Advertisement

Acquired Immunity in Metal Allergy: T Cell Responses

  • By Trine Hilkjær Petersen
  • Carsten Geisler
  • Charlotte Menné Bonefeld
Chapter

Abstract

Allergies to metals are common, with nickel allergy being the most frequent form of contact allergy. Contact allergies are classified as delayed-type hypersensitivity reactions in which T cells are the key players. In this chapter, we describe how metals are presented to T cells and discuss the current literature on the role of CD4+ and CD8+ T cells in contact allergies to metals.

Keywords

CD4+ T cells CD8+ T cells IFN-γ IL-17A IL-10 

References

  1. 1.
    Schmidt M, Goebeler M. Immunology of metal allergies. J Dtsch Dermatol Ges. 2015;13:653–9.PubMedGoogle Scholar
  2. 2.
    Vocanson M, Hennino A, Rozières A, Poyet G, Nicolas JF. Effector and regulatory mechanisms in allergic contact dermatitis. Allergy. 2009;64:1699–714.CrossRefGoogle Scholar
  3. 3.
    Martin S, Esser P, Weber F. Mechanisms of chemical-induced innate immunity in allergic contact dermatitis. Allergy. 2011;66:1152–63.CrossRefGoogle Scholar
  4. 4.
    Kaplan DH, Igyártó BZ, Gaspari AA. Early immune events in the induction of allergic contact dermatitis. Nat Rev Immunol. 2012;12:114–24.CrossRefGoogle Scholar
  5. 5.
    Thierse H-J, Gamerdinger K, Junkes C, Guerreiro N, Weltzien HU. T cell receptor (TCR) interaction with haptens: metal ions as non-classical haptens. Toxicology. 2005;209:101–7.CrossRefGoogle Scholar
  6. 6.
    Sinigaglia F, Scheidegger D, Garotta G, Scheper R, Pletscher M, Lanzavecchia A. Isolation and characterization of Ni-specific T cell clones from patients with Ni-contact dermatitis. J Immunol. 1985;135:3929–32.PubMedGoogle Scholar
  7. 7.
    Kapsenberg ML, Res P, Bos JD, Schootemijer A, Teunissen MB, Van Schooten W. Nickel-specific T lymphocyte clones derived from allergic nickel-contact dermatitis lesions in man: heterogeneity based on requirement of dendritic antigen-presenting cell subsets. Eur J Immunol. 1987;17:861–5.CrossRefGoogle Scholar
  8. 8.
    Moulon C, Vollmer J, Weltzien HU. Characterization of processing requirements and metal cross-reactivities in T cell clones from patients with allergic contact dermatitis to nickel. Eur J Immunol. 1995;25:3308–15.CrossRefGoogle Scholar
  9. 9.
    Büdinger L, Hertl M. Immunologic mechanisms in hypersensitivity reactions to metal ions: an overview. Allergy. 2000;55:108–15.CrossRefGoogle Scholar
  10. 10.
    Sinigaglia F. The molecular basis of metal recognition by T cells. J Invest Dermatol. 1994;102:398–401.CrossRefGoogle Scholar
  11. 11.
    Romagnoli P, Labhardt AM, Sinigaglia F. Selective interaction of Ni with an MHC-bound peptide. EMBO J. 1991;10:1303–6.PubMedPubMedCentralGoogle Scholar
  12. 12.
    Romagnoli P, Spinas GA, Sinigaglia F. Gold-specific T cells in rheumatoid arthritis patients treated with gold. J Clin Invest. 1992;89:254–8.CrossRefGoogle Scholar
  13. 13.
    Griem P. The antirheumatic drug disodium aurothiomalate inhibits CD4+ T cell recognition of peptides containing two or more cysteine residues. J Immunol. 1995;155(3):1575–87.PubMedGoogle Scholar
  14. 14.
    Lu L, Vollmer J, Moulon C, Weltzien HU, Marrack P, Kappler J. Components of the ligand for a Ni++ reactive human T cell clone. J Exp Med. 2003;197:567–74.CrossRefGoogle Scholar
  15. 15.
