Ontogeny of the immune system: γ/δ and α/β T cells migrate from thymus to the periphery in alternating waves

Journal of Experimental Medicine

Volumn 186, Issue 7, 1997, Pages 977-988

  Dunon, D ^a   Courtois, D ^a   Vainio, O ^b   Six, A ^c   Chen, C H ^c   Cooper, M D ^c   Dangy, J P ^d   Imhof, B A ^d,e  

^a CNRS   (France)

^b UNIVERSITY OF TURKU   (Finland)

^c UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^d BASEL INSTITUTE FOR IMMUNOLOGY   (Switzerland)

^e UNIVERSITY OF GENEVA MEDICAL SCHOOL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

T LYMPHOCYTE RECEPTOR;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CELL MIGRATION; EMBRYO; HEMATOPOIETIC STEM CELL; IMMUNE SYSTEM; NONHUMAN; ONTOGENY; PRIORITY JOURNAL; T LYMPHOCYTE; THYMOCYTE; THYMUS;

ADOPTIVE TRANSFER; AMINO ACID SEQUENCE; ANIMALS; BONE MARROW CELLS; CELL DIFFERENTIATION; CELL MOVEMENT; CHICK EMBRYO; CLONING, MOLECULAR; DNA PRIMERS; GENE REARRANGEMENT, T-LYMPHOCYTE; HEMATOPOIETIC STEM CELLS; KINETICS; MOLECULAR SEQUENCE DATA; PHENOTYPE; RECEPTORS, ANTIGEN, T-CELL, ALPHA-BETA; RECEPTORS, ANTIGEN, T-CELL, GAMMA-DELTA; RNA, MESSENGER; SEQUENCE HOMOLOGY, AMINO ACID; T-LYMPHOCYTE SUBSETS; THYMUS GLAND;

EID: 0030827915     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.186.7.977     Document Type: Article

References (50)

