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PMID: 10049941 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Cytotoxicity is mandatory for CD8(+) T cell-mediated contact hypersensitivity.

The Journal of experimental medicine ·Vol. 189 ·No. 5 ·1999-03-01 ·Pages 779-86

Kehren J, Desvignes C, Krasteva M, Ducluzeau MT, Assossou O, Horand F, Hahne M, Kägi D, Kaiserlian D, Nicolas JF

Abstract

Contact hypersensitivity (CHS) is a T cell-mediated skin inflammation induced by epicutaneous exposure to haptens in sensitized individuals. We have previously reported that CHS to dinitrofluorobenzene in mice is mediated by major histocompatibility complex (MHC) class I-restricted CD8(+) T cells. In this study, we show that CD8(+) T cells mediate the skin inflammation through their cytotoxic activity. The contribution of specific cytotoxic T lymphocytes (CTLs) to the CHS reaction was examined both in vivo and in vitro, using mice deficient in perforin and/or Fas/Fas ligand (FasL) pathways involved in cytotoxicity. Mice double deficient in perforin and FasL were able to develop hapten-specific CD8(+) T cells in the lymphoid organs but did not show CHS reaction. However, they did not generate hapten-specific CTLs, demonstrating that the CHS reaction is dependent on cytotoxic activity. In contrast, Fas-deficient lpr mice, FasL-deficient gld mice, and perforin-deficient mice developed a normal CHS reaction and were able to generate hapten-specific CTLs, suggesting that CHS requires either the Fas/FasL or the perforin pathway. This was confirmed by in vitro studies showing that the hapten-specific CTL activity was exclusively mediated by MHC class I-restricted CD8(+) T cells which could use either the perforin or the Fas/FasL pathway for their lytic activity. Thus, cytotoxic CD8(+) T cells, commonly implicated in the host defence against tumors and viral infections, could also mediate harmful delayed-type hypersensitivity reactions.

