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Immunology logoLink to Immunology
. 1991 Oct;74(2):234–239.

Regulation of T-cell sensitization at epithelial surfaces in the respiratory tract: suppression of IgE responses to inhaled antigens by CD3+ Tcr alpha-/beta- lymphocytes (putative gamma/delta T cells).

C McMenamin 1, J Oliver 1, B Girn 1, B J Holt 1, U R Kees 1, W R Thomas 1, P G Holt 1
PMCID: PMC1384598  PMID: 1836199

Abstract

Repeated exposure of Brown Norway rats to an aerosol of ovalbumin (OVA) induced a state of antigen-specific immunological tolerance, particularly in the IgE isotype. Tolerance was transferable to naive syngeneic animals by inoculation of splenic T cells from tolerant rats. Sequential depletion of tolerant spleen cells by sorting techniques prior to adoptive transfer, employing T-cell subset-specific monoclonal antibodies, indicated that the cells mediating tolerance were CD3+, CD4-, CD5+ and CD8+, but lacked alpha or beta chains in the T-cell receptor (TcR), suggesting that they may be part of the gamma/delta T-cell lineage. Consistent with this suggestion, the sorted population demonstrated considerable enrichment for TcR gamma chain-specific mRNA. As few as 2 x 10(3) cells are sufficient to adoptively transfer tolerance in 200-g adult rats in this model.