1. Cooper, M., D. Peterson, and R. Good. 1965. Delineation of the thymic and bursal lymphoid system in the chicken. Nature (Lond.). 205:143-146.
2. Moore, M.A.S., and J.J.T. Owen. 1967. Experimental studies on the development of the thymus. J. Exp. Med. 126:715-726.
3. Dieterlen-Lièvre, F., I. Godin, and L. Pardanaud. 1996. Ontogeny of hematopoiesis in the avian embryo: a general paradigm. Curr. Top. Microbiol. Immunol. 212:119-128.
4. Jotereau, F.V., E. Houssaint, and N.M. Le Douarin. 1980. Lymphoid stem cell homing to the early thymic primordium of the avian embryo. Eur. J. Immunol. 10:620-627.
5. Jotereau, F.V., and N.M. Le Douarin. 1982. Demonstration of a cyclic renewal of the lymphocyte precursor cells in the quail thymus during embryonic and perinatal life. J. Immunol. 129:1869-1877.
6. Le Douarin, N.M., F.V. Jotereau, E. Houssaint, and J.P. Thiery. 1984. Primary lymphoid organ ontogeny in birds. In Chimeras in Developmental Biology. N.M. Le Douarin and A. McLaren, editors. Academic Press, London. 179-216.
7. Coltey, M., F.V. Jotereau, and N.M. Le Douarin. 1987. Evidence for a cyclic renewal of lymphocyte precursor cells in the embryonic chick thymus. Cell Differ. 22:71-82.
8. Coltey, M., R.P. Bucy, C.H. Chen, J. Cihak, U. Lösch, D. Char, N.M. Le Douarin, and M.D. Cooper. 1989. Analysis of the first two waves of thymus homing stem cells and their T cell progeny in chick-quail chimeras. J. Exp. Med. 170: 543-557.
9. Dunon, D., J. Kaufman, J. Salomonsen, K. Skjoedt, O. Vainio, J.P. Thiery, and B.A. Imhof. 1990. T cell precursor migration towards β2-microglobulin is involved in thymus colonization of chicken embryos. EMBO (Eur. Mol. Biol. Organ.) J. 9:3315-3322.
10. Vainio, O., D. Dunon, F. Aïssi, J.P. Dangy, K.M. McNagny, and B.A. Imhof. 1996. HEMCAM, an adhesion molecule expressed by c-kit+ hemopoietic progenitors. J. Cell Biol. 135:1655-1668.
11. Dunon, D., M. Cooper, and B. Imhof. 1993. Thymic origin of embryonic intestinal γ/δ T cells. J. Exp. Med. 177:257-263.
12. Dunon, D., M.D. Cooper, and B.A. Imhof. 1993. Migration patterns of thymus derived γδ T cells during chicken development. Eur. J. Immunol. 23:2545-2550.
13. 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 Vβ1 repertoire selection. EMBO (Eur. Mol. Biol. Organ.) J. 13:808-815.
14. Chen, C.H., A. Six, T. Kubota, S. Tsuji, F.K. Kong, T.W.F. Göbel, and M.D. Cooper. 1996. T cell receptors and T cell development. Curr. Top. Microbiol. Immunol. 212:37-53.
15. Rast, J., R. Haire, R. Litman, S. Pross, and G. Litman. 1995. Identification and characterization of T-cell antigen receptor-related genes in phylogenetically diverse vertebrate species. Immunogenetics. 42:204-212.
16. Six, A., J. Rast, W. McCormack, D. Dunon, D. Courtois, Y. Li, C. Chen, and M. Cooper. 1996. Characterization of avian T cell receptor γ genes. Proc. Natl. Acad. Sci. USA. 93: 15329-15334.
17. Sowder, J.T., C.H. Chen, L.L. Ager, M.M. Chan, and M.D. Cooper. 1988. A large subpopulation of avian T cells express a homologue of the mammalian T γ/δ receptor. J. Exp. Med. 167:315-321.
18. Bucy, R.P., C.L. Chen, and M.D. Cooper. 1990. Ontogeny of T cell receptors in the chicken thymus. J. Immunol. 144: 1161-1168.
19. Chen, C.H., J. Cihak, U. Lösch, and M.D. Cooper. 1988. Differential expression of two T cell receptors, TcR1 and TcR2, on chicken lymphocytes. Eur. J. Immunol. 18:539-543.
20. Char, D., P. Sanchez, C. Chen, R. Bucy, and M. Cooper. 1990. A third sublineage of avian T cells can be identified with a T cell receptor-3-specific antibody. J. Immunol. 145: 3547-3555.
21. Dunon, D., and B.A. Imhof. 1996. T cell migration during ontogeny and T cell repertoire generation. Curr. Top. Microbiol. Immunol. 212:79-93.
22. Haas, W., and S. Tonegawa. 1992. Development and selection of γδ T cells. Curr. Opin. Immunol. 4:147-155.
23. Ikuta, K., T. Kina, I. MacNeil, N. Uchida, B. Peault, Y. Chien, and I. Weissman. 1990. A developmental switch in thymic lymphocyte maturation potential occurs at the level of hematopoietic stem cells. Cell. 62:863-874.
24. Ikuta, K., and I. Weissman. 1991. The junctional modifications of a T cell receptor γ chain are determined at the level of thymic precursors. J. Exp. Med. 174:1279-1282.
25. Ikuta, K., N. Uchida, J. Friedman, and I. Weissman. 1992. Lymphocyte development from stem cells. Annu. Rev. Immunol. 10:759-783.
