Tracking human contact allergens: From mass spectrometric identification of peptide-bound reactive small chemicals to chemical-specific naive human T-cell priming

Toxicological Sciences

Volumn 117, Issue 2, 2010, Pages 336-347

  Dietz, Lisa ^a,b   Esser, Philipp R ^c,d   Schmucker, Sonja S ^e   Goette, Irina ^a,f   Richter, Anne ^e   Schnölzer, Martina ^b   Martin, Stefan F ^c   Thierse, Hermann Josef ^a,b  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^c UNIVERSITY OF FREIBURG   (Germany)

^d UNIVERSITY OF FREIBURG   (Germany)

^e MILTENYI BIOTEC GMBH   (Germany)

^f PROCTER AND GAMBLE COMPANY   (United States)

Author keywords

Alternatives; Contact allergen; Haptenation; Mass spectrometry; Skin sensitization; T cell

Indexed keywords

1 CHLORO 2,4 DINITROBENZENE; 2,4 DINITROBENZENESULFONIC ACID; 2,4 DINITROPHENOL; CONTACT ALLERGEN; GAMMA INTERFERON; HUMAN SERUM ALBUMIN; TRINITROPHENYL; UNCLASSIFIED DRUG;

ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CHEMICAL MODIFICATION; DENDRITIC CELL; HUMAN; HUMAN TISSUE; IN VITRO STUDY; IN VIVO STUDY; INTERFERON PRODUCTION; LYMPHOCYTE PROLIFERATION; MASS SPECTROMETRY; PH; RISK ASSESSMENT; SKIN; SKIN SENSITIZATION; T LYMPHOCYTE;

ALLERGENS; BENZENESULFONATES; CELLS, CULTURED; DENDRITIC CELLS; DERMATITIS, CONTACT; DINITROCHLOROBENZENE; HUMANS; LYMPHOCYTE ACTIVATION; PEPTIDE FRAGMENTS; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; T-LYMPHOCYTES;

EID: 77956898865     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfq209     Document Type: Article

References (45)

