Skip to main content
PMC home page
The Journal of Experimental Medicine logoLink to The Journal of Experimental Medicine
. 1990 Apr 1;171(4):1027–1041. doi: 10.1084/jem.171.4.1027

Loss of epidermal integrity by T cell-mediated attack induces long-term local resistance to subsequent attack. I. Induction of resistance correlates with increases in Thy-1+ epidermal cell numbers

PMCID: PMC2187841  PMID: 1969918

Abstract

The cutaneous graft-versus-host disease (GVHD) lesions induced by intradermal injection of cloned autoreactive T cells have been shown to subside rapidly and the epidermis returns to normal 2 wk after injection. Those mice that had spontaneously recovered from the cutaneous GVHD became resistant to subsequent attempts to induce the cutaneous GVHD by the T cells while maintaining their activity to mount delayed-type hypersensitivity (DTH) responses and to induce the enlargement of the popliteal lymph nodes (PLN). The resistance appeared to be restricted to the epidermal structures of the injection sites, suggesting the involvement of locally acting suppression mechanisms. This local resistance was not specific for the clonotype used for the induction of the resistance. A loss of the epidermal integrity by an attack of T cells capable of producing cutaneous GVHD was a prerequisite for the induction of the resistance. By up to at least 8 mo after injection of the T cells, no mice became susceptible to the cutaneous GVHD again, provided that the T cells were injected into the same footpad sites that had initially received the T cells. This resistance correlated well with the great increase (20-30-fold) in Thy- 1+ EC number. The great increase in the number of Thy-1+ EC following destruction of epidermal structures may be important in protecting the epidermal integrity from an additional attack by T cells.

