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. 1995 Feb;84(2):193–201.

Activated rat T cells synthesize and express functional major histocompatibility class II antigens.

C P Broeren 1, M H Wauben 1, M A Lucassen 1, M Van Meurs 1, P J Van Kooten 1, C J Boog 1, E Claassen 1, W Van Eden 1
PMCID: PMC1415087  PMID: 7750994

Abstract

In the present report, we studied the presence and functional significance of major histocompatibility complex (MHC) class II antigen on rat T cells. Most rat T-cell lines cultured in vitro were found to be MHC class II+. Also, these T-cell lines were shown to synthesize MHC class II molecules. Immunohistochemical and flow cytometric double stainings for T-cell receptor (TCR) and MHC class II showed that in vivo as well a large proportion of T cells was MHC class II+. The immunohistochemical staining of spleen sections enabled us to characterize the MHC class II+ and MHC class II- T cells. It was shown that resting T cells in vivo were MHC class II-. In contrast, activated T cells, as determined by their localization in the marginal zone of the spleen, proved to be MHC class II+. Finally, T-cell clones were found to be able to present peptidic antigens, but could only poorly present more complex exogenous antigens, probably due to inefficient uptake of such antigens. These features would endow activated rat T cells with the capacity to present cell-specific self-proteins, such as TCR, to regulatory CD4+ MHC class II-restricted T cells, as was described by our group elsewhere.

