Phenotypic and functional similarity of gut intraepithelial and systemic T cells in a teleost fish

Journal of Immunology

Volumn 176, Issue 7, 2006, Pages 3942-3949

  Bernard, David ^a   Six, Adrien ^b   Rigottier Gois, Lionel ^c   Messiaen, Sébastien ^a   Chilmonczyk, Stefan ^a   Quillet, Edwige ^c   Boudinot, Pierre ^a   Benmansour, Abdenour ^a  

^a INRA Institut National de la Recherche Agronomique   (France)

^b INSTITUT PASTEUR   (France)

^c CEMAGREF   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CD28 ANTIGEN; CD3 ANTIGEN; CD3 ANTIGEN EPSILON; CD4 ANTIGEN; CD8 ANTIGEN; IMMUNOGLOBULIN M; T LYMPHOCYTE RECEPTOR; T LYMPHOCYTE RECEPTOR BETA CHAIN; T LYMPHOCYTE RECEPTOR GAMMA CHAIN; T LYMPHOCYTE RECEPTOR VBETA4; T LYMPHOCYTE RECEPTOR ZETA; UNCLASSIFIED DRUG; BIOLOGICAL MARKER; LYMPHOCYTE ANTIGEN RECEPTOR;

ANIMAL CELL; ANIMAL TISSUE; ANTIGEN EXPRESSION; ARTICLE; CELL FUNCTION; GUT INTRAEPITHELIAL LYMPHOCYTE; IMMUNE RESPONSE; LYMPHOCYTE; LYMPHOCYTE HOMING; MESENTERY LYMPH NODE; NONHUMAN; NUCLEOTIDE SEQUENCE; PEYER PATCH; PHENOTYPE; POLYCLONAL ACTIVATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAINBOW TROUT; RHABDOVIRUS; SPLEEN CELL; T LYMPHOCYTE; TELEOST; VIRUS INFECTION; ANIMAL; CELL MOTION; CYTOLOGY; EPITHELIUM CELL; IMMUNOLOGY; INTESTINE; METABOLISM; VIRAL HEMORRHAGIC SEPTICEMIA VIRUS; VIROLOGY;

ANIMALS; BIOLOGICAL MARKERS; CELL MOVEMENT; EPITHELIAL CELLS; INTESTINES; NOVIRHABDOVIRUS; ONCORHYNCHUS MYKISS; PHENOTYPE; RECEPTORS, ANTIGEN, B-CELL; RHABDOVIRIDAE INFECTIONS; T-LYMPHOCYTES;

EID: 33646034651     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.176.7.3942     Document Type: Article

References (38)

