landeck, M. Visser, C. Skudlik, R. Brans, S. Kezic, and S.M. John No remarkable differences in rates of sensitization to common type I and IV allergens between FLG loss-of-function mutation carriers and wild-type subjects Contact Dermatitis 70 2014 27 34
25. K. Ross-Hansen, T. Menné, J.D. Johansen, B.C. Carlsen, A. Linneberg, and N.H. Nielsen Nickel reactivity and filaggrin null mutations - evaluation of the filaggrin bypass theory in a general population Contact Dermatitis 64 2011 24 31
26. L. Newell, M.E. Polak, J. Perera, C. Owen, P. Boyd, and C. Pickard Sensitization via healthy skin programs Th2 responses in individuals with atopic dermatitis J Invest Dermatol 133 2013 2372 2380
27. J. Rees, P.S. Friedmann, and J.N. Matthews Contact sensitivity to dinitrochlorobenzene is impaired in atopic subjects. Controversy revisited Arch Dermatol 126 1990 1173 1175
28. J.P. Thyssen, A. Linneberg, K. Engkilde, T. Menné, and J.D. Johansen Contact sensitization to common haptens is associated with atopic dermatitis: new insight Br J Dermatol 166 2012 1255 1261
29. M. Forsbeck, A. Hovmark, and E. Skog Patch testing, tuberculin testing and sensitization with dinitrochlorobenzene and nitrosodimethylaniline of patients with atopic dermatitis Acta Derm Venereol 56 1976 135 138
30. N. Dhingra, A. Shemer, J. Correa da Rosa, M. Rozenblit, M. Suárez-Fariñas, and J. Fuentes-Duculan Molecular profiling of contact dermatitis skin identifies allergen-dependent differences in immune response J Allergy Clin Immunol 134 2014 362 372
31. K. Lammintausta, K. Kalimo, and V.L. Fagerlund Patch test reactions in atopic patients Contact Dermatitis 26 1992 234 240
32. K.A. Zug, E.M. Warshaw, J.F. Fowler, H.I. Maibach, D.L. Belsito, and M.D. Pratt Patch-test results of the North American Contact Dermatitis Group 2005-2006 Dermatitis 20 2009 149 160
33. J.G. Marks, D.V. Belsito, V.A. DeLeo, J.F. Fowler, A.F. Fransway, and H.I. Maibach North American Contact Dermatitis Group patch test results for the detection of delayed-type hypersensitivity to topical allergens J Am Dermatol 38 1998 911 918
34. M.D. Pratt, D.V. Belsito, V.A. DeLeo, J.F. Fowler, A.F. Fransway, and H.I. Maibach North American Contact Dermatitis Group patch-test results, 2001-2002 study period Dermatitis 15 2004 176 183
35. E. Guttman-Yassky, M. Suárez-Fariñas, A. Chiricozzi, K.E. Nograles, A. Shemer, and J. Fuentes-Duculan Broad defects in epidermal cornification in atopic dermatitis identified through genomic analysis J Allergy Clin Immunol 124 2009 1235 1258
36. K.E. Nograles, L.C. Zaba, A. Shemer, J. Fuentes-Duculan, I. Cardinale, and T. Kikuchi 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 1252.e2
37. E. Guttman-Yassky, M.A. Lowes, J. Fuentes-Duculan, L.C. Zaba, I. Cardinale, and K.E. Nograles Low expression of the IL-23/Th17 pathway in atopic dermatitis compared to psoriasis J Immunol 181 2008 7420 7427
38. E. Guttman-Yassky, M.A. Lowes, J. Fuentes-Duculan, J. Whynot, I. Novitskaya, and I. Cardinale Major differences in inflammatory dendritic cells and their products distinguish atopic dermatitis from psoriasis J Allergy Clin Immunol 119 2007 1210 1217
39. M. Suárez-Fariñas, S. Tintle, A. Shemer, A. Chiricozzi, K. Nograles, and I. Cardinale Nonlesional atopic dermatitis skin is characterized by broad terminal differentiation defects and variable immune abnormalities J Allergy Clin Immunol 127 2011 954 964 e1-4
40. S. Tintle, A. Shemer, M. Suarez-Farinas, H. Fujita, P. Gilleaudau, and M. Sullivan-Whalen Reversal of atopic dermatitis with narrow-band UVB phototherapy and biomarkers for therapeutic response J Allergy Clin Immunol 128 2011 583 584
41. S. Eyerich, K. Eyerich, D. Pennino, T. Carbone, F. Nasorri, and S. Pallotta Th22 cells represent a distinct human T cell subset involved in epidermal immunity and remodeling J Clin Invest 119 2009 3573 3585
42. M.F. Nold, C.A. Nold-Petry, J.A. Zepp, B.E. Palmer, P. Bufler, and C.A. Dinarello IL-37 is a fundamental inhibitor of innate immunity Nat Immunol 11 2010 1014 1022
