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Nickel-Induced Contact Dermatitis Peripheral and Cutaneous T Cells Preferential Usage of TCR-Vβ17 by Peripheral and Cutaneous T Cells in Nickel-Induced Contact Dermatitis This information is current as Lioba Büdinger, Nicole Neuser, Uwe Totzke, Hans F. Merk of September 27, 2021. and Michael Hertl J Immunol 2001; 167:6038-6044; ; doi: 10.4049/jimmunol.167.10.6038 http://www.jimmunol.org/content/167/10/6038 Downloaded from References This article cites 30 articles, 8 of which you can access for free at: http://www.jimmunol.org/content/167/10/6038.full#ref-list-1 http://www.jimmunol.org/ Why The JI? Submit online. • Rapid Reviews! 30 days* from submission to initial decision • No Triage! Every submission reviewed by practicing scientists • Fast Publication! 4 weeks from acceptance to publication by guest on September 27, 2021 *average Subscription Information about subscribing to The Journal of Immunology is online at: http://jimmunol.org/subscription Permissions Submit copyright permission requests at: http://www.aai.org/About/Publications/JI/copyright.html Email Alerts Receive free email-alerts when new articles cite this article. Sign up at: http://jimmunol.org/alerts The Journal of Immunology is published twice each month by The American Association of Immunologists, Inc., 1451 Rockville Pike, Suite 650, Rockville, MD 20852 Copyright © 2001 by The American Association of Immunologists All rights reserved. Print ISSN: 0022-1767 Online ISSN: 1550-6606. Preferential Usage of TCR-V␤17 by Peripheral and Cutaneous T Cells in Nickel-Induced Contact Dermatitis1 Lioba Bu¨dinger,*† Nicole Neuser,* Uwe Totzke,‡ Hans F. Merk,* and Michael Hertl2*§ Nickel (Ni) is one of the most common contact sensitizers in man, and Ni-induced contact dermatitis is considered as a model of hapten-induced delayed type hypersensitivity. Previous studies indicated that Ni-reactive T cells derived from Ni-allergic indi- viduals preferentially express distinct TCR-V␤ chains. However, data on the TCR-V␤ repertoire of Ni-responsive T cells are not consistent. Therefore, the aim of this study was to identify the TCR-V␤ receptors of Ni-responsive peripheral and cutaneous T cells in a cohort of 17 donors with Ni-induced contact dermatitis in comparison with those of 6 healthy controls. Peripheral NiSO4- responsive T lymphocytes showed a significant overexpression of TCR-V␤17 and the frequency of TCR-V␤17؉ T cells correlated significantly with the in vitro reactivity of PBMC to NiSO4. In addition, the cutaneous infiltrate of Ni-induced patch test reactions ؉ ␤ Downloaded from consisted primarily of V 17 T cells. The majority of patch test-derived NiSO4-responsive T cells of three allergic donors were ␤ ؉ ␤ TCR-V 17 , whereas patch test-derived NiSO4 unresponsive T cells of four additional donors did not express TCR-V 17. Skin-derived Ni-responsive T cell lines from three donors uniformly secreted the Th2 cytokine, IL-5, but no IFN-␥ or IL-10. These in vitro and in vivo findings strongly suggest that T cells with a restricted TCR-V␤ repertoire, i.e., V␤17, predominate in NiSO4-induced contact dermatitis and may be crucial in the effector phase of Ni hypersensitivity. The Journal of Immunology, 2001, 167: 6038–6044. http://www.jimmunol.org/ ickel (Ni) is one of the most common contact sensitizers the aim of this study was a comprehensive analysis of TCR-V␤ causing delayed-type hypersensitivity in humans (1–4). expression of Ni-specific T cells by examining peripheral as well N Accordingly, the cellular immune response to Ni2ϩ ions as skin-derived T cells, by investigating sufficient numbers of in- has become a model system for studying hapten-induced hyper- dividuals for statistical evaluation, and by correlating both in vivo sensitivity (5–6). There are two key processes in hapten-induced and in vitro findings. immune responses: presentation of the hapten in association with endogenous or exogenous peptides by HLA molecules on the sur- face of the APC, and recognition of the Ag-HLA-complex by the Materials and Methods T cell via its specific Ag receptor (TCR). Ni-allergic and nonallergic individuals by guest on September 27, 2021 In Ni-sensitized individuals, the first step in this sequence ap- A total of 17 patients with a history of eczema and a positive epicutaneous pears to be rather unselective, because Ni is not preferentially pre- patch test reaction to NiSO4 and six healthy, nonallergic control individuals sented in association with distinct HLA-DR, -DQ, and -DP alleles participated in this study after giving written consent. Patch tests were performed with 5% NiSO4 in petrolatum and were evaluated after 48 and (4, 