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. 1998 Jan;93(1):11–19. doi: 10.1046/j.1365-2567.1998.00408.x

Antigen direction of specific T-cell clones into gingival tissues.

T Kawai 1, H Shimauchi 1, J W Eastcott 1, D J Smith 1, M A Taubman 1
PMCID: PMC1364100  PMID: 9536113

Abstract

This study was performed to investigate T-cell traffic to periodontal tissues during infection with a periodontal pathogen Actinobacillus actinomycetemcomitans (Aa). Rowett rat T-cell clones, A3 (CD4+ CD8-, alpha beta TCR+, NKRP-1-, specific to Aa) and G2 (CD4- CD8-, alpha beta TCR+, NKRP-1+, which reacts to Aa, Gram-negative and -positive bacteria), both expressed the same prominent adhesion molecules (LFA-1, VLA-4) to the same extent. Binding of both T-cell clones to rat endothelial cells in vitro was blocked by antibody to VLA-4. Rowett rats were infected with Aa and infused with Aa-stimulated, isogenic T-clone lymphocytes that had been labelled in vitro with 125IUdR. Radioactivity associated with recovery of clone A3, but not G2, was significantly elevated in the gingivae of infected rats, suggesting migration to infected animals' gingival tissues. Migration of radioactive Aa-specific A3 clone cells traced by autoradiography reached a maximum at 24 hr (1.2% of total lymphocytes as radiolabelled cells in infected gingiva versus 0.6% in noninfected), indicating an apparent antigen-directed retention in infected rats' gingival tissues. The G2 clone was not retained in the gingival tissues (0.20% of total lymphocytes as radiolabelled cells in infected gingiva versus 0.26% in non-infected). However, the possibility of A3 retention directed by inflammation or tissue-selective homing could not be excluded. In further experiments, other adoptively transferred T-clone lymphocytes [clones G23 (Th1) and F13 (Th2)] with specificity for the 29,000 MW outer membrane protein of Aa with the same prominent adhesion molecules could be recovered from rat gingivae previously challenged with this antigen. However, transferred T-clone lymphocytes [clone G26 (Th1)] with specificity for a different Aa antigen were not recovered. Therefore, the dynamics of cell entry into periodontal lesions vary for activated T lymphocytes with different antigenic specificities, indicating the significance of antigen in lymphocyte traffic to periodontal tissues.