    Vollmer J, Fritz M, Dormoy A, Weltzien HU, Moulon C. Dominance of the BV17 element in nickel-specific human T cell receptors relates to severity of contact sensitivity. Eur J Immunol. 1997;27:1865–74.CrossRefGoogle Scholar
  16. 16.
    Büdinger L, Neuser N, Totzke U, Merk HF, Hertl M. Preferential usage of TCR-Vbeta17 by peripheral and cutaneous T cells in nickel-induced contact dermatitis. J Immunol. 2001;167:6038–44.CrossRefGoogle Scholar
  17. 17.
    Wang Y, Dai S. Structural basis of metal hypersensitivity. Immunol Res. 2013;55:83–90.CrossRefGoogle Scholar
  18. 18.
    Yin L, Crawford F, Marrack P, Kappler JW, Dai S. T-cell receptor (TCR) interaction with peptides that mimic nickel offers insight into nickel contact allergy. Proc Natl Acad Sci U S A. 2012;109:18517–22.CrossRefGoogle Scholar
  19. 19.
    Weltzien HU, Martin SF, Nicolas J-F. T cell responses to contact allergens. In: Martin FS, editor. T lymphocytes as tools in diagnostics and immunotoxicology. Basel: Springer; 2014. p. 41–9.CrossRefGoogle Scholar
  20. 20.
    Gamerdinger K, Moulon C, Karp DR, Van Bergen J, Koning F, Wild D, Pflugfelder U, Weltzien HU. A new type of metal recognition by human T cells: contact residues for peptide-independent bridging of T cell receptor and major histocompatibility complex by nickel. J Exp Med. 2003;197:1345–53.CrossRefGoogle Scholar
  21. 21.
    Thierse H-J, Moulon C, Allespach Y, Zimmermann B, Doetze A, Kuppig S, Wild D, Herberg F, Weltzien HU. Metal-protein complex-mediated transport and delivery of Ni2+ to TCR/MHC contact sites in nickel-specific human T cell activation. J Immunol. 2004;172:1926–34.CrossRefGoogle Scholar
  22. 22.
    Griem P, Panthel K, Kalbacher H. Alteration of a model antigen by Au(III) leads to T cell sensitization to cryptic peptides. Eur J Immunol. 1996;26(2):279–87.CrossRefGoogle Scholar
  23. 23.
    Griem P, Von Vultée C, Panthel K, Best SL, Sadler PJ, Shaw CF. T cell cross-reactivity to heavy metals: identical cryptic peptides may be presented from protein exposed to different metals. Eur J Immunol. 1998;28:1941–7.CrossRefGoogle Scholar
  24. 24.
    De Wall SL, Painter C, Stone JD, Bandaranayake R, Wiley DC, Mitchison TJ, Stern LJ, DeDecker BS. Noble metals strip peptides from class II MHC proteins. Nat Chem Biol. 2006;2:197–201.CrossRefGoogle Scholar
  25. 25.
    Clayton GM, Wang Y, Crawford F, Novikov A, Wimberly BT, Kieft JS, Falta MT, Bowerman NA, Marrack P, Fontenot AP, Dai S, Kappler JW. Structural basis of chronic beryllium disease: linking allergic hypersensitivity and autoimmunity. Cell. 2014;158:132–42.CrossRefGoogle Scholar
  26. 26.
    Rogers PR, Croft M. Peptide dose, affinity, and time of differentiation can contribute to the Th1/Th2 cytokine balance. J Immunol. 1999;163:1205–13.PubMedGoogle Scholar
  27. 27.
    Kapsenberg ML, Wierenga EA, Stiekema FE, Tiggelman AM, Bos JD. Th1 lymphokine production profiles of nickel-specific CD4+T-lymphocyte clones from nickel contact allergic and non-allergic individuals. J Invest Dermatol. 1992;98:59–63.CrossRefGoogle Scholar
  28. 28.
    Werfel T, Hentschel M, Kapp A, Renz H. Dichotomy of blood- and skin derived IL-4-producing allergen-specific T cells and restricted Vb repertoire in nickel-mediated contact dermatitis. J Immunol. 1997;158:2500–5.PubMedGoogle Scholar
  29. 29.