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Selected References

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  1. Barnaba V., Watts C., de Boer M., Lane P., Lanzavecchia A. Professional presentation of antigen by activated human T cells. Eur J Immunol. 1994 Jan;24(1):71–75. doi: 10.1002/eji.1830240112. [DOI] [PubMed] [Google Scholar]
  2. Ben-Nun A., Strauss W., Leeman S. A., Cohn L. E., Murre C., Duby A., Seidman J. G., Glimcher L. H. An Ia-positive mouse T-cell clone is functional in presenting antigen to other T cells. Immunogenetics. 1985;22(2):123–130. doi: 10.1007/BF00563509. [DOI] [PubMed] [Google Scholar]
  3. Ben-Nun A., Wekerle H., Cohen I. R. The rapid isolation of clonable antigen-specific T lymphocyte lines capable of mediating autoimmune encephalomyelitis. Eur J Immunol. 1981 Mar;11(3):195–199. doi: 10.1002/eji.1830110307. [DOI] [PubMed] [Google Scholar]
  4. Benoist C., Mathis D. Regulation of major histocompatibility complex class-II genes: X, Y and other letters of the alphabet. Annu Rev Immunol. 1990;8:681–715. doi: 10.1146/annurev.iy.08.040190.003341. [DOI] [PubMed] [Google Scholar]
  5. Bevan D. J., Chisholm P. M. Co-expression of CD4 and CD8 molecules and de novo expression of MHC class II antigens on activated rat T cells. Immunology. 1986 Dec;59(4):621–625. [PMC free article] [PubMed] [Google Scholar]
  6. Boog C. J., de Graeff-Meeder E. R., Lucassen M. A., van der Zee R., Voorhorst-Ogink M. M., van Kooten P. J., Geuze H. J., van Eden W. Two monoclonal antibodies generated against human hsp60 show reactivity with synovial membranes of patients with juvenile chronic arthritis. J Exp Med. 1992 Jun 1;175(6):1805–1810. doi: 10.1084/jem.175.6.1805. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Broeren C. P., Lucassen M. A., van Stipdonk M. J., van der Zee R., Boog C. J., Kusters J. G., van Eden W. CDR1 T-cell receptor beta-chain peptide induces major histocompatibility complex class II-restricted T-T cell interactions. Proc Natl Acad Sci U S A. 1994 Jun 21;91(13):5997–6001. doi: 10.1073/pnas.91.13.5997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Brostoff S. W., Howell M. D. T cell receptors, immunoregulation, and autoimmunity. Clin Immunol Immunopathol. 1992 Jan;62(1 Pt 1):1–7. doi: 10.1016/0090-1229(92)90016-h. [DOI] [PubMed] [Google Scholar]
  9. Buus S., Werdelin O. Oligopeptide antigens of the angiotensin lineage compete for presentation by paraformaldehyde-treated accessory cells to T cells. J Immunol. 1986 Jan;136(2):459–465. [PubMed] [Google Scholar]
  10. Chesnut R. W., Grey H. M. Studies on the capacity of B cells to serve as antigen-presenting cells. J Immunol. 1981 Mar;126(3):1075–1079. [PubMed] [Google Scholar]
  11. Fukumoto T., McMaster W. R., Williams A. F. Mouse monoclonal antibodies against rat major histocompatibility antigens. Two Ia antigens and expression of Ia and class I antigens in rat thymus. Eur J Immunol. 1982 Mar;12(3):237–243. doi: 10.1002/eji.1830120313. [DOI] [PubMed] [Google Scholar]
  12. Gerrard T. L., Volkman D. J., Jurgensen C. H., Fauci A. S. Activated human T cells can present denatured antigen. Hum Immunol. 1986 Dec;17(4):416–425. doi: 10.1016/0198-8859(86)90301-0. [DOI] [PubMed] [Google Scholar]
  13. Holoshitz J., Matitiau A., Cohen I. R. Arthritis induced in rats by cloned T lymphocytes responsive to mycobacteria but not to collagen type II. J Clin Invest. 1984 Jan;73(1):211–215. doi: 10.1172/JCI111193. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Ko H. S., Fu S. M., Winchester R. J., Yu D. T., Kunkel H. G. Ia determinants on stimulated human T lymphocytes. Occurrence on mitogen- and antigen-activated T cells. J Exp Med. 1979 Aug 1;150(2):246–255. doi: 10.1084/jem.150.2.246. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Kumar V., Sercarz E. E. The involvement of T cell receptor peptide-specific regulatory CD4+ T cells in recovery from antigen-induced autoimmune disease. J Exp Med. 1993 Sep 1;178(3):909–916. doi: 10.1084/jem.178.3.909. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. LaSalle J. M., Ota K., Hafler D. A. Presentation of autoantigen by human T cells. J Immunol. 1991 Aug 1;147(3):774–780. [PubMed] [Google Scholar]
  17. Lanzavecchia A., Roosnek E., Gregory T., Berman P., Abrignani S. T cells can present antigens such as HIV gp120 targeted to their own surface molecules. Nature. 1988 Aug 11;334(6182):530–532. doi: 10.1038/334530a0. [DOI] [PubMed] [Google Scholar]