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Selected References

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

  1. Berman M. E., Xie Y., Muller W. A. Roles of platelet/endothelial cell adhesion molecule-1 (PECAM-1, CD31) in natural killer cell transendothelial migration and beta 2 integrin activation. J Immunol. 1996 Feb 15;156(4):1515–1524. [PubMed] [Google Scholar]
  2. Butcher E. C., Picker L. J. Lymphocyte homing and homeostasis. Science. 1996 Apr 5;272(5258):60–66. doi: 10.1126/science.272.5258.60. [DOI] [PubMed] [Google Scholar]
  3. Butcher E. C. The regulation of lymphocyte traffic. Curr Top Microbiol Immunol. 1986;128:85–122. doi: 10.1007/978-3-642-71272-2_3. [DOI] [PubMed] [Google Scholar]
  4. Dunkley M. L., Husband A. J. Distribution and functional characteristics of antigen-specific helper T cells arising after Peyer's patch immunization. Immunology. 1987 Aug;61(4):475–482. [PMC free article] [PubMed] [Google Scholar]
  5. Dunkley M. L., Husband A. J. Role of antigen in migration patterns of T cell subsets arising from gut-associated lymphoid tissue. Reg Immunol. 1989 Jul-Aug;2(4):213–224. [PubMed] [Google Scholar]
  6. Dunkley M. L., Husband A. J. The induction and migration of antigen-specific helper cells for IgA responses in the intestine. Immunology. 1986 Mar;57(3):379–385. [PMC free article] [PubMed] [Google Scholar]
  7. Dunkley M. L., Husband A. J. The role of non-B cells in localizing an IgA plasma cell response in the intestine. Reg Immunol. 1990;3(6):336–340. [PubMed] [Google Scholar]
  8. Eastcott J. W., Yamashita K., Taubman M. A., Harada Y., Smith D. J. Adoptive transfer of cloned T helper cells ameliorates periodontal disease in nude rats. Oral Microbiol Immunol. 1994 Oct;9(5):284–289. doi: 10.1111/j.1399-302x.1994.tb00072.x. [DOI] [PubMed] [Google Scholar]
  9. Eastcott J. W., Yamashita K., Taubman M. A., Smith D. J. Characterization of rat T-cell clones with bacterial specificity. Immunology. 1990 Sep;71(1):120–126. [PMC free article] [PubMed] [Google Scholar]
  10. Ford W. L., Gowans J. L. The traffic of lymphocytes. Semin Hematol. 1969 Jan;6(1):67–83. [PubMed] [Google Scholar]
  11. Husband A. J., Dunkley M. L., Cripps A. W., Clancy R. L. Antigen-specific response among T lymphocytes following intestinal administration of alloantigens. Aust J Exp Biol Med Sci. 1984 Dec;62(Pt 6):687–699. doi: 10.1038/icb.1984.65. [DOI] [PubMed] [Google Scholar]
  12. Husband A. J. Kinetics of extravasation and redistribution of IgA-specific antibody-containing cells in the intestine. J Immunol. 1982 Mar;128(3):1355–1359. [PubMed] [Google Scholar]
  13. Issekutz T. B. Dual inhibition of VLA-4 and LFA-1 maximally inhibits cutaneous delayed-type hypersensitivity-induced inflammation. Am J Pathol. 1993 Nov;143(5):1286–1293. [PMC free article] [PubMed] [Google Scholar]
  14. Mackay C. R., Marston W. L., Dudler L. Naive and memory T cells show distinct pathways of lymphocyte recirculation. J Exp Med. 1990 Mar 1;171(3):801–817. doi: 10.1084/jem.171.3.801. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Mackay C. R. T-cell memory: the connection between function, phenotype and migration pathways. Immunol Today. 1991 Jun;12(6):189–192. doi: 10.1016/0167-5699(91)90051-T. [DOI] [PubMed] [Google Scholar]
  16. Oppenheimer-Marks N., Davis L. S., Bogue D. T., Ramberg J., Lipsky P. E. Differential utilization of ICAM-1 and VCAM-1 during the adhesion and transendothelial migration of human T lymphocytes. J Immunol. 1991 Nov 1;147(9):2913–2921. [PubMed] [Google Scholar]
  17. Perry M. B., MacLean L. L., Gmür R., Wilson M. E. Characterization of the O-polysaccharide structure of lipopolysaccharide from Actinobacillus actinomycetemcomitans serotype b. Infect Immun. 1996 Apr;64(4):1215–1219. doi: 10.1128/iai.64.4.1215-1219.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Picker L. J., Butcher E. C. Physiological and molecular mechanisms of lymphocyte homing. Annu Rev Immunol. 1992;10:561–591. doi: 10.1146/annurev.iy.10.040192.003021. [DOI] [PubMed] [Google Scholar]
  19. Picker L. J., Terstappen L. W., Rott L. S., Streeter P. R., Stein H., Butcher E. C. Differential expression of homing-associated adhesion molecules by T cell subsets in man. J Immunol. 1990 Nov 15;145(10):3247–3255. [PubMed] [Google Scholar]
  20. Pierce N. F. The role of antigen form and function in the primary and secondary intestinal immune responses to cholera toxin and toxoid in rats. J Exp Med. 1978 Jul 1;148(1):195–206. doi: 10.1084/jem.148.1.195. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Pietschmann P., Cush J. J., Lipsky P. E., Oppenheimer-Marks N. Identification of subsets of human T cells capable of enhanced transendothelial migration. J Immunol. 1992 Aug 15;149(4):1170–1178. [PubMed] [Google Scholar]
  22. Pollack A., Bagwell C. B., Irvin G. L., 3rd Radiation from tritiated thymidine perturbs the cell cycle progression of stimulated lymphocytes. Science. 1979 Mar 9;203(4384):1025–1027. doi: 10.1126/science.424727. [DOI] [PubMed] [Google Scholar]
  23. Rose M. L., Parrott D. M., Bruce R. G. I. Effect of Trichinella spiralis infection on the migration of mesenteric lymphoblasts and mesenteric T lymphoblasts in syngeneic mice. Immunology. 1976 Nov;31(5):723–730. [PMC free article] [PubMed] [Google Scholar]
  24. Seymour G. J., Gemmell E., Reinhardt R. A., Eastcott J., Taubman M. A. Immunopathogenesis of chronic inflammatory periodontal disease: cellular and molecular mechanisms. J Periodontal Res. 1993 Nov;28(6 Pt 2):478–486. doi: 10.1111/j.1600-0765.1993.tb02108.x. [DOI] [PubMed] [Google Scholar]
  25. Seymour G. J., Taubman M. A., Eastcott J. W., Gemmell E., Smith D. J. CD29 expression on CD4+ gingival lymphocytes supports migration of activated memory T lymphocytes to diseased periodontal tissue. Oral Microbiol Immunol. 1997 Jun;12(3):129–134. doi: 10.1111/j.1399-302x.1997.tb00368.x. [DOI] [PubMed] [Google Scholar]
  26. Springer T. A. Traffic signals for lymphocyte recirculation and leukocyte emigration: the multistep paradigm. Cell. 1994 Jan 28;76(2):301–314. doi: 10.1016/0092-8674(94)90337-9. [DOI] [PubMed] [Google Scholar]
  27. Wilson M. E., Hamilton R. G. Immunoglobulin G subclass response of juvenile periodontitis subjects to principal outer membrane proteins of Actinobacillus actinomycetemcomitans. Infect Immun. 1995 Mar;63(3):1062–1069. doi: 10.1128/iai.63.3.1062-1069.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Yamamoto T., Yoneda K., Osaki T., Yoshimura N., Akagi N. Longer local retention of adoptively transferred T-LAK cells correlates with lesser adhesion molecule expression than NK-LAK cells. Clin Exp Immunol. 1995 Apr;100(1):13–20. doi: 10.1111/j.1365-2249.1995.tb03597.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Yamashita K., Eastcott J. W., Taubman M. A., Smith D. J., Cox D. S. Effect of adoptive transfer of cloned Actinobacillus actinomycetemcomitans-specific T helper cells on periodontal disease. Infect Immun. 1991 Apr;59(4):1529–1534. doi: 10.1128/iai.59.4.1529-1534.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Yoshie H., Taubman M. A., Ebersole J. L., Olson C. L., Smith D. J., Pappo J. Activation of rat B lymphocytes by Actinobacillus actinomycetemcomitans. Infect Immun. 1985 Jan;47(1):264–270. doi: 10.1128/iai.47.1.264-270.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Yoshie H., Taubman M. A., Ebersole J. L., Smith D. J., Olson C. L. Periodontal bone loss and immune characteristics of congenitally athymic and thymus cell-reconstituted athymic rats. Infect Immun. 1985 Nov;50(2):403–408. doi: 10.1128/iai.50.2.403-408.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Yoshie H., Taubman M. A., Ebersole J. L., Smith D. J., Olson C. L. Periodontal bone loss and immune characteristics of congenitally athymic and thymus cell-reconstituted athymic rats. Infect Immun. 1985 Nov;50(2):403–408. doi: 10.1128/iai.50.2.403-408.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]

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