    Borg L, Molin J, Kristiansen J, Henrik N. Nickel-induced cytokine production from mononuclear cells in nickel-sensitive individuals and controls with nickel allergy-related hand eczema before and after nickel challenge. Arch Dermatol Res. 2000;292(6):285–91.CrossRefGoogle Scholar
  30. 30.
    Rustemeyer T, von Blomberg BME, van Hoogstraten IMW, Bruynzeel DP, Scheper RJ. Analysis of effector and regulatory immune reactivity to nickel. Clin Exp Allergy. 2004;34:1458–66.CrossRefGoogle Scholar
  31. 31.
    Minang JT, Troye-Blomberg M, Lundeberg L, Ahlborg N. Nickel elicits concomitant and correlated in vitro production of Th1-, Th2-type and regulatory cytokines in subjects with contact allergy to nickel. Scand J Immunol. 2005;62:289–96.CrossRefGoogle Scholar
  32. 32.
    Minang JT, Areström I, Troye-Blomberg M, Lundeberg L, Ahlborg N. Nickel, cobalt, chromium, palladium and gold induce a mixed Th1- and Th2-type cytokine response in vitro in subjects with contact allergy to the respective metals. Clin Exp Immunol. 2006;146:417–26.CrossRefGoogle Scholar
  33. 33.
    Muris J, Feilzer AJ, Kleverlaan CJ, Rustemeyer T, Van Hoogstraten IMW, Scheper RJ, Von Blomberg BME. Palladium-induced Th2 cytokine responses reflect skin test reactivity. Allergy. 2012;67:1605–8.PubMedGoogle Scholar
  34. 34.
    Cavani A, Mei D, Guerra E, Corinti S. Patients with allergic contact dermatitis to nickel and nonallergic individuals display different nickel-specific T cell responses. Evidence for the presence of effector. J Invest Dermatol. 1998;111:621–8.CrossRefGoogle Scholar
  35. 35.
    Moulon C, Wild D, Dormoy A, Weltzien HU. MHC-dependent and -independent activation of human nickel-specific CD8+ cytotoxic T cells from allergic donors. J Invest Dermatol. 1998;111:360–6.CrossRefGoogle Scholar
  36. 36.
    Traidl C, Sebastiani S, Albanesi C, Merk HF, Puddu P, Girolomoni G, Cavani A. Disparate cytotoxic activity of nickel-specific CD8+ and CD4+ T cell subsets against keratinocytes. J Immunol. 2000;165:3058–64.CrossRefGoogle Scholar
  37. 37.
    Moed H, Boorsma DM, Stoof TJ, Von Blomberg BME, Bruynzeel DP, Scheper RJ, Gibbs S, Rustemeyer T. Nickel-responding T cells are CD4+ CLA+ CB45RO+ and express chemokine receptors CXCR3, CCR4 and CCR10. Br J Dermatol. 2004;151:32–41.CrossRefGoogle Scholar
  38. 38.
    Minang JT, Arestrom I, Zuber B, Jonsson G, Troye-Blomberg M, Ahlborg N. Nickel-induced IL-10 down-regulates Th1- but not Th2-type cytokine responses to the contact allergen nickel. Clin Exp Immunol. 2006;143:494–502.CrossRefGoogle Scholar
  39. 39.
    Dyring-Andersen B, Skov L, Løvendorf MB, Bzorek M, Søndergaard K, Lauritsen J-PH, Dabelsteen S, Geisler C, Bonefeld CM. CD4(+) T cells producing interleukin (IL)-17, IL-22 and interferon-γ are major effector T cells in nickel allergy. Contact Dermatitis. 2013;68:339–47.CrossRefGoogle Scholar
  40. 40.
    Schmidt JD, Ahlström MG, Johansen JD, Dyring-Andersen B, Agerbeck C, Nielsen MM, Poulsen SS, Woetmann A, Ødum N, Thomsen AR, Geisler C, Bonefeld CM. Rapid allergen-induced IL-17 and IFN-gamma secretion by skin-resident memory CD8+ T cells. Contact Dermatitis. 2016;76(4):218–27.CrossRefGoogle Scholar
  41. 41.