1. Aleksic, M., Pease, C. K., Basketter, D. A., Panico, M., Morris, H. R., and Dell, A. (2007). Investigating protein haptenation mechanisms of skin sensitisers using human serum albumin as a model protein. Toxicol. In Vitro 21, 723-733.
2. Aleksic, M., Pease, C. K., Basketter, D. A., Panico, M., Morris, H. R., and Dell, A. (2008). Mass spectrometric identification of covalent adducts of the skin allergen 2,4-dinitro-1-chlorobenzene and model skin proteins. Toxicol. In Vitro 22, 1169-1176.
3. Aleksic, M., Thain, E., Roger, D., Saib, O., Davies, M., Li, J., Aptula, A., and Zazzeroni, R. (2009). Reactivity profiling: covalent modification of single nucleophile peptides for skin sensitization risk assessment. Toxicol. Sci. 108, 401-411.
4. Askenase, P. W., Szczepanik, M., Itakura, A., Kiener, C., and Campos, R. A. (2004). Extravascular T-cell recruitment requires initiation begun by Valpha14+ NKT cells and B-1 B cells. Trends Immunol. 25, 441-449.
5. Basketter, D. A., Dearman, R. J., Hilton, J., and Kimber, I. (1997). Dinitrohalobenzenes: evaluation of relative skin sensitization potential using the local lymph node assay. Contact Dermatitis 36, 97-100.
6. Blum, H., Beier, H., and Gross, H. J. (1987). Improved silver staining of plant proteins, RNA and DNA in polyacrylamide gels. Electrophoresis 8, 93-99.
7. Brander, C., Mauri-Hellweg, D., Bettens, F., Rolli, H., Goldman, M., and Pichler, W. J. (1995). Heterogeneous T cell responses to beta-lactam- modified self-structures are observed in penicillin-allergic individuals. J. Immunol. 155, 2670-2678.
8. Bruchhausen, S., Zahn, S., Valk, E., Knop, J., and Becker, D. (2003). Thiol antioxidants block the activation of antigen-presenting cells by contact sensitizers. J. Invest. Dermatol. 121, 1039-1044.
9. Cavani, A. (2008). T regulatory cells in contact hypersensitivity. Curr. Opin. Allergy Clin. Immunol. 8, 294-298.
10. Dormeyer, W., Ott, M., and Schnolzer, M. (2005). Probing lysine acetylation in proteins: strategies, limitations, and pitfalls of in vitro acetyltransferase assays. Mol. Cell. Proteomics 4, 1226-1239.
11. Eilstein,J., Gimenez-Arnau, E., Duche, D.,Cavusoglu,N., Hussler,G.,Rousset, F., and Lepoittevin, J. P. (2008). Sensitization to p-amino aromatic compounds: study of the covalent binding of 2,5-dimethyl-p-benzoquinonediimine to a model peptide by electrospray ionization tandem mass spectrometry. Bioorg. Med. Chem. 16, 5482-5489.
12. Freudenberg, M. A., Esser, P. R., Jakob, T., Galanos, C., and Martin, S. F. (2009). Innate and adaptive immune responses in contact dermatitis: analogy with infections. G. Ital. Dermatol. Venereol. 144, 173-185.
13. Geiger, R., Duhen, T., Lanzavecchia, A., and Sallusto, F. (2009). Human naive and memory CD4+ T cell repertoires specific for naturally processed antigens analyzed using libraries of amplified T cells. J. Exp. Med. 206, 1525-1534.
14. Gerberick, G. F., Vassallo, J. D., Bailey, R. E., Chaney, J. G., Morrall, S. W., and Lepoittevin, J. P. (2004). Development of a peptide reactivity assay for screening contact allergens. Toxicol. Sci. 81, 332-343.
15. Gerberick, G. F., Vassallo, J. D., Foertsch, L. M., Price, B. B., Chaney, J. G., and Lepoittevin, J. P. (2007). Quantification of chemical peptide reactivity for screening contact allergens: a classification tree model approach. Toxicol. Sci. 97, 417-427.
16. Guironnet,G.,Dalbiez-Gauthier,C.,Rousset,F.,Schmitt,D.,and Peguet-Navarro, J. (2000). In vitro human T cell sensitization to haptens by monocyte-derived dendritic cells. Toxicol. In Vitro 14, 517-522.
17. Hirota, M., Suzuki, M., Hagino, S., Kagatani, S., Sasaki, Y., Aiba, S., and Itagaki, H. (2009). Modification of cell-surface thiols elicits activation of human monocytic cell line THP-1: possible involvement in effect of haptens 2,4-dinitrochlorobenzene and nickel sulfate. J. Toxicol. Sci. 34, 139-150.
18. Jenkinson, C., Jenkins, R. E., Aleksic, M., Pirmohamed, M., Naisbitt, D. J., and Park, B. K. (2010). Characterization of p-phenylenediamine-albumin binding sites and T-cell responses to hapten-modified protein. J. Invest. Dermatol. 130, 732-742.
19. Kagatani, S., Sasaki, Y., Hirota, M., Mizuashi, M., Suzuki, M., Ohtani, T., Itagaki, H., and Aiba, S. (2010). Oxidation of cell surface thiol groups by contact sensitizers triggers the maturation of dendritic cells. J. Invest. Dermatol. 130, 175-183.
20. Karlberg, A. T., Bergstrom, M. A., Borje, A., Luthman, K., and Nilsson, J. L. (2008). Allergic contact dermatitis-formation, structural requirements, and reactivity of skin sensitizers. Chem. Res. Toxicol. 21, 53-69.
21. Krasteva, M., Peguet-Navarro, J., Moulon, C., Courtellemont, P., Redziniak, G., and Schmitt, D. (1996). In vitro primary sensitization of hapten-specific T cells by cultured human epidermal Langerhans cells-a screening predictive assay for contact sensitizers. Clin. Exp. Allergy 26, 563-570.
22. Lepoittevin, J. P. (2006). Molecular aspects of allergic contact dermatitis. In Contact Dermatitis,4th ed.(P. J. Frosch, T. Menne, and J. P. Lepoittevin, Eds.), pp. 45-68. Springer-Verlag, Heidelberg, Germany.