  18. Lorber M. I., Loken M. R., Stall A. M., Fitch F. W. I-A antigens on cloned alloreactive murine T lymphocytes are acquired passively. J Immunol. 1982 Jun;128(6):2798–2803. [PubMed] [Google Scholar]
  19. Mason D. W., Gallico G. G. Tissue distribution and quantitation of Ia-like antigens in the rat. Eur J Immunol. 1978 Oct;8(10):741–748. doi: 10.1002/eji.1830081013. [DOI] [PubMed] [Google Scholar]
  20. McMaster W. R., Williams A. F. Identification of Ia glycoproteins in rat thymus and purification from rat spleen. Eur J Immunol. 1979 Jun;9(6):426–433. doi: 10.1002/eji.1830090603. [DOI] [PubMed] [Google Scholar]
  21. Pichler W. J., Wyss-Coray T. T cells as antigen-presenting cells. Immunol Today. 1994 Jul;15(7):312–315. doi: 10.1016/0167-5699(94)90078-7. [DOI] [PubMed] [Google Scholar]
  22. Reske-Kunz A. B., Reske K., Rüde E. Cloned murine Ia+ BK-BI-2.6.C6 T cells function as accessory cells presenting protein antigens to long-term-cultured antigen-specific T cell lines. J Immunol. 1986 Mar 15;136(6):2033–2040. [PubMed] [Google Scholar]
  23. Reske K., Möhle U., Sun D., Wekerle H. Synthesis and cell surface display of class II determinants by long-term propagated rat T line cells. Eur J Immunol. 1987 Jul;17(7):909–914. doi: 10.1002/eji.1830170703. [DOI] [PubMed] [Google Scholar]
  24. Roberts L. K., Spangrude G. J., Daynes R. A., Krueger G. G. Correlation between keratinocyte expression of Ia and the intensity and duration of contact hypersensitivity responses in mice. J Immunol. 1985 Nov;135(5):2929–2936. [PubMed] [Google Scholar]
  25. Sidhu S., Deacock S., Bal V., Batchelor J. R., Lombardi G., Lechler R. I. Human T cells cannot act as autonomous antigen-presenting cells, but induce tolerance in antigen-specific and alloreactive responder cells. J Exp Med. 1992 Sep 1;176(3):875–880. doi: 10.1084/jem.176.3.875. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Sopori M. L., Cohen D. A., Cherian S., Perrone R. S., Kaplan A. M. Antigen presentation in the rat. II. An Ia+ radiosensitive T cell can present antigen to primed Ia- T cells. J Immunol. 1985 Mar;134(3):1369–1373. [PubMed] [Google Scholar]
  27. Sopori M. L., Hurt Y. L., Cherian S., Kaplan A. M., Diamantstein T. Differential requirement for accessory cells in polyclonal T-cell activation. Cell Immunol. 1987 Mar;105(1):174–186. doi: 10.1016/0008-8749(87)90066-9. [DOI] [PubMed] [Google Scholar]
  28. Telerman A., Amson R. B., Romasco F., Wybran J., Galand P., Mosselmans R. Internalization of human T lymphocyte receptors. Eur J Immunol. 1987 Jul;17(7):991–997. doi: 10.1002/eji.1830170715. [DOI] [PubMed] [Google Scholar]
  29. Van den Eertwegh A. J., Noelle R. J., Roy M., Shepherd D. M., Aruffo A., Ledbetter J. A., Boersma W. J., Claassen E. In vivo CD40-gp39 interactions are essential for thymus-dependent humoral immunity. I. In vivo expression of CD40 ligand, cytokines, and antibody production delineates sites of cognate T-B cell interactions. J Exp Med. 1993 Nov 1;178(5):1555–1565. doi: 10.1084/jem.178.5.1555. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Vandenbark A. A., Hashim G., Offner H. TCR peptide therapy in autoimmune diseases. Int Rev Immunol. 1993;9(4):251–276. doi: 10.3109/08830189309051210. [DOI] [PubMed] [Google Scholar]
  31. Wyss-Coray T., Gallati H., Pracht I., Limat A., Mauri D., Frutig K., Pichler W. J. Antigen-presenting human T cells and antigen-presenting B cells induce a similar cytokine profile in specific T cell clones. Eur J Immunol. 1993 Dec;23(12):3350–3357. doi: 10.1002/eji.1830231243. [DOI] [PubMed] [Google Scholar]
  32. van Eden W., Thole J. E., van der Zee R., Noordzij A., van Embden J. D., Hensen E. J., Cohen I. R. Cloning of the mycobacterial epitope recognized by T lymphocytes in adjuvant arthritis. Nature. 1988 Jan 14;331(6152):171–173. doi: 10.1038/331171a0. [DOI] [PubMed] [Google Scholar]
  33. van de Water C., Haagsma N., van Kooten P. J., van Eden W. An enzyme-linked immunosorbent assay for the determination of chloramphenicol using a monoclonal antibody. Application to residues in swine muscle tissue. Z Lebensm Unters Forsch. 1987 Sep;185(3):202–207. doi: 10.1007/BF01042047. [DOI] [PubMed] [Google Scholar]

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