    Albanesi C, Cavani A, Girolomoni G. IL-17 is produced by nickel-specific T lymphocytes and regulates ICAM-1 expression and chemokine production in human keratinocytes: synergistic or antagonist effects with IFN-gamma and TNF-alpha. J Immunol. 1999;162:494–502.PubMedGoogle Scholar
  42. 42.
    Albanesi C, Scarponi C, Cavani A, Federici M, Nasorri F, Girolomoni G. Interleukin-17 is produced by both Th1 and Th2 lymphocytes, and modulates interferon-gamma- and interleukin-4-induced activation of human keratinocytes. J Invest Dermatol. 2000;115:81–7.CrossRefGoogle Scholar
  43. 43.
    Larsen JM, Bonefeld CM, Poulsen SS, Geisler C, Skov L. IL-23 and T(H)17-mediated inflammation in human allergic contact dermatitis. J Allergy Clin Immunol. 2009;123:486–92.CrossRefGoogle Scholar
  44. 44.
    Pennino D, Eyerich K, Scarponi C, Carbone T, Eyerich S, Nasorri F, Garcovich S, Traidl-Hoffmann C, Albanesi C, Cavani A. IL-17 amplifies human contact hypersensitivity by licensing hapten nonspecific Th1 cells to kill autologous keratinocytes. J Immunol. 2010;184:4880–8.CrossRefGoogle Scholar
  45. 45.
    Ricciardi L, Minciullo PL, Saitta S, Trombetta D, Saija A, Gangemi S. Increased serum levels of IL-22 in patients with nickel contact dermatitis. Contact Dermatitis. 2009;60:57–8.CrossRefGoogle Scholar
  46. 46.
    Watanabe H, Gaide O, Pétrilli V, Martinon F, Contassot E, Roques S, Kummer JA, Tschopp J, French LE. Activation of the IL-1beta-processing inflammasome is involved in contact hypersensitivity. J Invest Dermatol. 2007;127:1956–63.CrossRefGoogle Scholar
  47. 47.
    Li X, Zhong F. Nickel induces interleukin-1β secretion via the NLRP3-ASC-caspase-1 pathway. Inflammation. 2014;37:457–66.CrossRefGoogle Scholar
  48. 48.
    Vennegaard MT, Dyring-Andersen B, Skov L, Nielsen MM, Schmidt JD, Bzorek M, Poulsen SS, Thomsen AR, Woetmann A, Thyssen JP, Johansen JD, Odum N, Menné T, Geisler C, Bonefeld CM. Epicutaneous exposure to nickel induces nickel allergy in mice via a MyD88-dependent and interleukin-1-dependent pathway. Contact Dermatitis. 2014;71:224–32.CrossRefGoogle Scholar
  49. 49.
    Cho K-A, Suh JW, Lee KH, Kang JL, Woo S-Y. IL-17 and IL-22 enhance skin inflammation by stimulating the secretion of IL-1beta by keratinocytes via the ROS-NLRP3-caspase-1 pathway. Int Immunol. 2012;24:147–58.CrossRefGoogle Scholar
  50. 50.
    Nielsen MM, Lovato P, MacLeod AS, Witherden DA, Skov L, Dyring-Andersen B, Dabelsteen S, Woetmann A, Ødum N, Havran WL, Geisler C, Bonefeld CM. IL-1β-dependent activation of dendritic epidermal T cells in contact hypersensitivity. J Immunol. 2014;192:2975–83.CrossRefGoogle Scholar
  51. 51.
    Dhingra N, Shemer A, Correa Da Rosa J, Rozenblit M, Fuentes-Duculan J, Gittler JK, Finney R, Czarnowicki T, Zheng X, Xu H, Estrada YD, Cardinale I, Suárez-Fariñas M, Krueger JG, Guttman-Yassky E. Molecular profiling of contact dermatitis skin identifies allergen-dependent differences in immune response. J Allergy Clin Immunol. 2014;134:362–72.CrossRefGoogle Scholar
  52. 52.
    Diepgen TL, Ofenloch RF, Bruze M, Bertuccio P, Cazzaniga S, Coenraads P-J, Elsner P, Goncalo M, Svensson Å, Naldi L. Prevalence of contact allergy in the general population in different European regions. Br J Dermatol. 2016;174:319–29.CrossRefGoogle Scholar
  53. 53.
    Van Hoogstraten IM, Andersen KE, Von Blomberg BM, Boden D, Bruynzeel DP, Burrows D, Camarasa JG, Dooms-Goossens A, Kraal G, Lahti A. Reduced frequency of nickel allergy upon oral nickel contact at an early age. Clin Exp Immunol. 1991;85:441–5.CrossRefGoogle Scholar
