The Journal of Allergy and Clinical Immunology
Volume 119, Issue 6 , Pages 1470-1480 , June 2007

Chemokine responses distinguish chemical-induced allergic from irritant skin inflammation: Memory T cells make the difference

  • Stephan Meller, MD

      Affiliations

    • From the Department of Dermatology, Heinrich-Heine-University, Düsseldorf
    • These authors contributed equally to this work.
  • ,
  • Antti I. Lauerma, MD, PhD

      Affiliations

    • Control of Hypersensitivity Diseases, Finnish Institute of Occupational Health, Helsinki
    • These authors contributed equally to this work.
  • ,
  • Frank Michael Kopp, PhD

      Affiliations

    • Institute of Environmental Research, Heinrich-Heine University, Düsseldorf
    • These authors contributed equally to this work.
  • ,
  • Franziska Winterberg, PhD

      Affiliations

    • From the Department of Dermatology, Heinrich-Heine-University, Düsseldorf
    • These authors contributed equally to this work.
  • ,
  • Minna Anthoni, PhD

      Affiliations

    • Control of Hypersensitivity Diseases, Finnish Institute of Occupational Health, Helsinki
  • ,
  • Anja Müller, MD

      Affiliations

    • Department of Radiation Oncology, Heinrich-Heine University, Düsseldorf
  • ,
  • Michael Gombert, PhD

      Affiliations

    • From the Department of Dermatology, Heinrich-Heine-University, Düsseldorf
  • ,
  • Anna Haahtela, PhD

      Affiliations

    • Skin and Allergy Hospital, Helsinki University Central Hospital
  • ,
  • Harri Alenius, PhD

      Affiliations

    • Centre of Excellence in Immunotoxicology, Finnish Institute of Occupational Health, Helsinki
  • ,
  • Juliane Rieker, MD

      Affiliations

    • From the Department of Dermatology, Heinrich-Heine-University, Düsseldorf
  • ,
  • Marie-Caroline Dieu-Nosjean, PhD

      Affiliations

    • Institut National de la Santé et de la Recherche Médicale Unité 255, Laboratoire d'Immunologie Cellulaire et Clinique, Centre de Recherches Biomédicales des Cordeliers, Paris
  • ,
  • Robert Christof Kubitza

      Affiliations

    • From the Department of Dermatology, Heinrich-Heine-University, Düsseldorf
  • ,
  • Ernst Gleichmann, MD

      Affiliations

    • Institute of Environmental Research, Heinrich-Heine University, Düsseldorf
  • ,
  • Thomas Ruzicka, MD

      Affiliations

    • From the Department of Dermatology, Heinrich-Heine-University, Düsseldorf
  • ,
  • Albert Zlotnik, PhD

      Affiliations

    • Neurocrine Bioscience, San Diego
  • ,
  • Bernhard Homey, MD

      Affiliations

    • From the Department of Dermatology, Heinrich-Heine-University, Düsseldorf
    • Corresponding Author InformationReprint requests: Bernhard Homey, MD, Department of Dermatology, Heinrich-Heine-University, Moorenstr. 5, D-40225 Düsseldorf, Germany.

Received 9 August 2006 ,Revised 22 November 2006 ,Accepted 12 December 2006.