6). Therefore, much of the interest has recently been focusing 72 h. All patients, but none of the control persons, showed a positive result. on T cell recognition and the nature of the epitopes formed by Positive reactions ranged from erythema with few papules to multiple Ni2ϩ ions. Ni preferentially binds to cysteine and histidine resi- papulovesicles (Table I). Lymphocyte proliferation assays were performed dues of proteins/peptides and may be presented to T cells by pro- with PBMC immediately after patch testing. Skin biopsies were taken from cessing-dependent and -independent pathways, as shown for other six Ni-allergic patients and two nonallergic controls 24 h after performing an additional epicutaneous patch test with NiSO4. This particular time haptens (4, 6–7). With regard to the structural characteristics of the point was chosen because the number of Ni-specific T cells in the cutane- TCR used by Ni-specific T cells, previous studies strongly sug- ous infiltrate decreases over time due to the secondary influx of bystander gested that only a limited TCR-V␤ repertoire is expressed by Ni- T cells of unrelated Ag specificity. Biopsies were placed in the culture responsive peripheral T cells (8–11). However, the findings of the media without prior mechanical disaggregation, leading to the emigration of the cutaneous T cells into the culture media. After 7–10 days of culture, individual studies were inconsistent due to the different study de- 4–10 ϫ 106 skin-derived T cells were recovered from each 4-mm punch signs and the small numbers of individuals investigated. Therefore, biopsy. *Department of Dermatology and †Interdisciplinary Center for Clinical Research, Ags and media ‡ Rheinisch-Westfa¨lische Technische Hochschule, Aachen, Germany; MDS Pharma ϫ ␮ § The following Ags were used in this study: NiSO4 6H2O (20 M), Services, Hamburg, Germany; and Department of Dermatology, University of ␮ ␮ ␮ Erlangen, Erlangen, Germany PdCl2 (10 M), CoCl2 (1 M), CuCl2 (0.1–5 M; all from Sigma-Aldrich, Deisenhofen, Germany), PHA (1%, Life Technologies, Rockville, MD), Received for publication May 18, 2001. Accepted for publication September tetanus toxoid (TT3; 3.2 Lf/ml, Behring Diagnostics, Marburg, Germany). 13, 2001. PBMC and patch test-derived T cells were cultured in RPMI 1640 (Life The costs of publication of this article were defrayed in part by the payment of page Technologies) supplemented with 2 mM L-glutamine, penicillin/streptomy- charges. This article must therefore be hereby marked advertisement in accordance cin, 1 mM Na-pyruvate, 1ϫ nonessential amino acids (all from Life Tech- with 18 U.S.C. Section 1734 solely to indicate this fact. nologies), and 10% heat-inactivated pooled human AB serum (Sigma-Al- 1 This study was supported by a grant from the Interdisciplinary Center for Clinical drich) or 10% FCS and 40 U/ml hIL-2 (Biotest Diagnostics, Dreieich, Research of the Rheinisch-Westfa¨lische Hochschule (to L.B.) and by the Deutsche Germany), respectively. Forschungsgemeinschaft (He 1602/5-2 to M.H.). 2 Address correspondence and reprint requests to Dr. Michael Hertl, Department of Dermatology, University of Erlangen, Hartmannstrasse 14, D-91054 Erlangen, Ger- many. E-mail address: [email protected] 3 Abbreviations used in this paper: TT, tetanus toxoid; SI, stimulation index. Copyright © 2001 by The American Association of Immunologists 0022-1767/01/$02.00 The Journal of Immunology 6039 Table I. Reactivity of 17 Ni-allergic donors to metal ions in vivo and in vitro Patch Test Reactivitya Proliferative Response of PBMCb c NiSO4 CoCl2 PdCl2 No Ag Patient NiSO4 CoCl2 PdCl2 (SI) (SI) (SI) (cpm) M8 ϩϩ ϩ Ϫ 16.5 0.5 NT 3153 M24 ϩϪϪ1.4 1.2 1.1 2884 M26 ϩϩ Ϫ Ϫ 2.4 2.4 NT 515 M27 ϩϩ Ϫ Ϫ 3.0 0.7 1.2 712 M32 ϩϩ Ϫ Ϫ 3.8 2.1 0.9 1858 M34 ϩϩϩ Ϫ Ϫ 40.3 3.7 1.4 746 M35 ϩϪϪ2.5 NT NT 1366 M36 ϩϩ Ϫ Ϫ 2.7 0.7 NT 891 M37 ϩϩ Ϫ Ϫ 2.2 0.7 0.5 1000 M38 ϩϩϩ Ϫ Ϫ 30.3 6.3 2.1 439 M41 ϩϩ Ϫ Ϫ 8.6 1.6 1.4 209 M42 ϩϩϩ ϩϩ ϩ 8.8 1.7 1.2 2551 M43 ϩϩ Ϫ Ϫ 1.3 0.9 0.9 1220 M46 ϩϩ Ϫ Ϫ 10.4 2.9 1.9 291 M51 ϩϩ Ϫ Ϫ 5.8 1.5 1.4 1623 M52 ϩϩ Ϫ Ϫ 6.0 1.0 1.8 1118 Downloaded from M53 ϩϩ Ϫ Ϫ 4.4 1.1 2.0 325 a Patch test reactivity 48 h after epicutaneous application of Ag; ϩ, erythema; ϩϩ, papules/eczema; ϩϩϩ, papulo-vesicles; Ϫ, no cutaneous reaction. b Ն ␮ SI (cpm culture with Ag/cpm in culture without Ag); a SI 3 was considered significant (bold). Metal salts were used at final concentrations as follows: NiSO4,20 M; ␮ ␮ CoCl2/CuCl2,1 M; PdCl2,10 M; NT, not tested. c cpm, [3H]thymidine incorporation. http://www.jimmunol.org/ Proliferative assays with peripheral and cutaneous T cells (TCRBV)23S1 (all from Immunotech, Hamburg, Germany).
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