26. Vainio, O., T.V. Veromaa, E. Eerola, and P. Toivanen. 1987. Characterization of two monoclonal antibodies against chicken T lymphocytes surface antigen. In Avian Immunology. W.T. Weber and D.L. Ewert, editors. Alan R. Liss Inc., New York. 99-108.
27. Houssaint, E., A. Mansikka, and O. Vainio. 1991. Early separation of B and T lymphocyte precursors in chick embryo. J. Exp. Med. 174:397-406.
28. Cihak, J., H.W.S. Ziegler-Heitbrock, H. Trainer, I. Schranner, M. Merkenschlager, and U. Lösch. 1988. Characterization and functional properties of a novel monoclonal antibody which identifies a T cell receptor in chickens. Eur. J. Immunol. 18:533-537.
29. Dunon, D., O. Vainio, and B.A. Imhof. 1997. Lymphocyte migration in vivo: the chicken embryo model. In Immunology Manual Methods. I. Lefkovits, editor. Academic Press Ltd., London. 1345-1353.
30. Sambrook, J., E.F. Fritsch, and T. Maniatis. 1989. Molecular cloning. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
31. Keller, G., M. Kennedy, T. Papayannopoulo, and M. Wiles. 1993. Hematopoietic commitment during embryonic stem cell differentiation in culture. Mol. Cell. Biol. 13:473-486.
32. Kost, T., N. Theodorakis, and S. Hughes. 1983. The nucleotide sequence of the chick cytoplasmic beta-actin gene. Nucleic Acids Res. 11:8287-8301.
33. Chen, E., and P. Seeburg. 1985. Supercoil sequencing: a fast and simple method for sequencing plasmid DNA. DNA (NY). 4:165-170.
34. Sanger, F., S. Nicklen, and A. Coulson. 1977. DNA sequencing with chain terminating inhibitors. Proc. Natl. Acad. Sci. USA. 74:5463-5467.
35. Jotereau, F., F. Heuze, V. Salomon-Vie, and H. Gascan. 1987. Cell kinetics in the fetal mouse thymus: precursor cell input, proliferation, and emigration. J. Immunol. 138:1026-1030.
36. Morin, C., F. Jotereau, and A. Augustin. 1992. Patterns of responsiveness of T cell lines and thymocytes reveal waves of specific activity in the post-natal thymus. Int. Immunol. 4: 1091-1101.
37. Kyewski, B.A. 1987. Seeding of thymic microenvironments defined by distinct thymocyte-stromal interactions is developmentally controlled. J. Exp. Med. 166:520-538.
38. van Ewijk, W. 1991. T-cell differentiation is influenced by thymic microenvironments. Annu. Rev. Immunol. 9:591-615.
39. Pickel, J.M., W.T. McCormack, C.H. Chen, M.D. Cooper, and C.B. Thompson. 1993. Differential regulation of V(D)J recombination during development of avian B and T cells. Int. Immunol. 5:919-927.
40. Hein, W., and L. Dudler. 1993. Divergent evolution of T cell repertoires: extensive diversity and developmentally regulated expression of the sheep γδ T cell receptor. EMBO (Eur. Mol. Biol. Organ.) J. 12:715-724.
41. McVay, L., S. Carding, K. Bottomly, and A. Hayday. 1991. Regulated expression and structure of T cell receptor γ/δ transcripts during human ontogeny. EMBO (Eur. Mol. Biol. Organ.) J. 10:83-91.
42. Bogue, M., S. Candéias, C. Benoist, and D. Mathis. 1991. A special neo-repertoire in neonatal mice. EMBO (Eur. Mol. Biol. Organ.) J. 10:3647-3654.
43. Petrie, H., R. Scollay, and K. Shortman. 1992. Commitment to the T-cell receptor α/β or γ/δ lineages can occur just prior to the onset of CD4 and CD8 expression among immature thymocytes. Eur. J. Immunol. 22:2185-2188.
44. Wu, L., R. Scollay, M. Egerton, M. Pearse, G. Spangrude, and K. Shortman. 1991. CD4 expresssed on earliest T-lineage precursor cells in the adult murine thymus. Nature (Lond.). 349:71-74.
45. Cooper, M., C. Chen, R. Bucy, and C. Thompson. 1991. Avian T cell ontogeny. Adv. Immunol. 50:87-117.
46. Schweighoffer, E., and B.J. Fowlkes. 1996. Positive selection is not required for thymic maturation of transgenic γ/δ T cells. J. Exp. Med. 183:2033-2041.
47. Maki, K., S. Sunaga, Y. Komagata, Y. Kodaira, A. Mabuchi, H. Karasuyama, K. Yokomuro, J. Miyazaki, and K. Ikuta. 1996. Interleukin receptor-deficient mice lack γ/δ T cells. Proc. Natl. Acad. Sci. USA. 93:7172-7177.
48. Kasahara, Y., C.H. Chen, and M.D. Cooper. 1993. Growth requirements for avian γ/δ T cells include exogenous cytokines, receptor ligation and in vivo priming. Eur. J. Immunol. 23:2230-2236.
49. Raulet, D.H. 1994. How γ/δ T cells make a living. Curr. Biol. 4:246-248.
50. + α/β T cells. Eur. J. Immunol. 26:420-427.