Regional and global changes in TCRαβ T cell repertoires in the gut are dependent upon the complexity of the enteric microflora

Developmental and Comparative Immunology

Volumn 34, Issue 4, 2010, Pages 406-417

  Mwangi, William N ^a   Beal, Richard K ^a   Powers, Claire ^a   Wu, Xikun ^a   Humphrey, Tom ^b   Watson, Michael ^a   Bailey, Michael ^b   Friedman, Aharon ^d   Smith, Adrian L ^a,c  

^a INSTITUTE FOR ANIMAL HEALTH   (United Kingdom)

^b UNIVERSITY OF BRISTOL   (United Kingdom)

^c UNIVERSITY OF OXFORD   (United Kingdom)

^d HEBREW UNIVERSITY OF JERUSALEM   (Israel)

Author keywords

Clonality; Germ free; Microflora; Mucosal immunology; Spectratyping; T cell receptor

Indexed keywords

T LYMPHOCYTE RECEPTOR ALPHA CHAIN; T LYMPHOCYTE RECEPTOR BETA CHAIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELLULAR IMMUNITY; CHICKEN; CONTROLLED STUDY; GASTROINTESTINAL INFECTION; GERMFREE ANIMAL; GNOTOBIOTICS; IMMUNOGLOBULIN STRUCTURE; INTESTINE FLORA; MICROBIAL DIVERSITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; SEQUENCE ANALYSIS; SPLEEN; T LYMPHOCYTE SUBPOPULATION;

GALLUS GALLUS; MAMMALIA;

EID: 74449086730     PISSN: 0145305X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.dci.2009.11.009     Document Type: Article

References (47)