1. Guy-Grand, D., C. Griscelli, and P. Vassalli. 1978. The mouse gut T lymphocyte, a novel type of T cell: nature, origin, and traffic in mice in normal and graft-versus-host conditions. J. Exp. Med. 148: 1661-1677.
2. Hayday, A., E. Theodoridis, E. Ramsburg, and J. Shires. 2001. Intraepithelial lymphocytes: exploring the third way in immunology. Nat Immunol. 2: 997-1003.
3. Guy-Grand, D., and P. Vassalli. 2002. Gut intraepithelial lymphocyte development. Curr. Opin. Immunol. 14: 255-259.
4. + lymphocyte populations with different T cell receptors: a role for the gut epithelium in T cell differentiation. J. Exp. Med. 173: 471-481.
5. Poussier, P., P. Edouard, C. Lee, M. Binnie, and M. Julius. 1992. Thymus-independent development and negative selection of T cells expressing T cell receptor αβ in the intestinal epithelium: evidence for distinct circulation patterns of gut- and thymus-derived T lymphocytes. J. Exp. Med. 176: 187-199.
6. Regnault, A., A. Cumano, P. Vassalli, D. Guy-Grand, and P. Kourilsky. 1994. Oligoclonal repertoire of the CD8 αα and the CD8 αβ TCR-αβ murine intestinal intraepithelial T lymphocytes: evidence for the random emergence of T cells. J. Exp. Med. 180: 1345-1358.
7. Gross, G. G., V. L. Schwartz, C. Stevens, E. C. Ebert, R. S. Blumberg, and S. P. Balk. 1994. Distribution of dominant T cell receptor β-chains in human intestinal mucosa. J. Exp. Med. 180: 1337-1344.
8. Helgeland, L., F. E. Johansen, J. O. Utgaard, J. T. Vaage, and P. Brandtzaeg. 1999. Oligoclonality of rat intestinal intraepithelial T lymphocytes: overlapping TCR β-chain repertoires in the CD4 single-positive and CD4/CD8 double-positive subsets. J. Immunol. 162: 2683-2692.
9. Williams, A. M., P. W. Bland, A. C. Phillips, S. Turner, T. Brooklyn, G. Shaya, R. D. Spicer, and C. S. Probert. 2004. Intestinal αβ T cells differentiate and rearrange antigen receptor genes in situ in the human infant. J. Immunol 173: 7190-7199.
10. + intestinal intraepithelial lymphocytes in rats. Eur. J. Immunol. 22: 159-164.
11. Dunon, D., J. Schwager, J. P. Dangy, M. D. Cooper, and B. A. Imhof. 1994. T cell migration during development: homing is not related to TCR V β1 repertoire selection. EMBO J. 13: 808-815.
12. Umesaki, Y., H. Setoyama, S. Matsumoto, A. Imaoka, and K. Itoh. 1999. Differential roles of segmented filamentous bacteria and clostridia in development of the intestinal immune system. Infect. Immun. 67: 3504-3511.
13. Guarner, F., and J. R. Malagelada. 2003. Gut flora in health and disease. Lancet. 361: 512-519.
14. Helgeland, L., E. Dissen, K. Z. Dai, T. Midtvedt, P. Brandtzaeg, and J. T. Vaage. 2004. Microbial colonization induces oligoclonal expansions of intraepithelial CD8 T cells in the gut. Eur. J. Immunol. 34: 3389-3400.
15. Nelson McMillan, D., and C. Secombes. 1997. Isolation of rainbow trout (Oncorhynchus mykiss) intestinal intraepithelial lymphocytes (IEL) and measurement of their cytotoxic activity. Fish Shellfish Immunol. 7: 527-541.
16. Rombout, J. H., A. J. Taverne-Thiele, and M. I. Villena. 1993. The gut-associated lymphoid tissue (GALT) of carp (Cyprinus carpio L.): an immunocytochemical analysis. Dev. Comp. Immunol. 17: 55-66.
17. Picchietti, S., F. R. Terribili, L. Mastrolia, G. Scapigliati, and L. Abelli. 1997. Expression of lymphocyte antigenic determinants in developing gut-associated lymphoid tissue of the sea bass Dicentrarchus labrax (L.). Anat Embryol. 196: 457-463.
18. Matsunaga, T., and A. Rahman. 1998. What brought the adaptive immune system to vertebrates? The jaw hypothesis and the seahorse. Immunol. Rev. 166: 177-186.
19. Scapigliati, G., N. Romano, L. Abelli, S. Meloni, A. G. Ficca, F. Buonocore, S. Bird, and C. J. Secombes. 2000. Immunopurification of T-cells from sea bass Dicentrarchus labrax (L.). Fish Shellfish Immunol. 10: 329-341.
20. Rawls, J. F., B. S. Samuel, and J. I. Gordon. 2004. Gnotobiotic zebrafish reveal evolutionary conserved responses to the gut microbiota. Proc. Natl. Acad. Sci. USA 101: 4596-4601.