MeSH Terms
Animals CD8-Positive T-Lymphocytes/immunology Cell Movement Cytotoxicity, Immunologic Dermatitis, Contact/etiology,genetics,immunology Dinitrofluorobenzene/immunology Fas Ligand Protein Haptens Histocompatibility Antigens Class I/genetics,immunology Histocompatibility Antigens Class II/genetics,immunology Interferon-gamma/biosynthesis Lymphoid Tissue/immunology Membrane Glycoproteins/deficiency,genetics Mice Mice, Inbred C57BL Mice, Knockout Perforin Pore Forming Cytotoxic Proteins Skin/immunology fas Receptor/genetics
Chemicals
Fas Ligand Protein Fasl protein, mouse Haptens Histocompatibility Antigens Class I Histocompatibility Antigens Class II Membrane Glycoproteins Pore Forming Cytotoxic Proteins fas Receptor Perforin Interferon-gamma Dinitrofluorobenzene
Authors & Affiliations
10 authors, click to expand affiliations / ORCID
Kehren J
Institut National de la Santé et de la Recherche Médicale (INSERM) U503, Faculté Laennec, F-69372 Lyon Cedex 08, France.
Desvignes C
Krasteva M
Ducluzeau M T
Assossou O
Horand F
Hahne M
Kägi D
Kaiserlian D
Nicolas J F
References (38)
38 references, click to expand
  1. H-2-restricted cytotoxic effectors generated in vitro by the addition of trinitrophenyl-conjugated soluble proteins.
    J Exp Med. 1978 Feb 1;147(2):352-68 PMID: 75237
  2. CELLULAR AND VASCULAR COMPONENTS OF ALLERGIC CONTACT DERMATITIS.
    Am J Pathol. 1963 Dec;43:1031-53 PMID: 14099450
  3. Roles of CD4+ and CD8+ T cells in murine contact sensitivity revealed by in vivo monoclonal antibody depletion.
    J Immunol. 1990 Jun 1;144(11):4121-8 PMID: 1971294
  4. Normal development of mice deficient in beta 2M, MHC class I proteins, and CD8+ T cells.
    Science. 1990 Jun 8;248(4960):1227-30 PMID: 2112266
  5. Mice lacking MHC class II molecules.
    Cell. 1991 Sep 6;66(5):1051-66 PMID: 1909605
  6. The dendritic cell system and its role in immunogenicity.
    Annu Rev Immunol. 1991;9:271-96 PMID: 1910679
  7. Early molecular events in the induction phase of contact sensitivity.
    Proc Natl Acad Sci U S A. 1992 Feb 15;89(4):1398-402 PMID: 1741395
  8. Fas involvement in Ca(2+)-independent T cell-mediated cytotoxicity.
    J Exp Med. 1993 Jan 1;177(1):195-200 PMID: 7678113
  9. Early time course of recruitment of immune surveillance in human skin after chemical provocation.
    Clin Exp Immunol. 1993 Mar;91(3):351-6 PMID: 8443959
  10. Nickel chloride and cobalt chloride, two common contact sensitizers, directly induce expression of intercellular adhesion molecule-1 (ICAM-1), vascular cell adhesion molecule-1 (VCAM-1), and endothelial leukocyte adhesion molecule (ELAM-1) by endothelial cells.
    J Invest Dermatol. 1993 Jun;100(6):759-65 PMID: 7684425
  11. Differential cytokine expression in maternal blood and placenta during murine gestation.
    J Immunol. 1994 Mar 1;152(5):2411-20 PMID: 8133052
  12. Cytotoxicity mediated by T cells and natural killer cells is greatly impaired in perforin-deficient mice.
    Nature. 1994 May 5;369(6475):31-7 PMID: 8164737
  13. Optimization of the mouse ear swelling test for in vivo and in vitro studies of weak contact sensitizers.
    Contact Dermatitis. 1994 Apr;30(4):231-7 PMID: 8033550
  14. Fas and perforin pathways as major mechanisms of T cell-mediated cytotoxicity.
    Science. 1994 Jul 22;265(5171):528-30 PMID: 7518614
  15. Cytolytic T-cell cytotoxicity is mediated through perforin and Fas lytic pathways.
    Nature. 1994 Aug 25;370(6491):650-2 PMID: 7520535
  16. T cell recognition of haptens, a molecular view.
    Int Arch Allergy Immunol. 1994 May;104(1):10-6 PMID: 7524836
  17. A null mutation in the perforin gene impairs cytolytic T lymphocyte- and natural killer cell-mediated cytotoxicity.
    Proc Natl Acad Sci U S A. 1994 Nov 22;91(24):11571-5 PMID: 7972104
  18. Migration of skin-homing T cells across cytokine-activated human endothelial cell layers involves interaction of the cutaneous lymphocyte-associated antigen (CLA), the very late antigen-4 (VLA-4), and the lymphocyte function-associated antigen-1 (LFA-1).
    J Immunol. 1995 Feb 15;154(4):1543-50 PMID: 7836740
  19. The CTL's kiss of death.
    Cell. 1995 Apr 7;81(1):9-12 PMID: 7536631
  20. Effect of gene-targeted mutation in TNF receptor (p55) on contact hypersensitivity and ultraviolet B-induced immunosuppression.
    J Immunol. 1995 Oct 15;155(8):3801-5 PMID: 7561085
  21. Role of interferon-gamma in contact hypersensitivity assessed in interferon-gamma receptor-deficient mice.
    Toxicology. 1995 Sep 18;102(3):301-12 PMID: 7482569
  22. Major histocompatibility complex class I-restricted CD8+ T cells and class II-restricted CD4+ T cells, respectively, mediate and regulate contact sensitivity to dinitrofluorobenzene.
    Eur J Immunol. 1995 Nov;25(11):3006-10 PMID: 7489735
  23. Interferon-gamma-dependent stimulation of Fas antigen in SV40-transformed human keratinocytes: modulation of the apoptotic process by protein kinase C.
    J Invest Dermatol. 1995 Dec;105(6):810-5 PMID: 7490476
  24. Cytotoxic T cells deficient in both functional fas ligand and perforin show residual cytolytic activity yet lose their capacity to induce lethal acute graft-versus-host disease.
    J Exp Med. 1996 Feb 1;183(2):657-61 PMID: 8627178
  25. T cell populations primed by hapten sensitization in contact sensitivity are distinguished by polarized patterns of cytokine production: interferon gamma-producing (Tc1) effector CD8+ T cells and interleukin (Il) 4/Il-10-producing (Th2) negative regulatory CD4+ T cells.
    J Exp Med. 1996 Mar 1;183(3):1001-12 PMID: 8642241
  26. Interferon-gamma inducible protein (IP-10) expression is mediated by CD8+ T cells and is regulated by CD4+ T cells during the elicitation of contact hypersensitivity.
    J Invest Dermatol. 1996 Sep;107(3):360-6 PMID: 8751971
  27. Immune and inflammatory responses in TNF alpha-deficient mice: a critical requirement for TNF alpha in the formation of primary B cell follicles, follicular dendritic cell networks and germinal centers, and in the maturation of the humoral immune response.
    J Exp Med. 1996 Oct 1;184(4):1397-411 PMID: 8879212
  28. Decreased tumor surveillance in perforin-deficient mice.
    J Exp Med. 1996 Nov 1;184(5):1781-90 PMID: 8920866
  29. Cytokine gene expression during the elicitation phase of contact sensitivity: regulation by endogenous IL-4.
    J Invest Dermatol. 1997 Apr;108(4):406-11 PMID: 9077467
  30. MHC class I+/II- dendritic cells induce hapten-specific immune responses in vitro and in vivo.
    J Invest Dermatol. 1997 Oct;109(4):580-5 PMID: 9326394
  31. Cutaneous lymphocyte antigen is a specialized form of PSGL-1 expressed on skin-homing T cells.
    Nature. 1997 Oct 30;389(6654):978-81 PMID: 9353122
  32. Immunoregulatory mechanisms involved in elicitation of allergic contact hypersensitivity.
    Immunol Today. 1998 Jan;19(1):37-44 PMID: 9465487
  33. CD8+ T cells clear influenza virus by perforin or Fas-dependent processes.
    J Immunol. 1997 Dec 1;159(11):5197-200 PMID: 9548456
  34. Dual role of dendritic cells in the induction and down-regulation of antigen-specific cutaneous inflammation.
    J Immunol. 1998 Feb 1;160(3):1181-90 PMID: 9570532
  35. The chemokine family. Potential therapeutic targets from allergy to HIV infection.
    Eur J Dermatol. 1998 Apr-May;8(3):147-57 PMID: 9649701
  36. Intralesional cytokines in chronic oxazolone-induced contact sensitivity suggest roles for tumor necrosis factor alpha and interleukin-4.
    J Invest Dermatol. 1998 Jul;111(1):86-92 PMID: 9665392
  37. Contact dermatitis I. Pathophysiology of contact sensitivity.
    Eur J Dermatol. 1999 Jan-Feb;9(1):65-77 PMID: 9920992
  38. Two types of murine helper T cell clone. II. Delayed-type hypersensitivity is mediated by TH1 clones.
    J Immunol. 1987 Jun 1;138(11):3688-94 PMID: 2953788
Article Info
Journal
The Journal of experimental medicine
Abbr.
J Exp Med
ISSN
0022-1007
Published
1999-03-01
Pages
779-86
Language
English
Region
United States
NLM ID
2985109R
PMCID
PMC2192953
Subset
IM
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