References 

  1. Chew AL, Maibach HI. Occupational issues of irritant contact dermatitis. Int Arch Occup Environ Health. 2003;76:339–346
  2. Levin CY, Maibach HI. Irritant contact dermatitis: is there an immunologic component?. Int Immunopharmacol. 2002;2:183–189
  3. Chew AL. Biologic similarities of irritation and allergic contact dermatitis. In:  Chew AL,  Maibach HI editor. Irritant dermatitis. Berlin: Springer; 2006;
  4. Corsini E, Galli CL. Epidermal cytokines in experimental contact dermatitis. Toxicology. 2000;142:203–211
  5. Saint-Mezard P, Rosieres A, Krasteva M, Berard F, Dubois B, Kaiserlian D, et al. Allergic contact dermatitis. Eur J Dermatol. 2004;14:284–295
  6. Muller A, Homey B, Soto H, Ge N, Catron D, Buchanan ME, et al. Involvement of chemokine receptors in breast cancer metastasis. Nature. 2001;410:50–56
  7. Homey B, Alenius H, Muller A, Soto H, Bowman EP, Yuan W, et al. CCL27-CCR10 interactions regulate T cell-mediated skin inflammation. Nat Med. 2002;8:157–165
  8. Baggiolini M. Chemokines and leukocyte traffic. Nature. 1998;392:565–568
  9. Zlotnik A, Yoshie O. Chemokines: a new classification system and their role in immunity. Immunity. 2000;12:121–127
  10. Fregert S. Manual of contact dermatitis. 2nd ed.. Copenhagen, Denmark: Munksgaard; 1981;
  11. Homey B, Wang W, Soto H, Buchanan ME, Wiesenborn A, Catron D, et al. Cutting edge: the orphan chemokine receptor G protein-coupled receptor-2 (GPR-2, CCR10) binds the skin-associated chemokine CCL27 (CTACK/ALP/ILC). J Immunol. 2000;164:3465–3470
  12. 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
  13. Artik S, von Vultee C, Gleichmann E, Schwarz T, Griem P. Nickel allergy in mice: enhanced sensitization capacity of nickel at higher oxidation states. J Immunol. 1999;163:1143–1152
  14. Morales J, Homey B, Vicari AP, Hudak S, Oldham E, Hedrick J, et al. CTACK, a skin-associated chemokine that preferentially attracts skin-homing memory T cells. Proc Natl Acad Sci U S A. 1999;96:14470–14475
  15. Gombert M, Dieu-Nosjean MC, Winterberg F, Bunemann E, Kubitza RC, Da Cunha L, et al. CCL1-CCR8 interactions: an axis mediating the recruitment of T cells and Langerhans-type dendritic cells to sites of atopic skin inflammation. J Immunol. 2005;174:5082–5091
  16. Tibshirani R, Hastie T, Narasimhan B, Chu G. Diagnosis of multiple cancer types by shrunken centroids of gene expression. Proc Natl Acad Sci U S A. 2002;99:6567–6572
  17. Zlotnik A, Morales J, Hedrick JA. Recent advances in chemokines and chemokine receptors. Crit Rev Immunol. 1999;19:1–47
  18. Homey B, Zlotnik A. Chemokines in allergy. Curr Opin Immunol. 1999;11:626–634
  19. Kim CH, Rott L, Kunkel EJ, Genovese MC, Andrew DP, Wu L, et al. Rules of chemokine receptor association with T cell polarization in vivo. J Clin Invest. 2001;108:1331–1339
  20. Sallusto F, Lenig D, Mackay CR, Lanzavecchia A. Flexible programs of chemokine receptor expression on human polarized T helper 1 and 2 lymphocytes. J Exp Med. 1998;187:875–883
  21. Flier J, Boorsma DM, Bruynzeel DP, Van Beek PJ, Stoof TJ, Scheper RJ, et al. The CXCR3 activating chemokines IP-10, Mig, and IP-9 are expressed in allergic but not in irritant patch test reactions. J Invest Dermatol. 1999;113:574–578
  22. Goebeler M, Trautmann A, Voss A, Brocker EV, Toksoy A, Gillitzer R. Differential and sequential expression of multiple chemokines during elicitation of allergic contact hypersensitivity. Am J Pathol. 2001;158:431–440
  23. Moed H, Boorsma DM, Stoof TJ, von Blomberg BM, Bruynzeel DP, Scheper RJ, et al. Nickel-responding T cells are CD4+ CLA+ CD45RO+ and express chemokine receptors CXCR3, CCR4 and CCR10. Br J Dermatol. 2004;151:32–41
  24. Cole KE, Strick CA, Paradis TJ, Ogborne KT, Loetscher M, Gladue RP, et al. Interferon-inducible T cell alpha chemoattractant (I-TAC): a novel non-ELR CXC chemokine with potent activity on activated T cells through selective high affinity binding to CXCR3. J Exp Med. 1998;187:2009–2021
  25. Farber JM. Mig and IP-10: CXC chemokines that target lymphocytes. J Leukoc Biol. 1997;61:246–257