21. Pannetier, C., J. Even, and P. Kourilsky. 1995. T-cell repertoire diversity and clonal expansions in normal and clinical samples. Immunol. Today 16: 176-181.
22. Boudinot, P., S. Boubekeur, and A. Benmansour. 2001. Rhabdovirus infection induces public and private T cell responses in teleost fish. J. Immunol. 167: 6202-6209.
23. Boudinot, P., D. Bernard, S. Boubekeur, M. I. Thoulouze, M. Bremont, and A. Benmansour. 2004. The glycoprotein of a fish rhabdovirus profiles the virus-specific T-cell repertoire in rainbow trout. J. Gen. Virol. 85: 3099-3108.
24. Boudinot, P., S. Boubekeur, and A. Benmansour. 2002. Primary structure and complementarity-determining region (CDR) 3 spectratyping of rainbow trout TCRβ transcripts identify ten Vβ families with Vβ6 displaying unusual CDR2 and differently spliced forms. J. Immunol. 169: 6244-6252.
25. Hansen, J. D., and P. Strassburger. 2000. Description of an ectothermic TCR coreceptor, CD8 α, in rainbow trout. J. Immunol. 164: 3132-3139.
26. Collette, A., and A. Six. 2002. ISEApeaks: an Excel platform for GeneScan and Immunoscope data retrieval, management, and analysis. Bioinformatics 18: 329-330.
27. Collette, A., S. Bagot, M. E. Ferrandiz, P. A. Cazenave, A. Six, and S. Pied. 2004. A profound alteration of blood TCRB repertoire allows prediction of cerebral malaria. J. Immunol. 173: 4568-4575.
28. Mangin, I., R. Bonnet, P. Seksik, L. Rigottier-Gois, M. Sutren, Y. Bouhnik, C. Neut, M. D. Collins, J. F. Colombel, P. Marteau, and J. Dore. 2004. Molecular inventory of faecal microflora in patients with Crohn's disease. FEMS Microbiol. Ecol. 50: 25-36.
29. Hansen, J. D., E. D. Landis, and R. B. Phillips. 2005. Discovery of a unique Ig heavy-chain isotype (IgT) in rainbow trout: implications for a distinctive B cell developmental pathway in teleost fish. Proc. Natl. Acad. Sci. USA 102: 6919-6924.
30. Regnault, A., A. Cumano, P. Vassalli, D. Guy-Grand, and P. Kourilsky. 1994. Oligoclonal repertoire of the CD8 αα and the CD8 αβ TCR-αβ murine intestinal intraepithelial T lymphocytes: evidence for the random emergence of T cells. J. Exp. Med. 180: 1345-1358.
31. Wagner, N., J. Lohler, E. J. Kunkel, K. Ley, E. Leung, G. Krissansen, K. Rajewsky, and W. Muller. 1996. Critical role for β7 integrins in formation of the gut-associated lymphoid tissue. Nature 382: 366-370.
32. Kim, S. K., D. S. Reed, W. R. Heath, F. Carbone, and L. Lefrancois. 1997. Activation and migration of CD8 T cells in the intestinal mucosa. J. Immunol. 159: 4295-4306.
33. Buzoni-Gatel, D., H. Debbabi, M. Moretto, I. H. Dimier-Poisson, A. C. Lepage, D. T. Bout, and L. H. Kasper. 1999. Intraepithelial lymphocytes traffic to the intestine and enhance resistance to Toxoplasma gondii oral infection. J. Immunol. 162: 5846-5852.
34. Arstila, T., T. P. Arstila, S. Calbo, F. Selz, M. Malassis-Seris, P. Vassalli, P. Kourilsky, and D. Guy-Grand. 2000. Identical T cell clones are located within the mouse gut epithelium and lamina propia and circulate in the thoracic duct lymph. J. Exp. Med. 191: 823-834.
35. Holben, W. E., P. Williams, M. A. Gilbert, M. Saarinen, L. K. Sarkilahti, and J. H. Apajalahti. 2002. Phylogenetic analysis of intestinal microflora indicates a novel Mycoplasma phylotype in farmed and wild salmon. Microbiol. Ecol. 44: 175-185.
36. Huber, I., B. Spanggaard, K. F. Appel, L. Rossen, T. Nielsen, and L. Gram. 2004. Phylogenetic analysis and in situ identification of the intestinal microbial community of rainbow trout (Oncorhynchus mykiss, Walbaum). J. Appl. Microbiol. 96: 117-132.
37. Wilson, M., E. Hsu, A. Marcuz, M. Courtet, L. Du Pasquier, and C. Steinberg. 1992. What limits affinity maturation of antibodies in Xenopus, the rate of somatic mutation or the ability to select mutants? EMBO J. 11: 4337-4347.
38. Suetake, H., K. Araki, and Y. Suzuki. 2004. Cloning, expression, and characterization of fugu CD4, the first ectothermic animal CD4. Immunogenetics 56: 368-374.