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Selected References

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

  1. Allwood G. G., Asherson G. L. Depression of delayed hypersensitivity by pretreatment with Freund-type adjuvants. 3. Depressed arrival of lymphoid cells at recently immunized lymph nodes in mice pretreated with adjuvants. Clin Exp Immunol. 1972 Aug;11(4):579–584. [PMC free article] [PubMed] [Google Scholar]
  2. Allwood G. G., Asherson G. L. Depression of delayed hypersensitivity by pretreatment with Freund-type adjuvants. II. Mechanism of the phenomenon. Clin Exp Immunol. 1971 Aug;9(2):259–266. [PMC free article] [PubMed] [Google Scholar]
  3. Augustin A., Kubo R. T., Sim G. K. Resident pulmonary lymphocytes expressing the gamma/delta T-cell receptor. Nature. 1989 Jul 20;340(6230):239–241. doi: 10.1038/340239a0. [DOI] [PubMed] [Google Scholar]
  4. Bonneville M., Janeway C. A., Jr, Ito K., Haser W., Ishida I., Nakanishi N., Tonegawa S. Intestinal intraepithelial lymphocytes are a distinct set of gamma delta T cells. Nature. 1988 Dec 1;336(6198):479–481. doi: 10.1038/336479a0. [DOI] [PubMed] [Google Scholar]
  5. Borst J., van de Griend R. J., van Oostveen J. W., Ang S. L., Melief C. J., Seidman J. G., Bolhuis R. L. A T-cell receptor gamma/CD3 complex found on cloned functional lymphocytes. Nature. 1987 Feb 19;325(6106):683–688. doi: 10.1038/325683a0. [DOI] [PubMed] [Google Scholar]
  6. Carding S. R., Allan W., Kyes S., Hayday A., Bottomly K., Doherty P. C. Late dominance of the inflammatory process in murine influenza by gamma/delta + T cells. J Exp Med. 1990 Oct 1;172(4):1225–1231. doi: 10.1084/jem.172.4.1225. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Chomczynski P., Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem. 1987 Apr;162(1):156–159. doi: 10.1006/abio.1987.9999. [DOI] [PubMed] [Google Scholar]
  8. De Maria A., Malnati M., Moretta A., Pende D., Bottino C., Casorati G., Cottafava F., Melioli G., Mingari M. C., Migone N. CD3+4-8-WT31-(T cell receptor gamma+) cells and other unusual phenotypes are frequently detected among spontaneously interleukin 2-responsive T lymphocytes present in the joint fluid in juvenile rheumatoid arthritis. A clonal analysis. Eur J Immunol. 1987 Dec;17(12):1815–1819. doi: 10.1002/eji.1830171221. [DOI] [PubMed] [Google Scholar]
  9. Fujihashi K., Kiyono H., Aicher W. K., Green D. R., Singh B., Eldridge J. H., McGhee J. R. Immunoregulatory function of CD3+, CD4-, and CD8- T cells. Gamma delta T cell receptor-positive T cells from nude mice abrogate oral tolerance. J Immunol. 1989 Dec 1;143(11):3415–3422. [PubMed] [Google Scholar]
  10. Fujihashi K., Taguchi T., McGhee J. R., Eldridge J. H., Bruce M. G., Green D. R., Singh B., Kiyono H. Regulatory function for murine intraepithelial lymphocytes. Two subsets of CD3+, T cell receptor-1+ intraepithelial lymphocyte T cells abrogate oral tolerance. J Immunol. 1990 Oct 1;145(7):2010–2019. [PubMed] [Google Scholar]
  11. 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]
  12. Hirashima M., Yodoi J., Ishizaka K. Regulatory role of IgE-binding factors from rat T lymphocytes. IV. Formation of IgE-binding factors in rats treated with complete Freund's adjuvant. J Immunol. 1980 Nov;125(5):2154–2160. [PubMed] [Google Scholar]
  13. Holoshitz J., Koning F., Coligan J. E., De Bruyn J., Strober S. Isolation of CD4- CD8- mycobacteria-reactive T lymphocyte clones from rheumatoid arthritis synovial fluid. Nature. 1989 May 18;339(6221):226–229. doi: 10.1038/339226a0. [DOI] [PubMed] [Google Scholar]
  14. Holt P. G., Batty J. E., Turner K. J. Inhibition of specific IgE responses in mice by pre-exposure to inhaled antigen. Immunology. 1981 Mar;42(3):409–417. [PMC free article] [PubMed] [Google Scholar]
  15. Holt P. G., Britten D., Sedgwick J. D. Suppression of IgE responses by antigen inhalation: studies on the role of genetic and environmental factors. Immunology. 1987 Jan;60(1):97–102. [PMC free article] [PubMed] [Google Scholar]
  16. Holt P. G., McMenamin C. Defence against allergic sensitization in the healthy lung: the role of inhalation tolerance. Clin Exp Allergy. 1989 May;19(3):255–262. doi: 10.1111/j.1365-2222.1989.tb02380.x. [DOI] [PubMed] [Google Scholar]
  17. Ishizaka K. IgE-binding factors and regulation of the IgE antibody response. Annu Rev Immunol. 1988;6:513–534. doi: 10.1146/annurev.iy.06.040188.002501. [DOI] [PubMed] [Google Scholar]
  18. Janeway C. A., Jr Frontiers of the immune system. Nature. 1988 Jun 30;333(6176):804–806. doi: 10.1038/333804a0. [DOI] [PubMed] [Google Scholar]