1. Kawaguchi-Miyashita M., Shimizu K., Nanno M., Shimada S., Watanabe T., Koga Y., et al. Development and cytolytic function of intestinal intraepithelial T lymphocytes in antigen-minimized mice. Immunology 89 (1996) 268-273
2. Suzuki H., Jeong K.I., Itoh K., and Doi K. Regional variations in the distributions of small intestinal intraepithelial lymphocytes in germ-free and specific pathogen-free mice. Exp Mol Pathol 72 (2002) 230-235
3. Probert C.S., Williams A.M., Stepankova R., Tlaskalova-Hogenova H., Phillips A., and Bland P.W. The effect of weaning on the clonality of alpha beta T-cell receptor T cells in the intestine of GF and SPF mice. Dev Comp Immunol 31 (2007) 606-617
4. Williams A.M., Bland P.W., Phillips A.C., Turner S., Brooklyn T., Shaya G., et al. Intestinal alpha beta T cells differentiate and rearrange antigen receptor genes in situ in the human infant. J Immunol 173 (2004) 7190-7199
5. Balk S.P., Ebert E.C., Blumenthal R.L., McDermott F.V., Wucherpfennig K.W., Landau S.B., et al. Oligoclonal expansion and CD1 recognition by human intestinal intraepithelial lymphocytes. Science 20 253 (1991) 1411-1415
6. Van Kerckhove C., Russell G.J., Deusch K., Reich K., Bhan A.K., DerSimonian H., et al. Oligoclonality of human intestinal intraepithelial T cells. J Exp Med 175 (1992) 57-63
7. Blumberg R.S., Yockey C.E., Gross G.G., Ebert E.C., and Balk S.P. Human intestinal intraepithelial lymphocytes are derived from a limited number of T cell clones that utilize multiple V beta T cell receptor genes. J Immunol 150 (1993) 5144-5153
8. Gross G.G., Schwartz V.L., Stevens C., Ebert E.C., Blumberg R.S., and Balk S.P. Distribution of dominant T cell receptor beta chains in human intestinal mucosa. J Exp Med 180 (1994) 1337-1344
9. Helgeland L., Johansen F.E., Utgaard J.O., Vaage J.T., and Brandtzaeg P. Oligoclonality of rat intestinal intraepithelial T lymphocytes: overlapping TCR beta-chain repertoires in the CD4 single-positive and CD4/CD8 double-positive subsets. J Immunol 162 (1999) 2683-2692
10. Helgeland L., Vaage J.T., Rolstad B., Midtvedt T., and Brandtzaeg P. Microbial colonization influences composition and T-cell receptor V beta repertoire of intraepithelial lymphocytes in rat intestine. Immunology 89 (1996) 494-501
11. Urtishak S.L., McKenna E.A., and Mastro A.M. Prolactin and prolactin receptor expression in rat, small intestine, intraepithelial lymphocytes during neonatal development. Dev Immunol 8 (2001) 319-330
12. Chen C.H., Gobel T.W., Kubota T., and Cooper M.D. T cell development in the chicken. Poult Sci 73 (1994) 1012-1018
13. Lahti J.M., Chen C.L., Tjoelker L.W., Pickel J.M., Schat K.A., Calnek B.W., et al. Two distinct alpha beta T-cell lineages can be distinguished by the differential usage of T-cell receptor V beta gene segments. Proc Natl Acad Sci USA 88 (1991) 10956-10960
14. Tjoelker L.W., Carlson L.M., Lee K., Lahti J., McCormack W.T., Leiden J.M., et al. Evolutionary conservation of antigen recognition: the chicken T-cell receptor beta chain. Proc Natl Acad Sci USA 87 (1990) 7856-7860
15. Kaufman J., Milne S., Gobel T.W., Walker B.A., Jacob J.P., Auffray C., et al. The chicken B locus is a minimal essential major histocompatibility complex. Nature 401 (1999) 923-925
16. Char D., Sanchez P., Chen C.L., Bucy R.P., and Cooper M.D. A third sublineage of avian T cells can be identified with a T cell receptor-3-specific antibody. J Immunol 145 (1990) 3547-3555
17. Dunon D., Schwager J., Dangy J.P., Cooper M.D., and Imhof B.A. T cell migration during development: homing is not related to TCR V beta 1 repertoire selection. EMBO J 13 (1994) 808-815
18. Lillehoj H.S., and Chung K.S. Postnatal development of T-lymphocyte subpopulations in the intestinal intraepithelium and lamina propria in chickens. Vet Immunol Immunopathol 31 (1992) 347-360
19. Cihak J., Hoffmann-Fezer G., Ziegler-Heibrock H.W., Stein H., Kaspers B., Chen C.H., et al. T cells expressing the V beta 1 T-cell receptor are required for IgA production in the chicken. Proc Natl Acad Sci USA 88 (1991) 10951-10955
20. Beal R.K., Wigley P., Powers C., Hulme S.D., Barrow P.A., and Smith A.L. Age at primary infection with Salmonella enterica serovar Typhimurium in the chicken influences persistence of infection and subsequent immunity to re-challenge. Vet Immunol Immunopathol 100 (2004) 151-164
21. Brisbin J.T., Gong J., and Sharif S. Interactions between commensal bacteria and the gut-associated immune system of the chicken. Anim Health Res Rev 9 (2008) 101-110
22. Friedman A. Oral tolerance in birds and mammals: digestive tract development determines the strategy. J Appl Poult Res 17 (2008) 168-173