  26. Abbas AK, Murphy KM, Sher A. Functional diversity of helper T lymphocytes. Nature. 1996;383:787–793
  27. Wakabayashi T, Hu DL, Tagawa Y, Sekikawa K, Iwakura Y, Hanada K, et al. IFN-gamma and TNF-alpha are involved in urushiol-induced contact hypersensitivity in mice. Immunol Cell Biol. 2005;83:18–24
  28. Dufour JH, Dziejman M, Liu MT, Leung JH, Lane TE, Luster AD. IFN-gamma-inducible protein 10 (IP-10; CXCL10)-deficient mice reveal a role for IP-10 in effector T cell generation and trafficking. J Immunol. 2002;168:3195–3204
  29. Lehto M, Koivuluhta M, Wang G, Amghaiab I, Majuri ML, Savolainen K, et al. Epicutaneous natural rubber latex sensitization induces T helper 2-type dermatitis and strong prohevein-specific IgE response. J Invest Dermatol. 2003;120:633–640
  30. Imai T, Nagira M, Takagi S, Kakizaki M, Nishimura M, Wang J, et al. Selective recruitment of CCR4-bearing Th2 cells toward antigen-presenting cells by the CC chemokines thymus and activation-regulated chemokine and macrophage-derived chemokine. Int Immunol. 1999;11:81–88
  31. Bonecchi R, Sozzani S, Stine JT, Luini W, D'Amico G, Allavena P, et al. Divergent effects of interleukin-4 and interferon-gamma on macrophage-derived chemokine production:an amplification circuit of polarized T helper 2 responses. Blood. 1998;92:2668–2671
  32. Xiao T, Fujita H, Saeki H, Mitsui H, Sugaya M, Tada Y, et al. Thymus and activation-regulated chemokine (TARC/CCL17) produced by mouse epidermal Langerhans cells is upregulated by TNF-alpha and IL-4 and downregulated by IFN-gamma. Cytokine. 2003;23:126–132
  33. Mantovani A, Gray PA, Van Damme J, Sozzani S. Macrophage-derived chemokine (MDC). J Leukoc Biol. 2000;68:400–404
  34. Werfel T, Hentschel M, Kapp A, Renz H. Dichotomy of blood- and skin-derived IL-4-producing allergen-specific T cells and restricted V beta repertoire in nickel-mediated contact dermatitis. J Immunol. 1997;158:2500–2505
  35. Liao F, Rabin RL, Smith CS, Sharma G, Nutman TB, Farber JM. CC-chemokine receptor 6 is expressed on diverse memory subsets of T cells and determines responsiveness to macrophage inflammatory protein 3 alpha. J Immunol. 1999;162:186–194
  36. Nakayama T, Fujisawa R, Yamada H, Horikawa T, Kawasaki H, Hieshima K, et al. Inducible expression of a CC chemokine liver- and activation-regulated chemokine (LARC)/macrophage inflammatory protein (MIP)-3 alpha/CCL20 by epidermal keratinocytes and its role in atopic dermatitis. Int Immunol. 2001;13:95–103
  37. Piguet PF, Grau GE, Hauser C, Vassalli P. Tumor necrosis factor is a critical mediator in hapten induced irritant and contact hypersensitivity reactions. J Exp Med. 1991;173:673–679
  38. Vanbervliet B, Bendriss-Vermare N, Massacrier C, Homey B, de Bouteiller O, Briere F, et al. The inducible CXCR3 ligands control plasmacytoid dendritic cell responsiveness to the constitutive chemokine stromal cell-derived factor 1 (SDF-1)/CXCL12. J Exp Med. 2003;198:823–830
  39. Bangert C, Friedl J, Stary G, Stingl G, Kopp T. Immunopathologic features of allergic contact dermatitis in humans: participation of plasmacytoid dendritic cells in the pathogenesis of the disease?. J Invest Dermatol. 2003;121:1409–1418
  40. Wollenberg A, Wagner M, Gunther S, Towarowski A, Tuma E, Moderer M, et al. Plasmacytoid dendritic cells: a new cutaneous dendritic cell subset with distinct role in inflammatory skin diseases. J Invest Dermatol. 2002;119:1096–1102
  41. Sebastiani S, Danelon G, Gerber B, Uguccioni M. CCL22-induced responses are powerfully enhanced by synergy inducing chemokines via CCR4: evidence for the involvement of first beta-strand of chemokine. Eur J Immunol. 2005;35:746–756

 Supported by Contract QLK4-CT-2001-00366 Chemokine-Atopy from the European Commission (to A.I.L., B.H., H.A.) and by Grant SFB503/C9 from the German Research Foundation (to B.H.).Disclosure of potential conflict of interest: The authors have declared that they have no conflict of interest.

PII: S0091-6749(07)00115-7

doi: 10.1016/j.jaci.2006.12.654

The Journal of Allergy and Clinical Immunology
Volume 119, Issue 6 , Pages 1470-1480 , June 2007