  19. Karlsson T., Ellerson J. R., Haig D. M., Jarrett E. E., Bennich H. A radioimmunoassay for evaluation of the IgE and IgG antibody responses in the rat. Scand J Immunol. 1979 Mar;9(3):229–238. doi: 10.1111/j.1365-3083.1979.tb02726.x. [DOI] [PubMed] [Google Scholar]
  20. Kishimoto T., Hirai Y., Suemura M., Yamamura Y. Regulation of antibody response in different immunoglobulin classes. I. Selective suppression of anti-DNP IgE antibody response by preadministration of DNP-coupled mycobacterium. J Immunol. 1976 Aug;117(2):396–404. [PubMed] [Google Scholar]
  21. Lawetzky A., Tiefenthaler G., Kubo R., Hünig T. Identification and characterization of rat T cell subpopulations expressing T cell receptors alpha/beta and gamma/delta. Eur J Immunol. 1990 Feb;20(2):343–349. doi: 10.1002/eji.1830200217. [DOI] [PubMed] [Google Scholar]
  22. Mason D. W., Arthur R. P., Dallman M. J., Green J. R., Spickett G. P., Thomas M. L. Functions of rat T-lymphocyte subsets isolated by means of monoclonal antibodies. Immunol Rev. 1983;74:57–82. doi: 10.1111/j.1600-065x.1983.tb01084.x. [DOI] [PubMed] [Google Scholar]
  23. Modlin R. L., Pirmez C., Hofman F. M., Torigian V., Uyemura K., Rea T. H., Bloom B. R., Brenner M. B. Lymphocytes bearing antigen-specific gamma delta T-cell receptors accumulate in human infectious disease lesions. Nature. 1989 Jun 15;339(6225):544–548. doi: 10.1038/339544a0. [DOI] [PubMed] [Google Scholar]
  24. Morris M., Barclay A. N., Williams A. F. Analysis of T cell receptor beta chains in rat thymus, and rat C alpha and C beta sequences. Immunogenetics. 1988;27(3):174–179. doi: 10.1007/BF00346583. [DOI] [PubMed] [Google Scholar]
  25. Ohga S., Yoshikai Y., Takeda Y., Hiromatsu K., Nomoto K. Sequential appearance of gamma/delta- and alpha/beta-bearing T cells in the peritoneal cavity during an i.p. infection with Listeria monocytogenes. Eur J Immunol. 1990 Mar;20(3):533–538. doi: 10.1002/eji.1830200311. [DOI] [PubMed] [Google Scholar]
  26. Pauwels R., Bazin H., Platteau B., Van Der Straeten M. In vitro measurement of specific rat IgE antibodies. Ann Immunol (Paris) 1977 Apr-Jun;128C(3):675–685. [PubMed] [Google Scholar]
  27. Rivas A., Takada S., Koide J., Sonderstrup-McDevitt G., Engleman E. G. CD4 molecules are associated with the antigen receptor complex on activated but not resting T cells. J Immunol. 1988 May 1;140(9):2912–2918. [PubMed] [Google Scholar]
  28. Sedgwick J. D., Holt P. G. Down-regulation of immune responses to inhaled antigen: studies on the mechanism of induced suppression. Immunology. 1985 Dec;56(4):635–642. [PMC free article] [PubMed] [Google Scholar]
  29. Sedgwick J. D., Holt P. G. Induction of IgE-isotype specific tolerance by passive antigenic stimulation of the respiratory mucosa. Immunology. 1983 Dec;50(4):625–630. [PMC free article] [PubMed] [Google Scholar]
  30. Sedgwick J. D., Holt P. G. Induction of IgE-secreting cells and IgE isotype-specific suppressor T cells in the respiratory lymph nodes of rats in response to antigen inhalation. Cell Immunol. 1985 Aug;94(1):182–194. doi: 10.1016/0008-8749(85)90095-4. [DOI] [PubMed] [Google Scholar]
  31. Sedgwick J. D., Holt P. G. Suppression of IgE responses in inbred rats by repeated respiratory tract exposure to antigen: responder phenotype influences isotype specificity of induced tolerance. Eur J Immunol. 1984 Oct;14(10):893–897. doi: 10.1002/eji.1830141006. [DOI] [PubMed] [Google Scholar]
  32. Stingl G., Koning F., Yamada H., Yokoyama W. M., Tschachler E., Bluestone J. A., Steiner G., Samelson L. E., Lew A. M., Coligan J. E. Thy-1+ dendritic epidermal cells express T3 antigen and the T-cell receptor gamma chain. Proc Natl Acad Sci U S A. 1987 Jul;84(13):4586–4590. doi: 10.1073/pnas.84.13.4586. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Tada T. Regulation of reaginic antibody formation in animals. Prog Allergy. 1975;19:122–194. [PubMed] [Google Scholar]
  34. Tanaka T., Masuko T., Yagita H., Tamura T., Hashimoto Y. Characterization of a CD3-like rat T cell surface antigen recognized by a monoclonal antibody. J Immunol. 1989 Apr 15;142(8):2791–2795. [PubMed] [Google Scholar]
  35. Tung A. S., Chiorazzi N., Katz D. H. Regulation of IgE antibody production by serum molecules. I. Serum from complete Freund's adjuvant-immune donors suppresses irradiation-enhanced IgE production in low responder mouse strains. J Immunol. 1978 Jun;120(6):2050–2059. [PubMed] [Google Scholar]
  36. Weyand C. M., Goronzy J., Fathman C. G. Modulation of CD4 by antigenic activation. J Immunol. 1987 Mar 1;138(5):1351–1354. [PubMed] [Google Scholar]

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