43. T. Werfel, M. Hentschel, H. Renz, and A. Kapp Analysis of the phenotype and cytokine pattern of blood- and skin-derived nickel specific T cells in allergic contact dermatitis Int Arch Allergy Immunol 113 1997 384 386
44. M. Lindemann, J. Böhmer, M. Zabel, and H. Grosse-Wilde ELISpot: a new tool for the detection of nickel sensitization Clin Exp Allergy 33 2003 992 998
45. C. Traidl-Hoffmann, and J. Ring Is there an in vitro test for type IV allergy discriminating between sensitization and allergic disease? Clin Exp Allergy 38 2008 1412 1415
46. H. Moed, M. Blomberg von, D.P. Bruynzeel, R. Scheper, S. Gibbs, and T. Rustemeyer Improved detection of allergen-specific T-cell responses in allergic contact dermatitis through the addition of 'cytokine cocktails' Exp Dermatol 14 2005 634 640
47. C.M. Wilke, K. Bishop, D. Fox, and W. Zou Deciphering the role of Th17 cells in human disease Trends Immunol 32 2011 603 611
48. I. Kryczek, A.T. Bruce, J.E. Gudjonsson, A. Johnston, A. Aphale, and L. Vatan Induction of IL-17+ T cell trafficking and development by IFN-gamma: mechanism and pathological relevance in psoriasis J Immunol 181 2008 4733 4741
49. D.J. Cua, J. Sherlock, Y. Chen, C.A. Murphy, B. Joyce, and B. Seymour Interleukin-23 rather than interleukin-12 is the critical cytokine for autoimmune inflammation of the brain Nature 421 2003 744 748
50. N. Dhingra, N. Gulati, and E. Guttman-Yassky Mechanisms of contact sensitization offer insights into the role of barrier defects vs. intrinsic immune abnormalities as drivers of atopic dermatitis J Invest Dermatol 133 2013 2311 2314
51. P. Milanez-Almeida, F. Klawonn, M. Meyer-Hermann, and J. Huehn Differential control of immune cell homeostasis by Foxp3(+) regulatory T cells in murine peripheral lymph nodes and spleen Eur J Microbiol Immunol (Bp) 4 2014 147 155
52. J.J. Lindenberg, D. Oosterhoff, C.C. Sombroek, S.M. Loughseed, E. Hooijberg, and A.G. Stam IL-10 conditioning of human skin affects the distribution of migratory dendritic cell subsets and functional T cell differentiation PLoS One 8 2013 e70237
53. C. Wulfing, H.M. Tunbridge, and D.C. Wraith New inhibitory signaling by CTLA-4 Nat Immunol 15 2014 408 409
54. Y. Li, Z. Wang, T. Yu, B. Chen, J. Zhang, K. Huang, and Z. Huang Increased expression of IL-37 in patients with Graves' disease and its contribution to suppression of proinflammatory cytokines production in peripheral blood mononuclear cells PLoS One 9 2014 e107183
55. F.L. van de Veerdonk, A.K. Stoeckman, G. Wu, A.N. Boeckermann, T. Azam, and M.G. Netea IL-38 binds to the IL-36 receptor and has biological effects on immune cells similar to IL-36 receptor antagonist Proc Natl Acad Sci U S A 109 2012 3001 3005
56. L. Ye, L. Ji, Z. Wen, Y. Zhou, D. Hu, and Y. Li IL-37 inhibits the production of inflammatory cytokines in peripheral blood mononuclear cells of patients with systemic lupus erythematosus: its correlation with disease activity J Transl Med 12 2014 69
57. S. Sharma, N. Kulk, M.F. Nold, R. Gräf, S.H. Kim, and D. Reinhardt The IL-1 family member 7b translocates to the nucleus and down-regulates proinflammatory cytokines J Immunol 180 2008 5477 5482
58. X. Teng, Z. Hu, X. Wei, Z. Wang, T. Guan, and N. Liu IL-37 ameliorates the inflammatory process in psoriasis by suppressing proinflammatory cytokine production J Immunol 192 2014 1815 1823
59. H. Fujita, Y. Inoue, K. Seto, N. Komitsu, and M. Aihara Interleukin-37 is elevated in subjects with atopic dermatitis J Dermatol Sci 69 2013 173 175
60. S. Nakae, Y. Komiyama, A. Nambu, K. Sudo, M. Iwase, and I. Homma Antigen-specific T cell sensitization is impaired in IL-17-deficient mice, causing suppression of allergic cellular and humoral responses Immunity 17 2002 375 387
61. M. Peiser Role of Th17 cells in skin inflammation of allergic contact dermatitis Clin Dev Immunol 2013 2013 261037
62. M.K. Slifka, D.Y. Leung, E. Hammarlund, H.P. Raue, E.L. Simpson, and S. Tofte Transcutaneous yellow fever vaccination of subjects with or without atopic dermatitis J Allergy Clin Immunol 133 2014 439 447