23. Friedman A., Bar-shira E., and Sklan D. Ontogeny of gut associated immune competence in the chick. World Poult Sci J 59 (2003) 209-219
24. Honjo K., Hagiwara T., Itoh K., Takahashi E., and Hirota Y. Immunohistochemical analysis of tissue distribution of B and T cells in germfree and conventional chickens. J Vet Med Sci 55 (1993) 1031-1034
25. Imhof B.A., Dunon D., Courtois D., Luhtala M., and Vainio O. Intestinal CD8 alpha alpha and CD8 alpha beta intraepithelial lymphocytes are thymus derived and exhibit subtle differences in TCR beta repertoires. J Immunol 165 (2000) 6716-6722
26. Cooper M.D., Chen C.L., Bucy R.P., and Thompson C.B. Avian T cell ontogeny. Adv Immunol 50 (1991) 87-117
27. McCormack W.T., Tjoelker L.W., Stella G., Postema C.E., and Thompson C.B. Chicken T-cell receptor beta-chain diversity: an evolutionarily conserved D beta-encoded glycine turn within the hypervariable CDR3 domain. Proc Natl Acad Sci USA 88 (1991) 7699-7703
28. Shigeta A., Sato M., Kawashima T., Horiuchi H., Matsuda H., and Furusawa S. Genomic organization of the chicken T-cell receptor beta chain D-J-C region. J Vet Med Sci 66 (2004) 1509-1515
29. Harrison G.F. Production of Germ-free chicks: a comparison of the hatchability of eggs sterilized externally by different methods. Lab Anim 3 (1969) 51-59
30. Coates M.E., Fuller R., Harrison G.F., Lev M., and Suffolk S.F. A comparison of the growth of chicks in the Gustafsson germ-free apparatus and in a conventional environment, with and without dietary supplements of penicillin. Br J Nutr 17 (1963) 141-150
31. Laky K., Lefrancois L., and Puddington L. Age-dependent intestinal lymphoproliferative disorder due to stem cell factor receptor deficiency: parameters in small and large intestine. J Immunol 158 (1997) 1417-1427
32. Cebra J.J. Influences of microbiota on intestinal immune system development. Am J Clin Nutr 69 (1999) 1046-1051
33. Shi H.N., and Walker A. Bacterial colonization and the development of intestinal defences. Can J Gastroenterol 18 (2004) 493-500
34. Elson C.O., Cong Y., Iqbal N., and Weaver C.T. Immuno-bacterial homeostasis in the gut: new insights into an old enigma. Semin Immunol 13 (2001) 187-194
35. Macpherson A.J., and Harris N.L. Interactions between commensal intestinal bacteria and the immune system. Nat Rev Immunol 4 (2004) 478-485
36. Perdigon G., Fuller R., and Raya R. Lactic acid bacteria and their effect on the immune system. Curr Issues Intest Microbiol 2 (2001) 27-42
37. Blum S., and Schiffrin E.J. Intestinal microflora and homeostasis of the mucosal immune response: implications for probiotic bacteria?. Curr Issues Intest Microbiol 4 (2003) 53-60
38. Honda K., and Takeda K. Regulatory mechanisms of immune responses to intestinal bacteria. Mucosal Immunol 2 (2009) 187-196
39. Friman V., Nowrouzian F., Adlerberth I., and Wold A.E. Increased frequency of intestinal Escherichia coli carrying genes for S fimbriae and haemolysin in IgA-deficient individuals. Microb Pathog 32 (2002) 35-42
40. Diaz R.L., Hoang L., Wang J., Vela J.L., Jenkins S., Aranda R., et al. Maternal adaptive immunity influences the intestinal microflora of suckling mice. J Nutr 134 (2004) 2359-2364
41. Probert C.S., Saubermann L.J., Balk S., and Blumberg R.S. Repertoire of the alpha beta T-cell receptor in the intestine. Immunol Rev 215 (2007) 215-225
42. Helgeland L., Dissen E., Dai K.Z., Midtvedt T., Brandtzaeg P., and Vaage J.T. Microbial colonization induces oligoclonal expansions of intraepithelial CD8 T cells in the gut. Eur J Immunol 34 (2004) 3389-3400
43. Umesaki Y., Setoyama H., Matsumoto S., and Okada Y. Expansion of alpha beta T-cell receptor-bearing intestinal intraepithelial lymphocytes after microbial colonization in germ-free mice and its independence from thymus. Immunology 79 (1993) 32-37
44. Regnault A., Levraud J.P., Lim A., Six A., Moreau C., Cumano A., et al. The expansion and selection of T cell receptor alpha beta intestinal intraepithelial T cell clones. Eur J Immunol 26 (1996) 914-921
45. Edwards A.G., Weale A.R., Denny A.J., Edwards K.J., Helps C.R., Lear P.A., et al. Antigen receptor V-segment usage in mucosal T cells. Immunology 123 (2008) 181-186
46. Regnault A., Cumano A., Vassalli P., Guy-Grand D., and Kourilsky P. Oligoclonal repertoire of the CD8 alpha alpha and the CD8 alpha beta TCR-alpha/beta murine intestinal intraepithelial T lymphocytes: evidence for the random emergence of T cells. J Exp Med 180 (1994) 1345-1358
47. Parry S.H., Allen W.D., and Porter P. Intestinal immune response to E. coli antigens in the germ-free chicken. Immunology 32 (1977) 731-741