23. Martin, S., Ortmann, B., Pflugfelder, U., Birsner, U., and Weltzien, H. U. (1992). Role of hapten-anchoring peptides in defining hapten-epitopes for MHC-restricted cytotoxic T cells. Cross-reactive TNP-determinants on different peptides. J. Immunol. 149, 2569-2575.
24. Martin, S., von Bonin, A., Fessler, C., Pflugfelder, U., and Weltzien, H. U. (1993). Structural complexity of antigenic determinants for class I MHC- restricted, hapten-specific T cells. Two qualitatively differing types of H-2Kb-restricted TNP epitopes. J. Immunol. 151, 678-687.
25. Martin, S. F. (2004). T lymphocyte-mediated immune responses to chemical haptens and metal ions: implications for allergic and autoimmune disease. Int. Arch. Allergy Immunol. 134, 186-198.
26. Martin, S. F., Esser, P., Schmucker, S., Dietz, L., Naisbitt, D. J., Park, B. K., Vocanson, M., Nicolas, J. F., Keller, M., Pichler, W. J., et al. T cell recognition of chemicals, protein allergens and drugs: towards the development of in vitro assays. Cell Mol. Life. Sci. (Forthcoming).
27. Martin, S. F., Merfort, I., and Thierse, H. J. (2006). Interactions of chemicals and metal ions with proteins and role for immune responses. Mini Rev. Med. Chem. 6, 247-255.
28. Megherbi, R., Kiorpelidou, E., Foster, B., Rowe, C., Naisbitt, D. J., Goldring, C. E., and Park, B. K. (2009). Role of protein haptenation in triggering maturation events in the dendritic cell surrogate cell line THP-1. Toxicol. Appl. Pharmacol. 238, 120-132.
29. Moulon, C., Vollmer, J., and Weltzien, H. U. (1995). Characterization of processing requirements and metal cross-reactivities in T cell clones from patients with allergic contact dermatitis to nickel. Eur. J. Immunol. 25, 3308-3315.
30. Natsch, A., and Gfeller, H. (2008). LC-MS-based characterization of the peptide reactivity of chemicals to improve the in vitro prediction of the skin sensitization potential. Toxicol. Sci. 106, 464-478.
31. Ohman, H., and Vahlquist, A. (1994). In vivo studies concerning a pH gradient in human stratum corneum and upper epidermis. Acta Derm. Venereol. 74, 375-379.
32. Ortmann, B., Martin, S., von Bonin, A., Schiltz, E., Hoschutzky, H., and Weltzien, H. U. (1992). Synthetic peptides anchor T cell-specific TNP epitopes to MHC antigens. J. Immunol. 148, 1445-1450.
33. Padovan, E., Bauer, T., Tongio, M. M., Kalbacher, H., and Weltzien, H. U. (1997). Penicilloyl peptides are recognized as T cell antigenic determinants in penicillin allergy. Eur. J. Immunol. 27, 1303-1307.
34. Padovan, E., Mauri-Hellweg, D., Pichler, W. J., and Weltzien, H. U. (1996). T cell recognition of penicillin G: structural features determining antigenic specificity. Eur. J. Immunol. 26, 42-48.
35. Pickard, C., Louafi, F., McGuire, C., Lowings, K., Kumar, P., Cooper, H., Dearman, R. J., Cumberbatch, M., Kimber, I., Healy, E., et al. (2009). The cutaneous biochemical redox barrier: a component of the innate immune defenses against sensitization by highly reactive environmental xenobiotics. J. Immunol. 183, 7576-7584.
36. Pickard, C., Smith, A. M., Cooper, H., Strickland, I., Jackson, J., Healy, E., and Friedmann, P. S. (2007). Investigation of mechanisms underlying the T-cell response to the hapten 2,4-dinitrochlorobenzene. J. Invest. Dermatol. 127, 630-637.
37. Rustemeyer, T., van Hoogstraten, I. M. W., von Blomberg, B. M., and Scheper, R. J. (2006). Mechanisms in allergic contact dermatitis. In Contact Dermatitis (P. J. Frosch, T. Menne, and J. P. Lepoittevin, Eds.). Springer-Verlag, Berlin, Germany.
38. Sallusto, F. (2001). Origin and migratory properties of dendritic cells in the skin. Curr. Opin. Allergy Clin. Immunol. 1, 441-448.
39. Sallusto, F., Mackay, C. R., and Lanzavecchia, A. (2000). The role of chemokine receptors in primary, effector, and memory immune responses. Annu. Rev. Immunol. 18, 593-620.
40. Smith Pease, C. K. (2003). From xenobiotic chemistry and metabolism to better prediction and risk assessment of skin allergy. Toxicology 192, 1-22.
41. Suzuki, M., Hirota, M., Hagino, S., Itagaki, H., and Aiba, S. (2009). Evaluation of changes of cell-surface thiols as a new biomarker for in vitro sensitization test. Toxicol. In Vitro 23, 687-696.
42. Thierse, H. J., Gamerdinger, K., Junkes, C., Guerreiro, N., and Weltzien, H. U. (2005). T cell receptor (TCR) interaction with haptens: metal ions as non-classical haptens. Toxicology 209, 101-107.
43. Thierse, H. J., Moulon, C., Allespach, Y., Zimmermann, B., Doetze, A., Kuppig, S., Wild, D., Herberg, F., and Weltzien, H. U. (2004). Metal-protein complex-mediated transport and delivery of Ni2+ to TCR/MHC contact sites in nickel-specific human T cell activation. J. Immunol. 172, 1926-1934.
44. Vocanson, M., Cluzel-Tailhardat, M., Poyet, G., Valeyrie, M., Chavagnac, C., Levarlet, B., Courtellemont, P., Rozieres, A., Hennino, A., and Nicolas, J. F. (2008). Depletion of human peripheral blood lymphocytes in CD25+ cells allows for the sensitive in vitro screening of contact allergens. J. Invest. Dermatol. 128, 2119-2122.
45. Weltzien, H. U., and Padovan, E. (1998). Molecular features of penicillin allergy. J. Invest. Dermatol. 110, 203-206.