Full Text

The Full Text of this article is available as a PDF (1.1 MB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Asarnow D. M., Kuziel W. A., Bonyhadi M., Tigelaar R. E., Tucker P. W., Allison J. P. Limited diversity of gamma delta antigen receptor genes of Thy-1+ dendritic epidermal cells. Cell. 1988 Dec 2;55(5):837–847. doi: 10.1016/0092-8674(88)90139-0. [DOI] [PubMed] [Google Scholar]
  2. Bandeira A., Coutinho A., Carnaud C., Jacquemart F., Forni L. Transplantation tolerance correlates with high levels of T- and B-lymphocyte activity. Proc Natl Acad Sci U S A. 1989 Jan;86(1):272–276. doi: 10.1073/pnas.86.1.272. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bluestone J. A., Matis L. A. TCR gamma delta cells--minor redundant T cell subset or specialized immune system component? J Immunol. 1989 Mar 15;142(6):1785–1788. [PubMed] [Google Scholar]
  4. Caspi R. R., Roberge F. G., Nussenblatt R. B. Organ-resident, nonlymphoid cells suppress proliferation of autoimmune T-helper lymphocytes. Science. 1987 Aug 28;237(4818):1029–1032. doi: 10.1126/science.2956685. [DOI] [PubMed] [Google Scholar]
  5. Ellerman K. E., Powers J. M., Brostoff S. W. A suppressor T-lymphocyte cell line for autoimmune encephalomyelitis. Nature. 1988 Jan 21;331(6153):265–267. doi: 10.1038/331265a0. [DOI] [PubMed] [Google Scholar]
  6. Gaspari A. A., Jenkins M. K., Katz S. I. Class II MHC-bearing keratinocytes induce antigen-specific unresponsiveness in hapten-specific Th1 clones. J Immunol. 1988 Oct 1;141(7):2216–2220. [PubMed] [Google Scholar]
  7. Glucksberg H., Storb R., Fefer A., Buckner C. D., Neiman P. E., Clift R. A., Lerner K. G., Thomas E. D. Clinical manifestations of graft-versus-host disease in human recipients of marrow from HL-A-matched sibling donors. Transplantation. 1974 Oct;18(4):295–304. doi: 10.1097/00007890-197410000-00001. [DOI] [PubMed] [Google Scholar]
  8. Goodman T., Lefrançois L. Expression of the gamma-delta T-cell receptor on intestinal CD8+ intraepithelial lymphocytes. Nature. 1988 Jun 30;333(6176):855–858. doi: 10.1038/333855a0. [DOI] [PubMed] [Google Scholar]
  9. Kimura H., Pickard A., Wilson D. B. Analysis of T cell populations that induce and mediate specific resistance to graft-versus-host disease in rats. J Exp Med. 1984 Sep 1;160(3):652–658. doi: 10.1084/jem.160.3.652. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Koning F., Stingl G., Yokoyama W. M., Yamada H., Maloy W. L., Tschachler E., Shevach E. M., Coligan J. E. Identification of a T3-associated gamma delta T cell receptor on Thy-1+ dendritic epidermal Cell lines. Science. 1987 May 15;236(4803):834–837. doi: 10.1126/science.2883729. [DOI] [PubMed] [Google Scholar]
  11. Kosmatopoulos K., Scott-Algara D., Cabannes J., Orbach-Arbouys S. Specific and nonspecific resistance to local graft-versus-host reaction in F1 hybrids pretreated intravenously with parent-strain spleen cells. I. Two distinct mechanisms. Transplantation. 1987 Aug;44(2):267–273. doi: 10.1097/00007890-198708000-00018. [DOI] [PubMed] [Google Scholar]
  12. Lerner K. G., Kao G. F., Storb R., Buckner C. D., Clift R. A., Thomas E. D. Histopathology of graft-vs.-host reaction (GvHR) in human recipients of marrow from HL-A-matched sibling donors. Transplant Proc. 1974 Dec;6(4):367–371. [PubMed] [Google Scholar]
  13. Lider O., Reshef T., Beraud E., Ben-Nun A., Cohen I. R. Anti-idiotypic network induced by T cell vaccination against experimental autoimmune encephalomyelitis. Science. 1988 Jan 8;239(4836):181–183. doi: 10.1126/science.2447648. [DOI] [PubMed] [Google Scholar]
  14. Lider O., Reshef T., Beraud E., Ben-Nun A., Cohen I. R. Anti-idiotypic network induced by T cell vaccination against experimental autoimmune encephalomyelitis. Science. 1988 Jan 8;239(4836):181–183. doi: 10.1126/science.2447648. [DOI] [PubMed] [Google Scholar]
  15. Nixon-Fulton J. L., Hackett J., Jr, Bergstresser P. R., Kumar V., Tigelaar R. E. Phenotypic heterogeneity and cytotoxic activity of Con A and IL-2-stimulated cultures of mouse Thy-1+ epidermal cells. J Invest Dermatol. 1988 Jul;91(1):62–68. doi: 10.1111/1523-1747.ep12463290. [DOI] [PubMed] [Google Scholar]
  16. Perez M., Edelson R., Laroche L., Berger C. Inhibition of antiskin allograft immunity by infusions with syngeneic photoinactivated effector lymphocytes. J Invest Dermatol. 1989 May;92(5):669–676. doi: 10.1111/1523-1747.ep12696853. [DOI] [PubMed] [Google Scholar]
  17. Piguet P. F., Janin-Mercier A., Vassalli P., Saurat J. H. Epidermal lesions of the GVHR: evaluation of the role of different MHC and non MHC loci and of the Ly-2+ and L3T4+ T lymphocytes. J Immunol. 1987 Jul 15;139(2):406–410. [PubMed] [Google Scholar]
  18. Raulet D. H. Immunology. Antigens for gamma/delta T cells. Nature. 1989 Jun 1;339(6223):342–343. doi: 10.1038/339342a0. [DOI] [PubMed] [Google Scholar]
  19. Shiohara T., Moellmann G., Jacobson K., Kuklinska E., Ruddle N. H., Lerner A. B. Anti-tumor activity of class II MHC antigen-restricted cloned autoreactive T cells. II. Novel immunotherapy of B16 melanomas by local and systemic adoptive transfer. J Immunol. 1987 Mar 15;138(6):1979–1986. [PubMed] [Google Scholar]
  20. Shiohara T., Moriya N., Gotoh C., Hayakawa J., Saizawa K., Yagita H., Nagashima M. Differential expression of lymphocyte function-associated antigen 1 (LFA-1) on epidermotropic and non-epidermotropic T-cell clones. J Invest Dermatol. 1989 Dec;93(6):804–808. doi: 10.1111/1523-1747.ep12284430. [DOI] [PubMed] [Google Scholar]
  21. Shiohara T., Moriya N., Gotoh C., Saizawa K., Nagashima M. Locally administered monoclonal antibodies to lymphocyte function-associated antigen 1 and to L3T4 prevent cutaneous graft-vs-host disease. J Immunol. 1988 Oct 1;141(7):2261–2267. [PubMed] [Google Scholar]
  22. Shiohara T., Moriya N., Mochizuki T., Nagashima M. Lichenoid tissue reaction (LTR) induced by local transfer of Ia-reactive T-cell clones. II. LTR by epidermal invasion of cytotoxic lymphokine-producing autoreactive T cells. J Invest Dermatol. 1987 Jul;89(1):8–14. [PubMed] [Google Scholar]
  23. Shiohara T., Narimatsu H., Nagashima M. Induction of cutaneous graft-versus-host disease by allo- or self-Ia-reactive helper T cells in mice. Transplantation. 1987 May;43(5):692–698. doi: 10.1097/00007890-198705000-00018. [DOI] [PubMed] [Google Scholar]
  24. Shiohara T., Ruddle N. H., Horowitz M., Moellmann G. E., Lerner A. B. Anti-tumor activity of class II MHC antigen-restricted cloned autoreactive T cells. I. Destruction of B16 melanoma cells mediated by bystander cytolysis in vitro. J Immunol. 1987 Mar 15;138(6):1971–1978. [PubMed] [Google Scholar]
  25. Takagaki Y., DeCloux A., Bonneville M., Tonegawa S. Diversity of gamma delta T-cell receptors on murine intestinal intra-epithelial lymphocytes. Nature. 1989 Jun 29;339(6227):712–714. doi: 10.1038/339712a0. [DOI] [PubMed] [Google Scholar]

Articles from The Journal of Experimental Medicine are provided here courtesy of The Rockefeller University Press

RESOURCES