  54. 54.
    Cavani A, Nasorri F, Ottaviani C, Sebastiani S, De Pita O, Girolomoni G. Human CD25+ regulatory T cells maintain immune tolerance to nickel in healthy, nonallergic individuals. J Immunol. 2003;171:5760–8.CrossRefGoogle Scholar
  55. 55.
    van Hoogstraten IM, Boden D, von Blomberg ME, Kraal G, Scheper RJ. Persistent immune tolerance to nickel and chromium by oral administration prior to cutaneous sensitization. J Invest Dermatol. 1992;99:608–16.CrossRefGoogle Scholar
  56. 56.
    Van Hoogstraten IM, Boos C, Boden D, Von Blomberg ME, Scheper RJ, Kraal G. Oral induction of tolerance to nickel sensitization in mice. J Invest Dermatol. 1993;101:26–31.CrossRefGoogle Scholar
  57. 57.
    Ishii N, Moriguchi N, Nakajima H, Tanaka S, Amemiya F. Nickel sulfate-specific suppressor T cells induced by nickel sulfate in drinking water. J Dermatol Sci. 1993;6:159–64.CrossRefGoogle Scholar
  58. 58.
    Artik S, Haarhuis K, Wu X, Begerow J, Gleichmann E. Tolerance to nickel: oral nickel administration induces a high frequency of anergic T cells with persistent suppressor activity. J Immunol. 2001;167:6794–803.CrossRefGoogle Scholar
  59. 59.
    Roelofs-Haarhuis K, Wu X, Nowak M, Fang M, Artik S, Gleichmann E. Infectious nickel tolerance: a reciprocal interplay of tolerogenic APCs and T suppressor cells that is driven by immunization. J Immunol. 2003;171:2863–72.CrossRefGoogle Scholar
  60. 60.
    Roelofs-Haarhuis K, Wu X, Gleichmann E. Oral tolerance to nickel requires CD4+ invariant NKT cells for the infectious spread of tolerance and the induction of specific regulatory T cells. J Immunol. 2004;173:1043–50.CrossRefGoogle Scholar
  61. 61.
    Nowak M, Kopp F, Roelofs-Haarhuis K, Wu X, Gleichmann E. Oral nickel tolerance: Fas ligand-expressing invariant NK T cells promote tolerance induction by eliciting apoptotic death of antigen-carrying, effete B cells. J Immunol. 2006;176:4581–9.CrossRefGoogle Scholar
  62. 62.
    Wu X, Roelofs-Haarhuis K, Zhang J, Nowak M, Layland L, Jermann E, Gleichmann E. Dose dependence of oral tolerance to nickel. Int Immunol. 2007;19:965–75.CrossRefGoogle Scholar
  63. 63.
    Cavani A, Nasorri F, Prezzi C, Sebastiani S, Albanesi C, Girolomoni G. Human CD4+ T lymphocytes with remarkable regulatory functions on dendritic cells and nickel-specific Th1 immune responses. J Invest Dermatol. 2000;114:295–302.CrossRefGoogle Scholar
  64. 64.
    Xu H, DiIulio N, Fairchild R. T cell populations primed by hapten sensitization in contact sensitivity are distinguished by polarized patterns of cytokine production: interferon gamma-producing (Tc1). J Exp Med. 1996;183:1001–12.CrossRefGoogle Scholar
  65. 65.
    Liu J, Harberts E, Tammaro A, Girardi N, Filler RB, Fishelevich R, Temann A, Licona-Limón P, Girardi M, Flavell RA, Gaspari AA. IL-9 regulates allergen-specific Th1 responses in allergic contact dermatitis. J Invest Dermatol. 2014;134:1903–11.CrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • By Trine Hilkjær Petersen
    • 1
  • Carsten Geisler
    • 1
  • Charlotte Menné Bonefeld
    • 1
  1. 1.Department of Immunology and Microbiology, Faculty of Health and Medical SciencesUniversity of CopenhagenCopenhagenDenmark

Personalised recommendations